&EPA
United States
Environmental Protection
Agency
EPA/600/R-13/350 | December 2014
         www.epa.gov/ord
                                   Workshop on
                                   Biological  Integrity
                                   of Coral  Reefs
                    Caribbean Coral Reef Institute
                Isla Magueyes, La Parguera, Puerto Rico

                          August 21-22,2012
        Office of Research and Development
        National Health and Environmental Effects Research Laboratory

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                                                                             EPA/600/R-13/350
                                                                                December 2014
                                                                             www.epa.gov/ord
                     Workshop on Biological Integrity of Coral Reefs
                                    August 21-22, 2012
                              Caribbean Coral Reef Institute
                         Isla Magueyes, La Parguera, Puerto Rico
                                             by
Patricia Bradley
US EPA
Atlantic Ecology Division
NHEERL, ORD
33 East Quay Road
Key West, FL 33040
Deborah L. Santavy
US EPA
Gulf Ecology Division
NHEERL, ORD
1 Sabine Island Drive
Gulf Breeze, FL 32561
Jeroen Gerritsen
Tetra Tech Inc.
400 Red Brook Boulevard
Suite 200
Owings Mills, MD 21117
                                  Contract No. EP-C-09-001
                                    Work Assignment 3-01
                            Great Lakes Environmental Center, Inc.
Project Officer:
Shirley Harrison
US EPA
Office of Water
Office of Science and Technology
Washington, DC 20460
                Work Assignment Manager:
                Susan K. Jackson
                US EPA
                Office of Water
                Office of Science and Technology
                Washington, DC 20460
                  National Health and Environmental Effects Research Laboratory
                             Office of Research and Development
                                    Washington, DC 20460
     Printed on chlorine free 100% recycled paper
with 50% post-consumer fiber using vegetable-based ink.

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Notice and Disclaimer
The US Environmental Protection Agency (EPA) through its Office of Research and Development and
Office of Water funded and collaborated in the research described here under EP-C-09-001,
Work Assignment #3-01, to Great Lakes Environmental Center, Inc. It has been subjected to the
Agency's peer and administrative review and has been approved for publication as an EPA
document. Mention of trade names or commercial products does not constitute endorsement or
recommendation for use.

Under authority of the Clean Water Act (CWA), EPA is committed to protecting the biological
integrity of the Nation's waters, including marine coastal habitats such as mangroves, seagrasses
and coral reefs that lie within the 3-mile territorial waters.

This report summarizes an EPA-sponsored workshop on coral reef biological integrity held at the
Caribbean Coral Reef Institute in La Parguera, Puerto Rico, on August 21-22, 2012. The workshop
brought together scientists with expertise in coral reef taxonomic groups (e.g., stony corals, fishes,
sponges, gorgonians, algae, seagrasses and macroinvertebrates), specializing in community
structure, organism condition, ecosystem function and ecosystem connectivity.

The experts evaluated photos and videos for 12 stations collected during EPA coral reef surveys
(2010 and 2011)  from  Puerto Rico coral reefs exhibiting a wide range of conditions. The experts
individually rated each station as to observed condition (good, fair or poor) and documented their
rationale for the  assignment. The group discussed the reef attributes that characterize biological
integrity (or the natural condition) for Puerto  Rico's coral reefs, which will serve  as the baseline
condition, since the CWA is grounded in the concept of natural, undisturbed conditions.

The long-term goal is to derive scientifically defensible thresholds for different levels of coral reef
condition with a  well-defined narrative for each level. Managers  will be able to use the narratives to
determine which level most appropriately describes the current condition of their coral reefs and
which level is the desired condition. From this, managers can set easily communicated, quantitative
goals for achieving those conditions. The conceptual model will serve as an interpretative
framework to explicitly link science and monitoring information to management and decision-
making.

This is a contribution to the EPA Office of Research and Development's Safe and Sustainable Waters
Research Program, characterizing the effects of land use on estuarine and coastal resources.

The appropriate citation for this report is:
Bradley P, Santavy DL and Gerritsen J. 2014. Workshop on Biological Integrity of Coral Reefs,
August 21-22, 2012, Caribbean Coral Reef Institute, Isla Magueyes, La Parguera,  Puerto Rico.
US Environmental Protection Agency, Office of Research and Development, Atlantic Ecology
Division, Narragansett, Rl. EPA/600/R-13/350.

This document can be downloaded from:
http://water.epa.gov/scitech/swguidance/standards/criteria/aqlife/biocriteria/technical_index.cfm
      Workshop on Biological Integrity of Coral Reefs

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Table of Contents
Figures and Tables	v
Acknowledgements	vii
Executive Summary	viii
Chapter 1.  Introduction
    1.1 Coral Reef Ecosystems	1-2
    1.2 Puerto Rico's Coral Reef Ecosystems	1-2
    1.3 Timelines	1-4
       1.3.1 Condition Timeline	1-4
       1.3.2 Anthropogenic Activity Timeline	1-7
    1.4 Southwestern Puerto Rico	1-9
    1.5 The Clean Water Act	1-10
    1.6 Why a Coral Reef Ecosystem Conceptual Model is Needed	1-11
    1.7 The Framework: The Biological Condition Gradient (BCG) 	1-11
       1.7.1 How is the BCG Constructed? 	1-12
Chapter 2.  Approach
    2.1 Video and Photo Evaluations	2-2
    2.2 Summary of Ratings	2-5
       2.2.1 Best Station, Ranked #1 	2-5
       2.2.2 Worst Station, Ranked #12  	2-6
       2.2.3 Stations Rated Fair 	2-7
       2.2.4 Station Rated Poor	2-8
    2.3 Summary of Attributes  	2-8
    2.4 Reference Condition for Biological Integrity 	2-9
       2.4.1 Experts' Examples of Reference Condition for Biological Integrity 	2-10
       2.4.2 Summary Discussion 	2-14
    2.5 Attributes of a Very Good to Excellent Station 	2-14
       2.5.1 Three-dimensional Topographic Complexity	2-14
       2.5.2 Stony Coral Attributes	2-19
       2.5.3 Gorgonian Attributes 	2-19
       2.5.4 Sponge Attributes 	2-20
       2.5.5 Fish Attributes	2-20
       2.5.6 Large Vertebrate Attributes	2-20
       2.5.7 Other Invertebrate Attributes	2-21
       2.5.8 Algae Attributes 	2-21
       2.5.9 Condition	2-21
Chapter 3.  Discussion and Next Steps
     3.1 Discussion  	3-1
     3.2 Next Steps  	3-1
        3.2.1 Second Workshop  	3-1
        3.2.2 Species Tolerance Database	3-2
        3.2.3 Assembling the Monitoring Data  	3-2
        3.2.4 Calibrating the BCG 	3-3
        3.2.5 Economic Valuation of Coastal Ecosystem  Services	3-4
     3.3 Final Thoughts	3-6
                                                                              Table of Contents
                                                                                                ill

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Appendices
    A.  References 	A-l
    B.  Workshop Participants	B-l
    C.  Workshop Agenda 	C-l
    D.  Tally Sheet - Rating Condition of Coral Reef Videos (1st)	D-l
    E.  Tally Sheet - Rating Condition of Coral Reef Videos (2nd)	E-l
    F.  Notes Sheet - Rating Condition of Coral Reef Videos 	F-l
    G.  Supporting Photos - Rating Condition of Coral Reef Videos	G-l
    H.  Workshop Glossary	H-l
    I.  Summary Data Results for BCG Stations	1-1
    J.  Formulas Used for Calculating Condition Metrics 	J-l
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Figures
1-1.  The Biological Condition Gradient (BCG) 	1-13
2-1.  Map with locations of the 12 EPA stations along the southern coast of Puerto Rico  	2-2
2-2.  Recent changes from 2009 to 2012 in Montastraea populations on a coral reef in Curacao
     (Watamula) that were caused by a 2010 bleaching event 	2-10
2-3.  Two experts suggested Cordelia Banks near Roatan, Honduras, as an example of a reference site
     for excellent coral condition  	2-11
2-4.  Monitoring of massive Acropora cervicornis banks at Cordelia Banks located off a major airport
     in Roatan, Honduras	2-12
2-5.  Panoramic view of Acropora cervicornis banks at Cordelia Banks, Roatan, Honduras	2-12
2-6.  Cover for the book, Beneath the Waves, by Hector J. Ruiz Torres 	2-13
1-1.  Comparison of the density of the major sessile invertebrates assessed in the 12 BCG stations 	1-2
1-2.  Comparison of density for fish carnivores vs. herbivores at BCG stations 	1-3
1-3.  Comparison of biomass for fish carnivores vs. herbivores at BCG stations	1-3
1-4.  Percentages of stony coral species, gorgonian morphologies and sponge morphologies
     for BCG Station 1 	1-4
1-5.  Percentages of stony coral species and  sponge morphologies for BCG Station 2	1-6
1-6.  Percentages of stony coral species, gorgonian morphologies and sponge morphologies
     for BCG Station 3 	1-8
1-7.  Percentages of stony coral species and  sponge morphologies for BCG Station 4	1-10
1-8.  Percentages of stony coral species and  sponge morphologies for BCG Station 5	1-12
1-9.  Percentages of stony coral species, gorgonian morphologies and sponge morphologies
     for BCG Station 6 	1-14
1-10. Percentages of stony coral species and  gorgonian morphologies for BCG Station 7 	1-16
1-11. Percentages of stony coral species and  gorgonian morphologies for BCG Station 8 	1-18
1-12. Percentages of stony coral species, gorgonian morphologies and sponge morphologies
     for BCG Station 9 	1-20
1-13. Percentages of stony coral species, gorgonian morphologies and sponge morphologies
     for BCG Station 10 	1-22
1-14. Percentages of stony coral species, gorgonian morphologies and sponge morphologies
     for BCG Station 11 	1-24
1-15. Percentages of stony coral species, gorgonian morphologies and sponge morphologies
     for BCG Station 12	1-26

Tables
1-1.  Number of currently reported species in each of the major marine taxa for Puerto Rico	1-3
1-2.  Complex relationships between stressors exist in southwestern  Puerto Rico 	1-10
1-3.  Biological and other ecological attributes used to characterize the freshwater streams BCG  	1-14
1-4.  Ecological attributes used to characterize the estuarine BCG 	1-16
2-1.  Shallow inshore linear reefs used for BCG workshop stations that correspond to
     US EPA stations sampled along the southern coast of Puerto Rico	2-2
                                                                            Figures and Tables    v

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2-2.  Coral reef condition evaluated by the experts 	2-4
2-3.  Rankings given by experts after visually evaluating videos and photographs for 12 EPA stations ... 2-4
2-4.  Summary of attributes and their relationships for assessing coral reef condition
     from station evaluations	2-8
2-5.  Summary of descriptions of four condition categories (very good to poor) based on
     expert assessments of individual stations 	2-15
2-6.  Condition levels and associated attributes	2-17
3-1.  Coral reef ecosystem services and reef attributes 	3-5
1-1.  Scleractinian coral summary statistics for BCG stations	1-1
1-2.  Gorgonian summary statistics for BCG stations	1-1
1-3.  Sponge summary statistics for BCG stations	1-2
1-4.  BCG Station 1 data summary for corals and subgroups 	1-4
1-5.  Fish species found in BCG Station 1, with density and biomass for 100m2 transect	1-5
1-6.  BCG Station 2 data summary for corals and subgroups 	1-6
1-7.  Fish species found in BCG Station 2, with density and biomass for 100m2 transect	1-7
1-8.  BCG Station 3 data summary for corals and subgroups 	1-8
1-9.  Fish species found in BCG Station 3, with density and biomass for 100m2 transect	1-9
1-10. BCG Station 4 data summary for corals and subgroups 	1-10
1-11. Fish species found in BCG Station 4, with density and biomass for 100m2 transect	1-11
1-12. BCG Station 5 data summary for corals and subgroups 	1-12
1-13. Fish species found in BCG Station 5, with density and biomass for 100m2 transect	1-13
1-14. BCG Station 6 data summary for corals and subgroups 	1-14
1-15. Fish species found in BCG Station 6, with density and biomass for 100m2 transect	1-15
1-16. BCG Station 7 data summary for corals and subgroups 	1-16
1-17. Fish species found in BCG Station 7', with density and biomass for 100m2 transect	1-17
1-18. BCG Station 8 data summary for corals and subgroups 	1-18
1-19. Fish species found in BCG Station 8, with density and biomass for 100m2 transect	1-19
1-20. BCG Station 9 data summary for corals and subgroups 	1-20
1-21. Fish species found in BCG Station 9, with density and biomass for 100m2 transect	1-21
1-22. BCG Station 10 data summary for corals and subgroups 	1-22
1-23. Fish species found in BCG Station 10, with density and biomass for 100m2 transect	1-23
1-24. BCG Station 11 data summary for corals and subgroups 	1-24
1-25. Fish species found in BCG Station 11, with density and biomass for 100m2 transect	1-25
1-26. BCG Station 12 data summary for corals and subgroups 	1-26
1-27. Fish species found in BCG Station 12, with density and biomass for 100m2 transect	1-27
J-l.  Stony corals included in Western Atlantic and Caribbean assessments with the three-letter
     identification code and the morphological conversion factor for calculating 3-D surface area 	J-2
J-2.  Gorgonian morphological shapes, abbreviations, simulated model, in situ example and
     regression models to estimate three-dimensional surface area 	J-6
J-3.  Sponge morphological shapes, abbreviations, simulated model, in situ example and
     regression models to estimate surface area	J-8
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Acknowledgements
The US Environmental Protection Agency (EPA) Office of Research and Development (ORD)
prepared this coral reefs report.

This is ORD tracking number ORD-007028, Atlantic Ecology Division, Narragansett, Rl. EPA was
supported in the development of this report by the Great Lakes Environmental Center, Inc.,
through contract EP-C-09-001.

The production of  this report would not have been possible without the workshop participants.

Photos from: Charles LoBue, Peggy Harris, Mel Parsons, Alan Humphries, Scott Grossman,
Richard Henry, Alina Szmant and Melanie McField.

The report was peer reviewed by Dr. Ku'ulei Rogers (University of Hawaii), Dr. Wendy Wiltse
(US EPA, Region 9), Ms. Susan K. Jackson (US EPA, Office of Water), and Dr. Giancarlo Cicchetti
and Dr. Marguerite (Peg) Pelletier (US EPA, Office of Research and Development).

We would like to thank the Caribbean Coral Reef Institute, and Drs. Richard Appeldoorn and
Francisco Pagan for hosting the workshop and providing the conference facilities on Magueyes
Island.

We would also like to thank Mr. Roberto Viquiera (Protectores de Cuencas) for assisting with the
logistics, including providing the dormitory facilities in Yauco for visiting scientists.
Acknowledgements
vii

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Executive Summary
EPA's Office of Research and Development (ORD) and Office of Water (OW) hosted a workshop on
coral reef biological integrity that brought together scientists with expertise in coral reef taxonomic
groups (e.g., stony corals, fishes, sponges, gorgonians, algae, seagrasses and macroinvertebrates),
specializing in community structure, organism condition, ecosystem function and ecosystem
connectivity. The goals of this first workshop were to:

    •  Identify key qualitative and quantitative ecological characteristics (reef attributes) that
      determine the condition of linear coral reefs inhabiting shallow waters (<12 m) in
      southwestern Puerto Rico.
    •  Use those reef attributes to recommend categorical condition rankings for establishing a
      biological condition gradient.
    •  Ascertain through expert consensus those reef attributes that characterize biological integrity
      (a natural, fully-functioning system of organisms and communities) for coral reefs.
    •  Develop a conceptual, narrative model that describes how biological attributes of coral reefs
      change along a gradient of increasing anthropogenic (human-generated) stress.
The long-term goal is to derive scientifically defensible thresholds for different levels of coral reef
condition that can be coupled with management objectives and used to evaluate alternative decision
options.

The experts evaluated photos and  videos for 12 stations collected in 2010 and 2011 during EPA coral
reef surveys from  Puerto Rico coral reefs exhibiting a wide range of conditions. The experts
individually rated  each station as to observed condition (good, fair or poor) and documented their
rationale for the assignment. The group discussed the reef attributes that characterize  biological
integrity (or the natural condition) for Puerto Rico's coral reefs. These attributes will be further
developed to characterize the baseline condition, an  important concept for achieving Clean Water
Act goals.

The attributes and thresholds will be organized into a conceptual, narrative model that describes
how biological attributes of coral reefs change along  a gradient of increasing anthropogenic stress.
By providing the explicit characterization of how attributes of the biological system change as human
disturbance increases, decision-makers will be able to use the narratives to determine which level
most appropriately describes the current condition of their coral  reefs and which level  is the desired
condition. From this, managers can set easily communicated, quantitative goals for achieving those
conditions.

This is the first in a series of facilitated workshops and webinars with this group of coral reef experts.
 viii   Workshop on Biological Integrity of Coral Reefs

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Chapter 1. Introduction
The approach described in this report will assist in developing a conceptual, narrative model that
describes how biological attributes of coral reefs change along a gradient of increasing
anthropogenic stress. The framework is expected to serve multiple purposes.

  • It will assist decision-makers in understanding the current conditions of the Puerto Rico coral
    reefs relative to natural, undisturbed conditions, the critical attributes of the coral reefs and
    how each attribute changes in response to stress. Through this framework, decision-makers can
    set realistic goals for their coral reefs and establish monitoring (measurement) endpoints that
    are meaningful based upon the attributes identified by the scientific community.
  • It will be used to support the development of an economic survey of Puerto Rico's
    coral reefs (another project being conducted in collaboration with the National Oceanic
    and Atmospheric Administration's Office of National Marine Sanctuaries).
  • It will inform the Bayesian Belief Network (BBN) and Dynamic Systems Models being developed
    by the EPA modelers.
  • It will contribute to the development of coral reef biological criteria for water quality standards
    under the Clean Water Act (CWA) for Puerto Rico.
To initiate the process, scientists with expertise in coral reef taxonomy, ecology, and management
of stony corals, fishes, sponges, gorgonians, algae, seagrasses, and macroinvertebrates, specializing
in community structure, organism condition, ecosystem function and ecosystem connectivity were
brought together. These experts participated in the first workshop, held August 21-22, 2012,  in
La Parguera, Puerto Rico. (See Appendix B for a list of workshop participants.)

The goals of this first workshop were to:

  • Identify key qualitative and quantitative ecological characteristics (reef attributes) that
    determine the condition of linear coral reefs inhabiting shallow waters (< 12 m) in
    southwestern Puerto Rico.
  • Use those reef attributes to recommend categorical condition rankings for establishing
    a biological condition gradient.
  •  Ascertain through expert consensus those reef attributes that characterize biological integrity
    (a natural, fully-functioning system of organisms and communities) for coral reefs.
  • Develop a conceptual, narrative model that describes how biological attributes of coral reefs
    change along a gradient of increasing anthropogenic stress.
The long-term goal is to derive scientifically defensible thresholds for different levels of coral  reef
condition that can be coupled with management objectives and used to evaluate alternative decision
options.
Chapter 1.
Introduction
1-1

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1.1 Coral Reef Ecosystems
Coral reefs are the earth's most biologically diverse marine ecosystems (Sebens 1994; Odum 1997).
Scleractinian (stony) corals, octocorals and sponges provide structural habitat that supports
harvestable fish species and attracts tourists (Bradley et al. 2008). Stony corals also protect
shorelines from erosion by physically blocking current and wave energy (Wilkinson 1996), and
coral reefs provide food and income for 500 million people globally (TNC 2006).

Corals are generally found in clear, shallow tropical oceans,  and their growth is limited by
temperature, salinity, light intensity, water clarity, and other chemical and water quality
characteristics (Wells 1957; Brown and Howard 1985; Hubbard 1997; Ogden 1997; Hoegh-Guldberg
1999). Coral reefs are sensitive to relatively small changes in the environment (Richmond 1993) and
their lack of resilience to environmental change has led some to regard coral reefs as sentinels of
oceanic environmental quality (Hatcher et al. 1987; Andrews and Pickard 1990; Barber et al. 2001).

Healthy stony corals appear to be critical for fish productivity, species richness and fish biomass, all
of which have been reported to decrease with a decline in stony coral health (Warren-Rhodes et al.
2003). Additionally, there appears to be a strong positive  correlation of habitat complexity to the
biodiversity and ecosystem functions of a reef community (Alvarez-Filip et al. 2009), including fish
species richness (Walker et al. 2009; Pittman et al. 2007a, b). The rich  diversity of coral reefs is partly
dependent on the provision of habitable surface area and partly on the variability of that surface
area (Principe et al. 2012).

The adjacent habitats of seagrass meadows and mangrove forests are linked with coral reefs to form
a complex dynamic mosaic that provides critical nurseries, foraging areas, and refugia for fish and
invertebrates (Christensen et al. 2003; Mumby et al. 2004, 2008; Aguilar-Perera and Appeldoorn
2007; McField and Kramer 2007; Meynecke et al. 2008). Mangroves and seagrasses can also trap
sediments, nutrients, and pollutants, which can improve the water quality on nearby reefs
(Grimsditch and Salm 2006). Many juvenile fishes occupy  shallow-water habitats  such as mangroves
and seagrasses, while the adult  forms are found in adjacent coral reefs (Nagelkerken et al. 2000;
Adams et al. 2006; Cerveny 2006; Dahlgren et al. 2006; Clark et al. 2009; Pittman et al. 2010).

1.2 Puerto Rico's Coral Reef Ecosystems
The US territory of Puerto Rico encompasses the main island of Puerto Rico, two  inhabited islands
(Culebra and Vieques) and three uninhabited islands  (Mona, Monito and Desecheo). Puerto Rico has
an estimated coastline of 930 km, a land area of 8,950 km2 and fringing coral reefs with a total area
of 3,370 km2 off the east, south and west coasts (Wilkinson  2004; Burke and Maidens 2004).

The coral reef ecosystem in Puerto Rico is a complex  mosaic of interrelated habitats, including
mangrove forests, seagrass beds and coral reefs, as well as other coral communities (Garcia-Sais
et al. 2008). Ballantine et al. (2008) listed 69 shallow-water (<40 m) scleractinian  species, 260 fish
species, 46 shallow-water alcyonarian species and 500 species of benthic marine  algal flora,
excluding cyanobacteria (Table 1-1).
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Table 1-1. Number of currently reported species in each of the major marine taxa for Puerto Rico
(adapted from Weil 2005).
Taxon
Algae (diatoms; red, green,
blue-green and brown algae)
Mangroves
Seagrasses (Marine Phanerogams)
Sponges (Phylum Porifera)
Corals, anemones, jellyfish
(Phylum Cnidaria)
Unsegmented worms
(Phylum Nemertea)
Bivalves, snails, octopus, mollusks,
nudibranchs (Phylum Mollusca)
Segmented worms, polychaetes
(Phylum Annelida)
Ostracods, crabs, shrimp
(Phylum Arthropoda)
Starfish, sea urchins, brittle stars
(Phylum Echinodermata)
Bryozoans (Phylum Ectoprocta)
Fishes (Superclass Osteichthyes),
sharks, rays (Class Chondrichthyes)
Reptiles (turtles, snakes)
Mammals
# Species
492
5
7
61
171
8
1,176
129
342
165
131
677
5
18
Source
Ballantine and Aponte 1997a, b; Ballantine and
Aponte 2002
Cerame-Vivas 2001
Vicente 1992
Wilson 1902; Weil 2005
Vaughan 1902; Hargitt and Rogers 1902; Almy and
Carrion-Torres 1963; Garcia et al. 2003; Weil 2005
Coe 1902
Dall and Simpson 1902; Grana 1993; Ortiz 1998;
Garcia-Rios 2003
Treadwell 1902, 1939; Long 1975
Benedict 1902; Bigelow 1902; Moore 1902;
Rathbun 1902; Menzies and Glynn 1968
Clark 1902, 1933
Osburn 1940
Dennis 2000; Dennis et al. 2004
Rivero 1978
Belleretal. 1999
While over 60 species of scleractinian corals inhabit the Western Caribbean, reefs in Puerto Rico
were historically dominated by the reef-building coral taxa Montastraea annularis complex1,
Agaricia agaricites, Montastraea cavernosa, Porites astreoides and Colpophyllia natans. Additionally,
Acropora palmata and Acropora cervicornis often formed dense, high-relief monospecific thickets;
A. palmata in shallow exposed fore-reef habitats and A. cervicornis on fore-reefs and in shallow,
protected back-reefs (Morelock et al. 2001).
Recent studies in Puerto Rico show that large corals of the genus Montastraea are critical for the
biodiversity offish and invertebrates and for maintaining the structure, function, and flow of reef
ecosystem services (Beets and Friedlander 1998; Mumby et al. 2008). Mumby et al. (2008) found
that one-fourth to one-third of benthic invertebrates and fish occurred in the Montastraea-
dominated fore-reefs in the Caribbean. A. palmata and A. cervicornis, which have recently been
listed as threatened species in the Caribbean, also significantly contribute to reef growth and
development and provide essential fish habitat (NOAA 2012a; Principe et al. 2012).
1 This report does not adopt the new classifications for the Montastraea annularis species complex (Montastraea
annularis, Montastraea faveolata and Montastraea franksi) reclassified as the original genus Orbicella
 (Buddetal. 2012).
Chapter 1.
Introduction
1-3

