The Role of Threespot Damselfish (Stegastes Planifrons)

THE ROLE OF THREESPOT DAMSELFISH (STEGASTES PLANIFRONS)

AS A KEYSTONE SPECIES IN A BAHAMIAN PATCH REEF

A thesis presented to

the faculty of

the College of Arts and Sciences of Ohio University

In partial fulfillment

of the requirements for the degree

Masters of Science

Brooke A. Axline-Minotti

August 2003

This thesis entitled

THE ROLE OF THREESPOT DAMSELFISH (STEGASTES PLANIFRONS)

AS A KEYSTONE SPECIES IN A BAHAMIAN PATCH REEF

BROOKE A. AXLINE-MINOTTI

has been approved for

the Program of Environmental Studies

and the College of Arts and Sciences by

Molly R. Morris

Associate Professor of Biological Sciences

Leslie A. Flemming

Dean, College of Arts and Sciences

Axline-Minotti, Brooke A. M.S. August 2003. Environmental Studies

The Role of Threespot Damselfish (Stegastes planifrons) as a Keystone Species in a Bahamian Patch Reef. (76 pp.)

Director of Thesis: Molly R. Morris

Abstract

The purpose of this research is to identify the role of the threespot damselfish

(Stegastes planifrons) as a keystone species. Measurements from four functional groups

(algae, coral, fish, and a combined group of slow and sessile organisms) were made in various territories ranging from zero to three damselfish. Within territories containing damselfish, attack rates from the damselfish were also counted. Measures of both aggressive behavior and density of threespot damselfish were correlated with components of biodiversity in three of the four functional groups, suggesting that damselfish play an important role as a keystone species in this community. While damselfish density and measures of aggression were correlated, in some cases only density was correlated with a functional group, suggesting that damselfish influence their community through mechanisms other than behavior. Knowledge of the range in which a relative balance of biodiversity exists has potential for utilization in marine conservation.

Approved:

Molly R. Morris

Associate Professor of Biological Sciences

Dedication

This thesis is dedicated to my husband, my daughter, my mother, and my dogs.

Acknowledgments

I would like to thank Dr. Gene Mapes and Dr. Royal Mapes for introducing me to my future and Dr. Donald Miles for his help and patience with data analysis. I especially thank Dr. Molly Morris for the suggestions and encouragement that led to both this paper and fieldwork.

TABLE OF CONTENTS

Page

ABSTRACT 3

DEDICATION 4

ACKNOWLEDGMENTS 5

LIST OF TABLES 8

LIST OF FIGURES 9

I. INTRODUCTION 10 A. Importance of coral reefs 10 B. Intermediate Disturbance Hypothesis 10 C. Keystone species and their utilization 11 D. Damselfish as Keystone species 13

II. INFLUENCE OF DAMSELFISH ON CORAL REEF COMMUNITIES 14 A. Territories 14 B. Algae 15 C. Coral 22 D. Cryptofauna 28 E. Competitive Interactions 30 Damselfish 30 Herbivorous fish 32 Herbivorous urchins and seastars 35 F. Overview 36

III. MATERIALS AND METHODS 38 A. Study area 38 B. Experimental sites 39 C. Biodiversity 40 D. Aggression 43 E. Data analysis 44

IV. RESULTS 45

V. DISCUSSION 53 A. Functional groups 53 B. Biodiversity 58 C. Research applications 60 D. Direct conservation efforts at Three Sister’s Patch Reef 62

LITERATURE CITED 67

APPENDIX 76 A. Differences in coral reefs in different geographic regions 76

LIST OF TABLES

Table Page

2.1 A partial list of phyla and classes found inside damselfish algal mats 29 (derived from Lobel 1980).

3.1 Taxonomic variables in each functional group, method and 42 order of observation, as well as the study from which they were derived.

4.1 Mean measures of aggression level and aggression index, as well as mean 45 percent cover algae within each threespot density.

4.2 Mean aggression level and aggression index as well as mean percent cover 47 coral variables and total coverage within each threespot density. The symbol (l) denotes live coral and (d) denotes dead coral.

4.3 Results of the main effects on all functional groups and all taxa. Results in 52 bold indicate those that were found to be significant.

LIST OF FIGURES

Figure Page

3.1 Census plots on Three Sister’s Patch Reef. 40

4.1 Mean percent cover red, green filamentous, green branching, brown, and 46 total algae within each threespot population density.

4.2 The effects of mean aggression level at each threespot population density 48 on percent cover dead coral.

4.3 The effects of aggression index on percent cover live coral. 48

4.4 The effects of each threespot population density on mean percent cover 49 total coral.

4.5 The effects of aggression level on total percent cover of live and dead coral. 49

4.6 The effects of aggression index on total percent cover live and dead coral. 50

4.7 The affects of aggression index on the number of fish in each territory. 51

5.1 A comparison of the algae and coral functional groups at different 60 damselfish densities.

5.2 Marine Replenishment Zones and Scientific Monitoring Zones in Central 65 Andros National Park (Bahamas National Trust 2001).

I. INTRODUCTION

It is estimated that thirty percent of all coral reefs world-wide are in critical condition (Tuxill 1998) and seventy percent of reefs are under direct threat from human activities (Carlton et al. 1999).

A. Importance of coral reefs

Coral reefs are among the most biologically complex ecosystems known. Yet in recent decades, the coral reefs of the Bahamas, as elsewhere, have been damaged by habitat alteration, pollution, and other human activities. Coral reefs provide food, medicine, income, and an intangible richness to our lives; however, destruction of this habitat is increasing and is among the most deleterious of any known ecosystem.

Maintenance of species diversity and genetic variability are imperative in securing survival of these ecosystems. Biodiversity increases the probability that community members will respond differently to variable environmental conditions and perturbations, therefore reducing the risk of species and habitat extinction (Sole and Montoya 2001).

Deterioration in reef ecosystems create an urgent need for research and further understanding of natural interactions for implementation of effective management and rehabilitation plans.

B. Intermediate Disturbance Hypothesis

The intermediate disturbance hypothesis, originally formulated by Paine and

Vadas in 1969 and in large part by Connell in 1978, is described as “agents of physical disturbance or consumers at intermediate intensity enhance diversity by reducing competitive exclusion and preventing competitively superior species from attaining population sizes that are large enough to monopolize all of the limiting resources”

(Wootton, 1998 p. 803). Therefore, at intermediate disturbance, the community becomes

11 a mosaic of patches at various succession stages of regeneration, allowing for a full variety of species diversity (Ricklefs and Miller 2000). The intermediate disturbance hypothesis was later elaborated by Huston (1979) to include the concept that “rates of population growth and competitive displacement of the species in the community as well as the extent of disturbance in the community are the primary explanations for the existence of highly diverse communities” (Ricklefs and Miller 2000, p. 612). These studies have shown the imperative role of intermediate disturbance in developing community structure.

C. Keystone species and their utilization

A “keystone” is the pivotal block of stone that secures the structure of an archway: without the stone, the archway falls. A keystone species is a species whose presence is essential to the diversity of life for a given ecosystem (Sole and Montoya

2001). Within a habitat, each species depends on other species for survival and, in turn, contributes to the overall condition of the habitat. Plants provide essential nutrients and energy to browsing and grazing animals and, ultimately, to the carnivores that feed on these herbivores. While each species contributes to habitat operation, some species apparently do more than others. One particular species may provide essential services that are unique. Without the work of these key species, the habitat changes significantly.

When this keystone species disappears from its habitat, the environment changes causing loss of other resident species and, eventually, the intricate connections among the remaining residents begin to change dramatically.

Identification of keystone species and insight into their behavior is fundamental in understanding the complex interactions of the animals of coral reef ecosystems and the

12 ways in which these species can play a role in proper management. One family playing a fundamental role in maintenance of coral reef diversity is the aggressive damselfish

(Family Pomacentridae). Only limited research on the specific role of damselfish in small-scale disturbances has been done to the present in Bahamian reefs. The barrier reef on the east side of Andros Island, Bahamas offers a prime location for additional research on damselfish because it is the third longest barrier reef in the world (Lecard 2001), portions of this reef are currently being established as a division of Central Andros

National Park (Bahamas National Trust 2002). The study of damselfish in this region and identification of their role in structuring the surrounding reef ecosystem will ultimately contribute to marine resource conservation and management in Andros, as well as on other reef tracts in other parts of the Bahamas and the Caribbean. McCook (2002) presented research showing how community based Marine Protected Areas where fishing is excluded (called no-take-zones) may provide a sustainable supply of fish to adjacent reef areas. If damselfish demonstrate a favorable effect on community members, including commercially desirable species, areas where damselfish reside may then be considered ecologically significant areas and designated as no-take-zones, becoming nurseries for other species including commercially important taxa. This increased supply of commercially important fish species would be important to the people of Andros as well as to fisheries near more populated cities such as Nassau, the capitol of the

Bahamas, where a large stock is needed to feed tourists. In addition, specific patch reef areas with damselfish may wisely be designated no-take-zones because these patch reefs will act as corridors and stepping-stones for species that migrate between and among mangrove swamps, other patch reefs, and the barrier reef areas. Thus, preserving patches

13 of reef inhabited by damselfish could help preserve populations of these migrating species as well.

D. Damselfish as Keystone species

Damselfish have been termed keystone species because of their role in creating intermediate disturbances through maintenance and protection of their territories.

Research on this theory has been studied in areas throughout the world: the Caribbean,

Puerto Rico, the Pacific coast of Panama, Jamaica, Hawaii, and Australasia (Kaufman

1977, Williams 1980, Wellington 1982, Hinds and Ballantine 1987, Hixon and Brostoff

1983, 1996, Jones 1992, respectively). The position as a keystone species can be determined through the role they play in creating an intermediate disturbance effect through maintenance and aggressive protection of territories. In this paper I will discuss four primary aspects of community structure as they are impacted by behavior of the damselfish: 1) influences in algal community structure (Kaufman 1977, Williams 1980,

1981, Hixon and Brostoff 1983, 1996, Hixon 1996), 2) contributions to the abundance and distribution in coral communities (Wellington 1982), 3) provisions of refuge for juvenile invertebrates and demersal plankton (Wellington 1982), and 4) modification of grazing activities and distribution of other herbivorous organisms (Jones 1992). In addition, I will evaluate my own hypothesis which is the threespot damselfish (Stegastes planifrons) is a keystone species in a patch reef near Andros Island, Bahamas. Resolving this hypothesis and using similar studies of intermediate disturbance events and analysis of multitrophic level interactions will be useful in developing methods of reef management (Wootton 1998).