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1.3 Timelines

1.3.1 Condition Timeline
1000: Coral reefs would have been regarded as mostly pristine by current standards with healthy
      corals, large, well-structured fish and invertebrate communities, with probably only a
      depletion of some of the larger fauna (Wilkinson 2004).
1800: Large vertebrates such as the green turtle, hawksbill turtle, manatee and Caribbean monk seal
      were decimated in the central and northern Caribbean Sea (Jackson 1997).
1880s: Early taxonomic studies of reefs on Puerto Rico (e.g., mollusks [Gundlach 1883]; crustaceans
      [Gundlach 1887]; fishes [Poey 1881]; polyps, worms, fishes and crustaceans [Stahl 1883];
      algae [Hauck 1888]; and coral  [Vaughn 1902]).
1900: Most coral reefs were healthy and dominated by healthy branching corals, urchins, large
      schools of game fish, sharks and algal grazers. Waters were clear with low nutrient levels
      (Wilkinson 2004).
1952: The last confirmed sighting of the Caribbean monk seal was at Serranilla Bank between
      Jamaica and Nicaragua (Debrot 2000).
Late 1950s and early 1960s: Massive fishing pressure began in Puerto Rico (Appeldoorn personal
      communication). Herbivores and predators were reduced to very small fishes and sea urchins
      (Jackson 1997).
1969: An intensive and extensive coral bleaching event occurred  on coral reefs of southwestern
      Puerto Rico. The bleaching was probably caused by 38.1 cm of rain during a hurricane that
      preceded the bleaching (Williams and Bunkley-Williams 1990).
Late 1970s: Extensive thickets of Acropora palmata were present in 40% of locations surveyed
      around Puerto Rico; 20% of these reefs had dense A. palmata patches and abundant colonies
      of A. cervicornis (Weil et al. 2003).
Late 1970s and early 1980s: A white-band disease (WBD) epizootic event caused extensive mass
      mortality of Acroporid corals throughout their range in the Caribbean with losses up to 95%
      (Gladfelter 1982; Weil et al. 2003, 2009; Weil and Rogers 2011).
1981: Minor but widespread bleaching caused  by elevated sea surface temperatures (SST) occurred
      in southwestern and western Puerto Rico (Williams and Bunkley-Williams 1989, 1990).
1983: Diadema antillarum mass mortality, with 85-100% population declines (Bak et al. 1983; Lessios
      et al. 1984; Lessios 1988, 2005; Osborne 2000). The Diadema antillarum mortality was first
      observed in Puerto Rico in January 1984 in the coral reefs off La Parguera (Vicente and
      Goenega 1984b).
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Late 1980s: Massive coral bleaching and mortality caused by elevated SST. Extensive partial coral
      colony mortalities and some total mortalities of coral reef organisms, including death of some
      400-500 year-old coral colonies (Velazco-Dominguez et al. 2003; Burke and Maidens 2004).
      Massive coral bleaching events in Puerto Rico were first reported by Williams et al. 1987 and
      Goenega etal. 1989.
1990: Severe bleaching in the western north Atlantic caused by elevated SST and doldrum surface
      waters (from Bermuda, Texas, Florida, throughout the Caribbean, south to Brazil). High
      mortalities of fire corals, scleractinian corals, gorgonians, sponges and other coral reef
      organisms (Velazco-Dominguez et al. 2003).
1994: Cumulative impacts of disease, coastal development, coral bleaching and over-fishing have
      resulted in heavily damaged reefs. The more isolated reefs were in better condition because
      they were not affected by land-based stressors (Wilkinson 2004).
1996: Caribbean yellow-band disease (YBD) first observed in Puerto Rico with very low prevalence
      (Bruckner and Bruckner 1997, 2006; Weil et  al. 2009). The disease was highly seasonal
      (summer-fall). YBD affects three species of the former Montastraea annularis species-complex
      (M.faveolata, M. annularis and M. franksi), the most important reef-building corals for this
      area (Bruckner and Bruckner 2006;  Croquer  and Weil 2009; Harvell et al. 2009).
1998: Severe bleaching event in Puerto  Rico caused by elevated SST (July-September); 99% of the
      colonies completely recovered after 9 months; 15% of the colonies bleached again in 1999 and
      recovered by January 2000  (Velazco-Dominguez et al. 2003).
2000: Diadema seem to be making a slow return in many localities in the Caribbean, including
      La Parguera, PR (Weil et al.  2005).
2003: YBD became chronic and colonies showed disease signs all year (Weil et al. 2009). Surveys
      of over 100 reefs along the  coast and islands found that Acroporid populations continued
      to decline in some areas from persistent disease, storms and sedimentation coupled with the
      poor coastal environmental conditions (high turbidity, sub-optimal water quality, etc.) and
      algal overgrowth.
2004: Most inshore reefs show advanced stages of degradation. Montastraea annularis species-
      complex was the dominant stony coral, but it was virtually absent on reefs with low coral
      cover. The encrusting octocoral Erythropodium caribaeorum occurred  at most stations, and
      zoanthids (particularly the encrusting Palythoa species) and sponges were the dominant
      sessile benthic invertebrates in shallow waters. Macroalgae and turf algae were dominant
      instead of corals on most intermediate-depth reefs (Garcia-Sais et al. 2008).
2005: A major  bleaching event caused by elevated  SST in the fall of 2005, followed in 2006 by mass
      cnidarian mortality, had a dramatic impact on Puerto Rican coral reefs. A total of 82 cnidarian
      species were impacted by the bleaching, including 52 scleractinians, 13 octocorals, four
      hydrocorals, four zoanthideans, four actiniarians, three corallimorpharians and two
      scyphozoans (Garcia-Sais et al. 2006, 2008). The most severe bleaching was observed among
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      Montastraea annularis species-complex (94%), Helioseris cucullata (94%), Colpophyllia natans
      (83%), Siderastrea siderea (65%), Millepora species (63%), Mycetophyllia species (2%), Diploria
      species2 (54%), Agaricia species (48%) and Montastraea cavernosa (46%). Three genera
      appeared to be less susceptible to bleaching: Eusmiliafastigiata (22%), Meandrina meandrites
      (26%) and all Porites species (36%). Millepora alcicornis was completely bleached at all
      stations, and most colonies (>65%) had died by December 2005. In August 2006, most corals
      had regained normal coloration, with the exception of Montastraea annularis species colonies,
      which experienced extensive partial and full colony mortality throughout the region. Total
      coral cover declined throughout the region by 40-60%. Disease epizootics followed, including a
      white plague outbreak on the east and southern coasts, and Caribbean yellow-band disease
      (YBD) that primarily affected the Montastraea annularis species-complex that occurred right
      after the peak of the 2005 bleaching event (Garcia-Sais et al. 2008).
      Intense bleaching of octocorals was first noted in late September to early October beginning
      with Erythropodium caribaeorum, followed by Muricea, Briareum and Plexaurella and later by
      Pseudoplexeaura and Pterogorgia species. Bleaching in scleractinian corals, hydrocorals and
      the zoanthid Palythoa caribaeorum, preceded bleaching of octocorals, suggesting octocorals
      may have higher tolerance to thermal stress compared to the other major cnidarian taxa. By
      late November 2005, the majority of the affected octocoral colonies had not died. The
      exceptions were the bleached colonies of Muricea, which had 90% mortality (Prada et al.
      2009).
2006: NOAA's National Marine Fisheries Service (NMFS) listed Acropora palmata and Acropora
      cervicornis corals as threatened throughout their known range by authority of the Endangered
      Species Act (ESA). This designation became final in May 2006 (Federal Register 2006).
2008: The Caribbean monk seal was officially declared extinct after an exhaustive five-year search by
      NOAANMFS.
2014: NOAA NMFS proposed seven Atlantic/Caribbean corals as endangered: Acropora cervicornis,
      Acropora palmata, Dendrogyra cylindrus, Orbicella annularis, Orbicellafaveolata, Orbicella
      franksi and Mycetophyllia ferox and two species as threatened: Agaricia lamarcki and
      Dichocoenia stokesii (Brainard et al. 2011). In their final rule (August 27, 2014), NOAA listed
      0. annularis, 0. faveolata, 0. franksi, D. cylindrus and M. ferox as threatened species and
      determined that D. stokesii and A. lamarcki did not warrant listing. NOAA also determined that
      the listing of Acropora cervicornis and Acropora palmata as threatened in 2006 is still
      warranted.
2 This report does not adopt the new classifications Diploria strigosa and Diploria clivosa as the genus Pseudodiploria
(Buddetal. 2012).
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1.3.2 Anthropogenic Activity Timeline
~2000-3000 B.C.: The Ortoiroid people from the Orinoco region in South America settled in Puerto
      Rico. The Saladoid and Arawak Indians populated the island between 430 BC and 1000 AD. By
      1000 AD the Taino culture was dominant (Rouse 1992). These early populations exploited
      coral reef resources, and there is strong archaeological evidence of major harvesting of fishes,
      molluscs, manatees and turtles (Wilkinson 2004).
1493: Christopher Columbus landed in Puerto Rico, beginning an intense period of colonization and
      resource extraction (mainly gold). The early explorers found the indigenous population
      cultivating, blending, rolling and smoking tobacco. Europeans had never seen tobacco. This
      discovery marked the start of an international passion for "New World" tobacco and its much
      sought after byproduct, the cigar.
1496-1660: Tobacco was the major crop. Half the shipping tonnage  between Puerto Rico and Europe
      (mainly Spain) was comprised of tobacco.
1508: Juan Ponce de Leon founded a town (Guaynia, meaning "a place with water") on the shores of
      Guanica Bay. The narrow channel  and calm waters of Guanica Bay made it a natural refuge for
      ships sailing the Caribbean Sea.
Early 1500s: Sugar was introduced (perhaps when Juan Ponce de  Leon began colonizing the island),
      and many small landowners relied on its export as a source of income.
1548: Hundreds of sugar mills operated by waterpower. The industry was in the hands of small
      landowners whose enterprises succeeded or failed depending on the price of sugar  in the
      market or the whims of the Spanish Crown.
1736: Coffee plants introduced to Puerto Rico, grown mostly for personal and domestic use.
Mid-1800s: French immigrants from the Mediterranean island of Corsica settled around Yauco and
      became well  known as premium coffee exporters to Europe.
1867: (San Narciso), 1899 (San Ciricao), 1928 (San Felipe) and 1932 hurricanes virtually destroyed
      most coffee plantations and tobacco crops.  Many farms never recovered.
1873: First "Centrales" or sugar factories with equipment operated by steam were established.
      Centrifuges were used to separate the sugar crystals from the molasses.
1898: Puerto Rico was ceded to US as a result of the Spanish American War. US markets opened
      to Puerto Rico products (tariff free). Sugar cane was the most important cash crop for the
      territory.
1900: The US enacted the Foraker Act, which removed the previous land ownership cap of 500 acres.
      Large monoculture farming began (primarily sugar).
1901: The South Porto Rico Sugar Company of New Jersey, USA, began construction of the Central
      Guanica sugar mill. The Central Guanica organized a company town around the sugar mill that
      included a hospital, school and housing facilities. This sugar mill was one of the largest in the
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      Caribbean and was one of the largest in the world until World War I (Ayala 1999;
      Wikipedia 2013).
1900-1927: Puerto Rico produced around 35 million pounds of tobacco a year. Tobacco represented
      38% of the value of commercial crops in 1920 (sugar accounted for 25%). In 1910,14% of
      farms reported the cultivation of coffee. 75% of the employed people in Puerto Rico were
      involved in the sugar industry controlled by US corporations (Miller and Lugo 2009).
Early 1930s: The Roosevelt Administration created the Puerto Rico Emergency Relief Administration,
      which became the Puerto Rican Reconstruction Administration in 1935. Rural resettlement
      communities and demonstration farms were established, and coffee and fruit production
      was reorganized.
1934: Jones-Costigan Act set a quota on the amount of sugar that could be exported to the
      US tariff free.
1940s: The Puerto Rico Water Resources Authority (PRWRA) initiated the Southwestern Puerto Rico
      Project (SWPRP). The SWPRP connected five watersheds and a retention pond through
      construction of dammed reservoirs and an underground aqueduct system that diverted water
      south into the Guanica Bay/Rio Loco watershed. This increased the watershed drainage area
      from approximately 57,000 to 97,000 acres.
1941: Land Reform Act was passed, limiting land ownership to 202 hectares (500 acres) or less. Many
      rural residents were now able to buy 10 hectare (25 acre) parcels, allowing them to grow
      crops for profit for both export and internal use. This broke up the land monopoly of the large
      sugar companies (Miller and Lugo 2009).
Late 1940s: The US Department of Agriculture (USDA) ended sugar subsidies for Puerto Rican
      farmers. Annual production of sugar dropped soon after. Massive numbers of Puerto Ricans
      migrated to the  New York area.
1948: The Industrial Incentives Act (Operation Bootstrap) began to shift Puerto Rico from rural
      agriculture to more urbanized communities and industrial sources of income (shifts to
      manufacturing of Pharmaceuticals, chemicals, machinery and electronics).
1948: The Guanica fertilizer plant opened, with storage silos and a shipping pier.
1952: Peak sugar production in Puerto Rico.
1953: Puerto Rico passed Act No. 65, authorizing the Lajas Valley Irrigation System.
1954: The Lajas Valley  Irrigation (LVI)  project, developed under the guidance of experts from the
      USDA led efforts to remove sugar plantations that had long characterized the region. This
      project also started small-scale agricultural farming and introduced cultivated fruits, mainly
      pineapple. The LVI project channelized 200,000 acres of land via 25 miles of a concrete-lined
      main canal, 60 miles of concrete-lined and unlined lateral canals and the corresponding
      drainage system. Two hydroelectric dams and two additional water reservoirs were built.
      Shade-grown coffee was transplanted into sun-exposed areas.
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1955: Guanica Lagoon was drained to increase land available for agriculture.
1970s: Government subsidies and support for sun-grown coffee were implemented.
1981: Guanica sugar mill was closed.
1980s: Widespread conversion to sun-grown coffee reduced biodiversity (from loss of canopy
      habitat) and increased soil erosion from steep and now poorly vegetated, unprotected slopes.
      Soil washed from hillsides into streams and was trapped in the reservoirs, reducing their water
      storage capacity (Soler-Lopez 2001) and increasing sediment deposition in Guanica Bay.
1999: Puerto Rico passed an agricultural reserve law in an attempt to reverse the trend of
      declining agriculture.
2000: The final two sugar factories closed (Coloso and Roig Centrales).
2009: The US Coral Reef Task Force (USCRTF) selected the Guanica Bay watershed as the location for
      its first multi-agency watershed initiative in an attempt to reduce watershed impacts on coral
      reefs in the coastal zone.

1.4 Southwestern Puerto Rico
Southwestern Puerto Rico is relatively rural, with low population density compared to northeastern
Puerto Rico. There are, however, some population centers: Yauco (population 20,295), San German
(population 12,055), Guanica (population 9,224) and Sabana Grande (population 8,961). The human
presence has created a variety of environmental stresses in this region.

Agricultural growth in southwestern Puerto Rico has resulted in widespread land clearing and
modification. Nearly 90% of the area was deforested by the end of the 19th century (Warne et al.
2005), and the largest natural freshwater body in Puerto Rico, the Guanica  Lagoon, was drained in
1955 as  part of an agricultural development project (Sturm et al. 2012). These modifications have led
to increased watershed sediment and nutrient yield, thereby increasing sediment and nutrient
discharge to the coastal shelf (Warne et al. 2005).

Municipal growth has increased impervious cover, generation of stormwater runoff and human
sewage. Impervious cover increases the loading of nutrients, bacteria, sediments and contaminants
such as polycyclic aromatic hydrocarbons (PAHs), heavy metals and other pollutants associated with
automobiles. Stormwater accumulates debris, chemicals, dirt and  other pollutants, which are
untreated and then discharged into coastal rivers and bays. Sewage carries pathogens that can
transmit disease to humans and other animals, contains organic matter that can cause odor and
nuisance problems and nutrients that can cause eutrophication of receiving water bodies. Much of
the rural population  in southwestern Puerto Rico relies upon septic systems for their sewage
treatment. Too often these are failing, inadequate or improperly maintained. There are also several
wastewater treatment plants (WWTP) in the area, which only treat the sewage to eliminate
pathogens and solids. Some of these WWTPs are being upgraded to advanced secondary treatment,
which provides minimal nutrient reduction.
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Communities in the coastal region of southwestern Puerto Rico rely partially on fishing and tourism
for their livelihood. Fishing, if not conducted in a sustainable manner, can lead to overexploitation of
marine living resources (both target species and the marine system as a whole). Boat anchors, traffic
and groundings can adversely impact marine resources. For example, much of the seagrass in the
shallow shelf area near La Parguera is vulnerable to damage from boat propellers. Lost fishing gear,
such as hooks, lines, nets and lobster traps, can also be damaging to marine resources.

Finally, elevated SSTs are correlated with mass bleaching events (Goreau et al. 1992; Glynn 1988,
1991; Hoegh-Guldberg 1999; McClanahan et al. 2007; Meissner et al. 2012). Sea surface
temperatures have been higher during the past three decades than at any other time since reliable
observations began in 1880 (NOAA 2012b). Global warming is caused by human activities that emit
heat-trapping carbon dioxide and result in increased SSTs. A summary table illustrating some of the
major stressors and their sources is shown in Table 1-2.
Table 1-2. Complex relationships between stressors exist in southwestern Puerto Rico.
Source of Stressor
Agriculture
Urban development
Fishing
Increased global CO2 emissions
from power generation
and transportation
Stressors
Increased sediment, nutrient, pesticide and herbicide loads
to aquatic ecosystems
Increased sewage (nutrients and pathogens), stormwater
runoff (sediment, contaminants)
Overexploitation offish populations; by-catch; damage
from fishing gear and boats
Elevated sea surface temperature and acidification in the
marine environment
1.5 The Clean Water Act
The Clean Water Act (CWA) (33 U.S.C. § 1251 et seq. 1972) is the cornerstone for surface water
quality protection in the United States. The CWA objective is to restore and maintain the chemical,
physical and biological integrity of the Nation's waters. The CWA authorizes EPA to determine
"appropriate minimum levels" of protection and to provide oversight to states (states, territories and
commonwealths), which are required to establish water quality standards that define the goals
(designated uses) and pollution limits (water quality criteria) for all waters within their jurisdictions.
States are also required to monitor conditions regularly and  submit biannual  reports summarizing
water quality assessments. Waterbodies that do not meet the water quality criteria are reported as
"impaired", triggering a series of management actions to determine the cause of impairment and to
restore the condition of the waterbody and its resident biota.

Biological integrity is a long-term objective of the CWA, and water quality standards and criteria can
be defined to protect valued aquatic resources,  such as coral reef ecosystems. Biological assessments
directly measure the condition of the aquatic resource to be protected and the cumulative response
of the biological community to all sources of stress. Biological standards (biocriteria) set biological
quality goals.
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The President's Ocean Action Plan (US Commission on Ocean Policy 2004) required EPA to develop
the tools and knowledge necessary to protect coral reefs from land-based pollution using coral reef
biological criteria. A comprehensive guide (Bradley et al. 2010) describes the process for using the
CWA and biological criteria to enhance coral reef protection efforts.

1.6 Why a Coral Reef Ecosystem Conceptual  Model is Needed
Coral reef condition typically degrades as human disturbance increases. Human disturbances
threatening coral reefs include polluted runoff from agriculture and land-use practices, over-fishing,
ship groundings, coastal development, sewage discharge and climate change. Natural stressors such
as tropical storms can also adversely impact coral reefs. Both natural and anthropogenic stressors
can cause increases in coral bleaching and diseases. Reefs in the US Caribbean have declined from
50% total coral cover to less than 10% in just 25 years (Wilkinson 2004).

The biological communities of the coral reef reflect overall ecological integrity (i.e., chemical,
physical and biological integrity), integrate effects of multiple stressors and provide a  measure of
aggregate impact (Barbour et al. 1999). Coastal resource managers and coral reef scientists routinely
conduct biological assessments to evaluate the condition of coral reefs. This approach integrates the
cumulative impacts of chemical, physical and biological stressors on aquatic life. However, while the
stated intent of these biological assessments is to support decision-making, they more commonly
document the decline of the coral reefs. A missing component in this approach is a scientifically
derived process for identifying  thresholds that can be coupled with management objectives and used
to evaluate alternative decision options. A conceptual model can help to organize information and
make sense of system components and their interactions.

1.7 The Framework: The Biological Condition Gradient (BCG)
Beginning in the late 1990s, EPA collaborated with aquatic scientists and managers across the United
States to develop and implement the Biological Condition Gradient (BCG) for freshwater streams
(Davies and Jackson 2006). The BCG is a conceptual model that describes how biological attributes
of aquatic ecosystems (i.e., biological condition) might change along a gradient of increasing
anthropogenic stress (e.g., physical, chemical and biological impacts). The BCG was designed to
provide a means to map different indicators on a common scale of biological condition to facilitate
comparisons between programs and across jurisdictional boundaries in context of the CWA.

Since then, many states have used the BCG  to support water quality management, and several states
have used the BCG to more precisely define freshwater stream designated aquatic life uses, identify
impairment thresholds,  monitor status and  trends and track progress in restoration and protection
(EPA 2011). Additionally, stream BCGs have been developed at the regional and local government
scale throughout the US.

Since 2008 EPA has been collaborating with estuarine scientists and managers to adapt the stream
BCG framework to more complex estuarine waterbodies (EPA in review). Estuarine BCG pilot work
has focused on National Estuary Program (NEP) sites: Narragansett Bay (Rl), Casco Bay (ME), Mobile
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Bay (AL) and Tampa Bay (FL). NEPs play an important role as conveners of technical, management
and public interests. Their ability to create connections among these constituencies makes them
a valuable platform to work out the complexities of an estuarine BCG at different scales.

A BCG calibrated with field data can help states more  precisely define biological expectations for
their designated aquatic life uses, interpret current condition relative to CWA objectives and goals,
track biological community responses to management actions and communicate environmental
outcomes to the public. The model can serve as a template for organizing field data (biological,
chemical, physical, landscape) at an eco-regional, basin, watershed or waterbody scale. It provides
a framework for understanding current conditions relative to natural, undisturbed conditions.

In practice, the BCG is used to first identify the critical attributes of an aquatic community and then to
describe how each attribute changes in response to stress. Coral reef managers can use the BCG to
interpret biological condition along a standardized gradient, regardless of assessment method, and
apply that information to different programs.

The BCG model  provides a framework to help water quality managers do the following:

    •  Decide what environmental conditions are desired (goal-setting)—The BCG can provide a
      framework for organizing data and information and for setting achievable goals for
      waterbodies relative to natural conditions (e.g., condition comparable or close to undisturbed
      or minimally disturbed condition).
    •  Interpret the environmental conditions that exist (monitoring and assessment)—Practitioners
      can get a  more accurate picture of current waterbody conditions.
    •  Plan for how to achieve the desired conditions and measure effectiveness of restoration —
      The BCG framework offers water program managers a way to help evaluate the effects of
      stressors  on a waterbody, select management measures by which to alleviate those stresses
      and measure the effectiveness of management actions (EPA 2011: Case Example 3.16).
    •  Communicate with stakeholders—When biological and stress information is presented in this
      framework, it is easier for the public to understand the status of the aquatic resources relative
      to what high-quality places exist and what might have been lost.

1.7.1 How is the BCG Constructed?
The BCG has been divided into six levels of biological conditions along the stressor-response curve,
ranging from observable biological conditions found at no or very low levels of stress (level 1) to
those found at high levels of stress (level 6) (Figure 1-1).

The BCG was developed to serve as a scientific framework to synthesize expert knowledge with
empirical observations and develop testable  hypotheses on the response of aquatic biota to
increasing levels of stress.
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It is intended to support more consistent interpretations of the response of aquatic biota to stressors
and to clearly communicate this information to the public. It is being evaluated and piloted in several
regions and states.

Davies and Jackson (2006) provides a description of how 10 attributes of aquatic ecosystems change
in response to increasing levels of stressors along the gradient, from level 1 to 6. The attributes
include several aspects of community structure, organism condition, ecosystem function, spatial and
temporal extent and connectivity (Table 1-3).
               The Biological Condition Gradient:
  Biological Response to Increasing Levels of Stress
  Levels of Biological Condition
  Level 1. Natural structural, functional,
  and taxonomic integrity is preserved.

  Level 2. Structure & function similar
  to natural community with some
  additional taxa & biomass; ecosystem
  level functions are fully maintained.

  Level 3. Evident changes in structure
  due to loss of some rare native taxa;
  shifts in relative abundance; ecosystem
  level functions fully maintained.

  Level 4. Moderate changes in structure
  due to replacement of some sensitive
  ubiquitous taxa by more tolerant
  taxa; ecosystem functions largely
  maintained.

  Level 5. Sensitive taxa markedly
  diminished; conspicuously unbalanced
  distribution of major taxonomic groups;
  ecosystem function shows reduced
  complexity & redundancy.

  Level 6. Extreme changes in structure
  and ecosystem function; wholesale
  changes in taxonomic composition;
  extreme alterations from normal
  densities.
                              Watershed, habitat, flow regime
                              and water chemistry as naturally
                                      occurs.
Chemistry, habitat, and/or flow
 regime severely altered from
    natural conditions.
Figure 1-1. The Biological Condition Gradient (BCG) (modified from Davies and Jackson 2006).
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Table 1-3. Biological and other ecological attributes used to characterize the freshwater streams
Biological Condition Gradient (BCG) (Modified from Davies and Jackson 2006).
Attribute
Description
I. Historically documented,
  sensitive, long-lived, or
  regionally endemic taxa
Taxa known to have been supported according to historical, museum or
archeological records, or taxa with restricted distribution (occurring only in a
locale as opposed to a region), often due to unique life history requirements
(e.g., Sturgeon, American Eel, Pupfish, Unionid mussel species).
II. Highly sensitive
  (typically uncommon)
  taxa
Taxa that are highly sensitive to pollution or anthropogenic disturbance. Tend to
occur in low numbers, and many taxa are specialists for habitats and food type.
These are the first to disappear with disturbance or pollution (e.g., most
stoneflies, Brook Trout [in the east], Brook Lamprey).
 I. Intermediate sensitive
   and common taxa
Common taxa that are ubiquitous and abundant in relatively undisturbed
conditions but are sensitive to anthropogenic disturbance/pollution. They have
a broader range of tolerance than Attribute II taxa and can be found at reduced
density and richness in moderately disturbed stations (e.g., many mayflies,
many Darter fish species).
IV. Taxa of intermediate
   tolerance
Ubiquitous and common taxa that can be found under almost any conditions,
from undisturbed to highly stressed stations. They are broadly tolerant but
often decline under extreme conditions (e.g., filter-feeding caddisflies, many
midges, many Minnow species).
V. Highly tolerant taxa
Taxa that typically are uncommon and of low abundance in undisturbed
conditions but that increase in abundance in disturbed stations. Opportunistic
species able to exploit resources in disturbed stations. These are the last
survivors (e.g., tubificid worms, Black Bullhead).
VI. Non-native or
   intentionally
   introduced species
Any species not native to the ecosystem (e.g., Asiatic clam, zebra mussel, Carp,
European Brown Trout). Additionally, there are many fish native to one part of
North America that have been introduced elsewhere.
VII. Organism condition
Anomalies of the organisms; indicators of individual health
(e.g., deformities, lesions, tumors).
VIM. Ecosystem function
Processes performed by ecosystems, including primary and secondary
production; respiration; nutrient cycling; decomposition; their
proportion/dominance; and what components of the system carry the dominant
functions, for example, shift of lakes and estuaries to phytoplankton production
and microbial decomposition under disturbance and eutrophication.
IX. Spatial and temporal
   extent of detrimental
   effects
The spatial and temporal extent of cumulative adverse effects of stressors; for
example, groundwater pumping in Kansas resulting in change offish
composition from fluvial dependent to sunfish.
X. Ecosystem connectivity
Access or linkage (in space/time) to materials, locations and conditions required
for maintenance of interacting populations of aquatic life; the opposite of
fragmentation. For example, levees restrict connections between flowing water
and floodplain nutrient sinks (disrupt function); dams impede fish migration,
spawning.
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Each attribute provides some information about the biological condition of a waterbody. Combined
into a conceptual model like the BCG, the attributes can offer a more complete understanding of
current waterbody conditions and also provide a  basis for comparison with naturally expected
waterbody conditions. All states and tribes that have applied a BCG used the first five attributes that
describe the composition and structure of the biotic community on the basis of the tolerance of
species to stressors. Where available, states and tribes also included information on the presence
or absence of native and non-native species for fish and amphibians, as well as observations
of overall health and condition (e.g., size, weight, abnormalities, tumors and diseases).

The last three BCG  attributes (ecosystem function, spatial and temporal extent of detrimental effects
and ecosystem connectivity) can provide valuable information when evaluating the potential for a
waterbody to be protected or restored. Several of EPA's NEPs, in conjunction with EPA ORD, are
exploring application of those attributes at a whole-estuary scale (e.g., distribution and connectivity
of critical aquatic habitats and associated biota).

Additionally, individual attributes might uniquely respond to a specific stressor or group of
associated stressors (biological response signatures) (Yoderand Rankin 1995 a, b; Yoderand
Deshon 2003). That information could contribute to the causal analysis of biological impairment,
Stressor Identification  (SI) and Causal Analysis/Diagnosis Decision Information System (CADDIS)
(http://www.epa.gov/caddis/).

Currently, applications of the BCG that include development of a BCG-index (BCG-I) and
incorporation of the BCG in a state's water quality management have been used only on freshwater
streams. More recently,  ongoing pilot efforts at several NEPs are extending the BCG concept to
assessment and management of estuaries. Efforts to develop an estuarine conceptual model have
focused on five attributes (structure, condition, function, connectivity and non-native species
[Cicchetti 2010]) at scales ranging from the  whole estuary to the single habitat, or biotope (e.g.,
seagrass beds, salt  marshes and clam flats) (Table 1-4). This multi-scale approach is intended to
improve restoration and management efforts. At larger scales, managers can prioritize and develop
programs to restore the  historic balance of critical habitats (biotopes) relative to an undisturbed
historic benchmark, while also targeting restoration of all  living habitats, to the maximum extent
possible. The single habitat scale is assessed using biological assessments, which enjoy an established
history within management approaches (Cicchetti and Greening 2011; EPA 2011).

Extending the BCG  conceptual model to new waterbodies (coastal  waters) and new assemblages
(coral reef communities) is a multistep process. A successful process assembles a workgroup of
experts on the habitats and assemblages and elicits from these experts: descriptions of the native
aquatic assemblages under natural conditions, identifications of the predominant regional stressors
and descriptions of degradation levels corresponding to the BCG. Descriptions should include the
theoretical foundation and observed assemblage responses to stressors. In addition to expert
opinion, the process makes use of empirical monitoring data. During a workshop, experts familiar
with local conditions use the data to define the ecological attributes and set narrative statements.
The experts determine narrative decision rules for assigning stations to a BCG level on the basis of
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the biological information collected at the stations. Further development of quantitative decision
rules and a quantitative BCG is more involved and requires a greater time commitment from the
expert panel to participate in iterative calibration steps and review of more extensive monitoring
data.

Table 1-4. Ecological attributes used to characterize the estuarine Biological Condition Gradient
(BCG) (EPA in review).
Attributes
Potential Metrics and Description
Structure and
Compositional
Complexity
Community or habitat structure and complexity. May also recognize loss of habitats or
species due to human activities.

Examples include macroinvertebrate or fish indices, phytoplankton or zooplankton
community measures, epifaunal measures, biotope mosaics, presence/quality of
sensitive or susceptible taxa or biotopes, wetland vegetative indices, etc.
Condition
Measures condition of the waterbody, habitat or species. Also includes measures of
resiliency.

Examples include harmful algal blooms, disease outbreaks (locally or system-wide),
measure of habitat or biotope health, such as seagrass condition or wetland condition,
fish pathology or shellfish bed condition.
Function
Measures of energy flow, trophic linkages and material cycling. They may include proxy
or snapshot metrics that correlate to functional measures.

Examples include photosynthesis/respiration ratios, benthic: pelagic production rates,
chlorophyll a concentrations and macroalgal biomass.
Connectivity
Metrics of exchange or migrations of biota between adjacent waterbodies or habitats.
Important measures within the area being studied may be strongly affected by factors
adjacent to or larger than the immediate study area.

Proxies may need to be used as metrics. These may  include linkages, fragmentation or
hydrological measures.
Non-native
Taxa
Metrics of non-native species. May include measures of the impact of invasive species
and non-natives.

Examples include estimated numbers of species or individuals, biomass measures of
natives and non-natives or replacement of native species.
This report communicates the first results to apply the BCG conceptual model to the assessment of
the condition of coral reefs. The first stage reported here is a proof-of-concept to introduce the
conceptual model to coral reef experts and elicit a preliminary set of narrative decision rules for
assigning coral reef stations to levels of the BCG. If the conceptual model passes muster among the
experts, it will allow identification of the steps needed to develop and implement more
comprehensive quantitative decision models.
1-16  Workshop on Biological Integrity of Coral Reefs

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Chapter 2. Approach
The coral reef BCG will be developed through a series of facilitated expert workshops. In the
workshops, the experts assess the condition of coral reef sites based on biological data collected at
the sites (species composition, abundance,  health) and assign each site to a condition category
(level) of the BCG. The experts' reasoning for making assignments are developed into a set of
decision rules, at first qualitative, but through iteration, increasingly quantitative. The expert-derived
rules are translated to a quantitative decision algorithm, in this case using mathematical set theory
(e.g., Droesen 1996). The decision algorithm allows independent assessments with results
comparable to those of the expert panel. Furthermore, the decision rules are documented so that
modifications can be made as information and  needs change.