II. INFLUENCE OF DAMSELFISH ON CORAL REEF COMMUNITIES

A. Territories

Among Caribbean damselfish, only solitary damselfish defend territories.

Territories are roughly a meter in diameter (Kaplan 1982, Hixon 1996), are usually non- overlapping (Bay et al. 2001), and consist of a mass of living and dead coral from which the fish derives required resources: shelter from predators, a nest site (males only), and food from both a distinct mat of fleshy filamentous green algae (Robertson et al. 1981,

Hixon 1996) and invertebrate microfauna living within the mat (Lobel 1980, Hixon and

Brostoff 1983, Zeller 1988, Hixon 1996, Wilson and Bellwood 1997). Adults of both sexes maintain and defend these multi-purpose territories, termed damselfish “algal gardens” or “algal lawns,” within which they exclude browsing herbivores such as other damselfish (Family Pomacentridae), parrotfish (Family Scaridae), and sea urchins (Class

Echinoidea) (Hixon and Brostoff 1983, 1996, Kaufman 1977, Ogden and Lobel 1978) as well as potential competitors and egg predators (Robertson 1984, Hourigan 1986,

Cleveland 1999). Levels of aggression vary among genera and species (Robertson 1984,

Hourigan 1986, Cleveland 1999), however genus Stegastes is commonly recognized as highly territorial (Hourigan 1986, Cleveland 1999). Although many factors controlling the structure of tropical communities are poorly understood, damselfish territories may cover over 50% (Hixon 1996) to 60% (Wellington 1982) of shallow reef habitats; hence, the local effects on benthic community (Wellington 1982) and reef trophodynamics

(Klumpp and Polunin 1989) may be substantial. Specific mechanisms by which damselfish influence their community and create intermediate disturbance levels include intermediate feeding intensity and selectivity as well as “farming.” Farming behavior is

15 defined by Ceccarelli et al. (2001) to include all activities that promote the establishment and growth of algal crops such as: weeding, preparing substratum, fertilization and, importantly, herbivore exclusion. The following background text discusses the ways in which these behaviors influence different aspects of community structure in coral reef ecosystems.

B. Algae

Both present day ecological studies and paleontological considerations suggest that reef fishes are a primary force effecting community structure, especially herbivorous fish who account for large portions of the plant mass removed (Ogden and Lobel 1978,

Hatcher 1981, Sammarco 1983, Sale 1991, Sluka and Miller 2001). Herbivores comprise less than 25% of total fish species diversity and biomass (Ogden and Lobel 1978,

Meekan and Choat 1997). Their activities, however, control standing crops of many reef algae giving them high ecological importance relative to other trophic groups (Ceccareli et al. 2001). In areas where large herbivores have been excluded or removed through overfishing, macroalgae have been reported to overgrow reefs and reduce live coral cover

(Vine 1974, Brawley and Adey 1977, Montgomery 1980, Sammarco 1983, Hixon and

Brostoff 1983, 1996, Hixon 1996, Hay 1997). Algae provide much of the primary production at the base of the food chain as well as provide necessary reef building material (McCook 2002). Its abundance therefore directly affects both local diversity at primary and secondary trophic levels as well as the distribution of coral. Effects on coral distribution vary with different species of algae: encrusting coralline algae cements coral framework while other macroalgae destroys coral. Variations in algae species populations can therefore create overall varying results.

Territorial damselfish regulate grazing intensity of algal mats at a moderate level thereby creating intermediate disturbance effects. Moderate grazing decelerates succession of algae assemblages, prolonging a high-diversity of algae at mid-succession stage. These species provide a superior food source for the damselfish (Hixon 1996).

This moderate grazing also promotes algal species diversity and is an important factor in designating damselfish as a “keystone species” (Williams 1980, Hixon and Brostoff

1983, 1996, Hixon 1996). Regulated grazing intensity as well as other algal farming activities: selective feeding, weeding, and fertilization increase algal biomass and productivity in damselfish territories (Vine 1974, Brawley and Adey 1977, Potts 1977,

Ogden and Lobel 1978, Mahoney 1981, Sammarco and Carleton 1981, Sammarco 1983,

Hixon 1996). Behavioral mechanisms through which damselfish regulate grazing intensity as well as other algal farming methods are described below. Studies distinguishing between, and/or finding interrelatedness among the effects of intermediate herbivory and other farming behaviors that may also contribute to diversity are yet to be determined (Ceccarelli et al. 2001).

Survival and growth is largely dependent on availability of food. A primary objective of damselfish therefore is to establish territories with ample algae of high nutritional quality and palatability. Damselfish increase species productivity and thus the rates of energy flow available to them through characteristic feeding and algal farming behaviors. The cropping action, or intermediate feeding intensity of damselfish, keeps algae in a phase that maximizes growth rates, thereby assuring food supply (Lassuy 1980,

Montgomery 1980, Klumpp and Polunin 1989, Jones and Andrew 1990, Jones 1992,

Branch et al. 1992). This cropping mode of feeding is opposed to other fish grazers such

17 as parrotfish (Family Scaridae) that remove the algal holdfasts as well as part of the dead coral substratum with their modified jaws and teeth (Steneck 1988). This type of feeding is more destructive to the environment as it does not allow regrowth of the algae, whereas the cropping method of grazing by the damselfish allows and promotes regrowth. The biting method of other grazers also causes damage to the reef structure, aiding in bioerosion of the reef matrix (Hixon 1996). These behavior patterns of the damselfish contribute to the intermediate disturbance effect through nondestructive grazing. In areas where damselfish have been removed from territories and outside of the gardens, intense grazing is allowed, yielding a rapid reduction in biomass and diversity of algal assemblages (Hay 1981, Lewis 1986, Morrison 1988). Exposed areas compromise the competitive ability of nongrazer-resistant algal species and, thus, are not as diverse as territories where densities are kept below levels where resources may become limiting allowing the coexistence of many algae species to occur (Hixon 1996). Although areas of experimental fish exclusion (low feeding intensity) yield algal mats with a high biomass, they are ultimately less diverse because less competitive species are displaced by those with more rapid growth (Hixon and Brostoff 1983, 1996). These factors explain why areas of moderate grazing levels inside territories, a direct effect of moderate disturbance, allow for the highest diversity.

Another factor that contributes to high algal productivity inside territories is weeding. Weeding activities, or the discriminatory removal of low-productive or unwanted algae species, promotes new area for growth of more productive and/or preferred food algae such as filamentous or finely branched algae and non-coralline crusts (Lassuy 1980, Lobel 1980, Irvine 1980, Montgomery 1980, Klumpp et al. 1987,

Klumpp and Polunin 1989, Jones and Andrew 1990, Branch et al. 1992, Jones 1992).

The threespot damselfish (Stegastes planifrons) have been termed algal “farmers” because they maintain conspicuous mats of algae in their territories through processes such as weeding (Ceccarelli et al. 2001). Gardens of threespot damselfish (S. planifrons) are said to contribute 70-80% of the productivity of fore and back reefs at St. Croix in US

Virgin Islands (Brawley and Adey 1977). The act of preparing substratum to establish area for new algal growth also enhances the productivity of turf algae; although, it commonly involves killing coral (Potts 1977, Lobel 1980, Robertson et al. 1981,

Wellington 1982).

Damselfish territories may also indirectly affect nitrogen fixation on reefs.

Research on damselfish suggests that the increased nitrogen content in algal gardens is due to intentional damselfish defecation. This process recycles nutrients and fertilizes the algae thereby promoting a higher rate of productivity (Brawley and Adey 1977, Lobel

1980, Montgomery 1980, Klumpp et al. 1987, Polunin and Koike 1987, Polunin 1988,

Russ 1987, Branch et al. 1992, Hixon and Brostoff 1996, Ferreira et al. 1998). High levels of nitrogen may also be caused by an abundance of nitrogen-fixing blue-green algae (Cyanophyta), one of dominant algae groups in territories. Because nitrogen fixation promotes nutrient enrichment in the algae, damselfish may also be acting to increase reef nutrition (Brawley and Adey 1977, Lobel 1980, Klumpp et al. 1987).

Although some studies (Lobel 1980, Russ 1987) have found a positive correlation between damselfish gardens and an increase in blue-green algae, others (Montgomery

1980, Sammarco 1983) have found a negative correlation, favoring high blue-green algae populations outside territories, still others (Rutyer Van Steveninck 1984, Hixon and

Brostoff 1996) have found no difference in blue-green algae populations inside or outside territories. These discrepancies suggest possible regional differences in local distribution of blue-green algae (Hixon 1996).

Unlike the usual keystone species that enhance biodiversity by increasing predation intensity, damselfish increase biodiversity by decreasing predation and thus may better be described as “keystone species in reverse” (Hixon and Brostoff 1983).

Active exclusion of conspecifics and potential herbivore intruders regulates grazing intensity through intermediate disturbance effects which enhances algal productivity and diversity (Brawley and Adey 1977, Itzkowitz 1977, Lassuy 1980, Montgomery, 1980,

Hixon and Brostoff 1983, Sammarco 1983, Steneck 1988, Klumpp and Polunin 1989,

Jones and Andrew 1990, Itzkowitz and Slocum 1995, Hixon and Brostoff 1996). Feeding selectivity and territorial defense behaviors have been shown to account for an increase in algal productivity that is 47 times greater than surrounding turfs (Montgomery 1980).