The participants for the initial workshop were invited based on their scientific knowledge of the coral
reefs and reef organisms of Puerto Rico. As  a first step, participants were asked to evaluate and rank
coral reef condition from photos, videos and data collected during EPA's 2010 and 2011 coral reef
assessment surveys  in shallow waters (<12 m deep) of southwestern Puerto Rico. The biological
assemblages considered were stony corals,  fishes, sponges, gorgonians and benthic
macroinvertebrates. Rugosity, a reef-scale indicator of reef complexity, was determined using a
chain-transect method that compares the six-foot length of a chain draped along the top of corals
and along the bottom of the reef to the length of a taut line across the same linear distance.
Participants were asked to share videos and pictures of reefs from the present or past that they
believed exhibited full biological integrity.

A unique aspect of this workshop was that participants were reacting to the visual imagery of
the reefs and evaluating different levels of coral reef condition. Participants moved from a visual,
simple approach to more complex data-driven analysis.  The workshop was designed to encourage
brainstorming, facilitate discussion and not  get mired in EPA terminology or definitions at the
beginning of the workshop. Participants examined the visual media, rated the condition of various
coral reefs and provided rationale for their ratings. Descriptions of good and bad characteristics
relative  to ecological condition were  captured by facilitated discussions. A preliminary list was
generated describing attributes that would  characterize a coral reef with high (minimally disturbed
or reference) or good condition. A minimally disturbed condition provides a fixed point in time and
can help us to avoid  problems associated with shifting baselines (Pauly 1995; Stoddard et al. 2006). A
firm concept of minimally disturbed anchors ecological condition as a reference and helps us deal
with changes (e.g., climate change), which broadly affect conditions that occur after the anchored
point. Further, a clear picture of minimally disturbed provides a basis for effective public
communication of changes over time and can provide a reference point for certain indices of
ecological condition.

The workshop was designed to last three days; however Day 3 was cancelled because of Tropical
Storm Isaac. Certain planned activities from Day 3 were shifted into Day 2, and the remainder of
workshop information was communicated during webinars.
Chapter 2. Approach
2-1

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2.1 Video and Photo Evaluations
On the first day, panelists were asked to view and rate the coral reef condition of 12 EPA stations on
the south shore of Puerto Rico (Table 2-1).

      Table 2-1. Shallow inshore linear reefs used for BCG workshop stations that
      correspond to US EPA stations sampled along the southern coast of Puerto Rico.
Station
1
2
3
4
5
6
7
8
9
10
11
12
Year
2010
2011
2011
2011
2011
2010
2010
2010
2010
2011
2011
2011
EPA station
PR_2010_125
PR_2011_15
PR_2011_113
PR_2011_03
PR_2011_19
PR_2010_14
PR_2010_16
PR_2010_108
PR_2010_109
PR_2011_01
PR_2011_46
PR_2011_25
Latitude
17.92486
17.98198
17.95942
17.94420
17.94180
17.93875
17.93922
17.94085
17.95373
17.96380
17.93418
17.93670
Longitude
-66.20363
-66.77228
-67.03902
-66.91638
-66.88060
-67.10927
-67.06197
-67.07708
-67.05012
-67.04980
-67.10108
-66.88660
Depth (ft.)
20
23
21
21
12
27
24
12
16
11
17
17
Stations were limited to shallow (<12 m), near-shore (less than 3 nautical miles from shore) linear
reefs as designated by NOAA benthic maps (Kendall et al. 2001), see Figure 2-1.
        Figure 2-1. Map with locations of the 12 EPA stations along the
        southern coast of Puerto Rico.
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Workshop on Biological Integrity of Coral Reefs

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Videos of eight stations were examined in the morning and four stations in the afternoon. Videos
were displayed on four computers looping two stations per video in the morning and one station per
video in the afternoon. Each station presented video footage from both panoramic and linear
transect views, which began with 15 seconds showing the station number and the type of footage, to
allow reviewers time to prepare for each video. A 60-second period between each station allowed
panelists time to complete their evaluations before the next station video began. In addition to the
video clips (ranging from 30 seconds to 3 minutes long), eight still photographs for each station
(Appendix G) were provided in a notebook to supplement the videos and in particular, to capture
aspects of the station not represented in the videos (e.g., fish).

The panelists were instructed to draw upon their overall personal experience and expertise to rate
the reef condition for each station as either good, fair or poor based on what they viewed in videos
and photos. Workshop binders organized by station included a photo diary of key representative
photos, two ballots to rate the stations for each session (Appendices D and E) and note sheets
(Appendix F) to document the traits or characteristics that panelists used to support their ratings.
The panelists were asked to consider all aspects of the reef and specifically instructed to consider the
characteristics of the condition of corals, sponges, gorgonians, fish, algae, reef rugosity and
topographical heterogeneity. The facilitators suggested that panelists not compare ratings with each
other, but panelists were free to discuss and view videos as a group. The panelists were not asked to
rate any specific number of stations as good, fair or poor, but had free rein as they circulated around
and viewed the video loops at their own pace. The facilitators were available  if panelists had
questions.

The panelists asked about shifting baseline conditions, and they were encouraged to draw upon their
personal experience. Panelists also asked if each assemblage should be rated separately. Facilitators
responded that  it was all right to consider and document each assemblage, but they must finally
select one single rating for each station. When all stations were evaluated, panelists recorded their
individual ratings on the ballots and returned them to the facilitators. Note sheets were not
collected—they were for each panelist to reference during subsequent discussions.

After ballots were collected from the panelists, the facilitators tabulated all the scores by ranking the
stations in order from best condition to worst using a weighted ranking system (Table 2-2). Each
good vote was given a value of 10 points, each fair vote 5 points and each poor vote 1 point.
Table 2-3 shows the ranking given by each  expert after visually evaluating videos and photographs
for 12 EPA stations.

The panelists provided feedback on how to improve the process used to evaluate the stations. Many
found it challenging to assess reef condition based on the video quality, which was raw footage from
inexpensive video-enabled digital cameras. Still photos provided the best way to document fish
populations, because many fishes were disturbed during the assessments that occurred before the
video was taken. The fish surveyors were the first team to perform visual assessments, followed by
Chapter 2. Approach
2-3

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Table 2-2. Coral reef condition evaluated by the experts. Results were obtained from 20 coral reef
experts after viewing videos and photos of 12 stations, with the highest score bolded. Overall rank is
established by weighted ranking.
Station
No.
1
2
3
4
5
6
7
8
9
10
11
12
Table 2-3
stations.
between
No.
%
Good Good
1
0
13
0
0
0
4
0
1
5
2
6
. Rankings
5
0
65
0
0
0
20
0
5
25
10
30
given
Abbreviations: G
No.
Fair
9
0
7
2
10
6
16
15
12
14
17
12
%
Fair
45
0
35
10
50
30
80
75
60
70
85
60
by experts after
rated
No.
Poor
10
20
0
18
10
14
0
5
7
1
1
2
%
Poor
50
100
0
90
50
70
0
25
35
5
5
10
Majority
Rating
Poor/Fair
Poor
Good
Poor
Fair/Poor
Poor
Fair
Fair
Fair
Fair
Fair
Fair
visually evaluating videos
good; F rated fair;
P rated
Weighted Overall
Score
65
20
165
28
60
44
120
80
77
121
106
122
Rank
8
12
1
11
9
10
4
6
7
3
5
2
and photographs for
poor. Some ratings
were intermc
two classes.
                                          Station Number
Expert 1
Appeldoorn P
Ballantine F
Bauza F
Canals F
Cuevas F
Diaz F/G
Fisher P
Hutchins P
McField P/F
Miller F
Pagan F/P
Ramos F
Roberson P
Ruiz F
Sabat P
Smith P
Szmant P
Todd P
Vicente P
Yoshioka G/F
2
P
P
P
P
P
P
P
P
P-
P
P-
P
P
P
P
P
P-
P
P
P
3
G
G
G
F/G
G
F/G
G
F
F
G
G/F
G
F/P
G
G
F
G
G
F
G
4
P
F
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
F
5
F
F/P
F
P/F
F
F/P
P
P
F
P/F
P
P
P/F
F
P/F
P/F
F
P
F
F/G
6
P
P
P
P
P
F/P
P
P
P
P
F
P
F/P
F
P/F
P/F
P
P
F
F
7
F
F
G
F
F
F/G
G
F
F
F
F
F
F
G
F
F
F
G
F
F/G
8
F
F
F
F
F
F/P
F
P
P/F
P/F
F
P
P
F
F
F
F
F
F
F
9
F
G
F
P
P/F
F/P
F
P
P+
F
P
F
F/P
F
P
P
F/P
F
F
F/P
10
F
G
F
F
F
G
G
F
F+
G/F
F
P
F/P
G
F/G
F
F
F
F
F/G
11
F
G
F
F
F
F/P
F
F
F
F
F
F
P/F
G
F
F
F/G
F
F
F
12
F
G
F
F/G
F
F
G
F
P+
G
F
F
F
F
F
F
G
G
F
G/F
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Workshop on Biological Integrity of Coral Reefs

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the surveyors assessing other assemblages, including those photographing and video recording the
reef. The photographers began potentially after many fishes had been scared away. The panelists
also requested more details on the stations they were evaluating. Panelists felt they needed to know
the location of the reef, what specific reef habitat they were viewing, the depth, the wave exposure
and other features. They also wanted to know what stressors the station may have experienced.
Recommendations for the future included upgrading video camera quality, standardizing the
videography approach and providing more information to get a broader perspective of each station
and its surrounding reef.

A facilitated discussion followed on the attributes that the panelists had identified to justify their
ratings. The stations rated best and worst were considered first, with each panelist's comments
captured on flip charts. Panelists were encouraged to edit  posted pages of their comments if they
felt their thoughts were not accurately captured. All participants were given the opportunity to
submit comments on index cards if they wished to provide additional comments privately or
anonymously. A summary of the characteristics considered by the panelists in rating the stations is
provided in Section 2.2 for the best, worst and several fair stations.

2.2 Summary of Ratings
All of the photos given to the experts are found in Appendix G, ordered by station number.

2.2.1 Best Station, Ranked #1
The experts rated the condition of Station 3 as the best of the 12. It was rated good by 65% of the
experts and fair by 35%. No expert rated it as poor. The experts were asked what characteristics or
attributes were present that caused them to rate it as the best station. Their responses follow:

    •  Abundance of Montastraea annularis species-complex was high, with low partial mortality of
      tissue and large colony sizes indicative of older, mature coral  colonies.
    •  Reefs showed high structural complexity, surface heterogeneity and high rugosity or presence
      of three-dimensional structures, allowing better reef development than would a flat
      topography.
    •  Stony coral biodiversity was moderate and included Colpophyllia natans, Siderastrea siderea
      and Porites astreoides, as expected on near-shore linear reefs in southwestern Puerto Rico.
    •  The water column showed high  clarity with no visible sediment; experts also noted a lack of
      siltation or films covering the substrate.
    •  Coralline algae were more abundant than brown algae,  and Dictyota was rare or absent.
    •  Gorgonian coverage was high, with most sea fans intact and uninjured. Diadema was present.
      Stony coral colonies had no or few  boring clionid sponges.
    •  Damselfish were seen and the presence of additional fish species contributed to a good rating.
Chapter 2. Approach
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The experts, who rated the station as fair, expressed concern about the uncertainty in identifying fish
species because the visual media were not adequate to consider fish size distributions or trophic
status. A few grazing fish species were seen, but not enough to alleviate concerns of low grazing
potential. Another expert cited the presence of coral disease. Finally, sponge abundance and
diversity were low, with an absence of arborescent, vase and barrel morphologies, which are
dominant in high quality habitat.

   •  The experts were also asked what attributes were absent that caused them to not rate the
      station as excellent. Their responses follow:
   •  The station had lower than expected diversity of stony corals, fishes and sponges, with little
      evidence of any recruitment.
   •  Very few anemones and invertebrates were observed, again indicating low species diversity.
   •  One expert stated that sponges, because they are efficient filter feeders, might be one of the
      assemblages most sensitive to chemicals in the water column and could act as an indicator
      species.

2.2.2 Worst Station, Ranked #12
All the experts agreed that Station 2 was in the worst  condition, and rated it poor. This station was
characterized by:

   •  High sedimentation and turbidity in the water column, which appeared as large patches of
      flocculent material creating low visibility, which the experts judged to represent low water
      quality.
   •  The reef colors were drab brown or green.
   •  Thick goopy sediment (probably of terrigenous  origin) covered most of the bottom and
      organisms living on the bottom. Exposed hard substrate was absent, with no clear surfaces for
      attachment or  recruitment.
   •  Algal cover was high, with lots of Dictyota and cyanobacteria as evidenced by a slimy
      appearance with a "skuzzy fuzzy" texture.
   •  Abundance of coralline algae was low.
   •  The absence of reef relief was coupled with low rugosity and no or very few small and live
      coral colonies.
   •  No fish or gorgonians were observed, although a few Diadema were noted.
   •  Sponge morphologies were ropy or encrusting, indicative of poor habitat and water quality.
   •  Heterotrophic sponges dominated, with a high  abundance of filter feeders and no apparent
      autotrophic sponges. This is a characteristic typical of highly silted areas.
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Workshop on Biological Integrity of Coral Reefs

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2.2.3 Stations Rated Fair
Station 8 ranked #6. This station was ranked as the most centric station among those with a fair
rating. 75% of the experts rated it fair while 25% rated it poor. This station had the highest coverage
of Acropora palmata in all stations viewed, although overall coral cover was low, with lots of coral
rubble. A. palmata colonies varied greatly in size, condition and distribution and were present in
about 25% of the transect area. Some very mature and large colonies were present in varying
condition as evidenced by the amount of healthy coral tissue. Many of the A. palmata colonies
lacked significant tissue and showed characteristics ranging from signs of tissue recovery, partial
tissue mortality from white-band disease, lesions and white denuded tips,  perhaps from fish
predation. Some standing colonies were completely dead. The coral rubble on the bottom was
composed of many broken and dead pieces of A. palmata skeletons, but finer sediments were
absent. Several experts commented that the clean substrate and unconsolidated rubble showed
significant and recent hurricane damage. Although some reef was dead, it  showed signs of recovery
and resiliency with the persistence of corals.

The clean substrate provided suitable areas available for settlement and recruitment of corals and
other sessile invertebrates. Some coralline algae were present but overall algal diversity was low,
with some fleshy algae. Much of the substrate appeared as though it had been highly grazed by
Diadema antillarum. Palythoa, often considered an emerging opportunistic species, was prevalent
throughout the transect colonizing dead coral skeletons. Several species of fish swam in large schools
representing a decent diversity, including evidence of herbivores. The primary sources of rugosity
were the A. palmata colonies; most other coral  colonies showed relatively low relief. Few
invertebrates other than those already mentioned were observed, with the exception of some small
sea fans and low relief gorgonians.

Station 5 ranked #9. Half of the experts rated it fair and the other half rated it poor. This station
shared many attributes with Station 8, but was judged to be in poorer condition because of higher
sediment and turbidity, together with lower coral cover and diversity. The  transect video showed
substantial A. palmata coverage, but the colonies appeared to be in poorer condition than those
seen in Station 8. One expert described the station as a "beat up Apal zone" (A. palmata) with large
rubble between colonies. Thicker and larger algal turf patches and more sponges were present in
comparison to Station  8. Parrotfish biting scars and scrapes were observed. However, it was noted
that sedimentation, turbidity and water quality can vary with year, season  and time of day,  so the
apparent condition could be extremely variable and dependent on when the video was taken.

Station 10 ranked #3. This station was rated as good by 25% of experts, fair by 70% of experts and
poor by 5% of experts. Many of the features seen in the previous fair descriptions were also present
here. A novel observation was the presence of the boring sea urchin Echinometra, which bioerodes
coral skeletons; the herbivorous urchin Diadema is usually considered an indicator of better
condition.
Chapter 2. Approach
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2.2.4 Station Rated Poor
Station 6 ranked #10. This station was rated fair by 30% of experts and poor by 70% of experts.
There was evidence of significant bioerosion on the reef surfaces,  perhaps due to boring clionids and
the encrusting sponge Chondrilla nucula. One expert asked if this was a hard bottom station (not a
coral reef). Despite the poor condition of Station 6, all experts agreed that Station 2 was in the
poorest condition.

2.3 Summary of Attributes
Attributes developed by the experts were assembled into a list. In  a facilitated discussion, the
experts reached consensus about which direction (increase or decrease) the attribute would go at a
station with improving condition, and what types of measurements or sub-attributes would be
important. This information is summarized in Table 2-4.

Table 2-4. Summary of attributes and their relationships for assessing coral reef condition from
station evaluations.
                                  Attributes of good stations
Direction with
improving condition
increase
increase
increase
increase
increase
increase
decrease
increase
decrease
decrease
decrease
increase
increase
increase
increase
increase
decrease
increase
Attribute
3D structure
stony coral abundance
stony coral condition
stony coral diversity
stony coral population
structure
stony coral recruitment
dominance of weedy,
tolerant species
coralline algae
zoanthids
exotic species
filter feeders
fish abundance
balance in fish popula-
tion size and structure
fish biomass
balance in fish trophic
structure
fish diversity
fleshy algae
gorgonian abundance
Sub-attribute/measurements
rugosity, cover
Montastraea annularis complex, Acropora palmata,
Acropora cervicornis, Diploria strigosa, large stony corals
% live tissue, absence of disease
high number of stony coral species
large colonies

Colpophyllia natans, Siderastrea siderea, Porites
astreoides

Palythoa species
exotic fish, corals
heterotrophic sponges







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Workshop on Biological Integrity of Coral Reefs

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 Table 2.4 (continued)
Attributes of good stations
Direction with
improving condition
increase
increase
increase
increase
decrease
increase
increase
increase
decrease
Attribute
gorgonian condition
gorgonian diversity
other invertebrates
sponge abundance
sponge abundance
sponge diversity
substrate condition
water clarity
corallivores/bioeroders
Sub-attribute/measurements
% live tissue, absence of disease and predators (Cyphoma
gibbosum)

Diadema antillarum, conch, lobsters, crabs, anemones
autotrophic sponges
heterotrophic sponges

clean, no fuzzy algae (cyanobacteria), open space
recruitment

bioeroders, Coralliophila (large size), clionids
2.4 Reference Condition for Biological Integrity
The panel agreed that all of the stations were impaired at some level. Many of the experts had been
working in Puerto Rico for 30-40 years, while others had recently received their PhDs. The group had
a rather lengthy discussion about the historical condition of Puerto Rico's coral reefs in an attempt to
answer: What did the reefs look like before humans came along to stress them?

The term "reference condition" is used by BCG to define biological condition in the absence of
human disturbance (Stoddard et al. 2006). The concept of reference condition arose from the
objective of the Clean Water Act Section 101: "to restore and maintain the chemical, physical and
biological integrity of the nation's waters". Biological integrity is defined as "the community of
organisms having a species composition, diversity and functional organization comparable to those
of natural habitats within a region" (Karr 1991).

Unfortunately, human activities have significantly affected coral reefs. Puerto Rico's coral reefs were
severely degraded long before ecologists began to study them (Jackson 1997). According to Jackson
et al. 2001, ecological extinction caused by overfishing preceded all other pervasive human
disturbance to coastal ecosystems. Overfishing reduced species populations such as marine reptiles
(green turtle, hawksbill turtle [1700s]), mammals (manatee and extinct Caribbean monk seal
[1800s]), conch [1980s], fishes (Nassau and goliath groupers [1950s] and reef fishes [1970s]). By the
time scientific studies began in the 1950s, herbivores and predators were reduced to very small
fishes and sea urchins (Jackson 1997).

So, how can one estimate reference condition when no living human has ever seen a Puerto Rican
reef in natural condition? One approach is the reference station approach, where scientists use reefs
that are nearly unaffected by anthropogenic disturbance and the related stressors/exposures, or
reefs whose present-day good condition  is found in conjunction with the best available physical,
chemical and biological habitat conditions, as surrogates for natural reefs. However, these
Chapter 2. Approach
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approaches may fail to correctly identify the baseline population sizes, instead representing a shifted
baseline as reference condition (Pauly 1995).

Another approach is to apply ecological theory and empirical models to extrapolate reference
condition. A relatively recent method is the use of historical ecology, where scientists piece together
an understanding of what coral reef ecosystems used to be. The challenge is to use these approaches
to adjust our expectations of what a healthy coral reef baseline looks like and use that as reference
condition.

2.4.1 Experts' Examples of Reference Condition for Biological Integrity
Workshop panelists were urged to share examples of present or past reefs that they believed to
exhibit full biological integrity. Dr. Szmant reported that she had participated in a discussion about
shifting baselines with other experienced coral reef scientists. This led to a report (Sale and Szmant
2012) that summarized these scientists' reminiscences on historical reef condition over the last
40 years.

Dr. Szmant also showed photographs of recent changes from 2009 to 2012 in Montastraea
populations on a coral reef in Curacao (Watamula) that were caused by a 2010 bleaching event
(Figure 2-2). An estimated 50% of previously large healthy coral colonies on Watamula showed
partial or complete mortality in less than one year. She also showed photographs of extensive
Acropora cervicornis beds on Smith Bank (on the south coast of Roatan)  near the ones on Cordelia
Banks that Dr. McField surveyed (see below). Dr. Szmant has slides of The Buoy and other reef areas
in Puerto Rico and the Caribbean from the  1970s that she was willing to  share.
Figure 2-2. Recent changes from 2009 to 2012 in Montastraea populations on a coral reef in
Curacao (Watamula) that were caused by a 2010 bleaching event (photos: Dr. Alina Szmant).
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Workshop on Biological Integrity of Coral Reefs

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Dr. McField brought photos from Cordelia Banks on Roatan Island, Honduras (Figures 2-3, 2-4 and
2-5). Cordelia Banks is located near the airport and main port of Roatan, but strong onshore currents
likely keep land-based sources of pollution away most of the time. Cordelia Banks is a good
candidate for a reference site because it has:

   •  52 acres of healthy reef with the highest live coral cover in the Caribbean (up to 73%
      measured in transects and averaging just over 50%). Acropora cervicornis, which is one of the
      most important reef species for structural reef growth and fish nursery habitat, dominates this
      reef. Unfortunately, this species and Acropora palmata have been reduced by about 98% over
      the last three decades throughout the Caribbean by disease and bleaching.
   •  The presence of two important species of sharks - the nurse shark (Ginglymostoma
      cirratum) and the Caribbean reef shark (Carcharhinus perezii).
   •  Spawning aggregation sites for groupers and snappers.
 Figure 2-3. Two experts suggested Cordelia Banks near Roatan, Honduras, as an example of a
 reference site for excellent coral condition. This area contains 52 acres of threatened coral
 species, high fish abundance and other characteristics important in sustaining healthy reefs
 (photo: Dr. Melanie McField).
Chapter 2. Approach
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Figure 2-4. Monitoring of massive Acropora cervicornis banks at Cordelia Banks located off a
major airport in Roatan, Honduras (photo: Dr. Melanie McField).
Figure 2-5. Panoramic view of Acropora cervicornis banks at Cordelia Banks, Roatan, Honduras
(photo: Dr. Melanie McField).

Dr. McField also brought copies of the 2012 Report Card for the Mesoamerican Reef. Dr. McField's
program, Healthy Reefs for Healthy People Initiative, is an international, multi-institutional effort
that tracks the health of the Mesoamerican Reef (MAR), the human choices that shape it and the
progress to ensure its long-term integrity. The Healthy Reefs for Healthy People Initiative seeks to
address two overarching questions:
2-12
Workshop
on
Biological
lnte§
;rity of Coral
Reefs

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   1.  What is a healthy reef and how can we improve our tracking of reef health
       through a shared vision and common indicators or yardsticks?
   2.  How can we best convey consistent, scientific information to policymakers,
       decision-makers and the public, such that the connections between reef health and
       human health result in effective conservation action at an unprecedented scale?
The Healthy Reefs for Healthy People Initiative has developed a quantifiable, interpretive framework
of measurable indicators and  criteria to better understand and assess reef health in the MAR region.
The Initiative produces report cards on the condition of the  MAR resources, using a five-point
grading system from very good to critical for key indicators:  fish abundance, fleshy macroalgal index,
Diadema abundance, herbivorous fish abundance, coral mortality, conch abundance, coral
recruitment and coral cover. The report card also describes the main threats to the ecosystem and
evaluates management actions. More information about the Initiative can be found at:
http://www.healthyreefs.org

Dr. Weil stated that the average rainfall in Puerto  Rico has been  increasing steadily since 2000,
coinciding with changes in land use. Consequently, rain events have a greater impact on the decline
in coral reef condition. He has a draft report on this topic that he could send to other attendees. Dr.
Weil also reports that in La Parguera, Puerto Rico, the average winter SST has remained elevated
over the last decade. He suggests that water visibility is decreasing,  and sedimentation is  increasing.
Yellow-band disease, which affects the Montastraea annularis species-complex, is now chronic all
year, whereas it used to be seasonal and limited in distribution. Bleaching events in the area are
followed by white plague infection, which leads to increased coral mortality with little or  no
recovery, and bare coral substrate is colonized by macroalgae.

Mr. Ruiz Torres passed around his recent book Beneath the  Waves,  published by the Sea Grant
Program at the University of Puerto Rico  (Figure 2-6). It contains nearly a hundred photos
documenting the marine environment
along the entire coast of Puerto Rico,
including algae, fish, crustaceans,
mollusks and corals. A description of the
location, the depth and the characteristics
of the organisms accompany each image.
The text is written in English and Spanish.

Dr. Appeldoorn commented that good
water flow  (medium to high constant
speed) is important for high quality reefs.
He stated that fish trophic structure is
impaired in Puerto Rico because of the
low number of apex predators.
                                          Figure 2-6.  Cover for the book, Beneath the Waves,
                                          by  Hector J. Ruiz Torres.
Bajo las olas
Beneath the Waves
             Puerto Rico
       Hector J. Ruiz Tories
Chapter 2. Approach
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Dr. Vicente said that he has over 500 one-hour videos documenting reefs around Puerto Rico and
USVI that he is willing to share with the group. He will send an index so experts can request the
videos of interest.

2.4.2 Summary Discussion
The experts remarked that gorgonians were present in the videos of the best sites but not in high
abundance. At fair condition sites, gorgonians were most abundant, but reduced abundance was
seen again at poor coral reef condition (bell-shaped curve). The experts agreed that there is a need
to understand the ecology of relationships between these assemblages to predict where we find
certain species and abundance of corals and gorgonians, and why they are distributed that way. For
example: Are corals replaced by gorgonians when corals die on reefs in lower or poor condition?

2.5 Attributes of a Very Good to Excellent Station
Based on the videos and photographs, the experts identified the attributes of a very good - to
excellent station, which would be comparable to BCG  Level 2: near natural (minimally disturbed).
A summary of the attributes is shown in Table 2-5.

The attributes are reorganized in Table 2-6, into a format that can  be more efficiently used during
future workshops to facilitate establishing numeric criteria ranges.