Damselfish exhibit varied levels of aggression against different intruder species, these levels vary seasonally (Myberg and Thresher 1974) and with recent exposure to potential competitors (Eakin 1987). Similarity of food resources also correlates with intensity of aggression towards intruders (Myberg and Thresher 1974). In the Caribbean, well-kept algal mats attract other herbivores including destructive parrotfish that are capable of grazing at rates greater than 150,000 bites m2/d (Hixon 1996). Parrotfish (Family

Scaridae), as well as surgeonfish (Family Acanthuridae) and rabbitfish (Family

Siganidae), also contribute to the destruction of algal territories through the formation of dense aggregations (up to 10,000 individuals per ha) that overwhelm and denude territories (Hixon 1996). These families, Scaridae, Acanthuridae, and Siganidae

(Robertson et al. 1981, Hourigan 1986, Hixon 1996), as well as other damselfish (Family

Pomacentridae) (Eakin 1987) are most commonly attacked and excluded from territories.

This exclusion directly impacts the moderate disturbance effect created by damselfish. In a study by Myberg and Thresher (1974), conspecifics were attacked farthest from the center of the territory followed by congenerics and then other fish species. While larger damselfish are more capable of defending their territories, they must expend more effort

(Eakin 1987). Therefore, the extent of damselfish growth depends not only on the size and algal density of individual gardens, but also on the amount of energy lost in territory defense (Branch et al. 1992).

A grazing exclusion study conducted by Hixon and Brostoff (1983) in Hawaiian coral reefs examined algal successional patterns on dead coral surfaces subject to three levels of grazing exposure: within exclusion cages, within damselfish territories, and outside territories. Their results showed that in the caged areas the initial coverage was composed of filamentous green and brown algae, these were replaced by a high-diversity assemblage of mostly red filaments, and these were later replaced by a low diversity assemblage of coarsely branched species. Assemblages outside damselfish territories exposed to heavy grazing by herbivores (measured by bite rate densities) were composed initially of filaments but were quickly replaced by low-diversity grazer-resistant crustose species. Algal assemblages inside damselfish territories slowed and appeared to stop at a high-diversity midsuccesssional stage dominated by red filaments. After one year, algal diversity was highest in damselfish territories compared to the other exposure treatments

(Hixon and Brostoff 1983). A similar study by Sammarco (1983) showed that after 11-

12 months, algal species diversity was highest within territories of the lagoon damselfish

(Hemiglyphidodon plagiometopon) while diversity within cages and on substrate exposed to fish grazing were relatively low. Hinds and Ballantine (1987) also found that algal mats of the threespot damselfish (Stegastes planifrons) in Puerto Rico declined in diversity when caged, also suggesting the keystone species effect. These studies are important because they show that damselfish territories influence the standing crop, productivity, and community structure of coral reef algae. However, they do not prove that grazing at intermediate intensities is independent of other algal farming activities that also enhance algal biodiversity (Ceccarelli et al. 2001).

Even though most territorial damselfish maintain algal lawns of high species diversity, the giant blue damselfish (Microspathodon dorsalis) maintains low biomass, low-diversity monoculture mats through intense non-selective grazing (Montgomery

1980, Branch et al. 1992). Removal of these damselfish has led to an increase in territorial algal biomass indicating that some damselfish behavior is directed at maintaining an optimum biomass or state rather than a certain rate of productivity

(Ceccarelli et al. 2001).

It has already been stated that damselfish directly influence algae species diversity at the level of individual gardens (equivalent to α diversity) typically consisting of fast growing species such as finely branched or filamentous red or green algae and cyanophytes (Vine 1974, Montgomery 1980, Lassuy 1980, Sammarco 1983, Klumpp and

Polunin 1989, Branch et al. 1992). While these types of algae constitute a significant part of the overall species pool, they only represent a subset of the non-territorial pool.

Impacts by damselfish indirectly influence the overall heterogeneity of algal communities at larger spatial scales including zones in which the gardens occur (β diversity), and at

22 different zones or different depths (γ diversity) (Doherty 1983, Branch et al. 1992, Hixon and Brostoff 1996). By concentrating grazing in areas where they are less abundant, damselfish promote intense grazing outside their territories. This yields a rapid reduction in biomass and diversity in algal assemblages that are dominated by grazer-resistant algal crusts or turfs (Brawley and Adey 1977, Hay 1991, Sammarco 1983, Hixon and Brostoff

1983, Lewis 1986, Morrison 1988), filamentous cyanophytes (Sammarco, 1983), and other grazer resistant foliage algae such as Halimeda, Lobophora, and Dictyota species

(Branch et al. 1992). This action promotes development of more broad range of algae, including important coralline algae, by providing an opportunity for these species to achieve a sustainable population (Ogden and Lobel 1978, Branch et al. 1992). Because territorial damselfish occupy areas at a variety of spatial scales: among reefs at differing positions on the continental shelf (Williams 1982, Williams and Hatcher 1983), among habitats differing in wave exposure and topography (Robertson and Lassig 1980), and among zones within a habitat (Meekan et al. 1995), the variability in location and abundance of damselfish as well as variation in damselfish food preference and algal composition between reef zones contribute to the formation of a diverse range of algal species compositions.

C. Coral

The distribution and abundance of stony corals are influenced by many aspects of their physical environment, such as light, wave exposure, and sedimentation (Eakin 1987,

Wellington 1982); however, where coral growth is generally favored, coral species continuously compete for space. Common strategies used to eliminate neighboring coral include: extracoelenteric digestion of its tissues, direct overgrowth, and overtopping. The

23 results of these competitive interactions are often mediated by the effects of storms and predators: both of these activities open space for potential recruitment for less aggressive coral species (Kaufman 1977, Nybakken 2001).

Herbivores also contribute to the control of benthic community structure by mediating competition between fast growing benthic algae and slow-growing corals

(Sluka and Miller 2001). Regulation of the population of herbivores, therefore, becomes a factor in regulating algal growth. Fast-growing fleshy filamentous macroalgae, or turf algae, is competitively dominant for light and space over corals and their symbiotic zooxanthellae; therefore, herbivory promotes coral survival through reduction of competitive algae (Hatcher 1983). As previously stated, when herbivores are either removed from reefs or prevented from grazing by caging, coral is rapidly overgrown and killed by algae (Huston 1985, Hixon and Brostoff 1983, 1996). Conversely, heavy grazing can completely denude an area of both algae and coral (Nybakken 2001). Thus, because both large and small amounts of algae biomass on corals is unhealthy, intermediate amounts of grazing promote coral diversity through mediation of algal growth and, in turn, reduce interspecific contact and subsequent competition between coral colonies (Huston 1985). Through the process of territorial defense and nondestructive feeding intensity damselfish maintain territories at intermediate grazing frequencies and thus promote coral diversity and abundance (Sammarco and Carleton

1981, Sammarco and Williams 1982, Sammarco 1983, Huston 1985, Nybakken 2001).

Research and experimentation also show, however, that increased algal biomass due to maintenance of territories can negatively influence coral abundance (Kaufman 1977,

Robertson et al. 1981, Wellington 1982, Hixon 1996, Wood & Wood 2000).

Development of these positive and negative influences and their contributions to the distribution and community structure of hermatypic (stony) corals will be shown throughout this section.

The recruitment and survival of some coral species, particularly those which are rare in many areas, is generally higher in territories inhabited by damselfish, suggesting that rare species that would otherwise be damaged, benefit from the defense of damselfish against destructive grazers, such as parrotfish (Littler et al. 1989) and against coral eating species (Sammarco and Carleton 1981, Sammarco and Williams 1982,

Sammarco 1983, Huston 1985, Glynn and Colgan 1988, Nybakken 2001). The effect of increased representation of rare species increases coral diversity thereby influencing the role of coral patch formation and community structure (Sammarco and Williams 1982).

Research on coral recruitment and coral diversity by Sammarco and Carleton (1981) found that within their study site, 14% of the site area was comprised of territories of the lagoon damsel (Hemiglyphidodon plagiometapon). Further, within these territories, coral recruitment was five times greater than on substrate exposed to grazing. These figures suggest that 45% of coral recruitment in the area comes from territories maintained by this species of damselfish. In addition to coral recruitment, diversity of coral was higher inside territories than outside territories or within cages: a result consistent with the hypothesis that intermediate disturbance maintains high diversity via interference competition (Sammarco and Carleton 1981).

Exclusion of particular coral predators, such as the crown-of-thorns seastar

(Acanthaster planci), is especially effective in reducing coral mortality. The benefits of this specific exclusion are apparent during crown-of-thorns seastar (A. planci) outbreaks

25 on the Great Barrier Reef (Glynn and Colgan 1988) where the seastars not only kill large tracts of coral, but also increase the available substrata for algae growth, adversely effecting new coral growth (Hixon 1996). In the study by Glynn and Colgan (1988), damselfish maintain this exclusion through defensive actions against these seastars that include: nipping and removing spines and tube feet, lifting, carrying and removing, weak tail beating, and biting and rolling against the substrate (Glynn and Colgan 1988). This study also demonstrates that the seastar’s favorite prey, acroporid corals, are more abundant and diverse within damselfish territories and that coral species diversity index is also significantly higher inside these territories. Thus, damselfish territories increase the survivorship of preferred coral prey in Pacific reef communities during crown-of-thorns seastar (A. planci) outbreaks by providing protection of these populations within territories (Sammarco and Williams 1982, Glynn and Colgan 1988). Such exclusion practices also promotes coral patch diversity by increased growth potential as well as enhances recovery of corals in areas subject to high crown-of-thorns (A. planci) predation

(Glynn and Colgan 1988). These dynamics have also been confirmed by research on damselfish in other coral reef areas: Dick’s damsel (Plectroglyphidodon dickii) in

American Samoa, the dusky damselfish (Stegastes nigricans) in Tahiti, and the Acapulco major (S. acapulcoensis) in Panama, all of which defend hermatypic corals from crown- of-thorns seastar (A. planci) predation (Glynn and Colgan 1988).