2.5.1 Three-dimensional Topographic Complexity
The experts thought that very good - excellent stations would have high rugosity or three-
dimensional  topographic complexity, including substantial reef built above the  bedrock. High
topographic  complexity is known to be an important attribute (Friedlander and Parrish 1998; Zawada
2011). Coral  reefs with high topographic complexity have high species diversity (Talbot 1965; Risk
1972), primary productivity (Barnes 1988) and biomass density (Luckhurst and Luckhurst  1978;
Carpenter et al. 1981). These reefs provide refuge from predation (Steele 1999; Idjadi and Edmunds
2006) and supplement larval settlement space (Idjadi and Edmunds 2006). Topographic complexity
also provides hydrodynamic effects, determining water flow around, over and through  the reef
(Munk and Sargent 1954; Monismith 2007; Hearn 2008; Nunes and Pawlak 2008) and enhancing
energy dissipation thereby,  nutrient uptake and mass-transfer rates (Shashar et al. 1996;  Hearn  et al.
2001).
 2-14
Workshop on Biological Integrity of Coral Reefs

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Table 2-5. Summary of descriptions of four condition categories (very good to poor) based on
expert assessments of individual stations. The descriptions of good to poor condition are comparisons to
a very good condition station based on panelists' identifications of aspects missing from expectations for very
good stations.
Condition level
Very Good
Excellent
(approximate
BCG Level 1-2)
Good
(approximate
BCG Level 3)
Attribute descriptions
Physical structure: High rugosity or 3D structure; substantial reef built above
bedrock; many irregular surfaces provide habitat for fish; very clear water; no
sediment, floes or films
Corals: High species diversity including rare; large old colonies (Montastraea) with
high tissue coverage; balanced population structure (old and middle-sized colonies,
recruits); Acropora thickets present
Gorgonians: Gorgonians present but subdominant to corals
Sponges: Large autotrophic and highly sensitive sponges abundant
Fish: Populations have balanced species abundances, sizes and trophic interactions
Large vertebrates: Large, long-lived species present and diverse (turtles, eels,
sharks)
Other invertebrates: Diadema, lobster, small crustaceans and polychaetes
abundant; some large sensitive anemone species present
Algae: Crustose coralline algae abundant; turf algae present but cropped and grazed
by Diadema and herbivorous fish; low abundance of fleshy algae
Condition: Low prevalence of disease and tumors; mostly live tissue on colonies
Physical structure: Moderate to high rugosity; moderate reef built above bedrock;
some irregular cover for fish habitat; water slightly turbid; low sediment, floes or
films on substrate
Corals: Moderate coral diversity; large old colonies (Montastraea) with some tissue
loss; varied population structure (usually old colonies, few middle aged and some
recruits); Acropora thickets may be present; rare species absent
Gorgonians: Gorgonians more abundant than Levels 1-2
Sponges: Autotrophic species present but highly sensitive species missing
Fish: Decline of large apex predators (e.g., groupers, snappers) noticeable; small
reef fishes more abundant
Large vertebrates: Large, long-lived species locally extirpated (turtles, eels)
Other invertebrates: Diadema, lobster, small crustaceans and polychaetes less
abundant than Levels 1-2; large sensitive anemone species absent
Algae: Crustose coralline algae present but fewer than Levels 1-2; turf algae present
and longer, more fleshy algae present than Levels 1-2
Condition: Disease and tumor presence slightly above background level; more
colonies have irregular tissue loss
Chapter 2. Approach
2-15

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Table 2-5 (continued)
Condition level
Fair
(approximate
BCG Level 4)
Poor
(approximate
BCG Level 6)
Attribute descriptions
Physical structure: Low rugosity; limited reef built above bedrock; erosion of reef
structure obvious; water turbid; more sediment accumulation, floes and films;
Acropora usually gone or present as rubble for recruitment substrate
Corals: Reduced coral diversity; emergence of tolerant species, few or no living large
old colonies (Montastraea); Acropora thickets gone, large remnants mostly dead
with long uncropped turf algae
Gorgonians: Gorgonians more abundant than Levels 1-3, replacing sensitive coral
and sponge species
Sponges: Mostly heterotrophic tolerant species and clionids
Fish: Absence of small reef fishes (mostly Damselfish remain)
Large vertebrates: Large, long-lived species locally extirpated (turtles, eels)
Other invertebrates: Diadema absent; Palythoa overgrowing corals; crustaceans,
polychaetes and sensitive anemones conspicuously absent
Algae: Some coralline algae present but no crustose algae; turf is uncropped,
covered in sediment; abundant fleshy algae (e.g., Dictyota) with high diversity
Condition: High evidence of diseased corals, sponges, gorgonians; evidence high of
mortality; usually less tissue than dead portions on colonies
Physical structure: Very low rugosity; no or little reef built above bedrock; no or low
relief for fish habitat; very turbid water; thick sediment film and thick floe covering
bottom; no substrate for recruits
Corals: Absence of colonies, those present are small; only highly tolerant species
with little or no live tissue
Gorgonians: Small and sparse colonies; mostly small sea fans; often diseased
Sponges: Heterotrophic sponges buried deep in sediment; highly tolerant species
Fish: No large fishes; only a few tolerant species remain; lack of multiple trophic
levels
Large vertebrates: Usually devoid of vertebrates other than fishes
Other invertebrates: Few or no reef invertebrates; high abundance of sediment
dwelling organisms such as polychaetes and holothurians
Algae: High cover of fleshy algae (Dictyota); complete absence of crustose coralline
algae
Condition: High incidence of disease and low or no tissue coverage on small colonies
of corals, sponges and gorgonians, if present
2-16
Workshop
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Table 2-6. Condition levels and associated attributes
Condition
level
Very
Good-
Excellent














Good



















Ol
(3
u
GQ
1-2














3



















Physical
structure
High rugosity
or 3D
structure;
substantial
reef built
above
bedrock;
many
irregular
surfaces
provide
habitat for
fish; very
clear water;
no sediment,
floes or films


Moderate to
high rugosity;
moderate
reef built
above
bedrock;
some
irregular
cover for fish
habitat;
water slightly
turbid; low
sediment,
floes or film
on substrate





10
re
3
High species
diversity
including rare;
large old
colonies
(Montastraea)
with high
tissue
coverage;
balanced
population
structure (old
and middle-
aged colonies,
recruits);
Acropora
thickets
present
Moderate
coral diversity;
large old
colonies
(Montastraea)
with some
tissue loss;
varied
population
structure
(usually old
colonies, few
middle-aged
and some
recruitment);
Acropora
thickets may
be present;
rare species
absent
Gorgonians
Gorgonians
present but
sub-dominant
to corals














Gorgonians
more
abundant
than in Levels
1-2















i/i
Ol
00
o
Q.
to
Large
autotrophic
and highly
sensitive
sponge
species
abundant











Autotrophic
species
present but
highly
sensitive
species
missing













_(/>
1Z
Populations
have balanced
species
abundance,
sizes and
trophic inter-
actions











Decline of
large apex
predators (e.g.,
groupers,
snappers, etc.)
noticeable;
small reef fish
more
abundant than
Levels 1-2










Vertebrates
Large,
long-lived
species
present
and diverse
(turtles,
eels,
sharks)










Large,
long-lived
species
locally
extirpated
(e.g.,
turtles,
eels)












Other
invertebrates
Diadema,
lobster, small
crustaceans
and
polychaetes
abundant-
some large
sensitive
anemone
species








Diadema,
lobster, small
crustaceans
and
polychaetes
less abundant
than Levels
1-2; large
sensitive
anemone
species
missing








Algae/plants
Crustose
coralline algae
abundant; turf
algae present
but cropped
and grazed by
Diadema and
herbivorous
fish; low
abundance
fleshy algae







Crustose
coralline algae
present but less
than Levels 1-2;
turf algae
present and
longer; more
fleshy algae
present











Condition
Low
prevalence
of disease
or tumors;
mostly live
tissue on
colonies











Disease and
tumor
prevalence
slightly
above
background
level; more
colonies
have
irregular
tissue loss









Chapter 2. Approach
2-17

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Table 2.6 (continued)

o
'i3
1 «
3 1
Fair



















Poor
















Ol
£
(3
U
GO
4



















6
















0)
re £
.a 5
£S
£ «
Low rugosity,
limited reef
built above
bedrock;
erosion of
reef
structure
obvious;
water turbid;
more
sediment
accumula-
tion, floes
and films;
Acropora
usually gone
or present as
rubble for
recruitment
substrate
Very low
rugosity, no
or low reef
built above
bedrock or
poor for fish
habitat; very
turbid water;
thick
sediment
film and high
floes
covering
bottom; no
substrate for
recruits

10
re
3
Reduced coral
diversity;
emergence of
tolerant
species, few or
no large old
colonies
(Montastraea)
mostly dead;
Acropora
thickets gone;
large remnants
mostly dead
with long
un cropped turf
algae




Absence of
colonies, those
present are
small, only
highly tolerant
species, little
or no tissue









i/i
c
_re
'E
o
£?
o
13
Gorgonians
more
abundant
than in Levels
1 - 3; replace
sensitive coral
and sponge
species












Small and
sparse
colonies,
mostly small
sea fans,
often
diseased










i/i
Ol
00
o
Q.
to
Mostly
heterotrophic
sponges with
tolerant
species and
clionids














Heterotrophic
sponges
buried deep in
sediment;
highly tolerant
sponge
species










f
.—
1Z
Absence of
small reef fish
(mostly
Damsel fish)
















No large fish,
few tolerant
species, lack
of multiple
trophic levels











i/i
Ol
+j
£
&
01
e
Ol
>
Large, long-
lived species
locally
extirpated
(e.g., turtles,
eels)














Usually
devoid of
other
vertebrates












8
*j
re
k.
.2
01
1_ 4->
* 1
oj
Diadema
absent;
Palythoa
overgrowing
corals,
crustaceans,
polychaetes
and sensitive
anemones
conspicuously
absent









Low or no
reef
invertebrates;
high
abundance of
sediment
dwelling
organisms
(e.g.,
polychaetes,
holothurians)





i/i
4-1
_ro
Q.
"ST
re
00
<
Some coralline
algae; turf is
un cropped
covered in
sediment; lots of
fleshy algae with
high diversity
(e.g., Dictyota);
possibly covering
sessile
invertebrates; no
turf or coralline
algae; complete
absence of
crust ose
coralline algae




High cover of
fleshy algae
(Dictyota);
possibly covering
sessile
invertebrates; no
turf or coralline
algae; complete
absence of
crust ose
coralline algae






O
J5
^
3
High
incidence of
diseased
coral,
sponges,
gorgonians;
evidence of
high
mortality;
usually less
tissue than
dead
portions on
colonies






High
incidence
disease on
small
colonies
of corals,
sponges and
gorgonians;
if present,
low or no
tissue
coverage




 2-18
Workshop on Biological Integrity of Coral Reefs

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2.5.2 Stony Carol Attributes
For stony corals, attendees decided that very good - excellent stations would have high species
diversity that included large colonies of reef-building corals (i.e., Montastraea) and those colonies
would have high tissue coverage. The Montastraea annularis species-complex (Montastraea
annularis, Montastraea faveolata and Montastraea franksi) was historically one of the primary reef
framework builders of the Caribbean coral reefs, characterizing the "buttress zone" or "annularis
zone" in the  classical descriptions of Caribbean reefs (Goreau 1959). These corals have declined
dramatically throughout their range. The Montastraea annularis species-complex is susceptible to
bleaching (Oxenford et al. 2008; Brandt 2009; Bruckner and Hill 2009; Wagner et al. 2010), disease
(Bruckner and Hill 2009; Miller et al. 2009), sediment (Eakin et al. 1994; Carricart-Ganivet and Merino
2001; Torres and Morelock 2002) and nutrients (Marubini and Davies 1996).

The experts believed that the coral reef population should have a balanced size-class structure,
including large and middle-sized colonies as well as new recruits. Ecologists consider population
demographics to be vital statistics, particularly those statistics that can impact on present and future
population size (Hughes 1996; Edmunds 2013; Edmunds and Elahi 2007). Typically, expanding
populations have a large percentage  of young individuals, while declining populations have a large
percentage of older individuals and stable  populations have a relatively even size distribution among
age groups.

The experts also concluded that Acropora palmata thickets should be present. A. palmata was
formerly the dominant species in shallow water (3-16 ft. deep) throughout the Caribbean and on the
Florida Reef Tract, forming extensive, densely aggregated thickets in areas of heavy surf. These coral
colonies prefer the exposed reef crest and fore-reef environments in depths of < 20 ft., although
isolated corals may occur to depths of 65 ft. Since 1980, populations have collapsed throughout their
range from disease outbreaks, with losses  compounded locally by hurricanes, increased predation,
bleaching, elevated temperatures and other factors (Ruzicka et al. 2013). This species is also
particularly susceptible to damage from  sedimentation (NOAA 2013b).

2.5.3 Gorgonion Attributes
There was considerable discussion about the relative distribution of gorgonians and stony corals. The
experts decided that very good - excellent  stations would have gorgonians present, but the station
should be dominated by stony corals. Gorgonians form a major benthic component of Caribbean
reefs (Bayer  1973; Brazaeu and Lasker 1989) and can be very abundant  in some sites where stony
corals apparently are unable to proliferate. Factors controlling the distribution of shallow-water
gorgonians include water motion and substrate relief (Kinzie 1973; Yoshioka and Yoshioka  1989a, b)
and sediment transport (Yoshioka and Yoshioka 1989b, 2009).
Chapter 2. Approach
2-19

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2.5.4 Sponge Attributes
The experts agreed that very good - excellent stations would have high abundances of large
autotrophic and highly sensitive sponge species. Most sponges are heterotrophic organisms,
obtaining their food from the open water column. However, 35 species of common Caribbean
sponges possess photosynthetic endosymbionts (Vicente 1990) that supply food to their hosts
(Wilkinson 1983; Thacker and Freeman 2012). This is similar to the relationship between
zooxanthellae and their coral hosts. Roberts et al. (2006) found that exposure to shade and siltation
significantly reduced the growth and reproductive status of the temperate photosynthetic reef
sponge Cymbastela concentrica.

2.5.5 Fish Attributes
Workshop participants decided that populations should have balanced distributions of species
abundances, sizes and trophic interactions. Caribbean coral reefs can contain as many as 500-700
species of fishes (Lieske and Collins 2001). The mechanisms that lead to these concentrations of fish
species on coral reefs have been widely debated over the last 50 years. While many reasons have
been proposed there is no scientific consensus on a primary mechanism and it seems likely that a
number of factors contribute. These include the rich habitat complexity and diversity inherent in
coral reef ecosystems (Luckhurst and Luckhurst 1978; Gladfelter et al. 1980) and the variety and
temporal availability of food resources available to coral reef fishes (Randall 1967).

Puerto Rico reef fisheries have shown significant decline since the 1970s, and large reef fishes have
virtually disappeared from shallow reefs around Puerto Rico (Garcia-Sais et al. 2008). Fishing may
have direct and indirect effects on reef fish trophic structure. Removals of apex predators from the
reef complex may result  in shifts of species composition (e.g., through trophic and  ecological
cascades) and for some taxa, increased variability in population dynamics or potential effects on
species evolution.

2.5.6 Large Vertebrate Attributes
Several groups of large, long-lived vertebrate species (e.g., sea turtles and manatees) are considered
important contributors to Puerto Rican coral reef communities. Other groups (e.g., dolphins, whales,
seabirds) spend most of their life cycle in other habitat types but are occasionally seen hunting or
feeding in waters around coral reefs. Puerto Rico supports five species of marine turtles, two of
which (Hawksbill and Leatherback) are critically endangered. Four sharks (Blacktip Shark, Reef Shark,
Tiger Shark and Nurse Shark), eight eels (Brown Garden Eel, Sharptail Eel, Goldspotted Eel, Spotted
Snake Eel, Green Moray, Golden Moray, Spotted Moray, Purplemouth Moray) and  two rays (Spotted
Eagle Ray and Southern Stingray) can also be found on  Puerto Rico coral reefs. A recent study
(Jackson et al. 2012) found that the biomass of apex predators (sharks, large snappers and groupers)
was close to zero in Puerto Rico. The experts decided that large long-lived species should be present
and diverse at very good - excellent stations.
 2-20
Workshop on Biological Integrity of Coral Reefs

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2.5.7 Other Invertebrate Attributes
Queen conch, spiny lobsters and some crabs are harvested for food and have been declining
throughout the Caribbean for decades (Santavy et al. 2012). Conchs are generally acknowledged to
be over-exploited (Appeldoorn and Meyers 1993), and Puerto Rico has established catch limits for
these mollusks. Sea urchins (especially Diadema antillarum) are important herbivores that were
decimated by an  epizootic throughout the western Atlantic in the 1980s (Lessios et al. 1984; Lessios
1988, 2005). The  population status for the Caribbean spiny lobster stock is unknown (NOAA 2013a).

The experts decided that very good - excellent stations would have abundant Diadema, lobster,
small crustaceans and polychaetes. They also felt that some large sensitive anemone species should
be present.

2.5.8 Algoe Attributes
Macroalgae and turf algae compete for space with coral, sponge and  other sessile species. Excess
nutrients may alter competitive interactions and favor algae over coral. Many fishes and
invertebrates are key grazers, helping to maintain algal biomass and prevent algae from overgrowing
coral. A number of algal species (e.g., calcareous macroalgae and crustose coralline algae) deposit
calcium carbonate during growth and may contribute to  reef structural strength. Crustose coralline
algae may also facilitate recruitment of stony coral. Algae are primary producers and provide habitat
and resources for marine fish and  invertebrates but often not to the same degree as coral reef
habitat (Santavy et al. 2012). The experts decided that very good - excellent stations would have
abundant crustose coralline  algae, turf algae would be present but cropped and grazed and fleshy
algae would occur in low abundance.

2.5.9 Condition
Bleaching, disease or predation can affect health and condition of stony corals, gorgonians and
sponges.  An indicator of stony coral/gorgonian health is the amount of live tissue on the organism
or colony. However, coral reef fish rarely appear to suffer from tumors or lesions (Panek 2005).
The experts decided that there should be a very low prevalence of disease on very good - excellent
stations, with mostly live tissue on coral colonies and gorgonians, and low prevalence of tumors on
coral reef fish.
Chapter 2. Approach
2-21

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Chapter 3. Discussion and  Next Steps

3.1 Discussion
EPA convened a group of experts to attempt, for the first time, to develop a coral reef BCG. There
was a consensus among the experts that this was an important contribution, because "We have been
documenting the demise of coral reefs, instead of taking action to change the direction of their
existence".

A preliminary BCG based on stony corals, fishes, gorgonians, sponges, vertebrates and other
invertebrates has been assembled for shallow-water linear reefs of southwestern Puerto Rico. The
experts were able to identify four distinct levels of condition: very good - excellent, good, fair and
poor. Additional discussion is needed to develop reference condition for biological integrity (e.g.,
natural level).

Attribute development during the first workshop relied primarily on viewing videos and  photos from
individual coral reef monitoring sites. This approach resulted in attributes that were largely species-
based, with a single notable addition (e.g., organism condition).

EPA anticipates that ecosystem connectivity is also an appropriate attribute to include in a coral reef
BCG, since connectivity among coral reefs, mangroves, sea grass beds and lagoons provides a
complex and dynamic mosaic that is well documented as a critical ecosystem attribute (Christensen
et al. 2003; Cerveny 2006; Mumby et al. 2004, 2008; Aguilar-Perera and Appeldoorn 2007; McField
and Kramer 2007; Meynecke et al. 2008; Sale et al. 2008; Pittman et al. 2011).

EPA would like to suggest that considering the attributes at multiple scales, similar to  the approach
being developed for estuarine ecosystems,  may also be informative for coral reef ecosystems. The
estuarine BCG framework considers structure, function, condition, connectivity and non-native
species in waterbodies at multiple scales, using measures such as seagrass health, benthic faunal
indices and habitat mosaics (Cicchetti and Pryor 2010; EPA in review). This holistic and integrated
approach is intended to improve the understanding and management of the cumulative impacts of
multiple stressors in complex waterbodies and should work well for coral reefs.

3.2 Next Steps

3.2.1 Second Workshop
EPA is planning to hold a second workshop  in early 2014. At the second workshop EPA hopes to focus
more on: 1) different scales and attributes associated with the entire reef ecosystem,  2) tolerance of
coral reef species to various anthropogenic stressors and 3) the process for moving towards a
quantitative BCG, including development of a data portal to organize and share all of the available
data from Puerto Rican coral reef ecosystems. EPA would also like to continue the discussion of
reference condition and try to reach consensus on attributes for the reference condition level.
Chapter
3.
Discussion
and
Next Steps
3-1

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3.2.2 Species Tolerance Database
In preparation for the first workshop, Ms. Bradley and Dr. Santavy began developing spreadsheets of
coral reef taxa for each assemblage (e.g., stony corals, octocorals, sponges, other invertebrates,
fishes, reptiles, mammals, mangroves, seagrasses and algae) and their characteristics as related to
the ten attributes of the BCG, including tolerance levels to various stressors, vulnerabilities, habitat,
etc. Thresholds, when known, were documented.

Species lists for the database rows were derived from Miller and Lugo (2009). Some columns are
consistent across assemblages (e.g., scientific name, common name, common/rare, tolerance to
pollution, tolerance to temperature change, tolerance to wave energy and susceptibility to disease).
Other columns are  unique to specific assemblages (e.g., for stony corals: maximum colony size,
tolerance to acidity, collection or trade; while for fish: juvenile habitat, adult  habitat, food
preference, solitary/aggregating). Ms. Bradley and Dr. Santavy began to populate the spreadsheets
with data, beginning with information from the Humann and DeLoach field guides (Humann and
DeLoach  2002a, b; 2003) and Sefton and Webster (1986).

During the first workshop, Ms. Bradley gave a short presentation to introduce the spreadsheets.
The group then moved into a brief facilitated discussion. Workshop participants seemed to respond
very positively to the concept and were interested in collaboratively working to complete the
spreadsheets. The group will discuss how to go about completing the spreadsheets during the
second workshop.

3.2.3 Assembling the Monitoring Data
To complete the BCG, the group will utilize pre-existing data collected by others in laboratory and
field studies. In Phase 1, EPA is working with EPA and NOAA data for Puerto Rico and USVI (stony
corals, fish and benthic invertebrates). The initial biological data set will include fish measurements
from several studies conducted by NOAA and EPA. Both groups used the same survey methods for
fish, so standardization will easily occur as existing datasets  are compiled. The second data set
will include stony coral measurements from the same studies by NOAA and EPA. In this case, the
methods are very different and will require discussion with the  EPA coral reefs  BCG team to extract
the most meaningful and comparable data for standardized  reporting. The third data set will include
benthic invertebrates from the same studies by NOAA and EPA. The two survey methods are quite
similar, although NOAA counts lobsters, conch and Diadema, while EPA also counts crabs and
additional urchin species.

For all datasets, EPA will normalize taxonomic  naming protocols to the Integrated Taxonomic
Information System (ITIS). The standardized data set will contain data in the original format, a
crosswalk with translations for converting data and the final standardized format. The data set
will also include a field for the organization that generated the data (data owner).

EPA is planning on completing Phase 1 (as described above) prior to the second workshop and plans
to use these data during the workshop.
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Phase 2 activities will include direct submission into the STORE! Data Warehouse (short for STOrage
and RETrieval). STORE! is a repository for water quality, biological and physical data and is used by
state and territorial environmental agencies for their water quality data under the CWA. Phase 2 will
also include incorporation of additional data and fields, when additional datasets from the coral reef
BCG partners are provided (Puerto Rico Department of Natural and Environmental Resources, Puerto
Rico Environmental Quality Board, USVI Department of Planning and Environmental Resources,
University of Puerto Rico, University of the Virgin Islands, US Geological Survey and National Park
Service). The EPA Office of Water has agreed to make the necessary modifications to STORET to
include these data. Additionally, metadata for the database in STORET (with URL) will be developed
for inclusion in NOAA's Coral Reef Information System (CORIS).

3.2.4 Calibrating the BCG
The group will begin calibrating the BCG by using found (or existing) data to confirm the ecological
attributes developed during this first workshop. The experts have determined narrative decision
rules for assigning stations to a BCG level on the basis of the photographs and videos collected at
multiple stations. Documentation of expert opinion in assigning stations to BCG levels is critical to
the process. Next, a decision model will be developed that incorporates those rules and will be
tested with independent data sets. The decision model using the tested decision rules will provide
a transparent, formal and verifiable method for documenting and validating expert knowledge.
A quantitative data analysis  program can be developed using those rules.

BCG level descriptions in the conceptual model are qualitative (e.g., high diversity, reduced diversity;
Table 2-5) to allow for consistent assignments of stations to levels.  It is necessary to formalize and
quantify the expert knowledge by codifying level descriptions into a set of quantitative rules (e.g.,
Droesen 1996). If formalized and quantified, any person (with data) can follow the rules to obtain the
same level assignments as the group of experts. This makes the actual decision criteria transparent
to stakeholders and potentially applicable to similar types of coral reefs in other areas.

Rules are logic statements that experts use to make their decisions, for example: "If taxon richness is
high, then biological condition is high." Rules on attributes can be combined, for example: "If the
number of highly sensitive coral taxa (Attribute II) is high, and the number of tolerant colonies
(Attribute V) is low, then the assignment is to Level  2." The categories high, moderate, low, etc., are
ordinal categories: we know that moderate is greater  than low; but the boundaries of the categories
are fuzzy and somewhat subjective. In iterations of the process, the expert panel is asked to put
quantitative boundaries on the categories they have defined. The objective is to derive combined
rules, for example, "If there  are more than 10 highly sensitive coral taxa, and the percentage of
colonies of tolerant taxa is less than 15%, then assignment is Level  2." The quantitative rules
preserve the collective professional judgment of the expert group and set the stage for the
development of quantitative models that reliably assign stations to levels  without having to
reconvene the same expert group. In essence, the rules and the models capture the panel's
collective decision criteria.
Chapter
3.
Discussion
and
Next Steps
3-3

-------
The decision rule for a single level of the BCG does not usually rest on a single attribute (e.g., highly
sensitive taxa) and generally includes other attributes (intermediate sensitive taxa, tolerant taxa,
indicator species); such rules are termed Multiple Attribute Decision  Rules. After verification with
independent data, the quantified rules allow users to consistently assess stations according to the
same rules used by the expert panel and allow a computer algorithm, or other persons, to obtain the
same level assignments as the original panel. Documentation of the rules and algorithm allow new
panels to review and modify the decision rules as necessary.

3.2.5 Economic Valuation of Coastal Ecosystem Services
Despite their open-access nature and many contributions to the public good, coral reefs have often
been undervalued in decision-making (Brander et al. 2009). The natural features of a coral reef
(including  physical structure, water quality, biological organisms and  ecological functions) provide
many natural benefits to human societies, collectively known as ecosystem goods and  services. The
economic  values of some services (e.g., commercial fishing) are established in markets, while other
services provide nonmarket value for local, state/regional and national/international segments of the
population (Principe et al. 2012). Most ecosystem service studies have focused on market benefits,
which are  relatively easy to  incorporate in trade-off analyses, but coral reefs also provide numerous
nonmarket ecosystem services (e.g., existence value and cultural value) that can be estimated using
a variety of methods.

Estimates  of the global value of coral reefs range from  US $30 billion per year (Cesar et al. 2003) to
US $377 billion per year (Costanza  et al. 1997). However, global estimates are coarse and rarely
relevant to local management decisions. Decision contexts differ with reef type  and habitat, political
climate, stakeholder interests, decision authorities and responsibilities, knowledge, management
capacity and expertise. Every decision contains an element of valuation, but values are not always at
the forefront of finding optimal decisions (Keeney 1996). Consequences resulting from a decision are
often described in terms of value (Hastie 2001). Yet, the values of stakeholders often go ignored
before management strategies are implemented. Public and stakeholder values, cares, and priorities
should be  considered throughout in the focus and design of assessments and  management planning
and should not be an afterthought in the process.

The BCG effort focuses on how attributes of the coral reef ecosystem change in  response to
increasing anthropogenic stress. The attributes of the coral reef ecosystem represent the "glue"
(Pearce and Moran 1994; Turner et al. 2000) of the properly functioning ecosystem, supporting the
growth of  reef-building corals for ecosystem services (e.g., shoreline  protection, the presence of
unique and diverse species to attract tourists, the creation of potentially useful  natural products and
the maintenance of habitat  and nurseries for harvestable fish stocks). The development of concise,
rigorous definitions and levels of condition along the human disturbance gradient will provide the
fundamental understanding of the factors that affect delivery of ecosystem services.
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EPA and NOAA, in partnership with the University of Puerto Rico and the Puerto Rico Sea Grant, are
conducting a study to provide the economic valuation of tourism and recreation associated with
Puerto Rico's coral reefs to help improve our understanding of the real costs of decisions and
management options. Reef-related tourism activities include snorkeling, diving, fishing, viewing
wildlife, boating, beach  use and surfing. The project will consist of a modified form of the method
NOAA used in the Florida Keys National Marine Sanctuary (Leeworthy and Wiley 1996, 1997, 2003;
Leeworthy and Bowker  1997; Leeworthy and Vanasse 1999; Park et al. 2002; Bhat 2003; Shivlany et
al. 2008), in Southeast Florida (Johns et al. 2001) and in Hawaii (Bishop et al. 2011).

The study is estimating the use and associated market (spending and associated impacts on total
output/sales, income and employment) and non-market economic value (consumer's surplus or the
net value received by those doing recreation activities on the reef over and  above what they pay to
undertake the activities) and how those values change with changes in reef attributes. Linking the
relationships of how reef attribute values change with changes in the physical/natural levels of those
attributes can be used to measure the economic benefits of the changes and thus provide additional
performance measures  of management actions to protect and restore coral reef ecosystems.
Table 3-1 shows coral reef ecosystem services and examples of coral reef attributes that are
associated with them.

Table 3-1. Coral reef ecosystem services and reef attributes (adapted from Principe et al. 2012).
Ecosystem service(s)
Final
Recreational fishing
opportunity
Recreational diving/snorkeling
opportunity
Recreational underwater
photography opportunity
Recreational surfing
opportunity
Opportunity to view nature
and wildlife
Opportunity to sunbathe and
swim at the beach
Opportunity to collect objects
(beachcombing)
Intermediate
Production of benthic and aquatic prey
for consumption by recreational fish
Coral reef formation and maintenance;
maintenance of water clarity; production
of benthic and aquatic prey for
consumption by recreational fish
Coral reef formation and maintenance;
maintenance of water clarity; production
of benthic and aquatic prey for
consumption by recreational fish
Reef breaks
Biological integrity
Water quality, shoreline protection, sand
production
Water quality
Natural features
(reef attributes)
Fish diversity and abundance
Coral diversity, abundance and
health; fish diversity and
abundance; water clarity
Coral diversity, abundance and
health; fish diversity and
abundance; water clarity
3-D reef structure
Biodiversity (birds, marine
mammals, turtles)
White coralline sands; calm
waters
Wide sandy beaches,
biodiversity, occasional storms
Chapter
3.
Discussion
and
Next Steps
3-5

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Definitions

 • Final ecosystem service - Output of ecological functions or processes that directly contributes to
   social welfare or has the potential to do so in the future (sensu Boyd and Banzhaff 2007).
 • Intermediate ecosystem service - Output of ecological functions or processes that indirectly
   contributes to social welfare or has the potential to do so in the future.
 • Natural features - The biological, chemical and  physical attributes of an ecosystem or
   environment.
Estimates of use and value will be made for five regions in Puerto Rico to provide information on the
economic value of reefs in various levels of condition, including present condition. Use and economic
information can be used in evaluating the economic benefits of investments in protection and
restoration of the coral reef ecosystems. Results can be used by both private businesses and
government agencies responsible for managing coral reefs in marketing, education and outreach
efforts, including Puerto Rico's coral reef management activities in the four coral reef priority areas
(Culebra, the Northeast Reserve, Cabo Rojo and Guanica).

3.3 Final Thoughts
The first workshop was a new experience for all involved. While EPA has worked with states and
territories to develop BCGs for streams and estuaries, no one has ever attempted to  develop a BCG
for coral reefs. The experts met the challenge head-on and great progress was made. EPA anticipates
that this is just the first of several expert workshops. EPA will host conference calls and webinars as
appropriate. EPA has asked that the experts from the first workshop commit to working with us
throughout the process.  Experts who were not able to attend the first workshop will  also be invited
to participate in future workshops and webinars.
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Appendix A. References
Adams AJ, Dahlgren CP, Kellison GT, Kendall MS, Layman CA, LeyJA, Nagelkerken I and SerafyJE.
   2006. Nursery function of tropical back-reef systems. Marine Ecology Progress Series 318:
   287-301.
Aguilar-Perera A and Appeldoorn RS. 2007. Variation in juvenile fish density along the mangrove-
   seagrass-coral reef continuum in SW Puerto Rico. Marine Ecology Progress Series 348:139-148.
Almy CC and Carrion-Torres CC. 1963. Shallow-water stony corals of Puerto Rico. Caribbean Journal
   of Science 2/3:133-162.
Alvarez-Filip  L, Kulvy N, Gill JA, Isabelle M and Watkinson AR. 2009. Flattening of Caribbean coral
   reefs: region wide declines in architectural complexity. Proceedings of the Royal Society B,
   276:3019-3025.
Andrews JC and Pickard GL. 1990. The physical oceanography of coral-reef systems. In: Ecosystems of
   the World, Volume 25, Coral Reefs. Z. Dubinsky. (Ed.). New York. pp. 11-48.
Appeldoorn RS and Meyers S. 1993. Part Z. Puerto Rico and Hispaniola. In: Marine fishery resources
   of the Antilles. FAO Fisheries Technical Paper No. 326 Rome, FAO. pp. 99-158.
Ayala CJ. 1999. American sugar kingdom: the plantation economy of the Spanish Caribbean.
   UNC Press. ISBN 978-0-8078-4788-6.
Bak RPM, Carpay MJE and de Ruytervan Steveninck. (Eds). 1983.  Density of the sea urchin Diadema
   antillarum before and  after mass mortalities on the coral reefs of Curacao. Marine Ecology
   Progress Series 17:105-108.
Ballantine DL and Aponte NE. 1997a. A revised checklist of the benthic  marine algae known to
   Puerto Rico. Caribbean Journal of Science 33:150-179.
Ballantine DL and Aponte NE. 1997b. Notes on the benthic marine algae of Puerto Rico VI. Additions
   to the flora. Botanica Marina 40:39-44.
Ballantine DLand Aponte NE. 2002. A Checklist of the Benthic Marine Algae Known to Puerto Rico,
   Second Revision. Revised 2002, URL: http://128.32.109.44/fest PRCL/checklist.html.
Ballantine D, Appeldoorn R, Yoshioka P, Weil E, Armstrong R, Garcia J, Otero E,  Pagan F, Sherman C,
   Hernandez-Delgado E, Bruckner A and Lilyestrom C. 2008. Biology and Ecology of Puerto Rican
   Coral Reefs. In: Riegl BM, Dodge RE. (Eds). Coral Reefs of the USA. Springer, pp. 375-406.

Barber RT, Hilting AK and Hayes ML. 2001. The changing health of coral reefs. Human and Ecological
   Risk Assessment 7:1255-1270.
Barbour MT, Gerritsen J, Snyder BD and Stribling JB. 1999. Rapid Bioassessment Protocols for Use in
   Streams and Wadeable Rivers: Periphyton, Benthic Macroinvertebrates and  Fish, Second Edition.
   US Environmental Protection Agency, Office of Water, Washington, DC. EPA 841-B-99-002.
Appendix A. References
A-l

-------
Barnes DJ. 1988. Seasonality in community productivity and calcification at Davies Reef, central Great
  Barrier Reef. Proceedings of the Sixth International Coral Reef Symposium. 6: 521-527.
Bayer FM. 1973. Colonial organization in octocorals. In: Animal Colonies: Development and Function
  Through Time. Boardman RS, Cheetham AH and Oliver Jr. (Eds.). WA. Wiley and Sons, Inc.
  pp. 69-93.
Beets J and Friedland A. 1998. Evaluation of a conservation strategy: a spawning aggregation closure
  for red hind, Epinephelus guttatus, in the U.S. Virgin Islands. Environmental Biology of Fishes
  55:91-98.
Seller W, Casellas MA, Cerame-Vivas MJ, Duffy L, El KouryJ, Gelabert PA, Gonzales LiboyJA,
  Hernandez-Avila M, Maldonado N, Matos CA, Mignucci-Giannonni A, Pantoja-Garcia E, Rigau J,
  Shelley D, Tacher-Roffe M and N. Zerbi N. 1999. Puerto Rico and the Sea: An action program for
  marine affairs. Report to the governor, PR. Department of Natural Resources, San Juan, PR.
Benedict JE. 1902. Anomuran collection of Porto Rico. Bulletin of the United States Fish Commission
  20:129-148.
Bhat MG. 2003. Application of non-market valuation to the Florida Keys marine reserve
  management. Journal of Environmental Management 67:315-325.
Bigelow RP. 1902. The Stomatopoda of Porto Rico. Bulletin of the United States Fish Commission
  20:149-160.
Bishop RS, Chapman DJ, Kanninen BJ, KrosnickJA, Leeworthy B and Neade NF. 2011. Total Economic
  Value for Protecting and Restoring Hawaiian Coral Reef Ecosystems Final Report. Silver Spring,
  MD: NOAA Office of National Marine Sanctuaries, Office of Response and Restoration, and Coral
  Reef Conservation Program. NOAA Technical Memorandum CRCP 16,405 pp.
Bradley P, Fisher WS, Bell H, Davis WS, Chan V, LoBue C and Wiltse W. 2008. Development and
  implementation of coral reef biocriteria in US jurisdictions. Environmental Monitoring and
  Assessment 150:43-51.
Bradley P, Fore L, Fisher W and Davis W. 2010. Coral Reef Biological Criteria: Using the Clean Water
  Act to Protect a National Treasure. Narragansett (Rl): U.S. Environmental Protection Agency,
  Office of Research and Development, EPA/600/R-10/054, July 2010.
Brainard RE, Birkeland C, Eakin CM, McElhany P, Miller MW, Patterson M and Piniak GA. 2011. Status
  review report of 82 candidate coral species petitioned under the U.S. Endangered Species Act. US
  Department of Commerce. NOAA Technical Memorandum. NOAA-TM-NMFS-PIFSC-27, 530 p.  + 1
  Appendix.
Brander LM,  Rehdanz K, Tol RSJ and van Beukering PJH. 2009. The economic impact of ocean
  acidification on coral reefs. ESRI Working Paper No. 282.
Brandt ME. 2009. The effect of species and colony size on the bleaching response of reef-building
  corals in the Florida Keys during the 2005 mass bleaching event. Coral Reefs 28: 911-924.
Brazeau DA and Lasker HR. 1989. The reproductive cycle and spawning in a Caribbean gorgonian.
  Biological Bulletin 176:1-7.
 A-2  Workshop on Biological Integrity of Coral Reefs

-------
Brown BE and Howard LS. 1985. Assessing the effects of "stress" on reef coral. Advances in Marine
  Bio logy 22:1-63.
Bruckner AW and Bruckner RJ. 1997. Outbreak of coral disease in Puerto Rico. Coral Reefs 16:260.
Bruckner AW and Bruckner RJ. 2006. Consequences of yellow band disease (YBD) on Montastraea
  annularis (species complex) populations on remote reefs off Mona Island, Puerto Rico. Diseases
  of Aquatic Organisms 69:67-73.
Bruckner AW and Hill RL. 2009. Ten years of change to coral communities off Mona and Desecheo
  Islands, Puerto Rico, from disease and bleaching. Diseases of Aquatic Organisms 87:19-31.
Budd AF, Fukami H, Smith ND and Knowlton N. 2012. Taxonomic classification of the reef coral family
  Mussidae (Cnidaria: Anthozoa: Scleractinia). Zoological Journal of the Linnean Society
  166:465-529.
Burke L and Maidens J. 2004. Reefs at risk in the Caribbean. World Resources Institute,
  Washington, DC. 81 pp.
Carpenter KE, Miclat Rl, Albaladejo VD and Corpuz VT. 1981. The influence of substrate structure
  on the abundance and diversity of Philippine reef fishes. Proceedings of the Fourth International
  Coral Reef Symposium 2:497-502.
Carricart-Ganivet JP and Merino M. 2001. Growth responses of the reef-building coral Montastraea
  annularis along a gradient of continental influence in the southern Gulf of Mexico. Bulletin of
  Marine Science 68:133-146.
Cerame-Vivas MJ. (Ed.). 2001. Ecologia de Puerto Rico. Publications Puertorriquenas, xviii. 207 pp.
Cerveny K. 2006. Distribution patterns of reef fishes in southwest Puerto Rico, relative to structural
  habitat, cross-shelf location, and ontogenetic stage. Department of Marine Sciences, University of
  Puerto Rico, Mayaguez, Puerto Rico. Masters Thesis. 172 pp.
Cesar H, Burke L and Pet-Soede L. 2003. Economics of worldwide coral reef degradation. World
  Wildlife Foundation. Veenman Drukkers, Ede. Netherlands, pp. 24.
Christensen JD, Jeffrey CFG, Caldow C, Monaco ME, Kendall MS and Appeldoorn RS. 2003. Cross-
  Shelf Habitat Utilization Patterns of reef fishes in southwestern Puerto Rico. Gulf and Caribbean
  Research 14:9-27.
Cicchetti G and Greening H. 2011. Estuarine biotope mosaics and habitat management goals: An
  application in Tampa Bay, FL, USA. Estuaries and Coasts  34:1278-1292.
Cicchetti G. 2010. Summary of a Technical Workshop held October 28 and 29, 2009: Developing a
  Biological Condition Gradient for Narragansett Bay. US Environmental Protection Agency,
  Narragansett, Rl. Internal Report.
Cicchetti G and Pryor M. 2010. Summary of the Estuarine BCG Workgroup November 2008
  Workshop, and a Proposed Organizing Framework for Bioassessment of Estuaries. US
  Environmental Protection Agency, Narragansett, Rl. Internal Report, pp. 25.
Clark HL. 1902. The Echinoderms of Porto Rico. Bulletin of the United States Fish Commission
  20:231-263.
Appendix A. References
A-3

-------
Clark HL. 1933. Handbook of the littoral Echinoderms of Puerto Rico and other West Indian Islands.
  New York Academy of Science 16:1-147.
Clark RD, Pittman S, Caldow C, Christensen J, Roque B, Appeldoorn RS and Monaco ME. 2009.
  Nocturnal fish movement and trophic flow across habitat boundaries in a coral reef ecosystem
  (SW Puerto Rico). Caribbean Journal of Science 45:282-303.
Coe WR. 1902. The Nemerteans of Porto Rico. Bulletin of the United States Fish Commission
  20:223-229.
Costanza R, d'Arge R, de Groot R, Farber S, Grasso M, Hannon B, Naeem S, Limburg K, Paruelo J,
  O'Neill RV, Raskin R, Sutton P and van den Belt M. 1997. The value of the  world's ecosystem
  services and natural capital. Nature 387:253-260.
Croquer A and Weil E. 2009. Changes in Caribbean coral disease prevalence  after the 2005 bleaching
  event. Diseases of Aquatic Organisms 87:33-43.
DahlgrenCP, Kellison T, Adams AJ, Gillanders BM, Kendall MS, LeyJA, Nagelkerken I and SerafyJE.
  2006. Marine nurseries and effective juvenile habitats: concepts and applications. Marine Ecology
  Progress Series 312:291-295.
Dall WH and Simpson CT. 1902. The Mollusca of Porto Rico. Bulletin of the United States Fish
  Commission 20:353-524.
Davies SP and Jackson SK. 2006. The Biological Condition Gradient: a descriptive model for
  interpreting change in aquatic ecosystems. Ecological Applications 16:1251-1266.
Debrot A. 2000. A review of records of the extinct W. Indian monk seal. Marine Mammal Science
  16:834-837.
Dennis G. 2000. Annotated  checklist of shallow-water marine fishes from the Puerto Rico  Plateau
  including Puerto Rico, Culebra, Vieques, St. Thomas, St. John, Tortola, Virgin  Gorda and Anegada.
  http://www.fcsc. usgs.gov/Ma rine_Studies/Marine_Puerto_Rico_Plateau/marine_puerto_rico_pla
  teau.html.
Dennis GD,  Hensley DL, Colin PL and Kimmel GG. 2004. New records of marine fishes from the
  Puerto Rico Plateau. Caribbean Journal of Science 40:70-87.
Droesen WJ. 1996. Formalisation of ecohydrological expert knowledge applying fuzzy techniques.
  Ecological Modeling 85:75-81.
Eakin CM. Feingold JS and Glynn PW. 1994. Oil refinery impacts on coral reef communities in Aruba,
  N.A. In: Ginsburg RN. Proceedings of the Colloquium on Global Aspects of Coral Reefs: Health,
  Hazards and History. Rosenstiel School of Marine and Atmospheric Science, University  of Miami.
  1994. pp. 139-145.
Edmunds PJ. 2013. Decadal-scale changes in the community structure of coral reefs of St.  John, US
  Virgin Islands. Marine Ecology Progress Series 489:107-123.
Edmunds PJ and Elahi E. 2007. The demographics of a 15-year decline in cover of the Caribbean reef
  coral Montastraea annularis. Ecological Monographics 77: 3-18.
Federal Register. Rules and Regulations. 71:26852-26861.
  A-4  Workshop on Biological Integrity of Coral Reefs

-------
Fisher WS. 2007. Stony Coral Rapid Bioassessment Protocol. US Environmental Protection Agency,
  Office of Research and Development, Washington, D.C. EPA/600/R-06/167, 60 pp.
Friedlander AM and Parrish JD. 1998. Habitat characteristics affecting fish assemblages on a
  Hawaiian coral reef. Journal of Experimental Marine Biology and Ecology 224:1-30.
Garcia JR, Morelock J, Castro R, Goenaga C and Hernandez-Delgado EA. 2003. Puerto Rican reefs:
  research synthesis, present threats and management perspectives. In: Latin American Coral Reef.
  J. Cortes (Ed.), pp. 111-130. Amsterdam: Elsevier Science B.V.
Garcia-Rios Cl (Ed.). 2003. Los Chitones de Puerto Rico. Editorial Isla Negra.
Garcfa-Sais J, Appeldoorn R, Battista T, Bauer L, Bruckner A, Caldow C, Carrubba L, Corredor J, Diaz E,
  Lilyestrom C, Garcfa-Moliner G, Hernandez-Delgado E, Menza C, Morell J, Pait A, Sabater J, Weil E,
  Williams E and Williams S. 2008. The State of Coral Reef Ecosystems of Puerto Rico. In: The state
  of coral reef ecosystems of the United States and Pacific Freely Associated States: 2008. Waddell JE
  and Clarke AM. (Eds). NOAA Technical Memorandum NOS NCCOS 73. 569 pp.
Garcfa-Sais JR,  Castro  R, Sabater-Clavell J, Esteves R and Carlo M. 2006. Monitoring of coral reef
  communities from  natural reserves in Puerto Rico, 2006: Isla Desecheo, Rincon, Mayaguez Bay,
  Guanica, Ponce and Isla Caja de Muerto. Final Report submitted to the Department of Natural and
  Environmental Resources of Puerto Rico. San Juan, PR. 151 pp.
Gladfelter WB, Ogden JC and Gladfelter EH. 1980. Similarity and diversity among coral reef fish
  communities: a comparison between Tropical Western Atlantic (Virgin Islands) and Tropical
  Central Pacific (Marshall Islands) patch reefs. Ecology 61:1156-1168.
Gladfelter WB. 1982. White-Band Disease in Acropora palmata: implications for the structure and
  growth of shallow reefs. Bulletin of Marine Science 32:639-643.
Glynn PW. 1988. El-Nino Southern Oscillation 1982-1983. Near shore population, community, and
  ecosystem responses. Annual Review of Ecology and Systematics 19:309-345.
Glynn PW. 1991. Coral-reef bleaching in the 1980s and possible connections with global warming.
  Trends in Ecology and Evolution 6:175-179.
Goenaga C, Vicente VP and Armstrong RA. 1989. Bleaching Induced Mortalities in Reef Corals from La
  Parguera, Puerto Rico: A Precursor of Change in the Community Structure of Coral Reefs?
  Caribbean Journal of Science 25:59-65.
Goreau TF. 1959. The  ecology of Jamaican coral reefs. I. Species composition and zonation. Ecology
  40:67-90.
Goreau TJ, Hayes RH, Clark JW, Basta DJ and Robertson CN. 1992. Elevated Sea Surface Temperatures
  Correlate with Caribbean Coral Reef Bleaching. In: A Global Warming Forum: Scientific, Economic,
  and Legal Overview. Geyer RA. (Ed.). CRC Press, Boca Raton, Florida USA, Chapter 9,  pp. 225-255.
Grana FA. 1993. Catalogo de la nomenclatura de los Moluscos de Puerto Rico e Islas Virgenes.
  Technical report, Deptmento Recursos Naturales, Puerto Rico.
Grimsditch GD and Salm RV. 2006. Coral Reef Resilience and Resistance to Bleaching. IUCN, Gland,
  Switzerland. 52pp.
Appendix A. References
A-5

-------
Gundlach DJ. 1887. Apuntes para la Fauna Puerto-Riquena (VI). Crustaceos. Anales de la Sociedad
   Espanola de Historia Natural 16: 115-133.
Gundlach J. 1883. Apuntes para la Fauna Puerto-Riquena (V). Moluscos. Anales de la Sociedad
   Espanola de Historia Natural 12:441-484.
Hargitt CW and Rogers CG. 1902. The Alcyonaria of Puerto Rico. Bulletin of the United States Fish
   Commission 20:265-287.
Harvell CD, Altizer S, Cattadori IM, Harrington L and Weil E. 2009. Climate change and wildlife
   diseases: When does the host  matter the most? Ecology 90:912-920.
Hastie R. 2001. Problems for judgment and decision-making. Annual Review of Psychology
   52:653-683.
Hatcher BG, Imberger J and Smith SV. 1987. Scaling analysis of coral reef systems: An approach to
   problems of scale. Coral Reefs 5:171-181.
Hauck F. 1888. Meeresalgen von  Puerto-Rico. BotanischeJahrbucherfurSystematik.
   Pflanzengeschichte und Pflanzengeographie 9:457-470.
Healthy Reefs for Healthy People Initiative. 2012. Report Card for the Mesoamerican Reef 2012.
   25pp.
Hearn Q, Atkinson MJ and Falter JL. 2001. A physical derivation of nutrient uptakes in coral reefs:
   Effects of roughness and waves. Coral Reefs 20:347-356.
Hearn G. 2008. The Dynamics of Coastal Models. Cambridge University Press, 488 pp.
Hoegh-Guldberg 0. 1999. Climate change, coral bleaching and the future of the world's coral reefs.
   Marine and Freshwater Research 50:839-866.
Hubbard DK. 1997. Reefs as dynamic systems. In: Life and Death of Coral Reefs. Birkeland C. (Ed.).
   Chapman and Hall Publishing,  New York. pp. 43-67.
Hughes, TP. 1996.  Demographic approaches to community  dynamics: a coral reef example. Ecology
   77:2256-2260.
Humann P and DeLoach N. 2002.  Reef Coral Identification. New World  Publications, Inc., Jacksonville,
   FL 287 pp.
Humann P and DeLoach N. 2002.  Reef Fish Identification: Florida, Caribbean, Bahamas. New World
   Publications, Inc. 481 pp.
Humann P and DeLoach N. 2003.  Reef Creature Identification: Florida, Caribbean, Bahamas.
   New World Publications, Inc. 420 pp.
Idjadi JA and Edmunds PJ. 2006. Scleractinian corals as facilitators for other invertebrates on a
   Caribbean reef. Marine Ecology Progress Series 319:117-127.
Jackson J, Cramer K,  Donovan M, Friedlander A, Hooten A and Lam V. 2012. Tropical Americas Coral
   Reef Resilience Workshop. 29 April-5 May 2012, Tupper  Center, Smithsonian Tropical Research
   Center, Panama City, Republic of Panama.
  A-6  Workshop on Biological Integrity of Coral Reefs

-------
Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R,
   Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH,
   Steneck RS, Tegner MJ and Warner RR. 2001. Historical overfishing and the recent collapse of
   coastal ecosystems. Science 293:629-637.
Jackson JBC. 1997. Reefs since Columbus. Coral Reefs 16:523-532.
Johns GM, Leeworthy VR, Bell FW and Bonn MA. 2001. Socioeconomic study of reefs in southeast
   Florida. Report (Hazen and Sawyer) to Broward County, Palm Beach County, Miami-Dade County
   (Florida). Florida Fish and Wildlife Commission and the National Oceanic and Atmospheric
   Administration, 255 pp.
Karr JR. 1991.  Biological Integrity: A Long-Neglected Aspect of Water Quality Resource Management.
   Ecological Applications 1: 66-84.
Karr JR and Chu EW. 1999. Restoring life in running waters: Better biological monitoring. Island Press,
   Washington, DC, 206 pp.
Keeney RL. 1996. Value-focused thinking: Identifying decision opportunities and creating
   alternatives. European Journal of Operational Research 92:537-549.
Kendall MS, Monaco ME, Buja KR, Christensen JD, Kruer CR, Finkbeiner M and Warner RA. 2001.
   Methods used to map the benthic habitats  of Puerto Rico. NOAA Technical Memorandum NOS
   NCCOS CCMA 152.
Kinzie RA III. 1973. The zonation of West Indian gorgonians. Bulletin of Marine Science 23:93-155.
Leeworthy VR and Bowker JM. 1997. Nonmarket economic user values of the Florida Keys/Key West.
   NOAA, Silver Spring, MD.
Leeworthy VR and Vanasse P. 1999. Economic contribution of recreating visitors to the Florida
   Keys/Key West: updates for years 1996-97 and 1997-98. NOAA, Silver Spring, MD.
Leeworthy VR and Wiley PC. 1996. Importance and satisfaction ratings by recreating visitors to the
   Florida Keys/Key West. NOAA,  Silver Spring, MD.
Leeworthy VR and Wiley PC. 1997. A socioeconomic analysis of the recreation activities of Monroe
   County residents in the Florida Keys/Key West. NOAA, Silver Spring, MD.
Leeworthy VR and Wiley PC. 2003. Profiles and economic contribution: General visitors to Monroe
   County, Florida 2001-2001. NOAA, Silver Spring,  MD.
Lessios H. 2005. Diadema antillarum populations in  Panama twenty years following mass mortality.
   Coral Reefs 24:125-127.
Lessios HA, Robertson DR and Cubit JD. 1984.  Spread of Diadema mass mortality through the
   Caribbean.  Science 226:335-337.
Lessios HA. 1988. Mass mortality  of Diadema  antillarum in the Caribbean: What have  we learned?
   Annual Review of Ecology and  Systematics  19:371-393.
Lieske E and Myers  R.  2001.Cora/ Reef Fishes:  Indo-Pacific & Caribbean. Princeton University Press,
   Princeton, NJ, USA.
Appendix A. References
A-7

-------
Long C. 1975. The Polychaeta from La Parguera, Puerto Rico. University of Puerto Rico, Department
  of Marine Sciences.
Luckhurst BE and Luckhurst K. 1978. Analysis of the influence of substrate variables on coral reef fish
  communities. Marine Biology 49:317-323.
Marubini F and Davies PS. 1996. Nitrate increases zooxanthellae population density and reduces
  skeletogenesis in coral. Marine Biology 127:319-328.
McClanahan TR, Ateweberhan M, Muhando CA, Maina J and Mohammed MS. 2007. Effects of
  climate and seawater temperature variation on coral bleaching and mortality. Ecological
  Monographs 77:503-525.
McClanahan TR, Weil E, Cortes J, Baird A and Ateweberhan M. 2009. Consequences of coral
  bleaching for sessile organisms. In M. van Oppen and J. Lough (Eds.) Coral Bleaching: Patterns,
  Processes, Causes and Consequences. Ecological Studies, pp: 121-138. Springer-Verlag.
McField M and Kramer PR. 2007. Healthy Reefs for Healthy People: A Guide to Indicators of Reef
  Health and Social Well-being in the Mesoamerican Reef Region. 208 pp.
Meissner KJ, Lippmann T and Gupta AS. 2012. Large-scale stress factors affecting coral reefs: Open
  ocean sea surface temperature and surface seawater aragonite saturation over the next 400
  years. Coral Reefs 31: 309-319.
Menzies RJ and Glynn PW. 1968. The common marine Isopod crustaceans of Puerto Rico. In: Studies
  of the Fauna of Curasao and other Caribbean Islands 23:133.
Meynecke JO, Lee SY and Duke NC. 2008. Linking spatial metrics and fish catch reveals the
  importance of coastal  wetland connectivity to inshore fisheries in Queensland, Australia.
  Biological Conservation 141:981-996.
Miller GL and Lugo AE. 2009. Guide to the ecological systems of Puerto Rico. General Technical
  Report. IITF-GTR-35. San Juan, PR: US Department of Agriculture, Forest Service, International
  Institute of Tropical Forestry. 437 pp.
Miller J, Muller E, Rogers C, Waara R, Atkinson A, Whelan KRT, Patterson M and Witcher B. 2009.
  Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the
  US Virgin Islands. Coral Reefs 28:925-937.
Monismith SG. 2007. Hydrodynamics of coral reefs. Annual Reviews of Fluid Mechanics 39:37-55.
Moore HF. 1902. Porto Rican Isopoda. Bulletin of the United States Fish Commission 20:161-176.
Morelock J, Ramirez W, Bruckner A and Carlo M. 2001. Status of coral reefs, southwest Puerto  Rico.
  Caribbean Journal of Science, Online Special Publication 4:57. URL:
  www.uprm.edu/biology/cjs/reefstatus.htm.
Mumby PJ, Broad K, Brumbaugh  DR, Dahlgren CP, Harborne AR, Hastings A, Holmes KE, Kappel CV,
  Micheli F and Sanchirico JN. 2008. Coral reef habitats as surrogates of species, ecological
  functions, and ecosystem services. Conservation Biology 22:941-951.
 A-8  Workshop on Biological Integrity of Coral Reefs

-------
Mumby PJ, Edwards AJ, Arias-Gonzalez JE, Lindeman KC, Blackwell PG, Gall A, Gorczynska Ml,
   Harborne AR, Pescod CL, Renken H, Wabnitz CC and Llewellyn G. 2004. Mangroves enhance the
   biomass of coral reef fish communities in the Caribbean. Nature 427:533-536.
Munk W and Sargeant M. 1954. Adjustment of Bikini Atoll to ocean waves. US Geological Survey
   Professional Paper 260. pp. 275-280.
Nagelkerken I, Van der Velde G, Gorissen MW, Meijer GJ, van't Hof T and den Hartog C. 2000.
   Importance of mangroves, seagrass beds and the shallow coral reef as a nursery for important
   coral reef fishes, using a visual census technique. Estuarine, Coastal and Shelf Science 51:31-44.
National Oceanic and Atmospheric Administration (NOAA). 2012a. Marine Invertebrates and Plants.
   URLwww. nmfs.noaa.gov/pr/species/invertebrates/
National Oceanic and Atmospheric Administration (NOAA). 2012b. Laboratory for Satellite Altimetry:
   Sea level rise. URL:ibis.grdl.noaa.gov/SAT/SeaLevelRise/LSA_SLR_timeseries_global.php.
National Oceanic and Atmospheric Administration (NOAA). 2013a. Fish watch, Caribbean Spiny
   Lobster. URL:
   www.fishwatch.gov/seafood_profiles/species/lobster/species_pages/caribbean_spiny_lobster.
   htm.
National Oceanic and Atmospheric Administration (NOAA). 2013b. Elkhorn Coral (Acropora palmata).
   NOAA Fisheries, Office of Protected Resources. URL:
   www.nmfs.noaa.gov/pr/species/invertebrates/elkhorncoral.htm
Nunes V and Pawlak G. 2008. Observations of bed roughness of a coral reef. Journal of Coastal
   Research 24:39-50.
Odum E. 1997. Ecology: A bridge between science and society. Sinauer Associates, Inc., Sunderland,
   MA. 330  pp.
Ogden JC. 1997. Ecosystem interactions in the tropical coastal seascape. In: Life and death of coral
   reefs. Birkeland C. (Ed.). Chapman and Hall Publishing. New York. pp. 288-297.
Ortiz E. 1998. Los Moluscos recientes de Puerto Rico. Ph.D. thesis, Department of Marine Sciences,
   University of Puerto Rico, Mayaguez.
Osborne PL. 2000. Tropical Ecosystem and Ecological Concepts. Cambridge: Cambridge University
   Press. 464 pp.
Osburn RC. 1940. Bryozoa of Porto Rico with a resume of the West Indian Bryozoan fauna. New York
   Academy of Science 16:321-486.
Oxenford H, Roach R, Brathwaite A, Nurse L, Goodridge R, Hinds F, Baldwin K and Finney C. 2008.
   Quantitative observations of a major coral bleaching event in Barbados, southeastern Caribbean.
   Climatic Change 87:435-449.
Panek FM. 2005. Epizootics and disease of coral reef fish in the tropical western Atlantic and Gulf
   of Mexico.  Reviews in Fisheries Science 13:1-21.
Park T, Bowker JM and Leeworthy VR. 2002. Valuing snorkeling visits to the Florida Keys with stated
   and revealed  preference models. Journal of Environmental Management 65:301-312.
Appendix A. References
A-9