Territorial defense benefits some corals due to the protection from destructive herbivores and corallivores (Wellington 1982, Glynn and Colgan 1988). However, the increased algal biomass of territories also negatively interferes with the survival, settlement and growth of hermatypic corals in addition to the growth of reef building

26 coralline algae through processes of algal overgrowth, increased sedimentation (Vine

1974, Potts 1977, Ogden and Lobel 1978, Lobel 1980, Sammarco et al. 1986), and bioerosion (Kaufmann 1977, Potts 1977, Lobel 1980, Risk and Sammarco 1982). Algal mat overgrowth causes the corals to expend energy cleaning their surface and, thus, exhausting metabolic reserves. This is particularly dangerous during periods of minimum nutrient availability and can cause coral death (Potts 1977). In an experiment by Potts

(1977), coral colonies that were not adversely affected by direct overtopping or smothering from the algae were damaged by the increased sedimentation in coral tissue.

Settlement of corals is adversely effected by damselfish through smothering of juvenile recruits by defended algal mats (Hixon 1996). The presence of these fast-growing algae mats within damselfish territories also causes both overgrowth and exclusion of crustose coralline algae, thus prohibiting cementation of loose fragments of rubble needed to strengthen coral framework (Lobel 1980). Intense herbivory is therefore important for the growth of reef building algae: decrease in fast-growing mat algae provides increased growth of coralline algae that is unpalatable to most herbivorous species (Hixon 1996).

In areas where corals and coralline algae are absent, substrata do not contain part of the developing coral reef framework; therefore, damselfish territories contribute to the distribution of the corals on the scale of individual territories and thus account for local- scale patchiness of coral distribution (Hixon 1996).

While territorial defense somewhat reduces bioerosion caused by the destructive scraping feeding modes of certain fish, such as scarids (parrotfish) (Sammarco et al.

1986), territories also aid in the erosion of the reef framework by promoting habitat for bioeroders. The creation of algal lawns increases biomass of erect algae and exposes

27 more of the reef’s surface as a substrate for various associated boring microfauna that harbor within damselfish algal mats. These boring microfauna, or cryptofauna, increase bioerosion of the coral framework and thus contribute to its degradation (Kaufman 1977,

Risk and Sammarco 1982, Sammarco et al. 1986, Letourneur et al. 1997, Hixon 1996).

In territories of the lagoon damsel (Hemiglyphidodon plagiometapon) on the Great

Barrier Reef, density of internal bioeroders increased by 22% in comparison to areas outside territories (Risk and Sammarco 1982).

A primary adverse behavior by damselfish on coral growth is created through preparation of substratum for algal mats. Damselfish kill portions of adult coral communities through the process of biting live polyp tissue at the edge of the colonies

(Kaufman 1977, Wellington 1982, Hixon 1996, Wood & Wood 2000). The degree to this effect on the coral varies by species of damslefish. The threespot damselfish (Stegastes planifrons) and the Acapulco major (S. acapulcoensis) establish algal lawns on two major live reef building corals in the Caribbean, boulder star coral (Montastrea annularis) and staghorn coral (Acropora cervicornis) (Robertson et al. 1981 and Wellington 1982 respectively). Conversely, the dusky farmerfish (Eupomacentrus dorsopunicans) and the beaugregory (E. leucostictus) less frequently establish territories on tracts of living coral

(Kaufman 1977).

Interactions between damselfish and corals fluctuate from positive to negative associations. These interactions directly influence the local-scale patchiness of coral

(Hixon 1996). In addition to this local-scale contribution to coral abundance and distribution, damselfish directly influence the vertical distribution of massive and branching corals. In general, damselfish prefer shallow water habitats due to the higher

28 topographic complexity and greater amount of shelter than in deeper areas (Wellington

1982). As previously mentioned, high damselfish densities increase mortality of massive corals through the removal of existing coral polyps (Kaufman 1977, Potts 1977, Lobel

1980, Robertson et al. 1981, Wellington 1982). This action facilitates the settlement of branching coral species, which are in turn used for shelter. The lack of topographic complexity in deeper water limits damselfish populations, thus allowing massive colonies to achieve greater abundance (Wellington 1982).

Given the evidence produced in these earlier studies, there can be no doubt that the damselfish dramatically affect the abundance and distribution of coral by influencing recruitment, survivorship, growth, and diversity. However, it appears that the specific role of damselfish in determining coral community structure depends on the dynamics of individual systems as well as the species of damselfish under scrutiny.

D. Cryptofauna

As previously stated, the increase in biomass of erect algae within damselfish territories and the increase in various associated bioeroders harbored within these mats weakens coral framework (Kaufman 1977, Risk and Sammarco 1982, Sammarco et al.

1986, Hixon 1996, Letourneur et al. 1997). Although in this aspect maintenance of algal mats is detrimental to the reef, in other aspects maintenance of algal mats is important to the survival and reproduction for these boring organisms as well as for other reef benthos seeking refuge within algal turfs. Turfs are described as a culture medium or refuge for some benthic organisms where they receive food, shelter, and protection (Lobel 1980,

Hixon and Brostoff 1983, Zeller 1988, Klumpp and Polunin 1989, Hixon and Brostoff

1996). Organisms known to have a greater abundance inside algal turfs include juvenile

29 invertebrates, cryptofauna, and a variety of epiphytes (Lobel 1980, Hixon and Brostoff

1983, Zeller 1988, Klumpp and Polunin 1989, Hixon and Brostoff 1996) such as diatoms

(Lobel 1980, Choat 1991), and bacteria (Lobel 1980, Choat 1991) (Table 2.1). In addition, the increased abundance and species richness of zooplanktonic foraminiferas inside territories has been directly linked to habitat structuring by damselfish. In a study by Hata and Nishihira (2002), damselfish territories composed of W. setacea, a tall, complicated algae with tangled rhizoids, trapped larger amounts of sediment which in turn provided foraminifera with a stable habitat of food and shelter. It was thereby concluded that habitat conditioning by damselfish maintains and enhances multi-species coexistence in coral reefs (Hata & Nishihira 2002).