-------
Pauly D. 1995. Anecdotes and the shifting base-line syndrome of fisheries. Trends in Ecology and
  Evolution 10:430.
Pearce DW and Moran D. 1994. The Economic Value of Biodiversity. In association with the
  Biodiversity Programme, The World Conservation Union. London: Earthscan Publications, 172 pp.
Pittman SJ, Renchen GF, Clark R, Caldow C, Olsen D and Hill RL. 2011. Applications of estuarine and
  coastal applications in marine spatial planning. Treatise on Estuarine and Coastal Science 1:
  163-205.
Pittman SJ, Caldow C, Hile SD and Monaco ME. 2007a. Using seascape types to explain the spatial
  patterns of fish in the mangroves of SW Puerto Rico. Marine Ecology Progress Series 348:273-284.
Pittman SJ, Christensen JD, Caldow C, Menza C and Monaco ME. 2007b. Predictive mapping of fish
  species richness across shallow-water seascapes in the Caribbean. Ecological Modeling 204:9-21.
Pittman SJ, Hile SD, Jeffrey CFG, Caldow C, Kendall MS, Monaco ME, and Hillis-Starr Z. 2008. Fish
  assemblages and benthic habitats of Buck Island Reef National Monument (St. Croix, U.S. Virgin
  Islands) and the surrounding seascape: A characterization of spatial and temporal patterns.  NOAA
  Technical Memorandum NOS NCCOS 71. Silver Spring, MD. 96 pp.
Pittman SJ, Hile SD, Jeffrey CFG, Clark R, Woody K, Herlach BD, Caldow C,  Monaco ME and
  Appeldoorn R. 2010. Coral Reef Ecosystems of Reserva Natural La Parguera (Puerto Rico):
  Spatial and Temporal Patterns in Fish and Benthic Communities (2001-2007). NOAA Technical
  Memorandum NOS NCCOS 107, Silver Spring, MD. 202  pp.
Poey F. 1881. Peces. In: Gundlach DJ. Apuntes para la fauna Puerto-Riquena (III). Anales de la
  Sociedad Espanola de Historia Natural 10:317-350.
Prada C, Weil E and Yoshioka P. 2009. Octocoral bleaching under unusual thermal stress.  Coral Reefs
  29:41-45.
Principe P, Bradley P, Yee S, Fisher W, Johnson E, Allen P and Campbell D. 2012. Quantifying Coral
  Reef Ecosystem Services. US Environmental Protection Agency, Office of Research and
  Development, Research Triangle Park, NC. EPA/600/R-11/206.
Randall JE. 1967. Food habitats of reef fishes of the West Indies. Studies of Tropical Oceanography
  5:665-847.
Rathbun NJ. 1902. Brachyura and  Macrura of Porto Rico. Bulletin of the United States Fish
  Commission 20:1-127.
Richmond  RH. 1993. Coral reefs: Present problems and future concerns resulting from anthropogenic
  disturbance. American Zoologist 33:524-536.
Risk MJ. 1972. Fish diversity on a coral reef in the Virgin Islands. Atoll Research Bulletin 153:1-6.
Rivero JA. (Ed). 1978. Los anflbios y reptiles de Puerto Rico. Editorial Universitaria, Universidad  de
  Puerto Rico.
Roberts DE, Davis AR and Cummins SP. 2006. Experimental manipulation of shade, silt, nutrients and
  salinity on the temperate reef sponge Cymbastela concentrica. Marine Ecology Progress Series
  307:143-154.
 A-10  Workshop on Biological Integrity of Coral Reefs

-------
Rouse I. 1992. The Tainos: Rise and Decline of the People Who Greeted Columbus. Yale University
   Press. 232 pp.
Ruiz Torres H. 2012. Beneath the Waves. University of Puerto Rico, Sea Grant. 131 pp.
Ruzicka RR, Colella MA, Porter JW, Morrison JM, Kidney JA, Brinkhuis V, Lunz KS, MacaulayKA,
   Bartlett LA, Meyers MK and Colee J. 2013. Temporal changes in benthic assemblages on Florida
   Keys reefs 11 years after the 1997/1998 El Nino. Marine Ecology Progress Series 489:125-141.
Sale PF and Szmant AM. (Eds). 2012. Reef Reminiscences: Ratcheting back the shifted baselines
   concerning what reefs used to be. United Nations University Institute for Water, Environment
   and Health, Hamilton, ON,  Canada, 35 pp.
Sale PF, Jacob P  and Kritzer JP. 2008. Connectivity: What it is, how it is measured, and why it is
   important for management of reef fishes. In: Grober-Dunsmore R and Keller BD. (Eds).
   Caribbean connectivity: Implications for marine protected area management. Proceedings of a
   Special Symposium, 9-11 November 2006, 59th Annual Meeting of the Gulf and Caribbean
   Fisheries Institute, Belize City, Belize. Marine Sanctuaries Conservation Series ONMS-08-07. Silver
   Spring (MD):  US Department of Commerce, National Oceanic and Atmospheric Administration,
   Office of National  Marine Sanctuaries, pp. 16-30.
Santavy DL, Fisher WS, Campbell JG and Quarles RL. 2012. Field Manual for Coral Reef Assessments.
   US Environmental Protection Agency, Office of Research and Development, Gulf Ecology Division,
   Gulf Breeze, FL. EPA/600/R-12/029. 92 pp.
Santavy DL, Courtney LA, Fisher WS, Quarles RL and Jordan SJ. 2013. Estimating surface area of
   sponges and gorgonians as indicators of habitat availability on Caribbean coral reefs.
   Hydrobiologia 707:1-16.
Sebens KP. 1994. Biodiversity of coral reefs: What we are losing and why? American Zoologist
   34:115-133.
Sefton N and Webster SV. 1986. Caribbean Reef invertebrates. Sea Challengers. Monterey, CA.
   112pp.
Shashar N, Kinane S, Jokiel PL and Patterson MR. 1996. Hydromechanical boundary layers over a
   coral  reef. Journal of Experimental Marine Biology and Ecology 199:17-28.
Shivlany M, Leeworthy VR, Murray TJ, Suman DO and Tonioh F. 2008. Knowledge, attitudes and
   perceptions of management strategies and regulations of the Florida Keys National Marine
   Sanctuary by commercial fishers, dive operators, and environmental group members: A baseline
   characterization and 10-year comparison. National Oceanic and Atmospheric Administration,
   Silver Spring,  MD.
Soler-Lopez LR. 2001. Sedimentation Survey Results of the Principal Water Supply Reservoirs  of
   Puerto Rico. In: Sylva WF (Ed.). Proceedings of the Sixth Caribbean Islands Water Resources
   Congress, Mayaguez, Puerto Rico, February 22 and 23, 2001.
Stahl A.  1883. Fauna de Puerto Rico, Clasificacion sistematica de lo animates que corresponden a esta
  fauna, y catalogo del gabinete zoologica del Dr. A. Stahl en Bayamon.  San Juan, PR. 249 pp.
Appendix A. References
A-ll

-------
Steele MA. 1999. Effects of shelter and predators on reef fishes. Journal of Experimental Marine
   Biology and Ecology 233:65-79.
Stoddard JL, Larsen DP, Hawkins CP, Johnson RK and Norris RH. 2006. Setting expectations for the
   ecological condition of streams: The concept of reference condition. Ecological Applications
   16:1267-1276.
Sturm P, Viqueira R, Ferguson R and Moore T. 2012. Addressing land based sources of pollution in
   Guanica, Puerto Rico. In: D. Yellowlees and TP Huges, Proceedings of the 12th International Coral
   Reef Symposium, 9-13 July 2012 Cairns, Australia. URL:http://www.icrs2012.com/Proceedings.htm
Talbot FH. 1965. A description of the coral structure of Tutia reefs (Tanganyika territory, East Africa)
   and  its fish fauna. Proceedings of the Zoological Society of London 145:431-470.
Thacker RW and Freeman CJ. 2012. Chapter two - Sponge-Microbe Symbioses: Recent Advances and
   New Directions.  In: Advances in Marine Biology.  Becerro MA, Uriz MJ, Maldonado M and Turon X.
   (Eds.), Academic Press 62:57-111.
The Nature Conservancy (TNC). 2006. Are Florida's  reefs resilient? A guide to the Florida reef
   resilience program. Summerland Key,  Florida.
Torres JL and Morelock J. 2002. Effect of terrigenous sediment influx on coral cover and linear
   extension rates of three Caribbean massive coral species. Caribbean Journal of Science
   38:222-229.
Treadwell AL. 1902. Polychaetous annelids of Puerto Rico. Bulletin of the United States Fish
   Commission 20:181-210.
Treadwell AL. 1939. Polychaetous annelids of Puerto Rico and Vicinity. In: Scientific Survey of
   Porto Rico and the Virgin Islands 16:313. New York Academy of Sciences.
Turner RK, Brouwer R, Georgiou S and Bateman IJ. 2000. Ecosystem functions and services: An
   integrated framework and case study for environmental valuation. Norwich (UK): University of
   East Anglia, The Centre for Social  and  Economic  Research on the Global Environment (CSERGE),
   CSERGE Working Paper GEC 2000-21,  32 pp.
US Commission on Ocean Policy. 2004. US Ocean Action Plan. 41 pp.
US Environmental Protection Agency (EPA). 2005. Use of Biological Information to Better Define
   Designated Aquatic Life Uses in State and Tribal  Water Quality Standards: Tiered Aquatic Life Uses.
   EPA-822-R-05-001.
US Environmental Protection Agency (EPA). 2011. A Primer on Using Biological Assessments to
   Support Water Quality Management.  EPA 810-R-11-001. Washington, DC.
US Environmental Protection Agency (EPA). In review. A BCG Framework for Bioassessment of
   Estuaries and Coasts.
Vaughan TW. 1902. The Stony Corals of Porto Rico. Bulletin of the United States Fish Commission
   20:289-320.
Velazco-Domfnguez AT, Weil E and Bruckner A. 2003. Climate Change and Coral Bleaching in Puerto
   Rico: Efforts and Challenges. Presentation given  in  Oahu,  Hawaii.
 A-12  Workshop on Biological Integrity of Coral Reefs

-------
Vicente VP. 1990. Response of sponges with autotrophic endosymbionts during the coral-bleaching
   episode in Puerto Rico. Coral Reefs 8:199-202.
Vicente VP. 1992. A summary of ecological information on the seagrass beds of Puerto Rico. In:
   Coastal Plant Communities of Latin America, Seliger E. (Ed.). Academic Press, New York, pp.
   123-133.
Vicente VP and Goenaga C. 1984. Mass mortalities of the sea urchin Diadema antillarum (Philippi)
   in Puerto Rico. CEER- M-195:l-30.
Wagner DE, Kramer P and Woesik RV. 2010. Species composition, habitat, and water quality
   influence coral bleaching in southern Florida. Marine Ecology Progress Series 408:65-78.
Walker BK, Jordan 1KB and Spieler RE. 2009. Relationship of reef fish assemblages and topographic
   complexity on southeastern Florida coral reef habitats. Journal of Coastal Research 53:39-48.
Warne AG, Webb RMT and Larsen MC. 2005. Water, sediment, and nutrient discharge characteristics
   of rivers in Puerto Rico and their potential influence on coral reefs. USGS Science Investigative
   Report 2005-5206.
Warner GF, Smith SR, Jordan-Dahlgren E, Linton DM, Woodley JD, Alcolado  P, Bonaire K, Bone D,
   Buchan KC, Bush P, Cortes J, Croquer A, De Meyer K, Fernandez RG, Fonseca A, Garcia JR, Garcia-
   Parrado P, Garzon-Ferreira J, Gayle P, Gerace DT, Geraldes FX, Gunther J, Guppy R, Juman R,
   Koltes KH, Knobbe E,  Klein  E, Laydoo R, Losada F, Menendez G, Mow-Robinson JM, Ostrander G,
   Oxenford HA, Parker  C, Pors LPJJ, Perez D, Ramirez AR, Rodriguez R, Ruiz-Rentaria F, Ryan J,
   Tschirky JJ and Weil E. 2002. Status and temporal trends at CARICOMP coral reef sites.
   Proceedings of the 9th International Coral Reef Symposium, Bali, Indonesia, pp. 325-330.
Warren-Rhodes K, Sadovy Y and Cesar HSJ. 2003. Marine ecosystem appropriation in the Indo-
   Pacific: A case study of the live reef fish food trade. Ambio 32:481-488.
Weil E, Hernandez-Delgado EA, Bruckner AW, Ortiz AL, Nemeth M and Ruiz  H. (2003). Distribution
   and status of Acroporid coral (Scleractinia) populations in Puerto Rico. Proceedings of the
   Caribbean Workshop: Potential Application of the US Endangered Species Act (ESA) as a
   Conservation Strategy. NOAA-NMFS and NCORE-RSMAS.  University of Miami, pp. 71-92.
Weil E. 2005. Current Status of the Marine Biodiversity of Puerto Rico. In: Miloslavich P and Klein E.
   (Eds). Caribbean Marine Biodiversity: The known and unknown, pp. 85-109.  DEStech Publications
   Inc., Lancaster, PA, USA.
Weil E, Torres JL and Ashton M. 2005. Population characteristics of the black sea  urchin Diadema
   antillarum (Philippi) in La Parguera,  Puerto Rico, 17 years after the mass mortality event. Revista
   de Biologia Tropical 53:219-231.
Weil E, Croquer A and Urreiztieta I. 2009. Temporal variability and consequences of coral diseases
   and bleaching in La Parguera, Puerto Rico from 2003-2007. Caribbean Journal of Science
   45:221-246.
Weil E and Rogers CS. 2011. Coral reef disease in the Atlantic-Caribbean. In Z. Dubinski and N.
   Stambler. (Eds.). Coral Reefs: An Ecosystem in Transition.  Chapter 27.  pp. 465-492.
   Springer-Verlag.
Appendix A. References
A-13

-------
Wells JW. 1957. Scleractinia. In: Treatise on invertebrate paleontology. Part F. Coelentrata. Moore
   RC. (Ed.). Geological Society of America, Boulder, Colorado, pp. 328-444.
Wikipedia. 2013. Central Guanica. URL: http://en.wikipedia.org/wiki/CentraLGu%C3%A1nica.
Wilkinson C (Ed.). 2004. Status of coral reefs of the world: 2004. Vol.1. Townsville, Queensland,
   Australia: Australian Institute of Marine Science. 316pp.
Wilkinson CR. 1983. Net primary productivity in coral reef sponges. Science 219:410-412.
Wilkinson CR. 1996. Global change and coral reefs: Impacts on reefs, economies and human cultures.
   Global Change Biology 2:547-558.
Williams EH Jr. and Bunkley-Williams L. 1989. Bleaching of Caribbean coral reef symbionts in
   1987-1988. Proceedings of the 6th International Coral Reef Symposium 3:313-318.
Williams EH Jr. and Bunkley-Williams L. 1990. The world-wide coral reef bleaching cycle and related
   sources of coral mortality. Atoll Research Bulletin 335:1-71.
Williams EH Jr., Goenega C and Vicente V. 1987. Mass bleaching on Atlantic coral reefs. Science
   237:877-878.
Wilson HV. 1902. The sponges collected in Porto Rico in 1899 by the US Fish Commission 1900.
   Bulletin of the United States Fish Commission 20:375-411.
Yoder CO and DeShon JE. 2003. Using biological response signatures within a framework of multiple
   indicators to assess and diagnose causes and sources of impairments to aquatic assemblages in
   selected Ohio rivers and streams. In: Biological Response Signatures: Indicator Patterns Using
   Aquatic Communities. Simon TP. (Ed.). CRC Press, Boca Raton, FL. pp. 23-81.
Yoder CO and Rankin  ET. 1995a. Biological criteria program development and implementation in
   Ohio. In: Biological assessment and criteria: Tools for water resource planning and decision
   making. Davis WS and Simon TP. (Eds.). Lewis Publishers, Boca Raton, FL. pp.  109-144.
Yoder CO and Rankin  ET. 1995b. Biological response signatures and the area of degradation value:
   New tools for interpreting multimetric  data. In: Biological Assessment and Criteria: Tools for
   Water Resource Planning and Decision  Making. Davis WS and Simon TP. (Eds.). Lewis Publishers,
   Boca Raton, FL. pp. 236-286.
Yoshioka PM.  2009. Sediment transport and the distribution of shallow water gorgonians.  Caribbean
   Journal of Science 45:254-259.
Yoshioka PM and Yoshioka BB. 1989a. A multispecies, multiscale analysis of spatial pattern and its
   application to a shallow-water gorgonian community. Marine Ecological Progress Series
   54:257-264.
Yoshioka PM and Yoshioka BB. 1989b. Effects of wave energy, topographic relief and sediment
   transport on the distribution of shallow-water gorgonians  of Puerto Rico. Coral Reefs 8:145-152.
Zawada DG. 2011. Reef Topographic Complexity. In: Encyclopedia of Modern Coral Reefs: Structure,
   Form and Process.  Hopley D. (Ed.), pp. 902-906.
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Appendix B. Workshop Participants
 Mr. Aaron Hutchins
 The Nature Conservancy
 3052 Estate Little Princess
 Christiansted, St. Croix, VI 00820
 340-718-5575
 ahutchins@tnc.org

 Dr. Alberto Sabat
 University of Puerto Rico, Dept. of Biology
 P.O. Box 23360
 RioPiedras, PR 00931-3360
 787-764-0000 x2113
 amsabat@gmail.com

 Dr. Alina Szmant
 University of North Carolina, Wilmington
 Center for Marine Science
 5600 Marvin K. Moss Lane
 Wilmington, NC 28409
 910-962-2362
 szmanta@uncw.edu

 Ms. Antares Ramos Alvarez
 NOAA Office of Ocean and
 Coastal Resource Mgmt.
 654 Munoz Avenue, Suite 604
 San Juan, PR 00918
 787-766-5206 ext. 224
 Antares.ramos@noaa.gov

 Ms. Brandi Todd
 US EPA, Region 6
 1445 Ross Ave.
 Dallas, TX 75202
 214-665-2233
 todd.brandi@epa.gov

 Dr. David Ballantine
 University of Puerto Rico
 Department of Marine Sciences
 P.O. Box 9000
 Mayaguez, PR 00681-9013
 david.ballantine@upr.edu
Dr. David Cuevas
US EPA, Region 2
Caribbean Environ. Prot. Div.
City View Plaza II - Suite 7000
#48 RD. 165km 1.2
Guaynabo, PR 00968-8069
787-977-5856
cuevas.david@epa.gov

Dr. Deborah Santavy (Organizer)
US EPA, GED
1 Sabine Island Dr.
Gulf Breeze, FL 32561
850-934-9358
santavy.debbie@epa.gov

Mr. Ernesto Diaz
PR Department of Natural and Environment
   Resources (DNER)
Coastal Zone Management Director
P.O. Box 366147
San Juan, PR 00936
787-999-2200 x2729
ediaz@drna.gobierno.pr

Dr. Ernesto Weil
University of Puerto Rico,
Mayaguez Campus
P.O. Box 908
Lajas, PR 00667-0908
787-899-2048 x241, x272
eweil@caribe.net

Dr. Francisco Pagan
Caribbean Coral Reef Institute
University of Puerto Rico
Mayaguez, PR 00681-9013
Francisco.pagan@upr.edu

Mr. Hector Ruiz Torres
University of Puerto Rico
Department of Marine Sciences
Mayaguez, PR 00681-9013
787-691-7410
hectorruizt@me.com
Appendix
B.
Workshop
Participants
B-l

-------
Mr. Jeff Miller
Virgin Islands National Park
1300 Cruz Bay Creek
St. John, VI 00830
340-693-8950 x227
William J  Miller@nps.gov

Dr. Jeroen Gerritsen (Facilitator)
Aquatic Ecologist
Tetra Tech, Center for Ecological Sciences
400 Red Brook Blvd., Suite 200
Owings Mills, MD 21117
410-356-8993
jeroen.gerritsen@tetratech.com

Dr. Jorge Bauza
San Juan Bay Estuary Program
P.O. Box 9509
San Juan, PR 00908-9509
787-638-9979
jbauza@estuario.org

Dr. Loretta Roberson
University of Puerto Rico
College of Natural Sciences
Ponce de Leon Ave.
RioPiedras, PR 00931-3300
787-764-0000 xl-2713
Loretta.Roberson@gmail.com

Dr. Melanie McField
Smithsonian Institution
Director, Healthy Reefs for Healthy People
1755 Coney Dr.
Belize City, Belize, Central America
501-223-4898
mcfield@healthyreefs.org

Mr. Miguel Canals
PRDNER
Guanica State Forest
P.O. Box 1185
Guanica, PR 00653
787-821-5706
menqui@hotmail.com
Ms. Patricia Bradley (Organizer)
US EPA, AED
33 East Quay Road
Key West, FL 33040
305-809-4690
bradley.patricia@epa.gov

Dr. Paul Yoshioka
University of Puerto Rico
Department of Marine Sciences
Mayaguez, PR 00681-9000
Paul.yoshioka@upr.edu

Dr. Richard Appeldoorn
University of Puerto Rico
Department of Marine Sciences
Mayaguez, PR 00681-9013
787-899-2048x251
Richard.appeldoorn@upr.edu

Mr. Roberto Viqueira
Protectores de Cuencas
Guanica Coordinator
Box 673
Yauco, PR 00698
787-457-8803
rviqueira@hotmail.com

Dr. Tyler Smith
University of the Virgin Islands
#2 John Brewer's Bay
St. Thomas, VI 00802-9990
340-693-1394
tsmith@uvi.edu

Dr. Vance Vicente
Vicente and Associates, Inc.
Garden Hills Pz 1353 19
Guaynabo, PR 00966
787-781-6503
vance@prtc.net

Dr. William Fisher
US EPA, GED
ISabine Island Dr.
Gulf Breeze, FL 32561
850-934-9394
Fisher.william@epa.gov
B-2
Workshop on
Biological
Integrity
of Coral
Reefs

-------
Appendix C. Workshop Agenda
 (Workshop was compressed to two days due to Tropical Storm Isaac; times shown below are approximate)

Goal: To develop a conceptual, narrative model that describes how biological attributes of coral
reefs change along a gradient of increasing anthropogenic stress.

DAY 1 - Setting the Stage: A Visual Evaluation of Stations
9:00   Registration
9:30   Purpose of the Workshop
9:45   Introductions
       Purpose: Who is attending; organization they represent; what scientific expertise?
       Desired Outcomes: Relaxed atmosphere, prepare to work as a team.
10:00  Coral Reef Video Evaluations
       Purpose: Participants individually review coral reef videos, located throughout the 3 rooms in the
       conference center.
       Desired Outcomes: Every participant will have evaluated 8 videos.
12:00  Lunch
1:00   Complete Coral Reef Video Evaluations
       Purpose: Complete final 4 stations.
       Desired Outcomes: Participants have rated EPA stations and documented their rationale.
2:00   Break
2:15   Freshwater Stream and Estuarine Attributes
       Presenter: Jeroen Gerritsen (Brief introduction to the attributes developed for freshwater streams
       and estuaries).
       Purpose: Introduce the stream and estuarine attributes.
       Desired Outcomes: Understand where others have been and where we hope to go. Further explore
       the attribute  concept.
2:45   Presentation of Ratings and Discussion of Rationale
       Presenter: Debbie Santavy (ranked  stations)
       Purpose: Try to reach consensus on station assignments stating the  rationale for the decision.
       Desired Outcomes: Share rating of  stations; document criteria considered during selection and
       capture on flip charts.
Appendix C. Workshop Agenda
C-l

-------
4:30   Thresholds
       Presenter: Jeroen Gerritsen (management uses of BCG and how to move forward).
       Purpose: Establish preliminary thresholds for different levels of conceptual model.
       Desired Outcomes: What relative abundance of sessile invertebrates for each level: hard corals,
       sponges and gorgonians? What else defines each level? Fish, rugosity, other invertebrates? Any
       inclusion of water quality factors: both qualitative and quantitative.
5:15   Adjourn
DAY 2 - Biological Integrity
9:00   Biological Integrity Discussion
       Presenters: Debbie Santavy (results from coral reef video evaluations and attributes discussion);
       Experts (share their videos and photos that exhibit full biological integrity of a coral reef); Pat Bradley
       (reference condition); Pat Bradley (list of coral reef taxa).
       Purpose: Discuss biological integrity and reference condition.
10:30  Break
10:45  Reference Condition Discussion
       Desired Outcomes: Preliminary consensus on what the reference station should be. Begin to
       assemble the attributes.
12:30  Lunch
1:30   Using Data to Rank Stations
       Presenter: Debbie Santavy (overview of  EPA data).
       Purpose: Focus thinking about the attributes in breakout groups.
       Desired Outcomes: Begin thinking about levels of condition and lists of associated attributes.
3:00   Break
3:15   Attributes as Condition Changes
       Purpose: Begin to consider different levels of condition along a human disturbance gradient, using
       visual and data-derived attributes.
       Desired Outcomes: Begin to compile lists of both visual and data-derived attributes that are not
       station specific, but more overarching characteristics. Perhaps develop levels of attributes from data
       metrics to begin populating BCG framework.
5:00   Thank you and next steps
5:30   Adjourn
  C-2   Workshop on Biological Integrity of Coral Reefs

-------
Appendix D.
Tally Sheet - Rating Condition of Coral Reef Videos (1st)
                                    Name:
                             Ballot
Station
No.
1
2
3
4
5
6
7
8
Rating
(Good, Fair, Poor)








Rationale (indicate 3 most important
characteristics considered in ranking)








Appendix
D.
Tally
Sheet
(1
st)
D-l

-------

-------
Appendix E.
Tally Sheet - Rating Condition of Coral Reef Videos (2nd)
                                    Name:
                            Ballot
Station
No.
9
10
11
12
Rating
(Good, Fair, Poor)




Rationale (indicate 3 most important
characteristics considered in ranking)




Appendix
E.
Tally
Sheet -
(2nd)
E-l

-------

-------
Appendix F.
Notes Sheet - Rating Condition of Coral Reef Videos
Notes Sheet - Station 1                      Rating:  Good — Fair—Poor
                                               (Circle your condition rating)

Use this sheet to capture salient points about this station while viewing the video. You also have a
photo handout of key photos to assist you. The salient points should provide your rationale for
rating condition as good, fair or poor.
Appendix F.
Notes Sheet
F-l

-------

-------
Appendix G.
Supporting Photos - Rating Condition of Coral Reef Videos
The following pages show supporting photos for each station (1 page per station). The experts used
these as supplemental material to evaluate the videos.
Appendix
G.
Supporting
Photos
G-l

-------
Station 1
G-2
Workshop
on
Biological
Integrity
of
Coral
Reefs

-------
Station 2
Appendix
G.
Supporting
Photos
G-3

-------
Station 3
G-4
Workshop
on
Biological
Integrity
of
Coral
Reefs

-------
Station 4
Appendix
G.
Supporting
Photos
G-5

-------
Station 5
G-6
Workshop
on
Biological
Integrity
of
Coral
Reefs

-------
Station 6
Appendix
G.
Supporting
Photos
G-7

-------
Station 7
G-8
Workshop
on
Biological
Integrity
of
Coral
Reefs

-------
Station 8
Appendix
G.
Supporting
Photos
G-9

-------
Station 9
G-10
Workshop
on
Biological
Integrity
of
Coral
Reefs

-------
Station 10
Appendix
G.
Supporting
Photos
G-ll

-------
Station 11
G-12
Workshop
on
Biological
Integrity
of
Coral
Reefs

-------
Station 12
Appendix
G.
Supporting
Photos
G-13

-------

-------
Appendix H. Workshop Glossary
Attribute: Any measurable component of a biological system (Karr and Chu 1999).
Best attainable condition: A condition that is equivalent to the ecological condition of
(hypothetical) least disturbed stations where the best possible management practices are in use.
This condition can be determined using techniques such as historical reconstruction, best ecological
judgment and modeling, restoration experiments, or inference from data distributions.
Biological integrity: The ability of an aquatic ecosystem to support and maintain a balanced,
adaptive community of organisms having a species composition, diversity, and functional
organization comparable to that of natural habitats within a region.
Human disturbance: Human activity that alters the natural state and can occur at or across many
spatial and temporal scales.
Ecosystem-level functions: Processes performed by ecosystems, including, among other things,
primary and secondary production, respiration, nutrient cycling, and decomposition (EPA 2005).
Historical condition: The ecological condition at some previous point in history. Conditions
reflective of the historic time period may no longer exist in actual ecosystems in an area.
Least disturbed condition: The best available existing conditions with regard to physical, chemical,
and biological characteristics or attributes of a waterbody within a class or region. These waters
have the least amount of human disturbance in comparison to others within the waterbody class,
region or basin. Least disturbed conditions can be readily found but may depart significantly from
natural, undisturbed conditions or minimally disturbed conditions. Least disturbed condition may
change significantly over time as human  disturbances change (EPA 2005).
Minimally disturbed condition: The physical, chemical and biological conditions of a waterbody
with very limited or minimal human disturbance in comparison to others within the waterbody class
or region. Minimally disturbed conditions can change over time in response to natural processes
(EPA 2005).
Non-native species: Any species that is not naturally found in that ecosystem. Species introduced or
spread from one  region of the US to another outside their normal range  are non-native or non-
indigenous, as are species introduced from other continents (EPA 2005).
Reference condition: The  condition that approximates natural, unimpacted conditions (biological,
chemical, physical, etc.) for a waterbody. Reference condition (biological integrity) is best
determined by collecting measurements at a number of stations in a similar waterbody class or
region under undisturbed  or minimally disturbed conditions (by human activity), if they exist. Since
undisturbed or minimally disturbed conditions may be difficult or impossible to find, least disturbed
conditions combined with historical information, models or other methods, may be used to
approximate reference condition as long as the departure from natural or ideal is understood.
Reference condition is used as a  benchmark to determine how much other water bodies depart
from this condition due to human disturbance (EPA 2005).
Appendix
H.
Workshop
Glossary
H-l

-------
Reference station: A station selected for comparison with stations being assessed. The type of
stations selected and the type of comparative measures used will vary with the purpose of the
comparisons. For the purposes of assessing the ecological condition of stations, a reference station
is a specific locality on a waterbody that is undisturbed or minimally disturbed and is representative
of the expected ecological integrity of other localities on the same waterbody or nearby
waterbodies (EPA 2005).

Sensitive-rare taxa: Taxa that naturally occur in low numbers relative to total population density
but may make up large relative proportion of richness. May be ubiquitous in occurrence or may be
restricted to certain microhabitats, but because of low density recorded occurrence is dependent on
sample effort. Often stenothermic (having a narrow range of thermal tolerance) or cold-water
obligates, commonly k-strategists (populations maintained at a fairly constant level, slower
development, longer life-span), may have specialized food resource needs or feeding strategies.
Generally intolerant to significant alteration of the physical or chemical environment; are often the
first taxa observed to be lost from a community (EPA 2005).
Sensitive or regionally endemic taxa: Taxa with restricted, geographically isolated distribution
patterns (occurring only  in a locale as opposed to a region), often due to unique life history
requirements. May be long lived, late maturing, low fecundity, limited mobility or require
mutualistic relationships with  other species. May be listed as threatened, endangered or of special
concern species. Predictability of occurrence often low, therefore, requires  documented
observation. Recorded occurrence may be highly dependent on sample methods, station selection
and level of effort (EPA 2005).
Sensitive taxa: Taxa that are intolerant to a given anthropogenic stress, often the first species
affected by the specific stressor to which they are "sensitive" and the last to recover following
restoration (EPA 2005).
Taxa: A grouping of organisms given a formal taxonomic name such as species, genus, family, etc.
(EPA 2005).
Taxa of intermediate tolerance: Taxa that comprise a substantial portion of natural communities,
which may increase in number in waters which have moderately increased organic resources and
reduced competition,  but they are intolerant of excessive pollution loads  or habitat alteration.
These may be r-strategists (early colonizers with rapid turn-over times; boom/bust population
characteristics), eurythermal (having a broad thermal tolerance range), or have generalist or
facultative feeding strategies enabling them to utilize more diversified food types. They are readily
collected with conventional sample methods (EPA 2005).
Tolerant taxa: Taxa that comprise a low proportion of natural communities. Tolerant taxa often are
tolerant of a broader range of environmental conditions and are thus resistant to a variety of
pollution or habitat-induced stress. They may increase in number (sometimes greatly) in the
absence of competition. They are commonly r-strategists (early colonizers with rapid turn-over
times; boom/bust population characteristics), able to colonize when  stress conditions occur.
Last survivors (EPA 2005).
 H-2
Workshop on Biological Integrity of Coral Reefs

-------
Appendix I. Summary Data Results for BCG Stations

Table 1-1. Scleractinian coral summary statistics for BCG stations (Puerto Rico surveys in 2010
and 2011). Ave. 3D SA is average 3-dimensional surface area cm2/m2. SE=standard error of mean.
6
z
E
O
(5 "^
GQ (5?
1
2
3
4
5
6
7
8
9
10
11
12
e
CO
tin
rx o
uj Z
125
15
113
3
19
14
16
108
109
1
46
25
*Rugosity is the
bottom
Species
Richness
13
3
10
6
7
10
11
7
8
11
9
8
% Total
Abundance
11.61
2.68
8.93
5.36
6.25
8.93
9.82
6.25
8.04
9.82
8.04
7.14
linear ratio of 6m
No.
Colonies
51
4
79
21
31
54
73
71
87
70
44
95
divided
Shannon
Diversity Index
(H1)
2.040
1.040
1.657
1.234
1.261
1.793
1.971
1.512
1.410
1.784
1.827
1.469
Dy the taut
01
Q
3.40
0.16
3.16
0.84
1.24
3.6
4.87
4.73
5.80
2.8
1.16
3.8
CO
flj
^r* (N
£ E
O ^
Q 1
CO •«— •
6,560
185
9,518
2,706
18,228
5,359
14,210
19,637
20,080
11,026
11,635
9,199
CO
QJ
1"E
O ^
Q S
1,533
106
2,843
565
3,673
1,530
5,089
4,549
5,917
3,698
2,598
3,498
o
60
U.
2.18
1.12
1.52
1.52
1.54
1.71
1.83
1.48
1.88
1.48
1.12
1.25
linear distance of a 6m chain draped
o
60
UJ 3
to ce.
0.107
0.019
0.107
0.087
0.108
0.106
0.119
0.116
0.134
0.052
0.039
0.086
ja
60 — CO
B 11
(O ._ P
CC > 2.
poor/fair
poor (worst)
good (best)
poor
fair/poor
poor
fair
fair
fair
fair
fair
fair
60
'&
CO
ce.
"co
3
8
12
1
11
9
10
4
6
7
3
5
2









over the tops of corals and along the
Rugosity is a reef-scale indicator of reef contour or surface heterogeneity. See Appendix J for formulas.
Table 1-2. Gorgonian summary statistics for BCG stations (Puerto Rico surveys in 2010 and 2011).
Ave. 3D SA is average 3-dimensional surface area cm2/m2or per individual. Maximum number of
morphologies that can be
BCG Station
Station No. No.












1
2
3
4
5
6
7
8
9
10
11
12












125
15
113
3
19
14
16
108
109
1
46
25
present at one station is nine.
Morpho.
Richness3












4
0
7
0
0
6
8
2
4
2
7
8
No.
Individuals
21
0
24
0
0
27
37
6
7
10
52
86












Density Ave. 3D
#/m2 SAb/m2
4.2
0
4.8
0
0
5.4
7.4
1.2
1.4
2
10.4
17.2












5,154
0
30,346
0
0
38,352
33,342
86
11,229
17,649
26,954
58,558
Ave. 3D
SAc/ind
1,227
0
6,322
0
0
7,102
4,506
71
8,021
8,825
2,592
3,405


















a: Morphological shapes and regression equations for 3D surface estimation of an individual by morphology in
Santavy et al., 2012, pp. 36-38.
b: Ave. 3D SA/m2 = I Gorgonian surface area in transect area/total transect area
c: Ave.
3D SA/ind= I Gorgonian surface area in transect area/total # Gorgonians in transect. See Appendix J, Table J-2 for formulas
Appendix I. Summary Data Results for BCG Stations
1-1

-------
 Table 1-3. Sponge summary statistics for BCG stations (Puerto Rico surveys in 2010
 and 2011). Ave. 3D SA is average 3-dimensional surface area cm2/m2 or per individual.
 Maximum number of morphologies present at one station is eight.
BCG
Station No.
1
2
3
4
5
6
7
8
9
10
11
12
Station
No.
125
15
113
3
19
14
16
108
109
1
46
25
Morpho.
Richness3
3
3
1
2
1
2
0
0
3
5
3
5
No.
Individuals
22
20
5
7
5
8
0
0
7
33
21
28
Density
#/m2
4.4
4
1
1.4
1
1.6
0
0
1.4
6.6
4.2
5.6
Ave. 3D
SAb/m2
1,615
1,146
48
173
208
410
0
0
1,389
10,776
53,824
6,213
Ave. 3D
SAc/ind
367
286
48
124
208
256
0
0
992
1,633
12,815
1,110
 a: Morphological shapes and regression equations for 3D surface estimation of an individual by morphology in
   Santavy et al., 2012, pp. 36-38.
 b: Ave. 3D SA/m2 = I Sponge surface area in transect area/total transect area.
 c: Ave. 3D SA/ind= I Sponge surface area in transect area/total # Sponges in transect. See Appendix J, Table J-2 for formulas.
   I
   (0
        20
        15
        10
                               Density of sessile invertebrates no./m2
n Coral
DGorgonian
• Sponge
                               rfh  rm
              1234567
                                             Station no.
                                                       10     11     12
Figure 1-1. Comparison of the density of the major sessile invertebrates assessed in the 12 BCG
stations.
1-2
Workshop
on
Biolo;
l\ca\
Integrity
of Coral
Reefs

-------
350 -i

300 -
250 -

200 -
CM
E
=**:
150 -

100 -

50 -
n -




-J





in carnivores
• herbivores







1.13

11.34
ffi






0


-






51
n























5.45


0.75

—


—





















0.54
i r




















2.63
n

0.60
_ 0.22



. —

1.07



















r
—






03











1







0.27
^D
             1234567
                                          Station no.
                                                    10    11    12
Figure 1-2. Comparison of density for fish carnivores vs. herbivores at BCG stations. Number above
bar pairs is the ratio of carnivore/herbivore density.
                          Biomass of carnivores vs. herbivores
  D)
    25000 -i
    20000 -
    15000 -
in carnivores
• herbivores
                                                             0.24
                                     5.45
0000 -
5000 -
n -
0.17
3.01
^ rll
1.07
1

0.
0.67
• rid
15
0.
16

—


9
.23
n
1.
49
0.50
              12345678
                                          Station no.
                                                    10    11     12
   Figure 1-3. Comparison of biomass for fish carnivores vs. herbivores at BCG stations. Number
   above bar pairs is the ratio of carnivore/herbivore biomass.
Appendix
I.
Summary
Data
Results for
BCG
Stations
1-3

-------
                                 BCG Station 1

                          (Field Station 125_2010)

                         Coral Species Richness: 13

                   Photo rank and rating: 8, Poor/Fair

Table 1-4. BCG Station 1 data summary for corals and subgroups. See Appendix J for formulas used
and species abbreviations.
  Coral Parameters
                               All    Massive  Acroporid  Siderastrea   Forties
                             Species   Species    Species    siderea   astreoides
Colony density (#/m2)
Ave. 3D colony skeletal area (cm2)/colony
Ave. 3D colony skeletal area (cm2)/m2
Ave. 3D coral tissue area (cm2)/colony
Ave. 3D coral tissue area (cm2)/m2
Ave. 2D coral tissue area (cm2)/m2
3.40
2,146
7,297
1,929
6,560
1,533
0.53
2,462
1,313
2,284
1,218
228
0.13
20,077
2,677
16,446
2,193
198
0.13
417
56
417
56
54
0.73
435
319
435
319
16
          Cora! Species
                   Ssid
                   4%
                                      Gorgonian Morphs
                                              SWbr
                                              57%
        Mlam
         2%
            Mcom
             2%
                Mcav
                 14%
                            Sponge Morphs
                                                     mound
                                                      91%
Figure I -4. Percentages of stony coral species, gorgonian morphologies and sponge morphologies
for BCG Station 1.
  1-4
Workshop on Biological Integrity of Coral Reefs

-------
Table 1-5. Fish species found in BCG Station 1, with density and biomass for 100 m2 transect.
Fish Species
Ab udefduf saxa tills
Acanthurus coeruleus
Anisotremus surinamensis
Anisotremus virginicus
Caranx ruber
Gramma loreto
Haemulon flavolineatum
Halichoeres poeyi
Holacanthus bermudensis
Lut janus ana Us
Lutjanus a pod us
Microspathodon chrysurus
Ocyurus chrysurus
Ophioblennius macclurei
Pempheris schomburgkii
Scarus iseri
Sparisoma aurofrenatum
Sparisoma viride
Stegastes adustus
Thalassoma bifasciatum
Common Name
Sergeant Major
Blue Tang
Black Margate
Porkfish
Bar Jack
Fairy Basslet
French Grunt
Blackear Wrasse
Blue Angelfish
Mutton Snapper
Schoolmaster
Yellowtail Damselfish
Yellowtail Snapper
Redlip Blenny
Glassy Sweeper
Striped Parrotfish
Redband Parrotfish
Stoplight Parrotfish
Dusky Damselfish
Bluehead
Abundance/
100m2
2
5
1
1
1
3
1
1
1
1
1
5
8
3
1
2
1
3
49
55
Total Biomass
(g/100 m2)
90
167
1,274
9
17
1
40
5
11
637
215
174
242
12
33
15
40
3
510
198
Appendix
I.
Summary
Data
Results for
BCG
Stations
1-5

-------
                              BCG Station 2
                         (Field Station 15_2011)
                        Coral Species Richness: 3
               Photo rank and rating: 12, Poor (Worst)
 Table 1-6. BCG Station 2 data summary for corals and subgroups. See Appendix J for formulas
 used and species abbreviations.

Coral Parameters
Colony density (#/m2)
Ave. 3D colony skeletal area
Ave. 3D colony skeletal area
Ave. 3D coral tissue area (cm
Ave. 3D coral tissue area (cm
Ave. 2D coral tissue area (cm



(cm2)/colony
(cm2)/m2
2)/colony
2)/m2
2)/m2
All
Species
0.16
1,248
200
1,157
185
106
Massive
Species
0
0
0
0
0
0
Acroporid
Species
0
0
0
0
0
0
Siderastrea
siderea
0.08
980
78
822
66
37
Porites
astreoides
0
0
0
0
0
0
   Coral Species
Sponge Morphs
   Ssid
                           Sbou
                           25%
                                                             br. ropey
                                                               25%
                                                                mound
                                                                 10%
Figure 1-5. Percentages of stony coral species and sponge morphologies for BCG Station 2.
No gorgonians were present at BCG Station 2.
1-6
Workshop
on
Biolof
|ical
Integrity
of Coral
Reefs

-------
Table 1-7. Fish species found in BCG Station 2, with density and biomass for 100 m2 transect.
 Fish Species
Common Name
Abundance/
   100m2
Total Biomass
  (g/100 m2)
  Acanthurus bahianus
  Anisotremus virginicus
  Canthigaster rostrata
 Ocean Surgeonfish
 Porkfish
 Sharpnose Puffer
    10
     5
     1
    457
    220
       0
  Cephalopholis fulva
  Chaetodon capistratus
  Elacatinus saucrum
 Coney
 Foureye Butterflyfish
 Leopard Goby
     2
     7
     6
      68
     105
     298
  Haemulon flavolineatum
  Haemulon macrostomum
  Halichoeres poeyi
 French Grunt
 Spanish Grunt
 Blackear Wrasse
    10
     1
     1
    404
     40
     26
  Lachnolaimus maximus
  Mulloidichthys martinicus
  Ocyurus chrysurus
 Hogfish
 Yellow Goatfish
 Yellowtail Snapper
     1
     2
     7
      10
      81
    212
  Scarus iseri
  Stegastes adustus
  Stegastes diencaeus
 Striped Parrotfish
 Dusky Damselfish
 Longfin Damselfish
     1
     8
     4
      33
    496
    127
  Stegastes partitas
  Stegastes variabilis
 Bicolor Damselfish
 Cocoa Damselfish
     4
     5
       2
     49
Appendix
I.
Summary
Data
Results for
BCG
Stations
1-7

-------
                                 BCG Station 3

                          (Field Station 113_2011)

                         Coral Species Richness: 10
                  Photo rank and rating: 1, Good (Best)

Table 1-8. BCG Station 3 data summary for corals and subgroups. See Appendix J for formulas used
and species abbreviations.
 Coral Parameters
                              All    Massive   Acroporid  Siderastrea   Forties
                            Species  Species    Species    siderea   astreoides
Colony density (#/m2)
Ave. 3D colony skeletal area (cm2)/colony
Ave. 3D colony skeletal area (cm2)/m2
Ave. 3D coral tissue area (cm2)/colony
Ave. 3D coral tissue area (cm2)/m2
Ave. 2D coral tissue area (cm2)/m2
3.16
4,537
14,337
3,012
9,518
2,843
0.92
13,445
12,369
8,646
7,954
2,212
0
0
0
0
0
0
0.48
949
456
626
300
135
1.36
704
957
609
829
326
     Coral Species
                Aaga
          Ssid
          15%
             Ahum
              1% Dlab
                1% Male
                    3%
                       Mann
                        5%
Gorgonian Morphs

        SRunbr
          9%
                                       SRbush
                                        13%
     Past
     43%
fan 3D
' 13%
                                                                    plume
                                                                    13%
                                                               SRbr
                                                               44%
                         Sponge Morphs
                                               mound
                                               100%
Figure 1-6. Percentages of stony coral species, gorgonian morphologies and sponge morphologies
for BCG Station 3.
  1-8
Workshop on Biological Integrity of Coral Reefs

-------
Table 1-9. Fish species found in BCG Station 3, with density and biomass for 100 m2 transect.
Fish Species
Acanthurus bahianus
Acanthurus coeruleus
Canthigaster rostrata
Caranx ruber
Chaetodon capistratus
Coryphopterus glaucofraenum
Haemulon macrostomum
Halichoeres bivittatus
Hypoplectrus chlorurus
Lutjanus apodus
Microspathodon chrysurus
Scarus iseri
Serranus ti grin us
Sparisoma aurofrenatum
Sparisoma viride
Stegastes adustus
Stegastes partitas
Stegastes planifrons
Thalassoma bifasciatum
Common Name
Ocean Surgeonfish
Blue Tang
Sharpnose Puffer
Bar Jack
Foureye Butterflyfish
Bridled Goby
Spanish Grunt
Slippery Dick
Yellowtail Hamlet
Schoolmaster
Yellowtail Damselfish
Striped Parrotfish
Harlequin Bass
Redband Parrotfish
Stoplight Parrotfish
Dusky Damselfish
Bicolor Damselfish
Threespot Damselfish
Bluehead
Abundance/
100m2
1
9
2
2
1
15
1
5
3
2
2
51
1
5
6
30
4
2
21
Total Biomass
(g/100 m2)
46
638
14
34
15
10
242
574
43
431
324
5,749
7
482
979
360
32
13
106
Appendix
I.
Summary
Data
Results for
BCG
Stations
1-9

-------
                               BCG Station 4
                          (Field Station 3_2011)
                        Coral Species Richness: 6
                    Photo rank and rating: 11, Poor
 Table 1-10. BCG Station 4 data summary for corals and subgroups. See Appendix J for formulas
 used and species abbreviations.

Coral Parameters
Colony density (#/m2)
Ave. 3D colony skeletal area (cm2)/colony
Ave. 3D colony skeletal area (cm2)/m2
Ave. 3D coral tissue area (cm2)/colony
Ave. 3D coral tissue area (cm2)/m2
Ave. 2D coral tissue area (cm2)/m2
All
Species
0.84
4,251
3,571
3,221
2,706
565
Massive
Species
0.12
17,387
2,086
10,681
1,282
315
Acroporid
Species
0
0
0
0
0
0
Siderastrea
siderea
0
0
0
0
0
0
Porites
astreoides
0.04
157
6
141
6
4
Coral Species
         Ppor
          5%
                                         Sponge Morphs
                       Aaga
          Past
     Mfav
     14%
                             Ahum
                             5%
                                                          mound
                                                           25%
                               Mcom
                               62%
Figure 1-7. Percentages of stony coral species and sponge morphologies for BCG Station 4.
No gorgonians were present at BCG Station 4.
1-10
Workshop
on
Biolof
|ical
Integrity
of Coral
Reefs

-------
Table 1-11. Fish species found in BCG Station 4, with density and biomass for 100 m2 transect.
Fish Species
Acanthurus bahianus
Acanthurus chirurgus
Acanthurus coeruleus
Aulostomus maculatus
Canthigaster rostrata
Chaetodon capistratus
Decapterus macarellus
Gymnothorax sp.
Haemulon carbonarium
Haemulon chrysargyreum
Haemulon flavolineatum
Haemulon parr a
Halichoeres radio tus
Lutjanus apod us
Malacanthus plumieri
Microspathodon chrysurus
Odontoscion dentex
Rypticus saponaceus
Scarus iseri
Sparisoma aurofrenatum
Sparisoma rubripinne
Sparisoma viride
Stegastes adustus
Synodus intermedius
Thalassoma bifasciatum
Common Name
Ocean Surgeonfish
Doctorfish
Blue Tang
Trumpetfish
Sharpnose Puffer
Foureye Butterflyfish
Mackerel Scad
Moray Eel sp.
Caesar Grunt
Smallmouth Grunt
French Grunt
Sailors Choice
Puddingwife
Schoolmaster
Sand Tilefish
Yellowtail Damselfish
Reef Croaker
Greater Soapfish
Striped Parrotfish
Redband Parrotfish
Yellowtail Parrotfish
Stoplight Parrotfish
Dusky Damselfish
Sand Diver
Bluehead
Abundance/
100m2
1
6
5
1
1
1
2
1
5
5
5
1
1
9
13
8
1
1
10
3
1
1
33
1
3
Total Biomass
(g/100 m2)
129
629
1,081
256
7
15
395
3
1,024
475
609
404
168
2,193
318
1,296
21
82
1,119
580
401
314
384
339
31
Appendix
I.
Summary
Data
Results for
BCG
Stations
Ml

-------
                                BCG Station 5
                          (Field Station 19_2011)
                         Coral Species Richness: 7
                   Photo rank and rating: 9, Fair/Poor
Table 1-12. BCG Station 5 data summary for corals and subgroups. See Appendix J for formulas
used and species abbreviations.
 Coral Parameters
  All   Massive  Acroporid  Siderastrea   Forties
Species  Species   Species   siderea   astreoides
Colony density (#/m2)
Ave. 3D colony skeletal area (cm2)/colony
Ave. 3D colony skeletal area (cm2)/m2
Ave. 3D coral tissue area (cm2)/colony
Ave. 3D coral tissue area (cm2)/m2
Ave. 2D coral tissue area (cm2)/m2
1.24
23,116
28,664
14,700
18,228
3,673
0.2
5,030
1,006
2,950
590
71
0.8
34,248
27,399
21,764
17,411
3,526
0.08
520
42
520
42
16
0
0
0
0
0
0
    Coral Species
            Sponge Morphs
         Mfav
         10%
     Mcom
      3%
     Dstr
     3%
      Deli
      7%
                              mound
                               100%
Figure 1-8. Percentages of stony coral species and sponge morphologies for BCG Station 5.
No gorgonians were present at BCG Station 5.
1-12
Workshop
on
Biolof
|ical
Integrity
of Coral
Reefs

-------
Table 1-13. Fish species found in BCG Station 5, with density and biomass for 100 m2 transect.

Fish Species
Acanthurus bahianus
Acanthurus coeruleus
Anisotremus virginicus
Aulostomus maculatus
Bodianus rufus
Caranx ruber
Decapterus macarellus
Haemulon carbonarium
Haemulon chrysargyreum
Haemulon flavolineatum
Haemulon macrostomum
Heteropriacanthus cruentatus
Holocentrus adscensionis
Lutjanus apod us
Malacanthus plumieri
Microspathodon chrysurus
Mulloidichthys martinicus
Myripristis jacobus
Pempheris schomburgkii
Scarus iseri
Sparisoma aurofrenatum
Sparisoma viride
Stegastes adustus
Stegastes partitus
Thalassoma bifasciatum

Common Name
Ocean Surgeonfish
Blue Tang
Porkfish
Trumpetfish
Spanish Hogfish
Bar Jack
Mackerel Scad
Caesar Grunt
Smallmouth Grunt
French Grunt
Spanish Grunt
Glasseye Snapper
Squirrelfish
Schoolmaster
Sand Tilefish
Yellowtail Damselfish
Yellow Goatfish
Blackbar Soldierfish
Glassy Sweeper
Striped Parrotfish
Redband Parrotfish
Stoplight Parrotfish
Dusky Damselfish
Bicolor Damselfish
Bluehead
Abundance/
100m2
1
2
1
3
1
1
2
1
6
63
1
1
1
2
13
3
7
1
5
3
2
3
14
1
16
Total Biomass
(g/100 m2)
46
72
128
439
32
17
275
41
570
6,989
242
214
237
203
300
486
283
107
164
458
151
521
168
1
134
Appendix
I.
Summary
Data
Results for
BCG
Stations
1-13

-------
                                BCG Station 6

                          (Field Station  14_2010)

                         Coral Species Richness: 10
                     Photo rank and rating: 10, Poor

Table 1-14. BCG Station 6 data summary for corals and subgroups. See Appendix J for formulas
used and species abbreviations.

Coral Parameters
Colony density (#/m2)



Ave. 3D colony skeletal area (cm2)/colony
Ave. 3D colony skeletal area (cm2)/m2
Ave. 3D coral tissue area
Ave. 3D coral tissue area
Ave. 2D coral tissue area
(cm2)/colony
(cm2)/m2
(cm2)/m2
All
Species
3.6
5,431
19,552
1,489
5,359
1,530
Massive
Species
1.2
14,255
17,106
3,298
3,958
892
Acroporid
Species
0
0
0
0
0
0
Siderastrea
siderea
0.33
1,400
467
1,193
398
141
Porites
astreoides
1.4
466
653
443
621
330
     Coral Species   Aaga
               Unk 2%  Ahum
           Ssid   2%-) [  f 2%  Ma|c

           '     !•  j
       Ppor
       6%
                                     Gorgonian Morphs
                                        SWbush
                                         8%
fan 3D
 4%
                                                       fan
                                                       11%
                        Mcav
                        13%
                                       SRbr
                                       15%
                               Mfav
                               20%
                          Mmea
                          2%
                                                       plume
                                                        54%
                     Sponge Morphs
                     mound
                      67%
                                        br. ropey
                                          33%
Figure 1-9. Percentages of stony coral species, gorgonian morphologies and sponge morphologies
for BCG Station 6.
 1-14
Workshop on Biological Integrity of Coral Reefs

-------
Table 1-15. Fish species found in BCG Station 6, with density and biomass for 100 m2 transect.
Fish Species
Acanthurus bahianus
Acanthurus chirurgus
Chaetodon capistratus
Elacatinus genie
Epinephelus adscensionis
Halichoeres garnoti
Hypoplectrus chlorurus
Hypoplectrus puella
Lutjanus a pod us
Mulloidichthys martinicus
Ocyurus chrysurus
Scarus iseri
Sparisoma aurofrenatum
Sparisoma viride
Stegastes diencaeus
Stegastes leucostictus
Stegastes partitas
Stegastes planifrons
Thalassoma bifasciatum
Common Name
Ocean Surgeonfish
Doctorfish
Foureye Butterflyfish
Cleaning Goby
Rock Hind
Yellowhead Wrasse
Yellowtail Hamlet
Barred Hamlet
Schoolmaster
Yellow Goatfish
Yellowtail Snapper
Striped Parrotfish
Redband Parrotfish
Stoplight Parrotfish
Longfin Damselfish
Beaugregory
Bicolor Damselfish
Threespot Damselfish
Bluehead
Abundance/
100m2
1
1
4
1
1
2
1
1
1
2
1
36
5
11
3
4
7
12
12
Total Biomass
(g/100 m2)
129
121
60
0
174
195
19
19
649
472
177
632
466
1,606
36
31
24
229
55
Appendix
I.
Summary
Data
Results for
BCG
Stations
1-15

-------
                               BCG Station 7
                         (Field Station 16_2010)
                        Coral Species Richness: 11
                      Photo rank and rating: 4, Fair

Table 1-16. BCG Station 7 data summary for corals and subgroups. See Appendix J for formulas
used and species abbreviations.

Coral Parameters
Colony density (#/m2)
Ave. 3D colony skeletal area (cm2)/colony
Ave. 3D colony skeletal area (cm2)/m2
Ave. 3D coral tissue area (cm2)/colony
Ave. 3D coral tissue area (cm2)/m2
Ave. 2D coral tissue area (cm2)/m2
All
Species
4.87
3,529
17,173
2,920
14,210
5,089
Massive
Species
1.13
10,160
11,515
9,057
10,264
3,537
Acroporid
Species
0
0
0
0
0
0
Siderastrea
siderea
0.53
895
477
790
421
167
Porites
astreoides
1.53
567
870
469
720
303
    Coral Species
             Gorgonian Morphs
          Ssid
          11%
                Aaga
Deli 1%
DcyM%
Dsto 1%
                               Mcav
                                6%
                             Mfav
                             16%
SWbush
 14%
                                         SWbr
                                          13%
          SRunbr
            3%
            SRbush
             3%
                                              SRbr
                                              24%
fan 3D
 3%
                     plume
                      13%
Figure 1-10. Percentages of stony coral species and gorgonian morphologies for BCG Station 7.
No sponges were present at BCG Station 7.
1-16
Workshop
on
Biolof
|ical
Integrity
of Coral
Reefs

-------
Table 1-17. Fish species found in BCG Station 7, with density and biomass for 100 m2 transect.
 Fish Species
Common Name
Abundance/
   100m2
Total Biomass
  (g/100 m2)
 Acanthurus coeruleus
 Chaetodon striatus
 Chromis multilineata
Blue Tang
Banded Butterflyfish
Brown Chromis
     9
     2
    16
    414
    124
    126
 Haemulon aurolineatum
 Haemulon flavolineatum
 Holocentrus adscensionis
Tomtate
French Grunt
Squirrelfish
     3
     2
     2
     21
     81
    474
 Lutjanus apod us
 Microspathodon chrysurus
 Ocyurus chrysurus
Schoolmaster
Yellowtail Damselfish
Yellowtail Snapper
     1
    13
    10
    215
   1,133
    303
 Pomacanthus paru
 Scarus iseri
 Sparisoma aurofrenatum
French Angelfish
Striped Parrotfish
Redband Parrotfish
      1
    16
    17
    342
   1,515
    475
 Stegastes diencaeus
 Stegastes leucostictus
 Stegastes partitus
 Thalassoma bifasciatum
Longfin Damselfish
Beaugregory
Bicolor Damselfish
Bluehead
     8
     2
     3
    36
    294
     89
     31
    110
Appendix
I.
Summary
Data
Results for
BCG
Stations
1-17

-------
                               BCG Station 8
                         (Field Station 108_2010)
                        Coral Species Richness: 7
                      Photo rank and rating: 6, Fair
Table 1-18. BCG Station 8 data summary for corals and subgroups. See Appendix J for formulas
used and species abbreviations.

Coral Parameters
Colony density (#/m2)



Ave. 3D colony skeletal area (cm2)/colony
Ave. 3D colony skeletal area (cm2)/m2
Ave. 3D coral tissue area
Ave. 3D coral tissue area
Ave. 2D coral tissue area
(cm2)/colony
(cm2)/m2
(cm2)/m2
All
Species
4.73
4,938
23,372
4,149
19,637
4,549
Massive
Species
0.20
1,473
295
949
190
52
Acroporid
Species
1.47
14,658
21,499
12,274
18,002
3,964
Siderastrea
siderea
0.13
157
21
157
21
10
Porites
astreoides
1.93
258
499
239
462
273
     Coral Species
                Gorgonian Morphs
                Ssid
                                           SWbr
                                           50%
                              Deli
                              10%
             Mfav
             4%
Dstr
4%
Figure 1-11. Percentages of stony coral species and gorgonian morphologies for BCG Station 8.
No sponges were present at BCG Station 8.
1-18
Workshop
on
Bioloj
;ical
Integrity
of Coral
Reefs

-------
Table 1-19. Fish species found in BCG Station 8, with density and biomass for 100 m2 transect.
Fish Species
Abudefdufsaxatilis
Acanthurus bahianus
Acanthurus coeruleus
Aulostomus maculatus
Haemulon flavolineatum
Halichoeres bivittatus
Halichoeres maculipinna
Halichoeres radio tus
Lutjanus apod us
Microspathodon chrysurus
Ophioblennius macclurei
Pomacanthus paru
Scarus iseri
Sparisoma aurofrenatum
Sparisoma viride
Stegastes diencaeus
Stegastes partitas
Thalassoma bifasciatum
Common Name
Sergeant Major
Ocean Surgeonfish
Blue Tang
Trumpetfish
French Grunt
Slippery Dick
Clown Wrasse
Puddingwife
Schoolmaster
Yellowtail Damselfish
Redlip Blenny
French Angelfish
Striped Parrotfish
Redband Parrotfish
Stoplight Parrotfish
Longfin Damselfish
Bicolor Damselfish
Bluehead
Abundance/
100m2
3
3
31
1
1
4
6
1
4
28
1
1
69
4
2
54
6
98
Total Biomass
(g/100 m2)
99
386
1,479
130
111
182
24
0
341
961
4
156
4,592
332
326
603
3
331
Appendix
I.
Summary
Data
Results for
BCG
Stations
1-19

-------
                                BCG Station 9

                          (Field Station 109_2010)

                          Coral Species Richness: 9
                       Photo rank and rating: 7, Fair

Table 1-20. BCG Station 9 data summary for corals and subgroups. See Appendix J for formulas
used and species abbreviations.
Coral Parameters
     All    Massive  Acroporid  Siderastrea   Forties
   Species  Species   Species    siderea   astreoides
Colony density (#/m2)
Ave. 3D colony skeletal area (cm2)/colony
Ave. 3D colony skeletal area (cm2)/m2
Ave. 3D coral tissue area (cm2)/colony
Ave. 3D coral tissue area (cm2)/m2
Ave. 2D coral tissue area (cm2)/m2
5.80
9,091
52,731
3,462
20,080
5,917
3.47
8,102
28,088
4,040
14,006
4,015
0
0
0
0
0
0
0.53
806
430
734
391
213
0.67
781
521
739
493
298
      Coral Species
          Ssid
          9%
      Ppor
           Gorgonian Morphs
          SWbush
           20%
Mfav
60%
                                      SWbr
                                      20%
                       Sponge Morphs
                                               mound
                                                65%
Figure 1-12. Percentages of stony coral species, gorgonian morphologies and sponge
morphologies for BCG Station 9.
1-20
Workshop
on
Biolof
|ical
Integrity
of Coral
Reefs

-------
Table 1-21. Fish species found in BCG Station 9, with density and biomass for 100 m2 transect.
Fish Species
Ab udefduf saxatilis
Acanthurus bahianus
Acanthurus chirurgus
Acanthurus coeruleus
Anisotremus virginicus
Aulostomus maculatus
Cephalopholis cruentata
Chaetodon striatus
Coryphopterus glaucofraenum
Haemulon carbonarium
Haemulon plumierii
Halichoeres bivittatus
Holocentrus adscensionis
Hypoplectrus chlorurus
Lutjanus apod us
Microspathodon chrysurus
Mulloidichthys martinicus
Scarus iseri
Sparisoma aurofrenatum
Sparisoma viride
Stegastes diencaeus
Stegastes leucostictus
Stegastes partitus
Stegastes planifrons
Thalassoma bifasciatum
Common Name
Sergeant Major
Ocean Surgeonfish
Doctorfish
Blue Tang
Porkfish
Trumpetfish
Graysby
Banded Butterflyfish
Bridled Goby
Caesar Grunt
White Grunt
Slippery Dick
Squirrelfish
Yellowtail Hamlet
Schoolmaster
Yellowtail Damselfish
Yellow Goatfish
Striped Parrotfish
Redband Parrotfish
Stoplight Parrotfish
Longfin Damselfish
Beaugregory
Bicolor Damselfish
Threespot Damselfish
Bluehead
Abundance/
100m2
4
1
10
76
3
1
1
2
10
3
1
2
1
3
2
7
1
19
4
16
30
2
18
2
4
Total Biomass
(g/100 m2)
263
129
1,206
11,429
851
442
178
25
7
915
539
342
433
12
431
402
236
98
1,008
5,024
348
20
79
24
14
Appendix
I.
Summary
Data
Results for
BCG
Stations
1-21

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                                BCG Station 10
                            (Field Station 2011_1)
                         Coral Species Richness: 11
                       Photo rank and rating: 3, Fair

Table 1-22. BCG Station 10 data summary for corals and subgroups. See Appendix J for formulas
used and species abbreviations.
 Coral Parameters
                              All    Massive  Acroporid   Siderastrea    Porites
                             Species  Species   Species     siderea   astreoides
Colony density (#/m2)
Ave. 3D colony skeletal area (cm2)/colony
Ave. 3D colony skeletal area (cm2)/m2
Ave. 3D coral tissue area (cm2)/colony
Ave. 3D coral tissue area (cm2)/m2
Ave. 2D coral tissue area (cm2)/m2
2.8
7,205
20,174
3,938
11,026
3,698
1.88
10,095
18,979
5,549
10,432
3,496
0.04
9,503
380
0
0
0
0.08
3,662
293
1,405
112
50
0.4
794
317
640
256
94
     Coral Species
                   Aaga
               Ssid 2%
                                 Gorgonian Morphs
     Mfra
     3%
       Mfav
       14%
                      Mann
                      43%
                                             SWbr
                                             13%
                                                               plume
                                                                87%
                      Sponge Morphs
                                               br. ropey
                                                34%
                                          mound
                                           18%
Figure 1-13. Percentages of stony coral species, gorgonian morphologies and sponge morphologies
for BCG Station 10.
 1-22
Workshop on Biological Integrity of Coral Reefs

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Table 1-23. Fish species found in BCG Station 10, with density and biomass for 100 m2 transect.
 Fish Species
Common Name
Abundance/
  100m2
Total Biomass
 (g/100 m2)
Chaetodon capistratus
Decapterus macarellus
Haemulon flavolineatum
Hypoplectrus chlorurus
Malacanthus plumieri
Malacoctenus triangulatus
Odontoscion dentex
Pomacanthus paru
Scarus iseri
Sparisoma viride
Stegastes partitas
Stegastes planifrons
Foureye Butterflyfish
Mackerel Scad
French Grunt
Yellowtail Hamlet
Sand Tilefish
Saddled Blenny
Reef Croaker
French Angelfish
Striped Parrotfish
Stoplight Parrotfish
Bicolor Damselfish
Threespot Damselfish
2
4
22
2
1
4
14
2
6
15
3
96
30
250
2,441
24
24
1
804
2,161
45
789
2
1,982
Appendix
I.
Summary
Data
Results for
BCG
Stations
1-23

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                                BCG Station 11

                           (Field Station 46_2011)

                          Coral Species Richness: 9
                       Photo rank and rating: 5, Fair

Table 1-24. BCG Station 11 data summary for corals and subgroups. See Appendix J for formulas
used and species abbreviations.
Coral Parameters
                                 All    Massive Acroporid  Siderastrea  Forties
                               Species  Species   Species    siderea   astreoides
Colony density (#/m2)
Ave. 3D colony skeletal area (cm2)/colony
Ave. 3D colony skeletal area (cm2)/m2
Ave. 3D coral tissue area (cm2)/colony
Ave. 3D coral tissue area (cm2)/m2
Ave. 2D coral tissue area (cm2)/m2
1.76
8,236
14,495
6,610
11,635
2,598
0.16
639
102
495
79
41
0.60
21,258
12,755
16,902
10,141
2,187
0.20
1,210
242
491
98
44
0.60
422
253
363
218
96
Coral Species
                                      Gorgonian Morphs
                            Acer
                            21%
                                          SRunbr
                                            2%
                                                          fan 3D
                                                           2%  fan
                                       SRbush
                                        2%
                                Ahum
                                 2%
                                 Apal
                                 14%
                              Dstr
                              2%
                            Male
                      Mfav   5o/
                       9%

                      Sponge Morphs
                                                                 plume
                                                                  2%
                                                            SRbr
                                                            81%
                                               mound
                                                65%
Figure 1-14. Percentages of stony coral species, gorgonian morphologies and sponge morphologies
for BCG Station 11.
 1-24
   Workshop on Biological Integrity of Coral Reefs

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Table 1-25. Fish species found in BCG Station 11, with density and biomass for 100 m2 transect.
Fish Species
Acanthurus bahianus
Acanthurus coeruleus
Aulostomus maculatus
Caranx ruber
Cephalopholis cruentata
Chaetodon capistratus
Chaetodon striatus
Haemulon carbonarium
Haemulon chrysargyreum
Haemulon flavolineatum
Halichoeres garnoti
Halichoeres maculipinna
Halichoeres radiatus
Holocentrus rufus
Lutjanus apodus
Malacanthus plumieri
Microspathodon chrysurus
Myripristis jacobus
Scarus iseri
Sparisoma aurofrenatum
Stegastes adustus
Stegastes leucostictus
Stegastes partitus
Thalassoma bifasciatum
Common Name
Ocean Surgeonfish
Blue Tang
Trumpetfish
Bar Jack
Graysby
Foureye Butterflyfish
Banded Butterflyfish
Caesar Grunt
Smallmouth Grunt
French Grunt
Yellowhead Wrasse
Clown Wrasse
Puddingwife
Longspine Squirrelfish
Schoolmaster
Sand Tilefish
Yellowtail Damselfish
Blackbar Soldierfish
Striped Parrotfish
Redband Parrotfish
Dusky Damselfish
Beaugregory
Bicolor Damselfish
Bluehead
Abundance/
100m2
21
7
1
20
1
10
4
15
30
15
1
1
4
2
5
15
14
1
46
2
11
1
10
170
Total Biomass
(g/100 m2)
959
831
15
134
82
150
247
1,543
1,011
606
82
5
68
190
185
367
1,204
107
386
119
132
1
45
698
Appendix
I.
Summary
Data
Results for
BCG
Stations
1-25

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                                BCG Station 12

                           (Field Station 25_2011)

                          Coral Species Richness: 8
                       Photo rank and rating: 2, Fair

Table 1-26. BCG Station 12 data summary for corals and subgroups. See Appendix J for formulas
used and species abbreviations.
  Coral Parameters
  All    Massive  Acroporid  Siderastrea   Forties
Species  Species   Species    siderea  astreoides
Colony density (#/m2)
Ave. 3D colony skeletal area (cm2)/colony
Ave. 3D colony skeletal area (cm2)/m2
Ave. 3D coral tissue area (cm2)/colony
Ave. 3D coral tissue area (cm2)/m2
Ave. 2D coral tissue area (cm2)/m2
3.8
3,525
13,396
2,421
9,199
3,498
1.56
7,563
11,799
5,037
7,857
2,928
0
0
0
0
0
0
0.36
592
213
460
166
61
1.72
740
1,273
619
1,065
472
      Coral Species
                   Aaga
   Gorgonian Morphs
                              Mcav
                              22%
                                               SWbush
                                                 7%
     SWbr
     17%
plume
 14%
                                      SRunbr
                                        7%
                                        SRbush
                                         8%
                          SRbr
                          34%
                       Sponge Morphs
                                vase
                                 4%
                                                 br. ropey
                                                  50%
                          mound
                           11%
Figure 1-15. Percentages of stony coral species, gorgonian morphologies and sponge
morphologies for BCG Station 12.
1-26
Workshop
on
Biolof
|ical
Integrity
of Coral
Reefs

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Table 1-27. Fish species found in BCG Station 12, with density and biomass for 100 m2 transect.
 Fish Species
Common Name
Abundance/
   100m2
Total Biomass
  (g/100 m2)
 Acanthurus bahianus
 Acanthurus chirurgus
 Haemulon flavolineatum
Ocean Surgeonfish
Doctorfish
French Grunt
     2
     1
     3
      91
      44
    262
 Labrisomus nuchipinnis
 Lutjanus a pod us
 Myripristis jacobus
Hairy Blenny
Schoolmaster
Blackbar Soldierfish
                     33
                    101
                    107
 Scarus iseri
 Sparisoma aurofrenatum
 Sparisoma viride
 Stegastes adustus
Striped Parrotfish
Redband Parrotfish
Stoplight Parrotfish
Dusky Damselfish
     8
     6
     4
     1
      85
    247
    534
      12
Appendix
I.
Summary
Data
Results for
BCG
Stations
1-27

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Appendix J. Formulas Used for Calculating Condition Metrics
1. Stony Corals

Coral metrics
      Colony surface area
      Coral abundance
      Percent live tissue
      Live colony three-dimensional surface area
      Live colony two-dimensional surface area

Colony condition measurements
Every scleractinian coral within a 25 m2 transect area (25 m x 1 m) and greater than 10 cm was
identified to species. The maximum height and diameter of each colony was measured in cms, and
the percent of living coral tissue on the skeleton of the colony was estimated in 10% increments.
The percent tissue (living coral) was estimated for the entire colony in three dimensions, not only
from an aerial planar view. The observations and measurements made for each coral colony
included: scleractinian taxon, height (cm), maximum diameter (cm) and percent living colony tissue.

Formulas
Colony surface area (CSA) was the total three-dimensional colony surface area (cm2) including both
living and dead portions of a single coral colony.
             CSA = nr2 M
             r = [colony height (cm) + (colony diameter (cm)/2)] /2
             M = morphological conversion factor (values of 1, 2, 3, or 4 depending on coral
                species morphology), see Table J-l

Coral abundance (n) was total number of colonies in the entire transect area

% Live tissue (LT) was estimation of percent live tissue on a single coral colony over the entire
surface area. It was estimated for every coral colony in transect.

Live colony 3D surface area (LCSA_3D) was a calculated value for the total three-dimensional colony
surface area (cm2) of only living tissue on a single coral colony.

      LCSA_3D = CSA * (LT/100)
Live colony 2D surface area (LCSA_2D) was a calculated value for the total planar colony surface
area  (cm2) of living tissue on a single coral colony as though it were viewed from above. This
calculation assumes equal distribution of living tissue on a colony, which was initially recorded for
three dimensions rather than two. It approximates percent coral cover used as the standard in
many historical assessments.

      LCSA_2D = TT [colony diameter (cm)/2]2 * (LT/100)
Appendix J.
Formulas
Used
for Calculating
Condition
Metrics
J-l

-------
Coral metrics calculated for each BCG station
Ave. 3D colony skeletal area (cm2)/colony = I CSA/n
Ave. 3D colony skeletal area (cm2)/m2 = I CSA/area of transect
Ave. 3D coral tissue (live) area (cm2)/colony = I LCSA_3D/n
Ave. 3D coral tissue (live) area (cm2)/m2 = I LCSA_3D/area of transect
Ave. 2D coral tissue (live) area (cm2)/m2 = I LCSA_2D/area of transect

Table J-l. Stony corals included in Western Atlantic and Caribbean assessments (as provided by
Humann and DeLoach 2002) with the three-letter identification code and the morphological
conversion factor for calculating 3D surface area (Santavy et al. 2012).
Genus and Species
Acropora cervicornis
Acropora palmata
Acropora prolifera
Agaricia agaricites
Agaricia fragilis
Agaricia hum His
Agaricia lamarcki
Agaricia tenuifolia
Cladocora arbuscula
Colpophyllia natans
Dendrogyra cylindrus
Dichocoenia stokesii
Diploria clivosa1
Diploria labyrinthiformis
Diploria strigosa1
Eusmilia fastigiata
Favia fragum
Leptoseris cucullata
Isophyllastrea rigida
Isophyllia sinuosa
Madracis decactis
Madracis formosa
Madracis mirabilis
Madracis pharensis
Manicina areolata
Meandrina meandrites
Millepora complanata
Montastraea annularis2
Montastraea cavernosa
Montastraea faveolata2
ID Code
Acer
Apal
Apro
Aaga
Afra
Ahum
Alam
Aten
Carb
Cnat
Dcyl
Dsto
Deli
Dlab
Dstr
Efas
Ffra
Lcuc
Irig
Isin
Mdec
Mfor
Mmir
Mpha
Mare
Mmea
Mcom
Mann
Mcav
Mfav
Conversion Factor
4
4
4
1
1
1
1
3
2
2
3
2
2
2
2
3
2
1
2
2
3
3
3
1
2
2
3
3
2
2
J-2
Workshop
on
Biological
Integrity
of Coral
Reefs

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             Table J-l. (continued)
Genus and Species
Mussa angulosa
Mycetophyllia aliciae
Mycetophyllia danaana
Mycetophyllia ferox
Mycetophyllia lamarckiana
Oculina varicosa
Porites astreoides
Porites colonensis
Porites divaricata
Porites furcata
Porites porites
Siderastrea siderea
Solenastrea bournoni
Solenastrea hyades
Stephanocoenia intersepta
ID Code
Mang
Mali
Mdan
Mfer
Mlam
Ovar
Past
Pcol
Pdiv
Pfur
Ppor
Ssid
Sbou
Shya
Sint
Conversion Factor
2
1
1
1
1
3
2
1
3
3
3
2
2
3
2
         1: This report does not adopt the new classifications for Diploria sthgosa and Diploria clivosa as the
           original genus Pseudodiploria (Budd et al. 2012).
         2: This report does not adopt the new classification for the Montastraea annularis species-complex
           (Montastraea annularis, Montastraea faveolata and Montastraea franksi) which has been reclassified
           as the original genus Orbicella (Budd et al. 2012).
2. Rugosity

Rugosity measurement and metric
Rugosity was the linear ratio of a 6 m chain length compared to the taunt linear distance in
centimeters of a draped chain. Rugosity is a reef-scale indicator of reef contour. It was determined
using a chain-transect method that compares the length of a chain draped along the top of corals
and along the  bottom of the reef to the length of a taut line across the same linear distance using a
separate tape  measure, laid parallel but not on top of the transect tape. The linked chain was placed
such that it follows the relief of hard bottom substrate. The chain was placed on top of any hard
substrate encountered,  but not on top of gorgonians or sponges since only hard bottom rugosity
was being measured.

Formula
Rugosity was the ratio of the overall length of chain draped  over the reef contour divided by the
straight horizontal distance between the beginning and the  end of the chain. Therefore, if  6 m of
chain is laid out over a 4 m horizontal distance, the rugosity is 6/4 = 1.5 for that segment. Rugosity
will always be  > 1. Higher values relate to increased rugosity or reef relief. The average rugosity was
calculated per transect.
Appendix J.
Formulas Used for Calculating
Condition Metrics
J-3

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3. Fish

Fish metrics
       Abundance at lowest taxonomic level possible
       Length in cms
       Biomass offish in g/100 m2

Fish measurements
Fish contained within a 100 m2 transect area, 25 m length x 4 m width (height was water depth)
were recorded to the lowest taxonomic level possible. All fish greater than 3 cm in size were
included in the assessment. Each fish was scored as 5 cm size class increments up to 35 cm for fork
length  using visual estimation. If a fish was longer than 35 cm, an estimate of the actual fork length
was made. The fork length was measured from the fish snout (with mouth closed) to the fork at the
base of the tail or caudal fin. Observations and  measurements made for each fish included taxon
and size class.

Formulas
Abundance (n) was total number offish in the entire transect area
Density was the number of fish of a single taxon per 100 m2
Biomass (W) was the weight recorded as g/100 m2 of a single fish
       W = aLp
             L = fork length as midpoint between 5 cm increment class (e.g., 10-15 cm class using
                   12.5 as length in calculation). L > 35 cm uses actual length.

             a and 3 are species specific coefficients obtained from FishBase (www.fishbase.org)
                   for calculating fish biomass (see Appendix A in Santavy et al. 2013). Biomass
                   for species with no published length-weight relationships can be calculated
                   using terms for the closest congener based on morphology.


Fish metrics calculated for each BCG station

       Total biomass for each taxon per 100 m2 = £?=i W
J-4
Workshop
on
Biological
Integrity
of Coral
Reefs

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4. Gorgonians
Gorgonion metrics
       Density was the number of Individuals/m2

       Average three-dimensional surface area gorgonian/m2

       Average three-dimensional surface area gorgonian/individual

Gorgonian measurements
Every go rgonian > 10 cm (in any dimension) that falls within the quadrat was classified as one often
gorgonian morphologies (Table J-2). If the base of the gorgonian was in the quadrat, it was
considered  in the transect area. Colony height (greatest distance from substrate) and maximum
diameter (parallel to the substrate) were measured in cms. The observations and measurements
made for each individual were gorgonian colony shape, height and maximum diameter. Although
gorgonians  are prominent reef inhabitants, they are often excluded from monitoring programs. This
is partially because they are not widely recognized for their important functional contributions to
reef environments, and partially because taxonomic distinctions can be difficult. In this approach,
classification was based on morphology, categorized by predetermined shapes, which can be easier
to apply than taxonomy and still can influence their ecosystem functions.

Formulas and BCG station metrics
Abundance  (n) was total number of gorgonians in the entire transect area
Average three-dimensional surface area of each gorgonian morph/m2 =
                        n
                      I
     (regression equation for SA in Table J-2)
                 area of transect
Average three-dimensional surface area of each gorgonian morph/colony =
  n
I
                           (regression equation for SA in Table J — 2)
                                             n
Appendix J.
Formulas Used for Calculating
Condition Metrics
J-5

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Table J-2. Gorgonian morphological shapes, abbreviations, simulated model, in situ example
and regression models to estimate three-dimensional surface area (Santavy et al. 2013).
    Gorgonian
   Morphology
  Species Example
Simulated
  Model
in situ Example   Surface Area Estimations
Sea Fans
Planar (fan pi)
(Gorgonia
ventalina,
Leptogorgia)
Three-dimensional
(3D fan)
(Gorgonia
flabellum)

                                          \_
                             SA=0.68hi+0.66d-3.61
                                                                   SA=0.0113h3+106d-1190
Sea Rods            Unbranched (SR ub)
branch and          digitate form
branchlet diameter   (B"°reum)
> 15-<30  mm
                   Branched (SR br)
                   (Plexaura)
                   Bushy (SR bush)
                   (Eunicea fusca)
                   Planar (SR pi)
                   (Eunicea
                   tourneforti)
Sea Whips
branch and
branchlet diameter
>5-<15 mm
Branched (SW br)
(Pterogorgia)
                   Bushy (SW bush)
                   (Pterogorgia
                   guadalupensi)
                                                 SA=0.341d3+11.2h-127
                                                     SA=1.46d2+399
                                                    SA=0.0288h3+ 939
                                                     SA=76.4d-806
                              SA=-0.479h3+3.37h2-
                                  51.3h+354
                                                   SA=0.0672d3+1610
Sea Plumes
smallest branch
and branchlet
diameter usually
<5 mm
(Plume)
(Muriceopsis
flavida,
Pseudopterogorgia)
                                SA=4.77h-2990
Encrusting
Gorgonians
(Briareum,
Erythopodium)
 ft
                                    SA=dw
Minimum height (h) and diameter (d) of colony size required for use in the equations, h is the
maximum colony height measured in cm, d is the maximum colony diameter measured in cm.
J-6
Workshop on
Biological
Integrity
of Coral
Reefs

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5. Sponges

Sponge metrics
      Density was the number of Individuals/m2

      Average three-dimensional surface area of sponges/m2

      Average three-dimensional surface area of sponges/individual

Sponge measurements
Every sponge > 10 cm (in any dimension) falling within the quadrat was classified as one often
sponge morphologies (Table J-3). If the base of sponge was in the quadrat, it was considered in the
transect area. Colony height (greatest distance from substrate) and maximum diameter (parallel to
the substrate) were recorded in cms. The observations and measurements made for each sponge
were colony shape, height and maximum diameter. Although sponges are one of the most
prominent sessile invertebrates on coral reefs, they are often overlooked in monitoring programs.
This may be in part because sponge taxonomic classification is confounded by high diversity and
morphological plasticity. In this approach, classification was based on morphology rather than
taxonomy and can influence their ecosystem functions.

Formulas and BCG station metrics
Abundance (n) was total number of sponges in the entire transect area

Average three-dimensional surface area of each sponge morph/m2 =
                           (regression equation for SA in Table J-3)
                       ,-=1             area of transect
Average three-dimensional surface area of each sponge morph per individual =
Z
                           (regression equation for SA in Table J-3)
                                              n
Appendix J.
Formulas Used for Calculating
Condition Metrics
J-7

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Table J-3. Sponge morphological shapes, abbreviations, simulated model, in situ example and
regression models to estimate surface area (Santavy et al. 2013).
   Sponge
 Morphology
 Species Example
Simulated
  Model
 in situ
Example
Surface Area Estimations
Barrel
Vase
Xestospongia
muta,
Verongula
reiswigi
Callyspongia
plicifera,
Callyspongia
vaginalis
                                  SA=4.31d2+0.827h2+108
                                      SA=3.71h-161
Globe
Tube
Iricinia strobilina,
Spheciospongia
vesparium
Aplysina archeri,
Aplysina fistula ris
                                 SA=1.88h2 +0.0573d3+83.3
                                     SA=0.493cT+109
                                                 *   -..A-.
Mound
Rod
Bushy
Branched
Ropey
Encrusting
Oligoceras
hemorrhages,
Iricinia felix
Aplysina
cauliformis,
Niphates erecta
Aplysina fulva
lotrochota
birotulata
Amphimedon
compressa,
Chrondrilla
caribensis
                                   SA=30.0h+18.7d-193
                                   SA=7.69h+1.83d-33.5
                                 SA=0.462hi+0.834dN-19.3
                                   SA=18.8d+7.97h-132
                                          SA=dw
Minimum height (h) and diameter (d) of colony size required for use in the equations, h is the
maximum colony height measured in cm, d is the maximum colony diameter measured in cm.
J-8
Workshop on
Biological
Integrity
of Coral
Reefs

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