Table 2.1. A partial list of phyla and classes found inside damselfish algal mats (derived from Lobel 1980).

Crustaceans Echinoderms Annelids Mollusks Coelentrates Platyhelminthes Amphipods Ophiuroids Polychaetes Gastropods Zoanthids Isopods Serpulids Crabs Oligochaetes Stomatopods

Some species of damselfish are not capable of utilizing most food algae, which allows for the growth of algal mats on their territories. Therefore, in addition to providing refuge for benthic invertebrates, the damselfish territories function to supplement protein in the damselfishe’s diet by enhancing the availability of animal prey, such as demersal plankton and other benthic invertebrates, harbored inside the algal mat

(Lobel 1980, Montgomery 1980, Irvine 1981). The analysis of gut contents from the lagoon damselfish (Hemiglyphidodon plagiometapon) (Wilson and Bellwood 1997) and the Australian gregory (Stegastes apicalis) (Zeller 1988) support this theory. Further

30 observation of the eating behavior from the threespot damselfish (Eupomacentrus planifrons) revealed that they ate selectively from the epiphytic layer of the mat, containing the most microorganisms (Lobel 1980).

E. Competitive Interactions

The competitive process of resource consumption is also fundamental in understanding reef community structure (Thresher 1983) and can be seen both intraspecifically (within family Pomacentridae) and interspecifically (among other herbivores) in Caribbean damselfish. Territorial damselfish consume 25-38% of their mat, resident cryptofauna consume 31% of the mat, and invading fish consume approximately 14% of the mat (Branch et al. 1992). Both herbivorous fish and predatory invertebrates such as sea urchins consume algae, and thus are competitors to herbivorous damselfish (Pennings 1997). These competitive grazers are excluded from their territories through active defense (Itzkowitz 1977, Sammarco and Williams 1982,

Sammarco 1983, Glynn and Colgan 1988). Larger grazing fish and potential egg predators are also excluded (Itzkowitz and Slocum 1995). Defense of feeding territories, a form of interference competition, can affect the local distribution of damselfish and other herbivorous fish, as well as invertebrates such as herbivorous urchins, all of which are described below.

Damselfish

Habitat partitioning in herbivorous damselfish appears to be determined by a combination of processes including habitat selection at settlement (Ohman et al. 1998,

Bay et al. 2001), developmental changes in habitat preferences (Ohman et al. 1998), adult habitat choice, and competitive interactions among adults (Sale 1979, 1991, Robertson

1984, 1996, Gutierrez 1998, Ceccarelli et al. 2001). Differences among habitat patches

(Williams and Sale 1981), specialization, and certain ecological requirements also play a

key part in the coexistence of damselfish, although this is not always the case (Robertson

and Lassig 1980, Waldner and Robertson 1980). Another case, interference competition,

often affects damselfish distribution. Aggressive dominant species of damselfish reduce

the abundance of adults and juveniles of other damselfish (Sale 1979, 1991, Robertson

1984, 1996, Williams and Sale 1981). Prior residence, age (Sale 1979) and size

differences (Danilowicz 1997), and species-species differences in aggressiveness appear

to be the most important factors determining the outcome of competitive interactions

between species for space (Robertson and Lassig 1980). A study by Sale (1979) in the

Great Barrier Reef showed that the recruitment of juvenile Ward’s damsel (P. wardi) as

well as the adult survival of this species were both greater in patches where adults from

other species of damselfish had been removed as compared to undisturbed patches.

These results suggest that Ward’s damsel (P. wardi) is outcompeted by more dominant

damselfish for the space within rubble patches (Sale 1979). Another similar study by

Robertson (1984) in the Great Barrier Reef found that some species of damselfish had

overlapping territories while others did not. Adult feeding areas of two smaller

damselfish species, the dusky damselfish (Stegastes dorsopunicans) and the threespot

damselfish (E. planifrons), did not overlap. However, feeding areas of adult giant blue damselfish (Microspathodon chrysurus), the largest in the family, were superimposed on feeding areas of adults and juveniles of the smaller damselfish species. Although in this case the larger and smaller damselfish species are considered cohabitants that defend their feeding areas against the same set of herbivorous fishes, the giant blue damselfish

32 was involved in defense actions much less frequently than either of its smaller cohabitants, suggesting that giant blue damselfish are dependents that use their size-based dominance ability to obtain food from their cohabitants (Waldner and Robertson 1980,

Robertson 1984). This aggressive behavior, as well as the results of juvenile dispersal, prevents damselfish from attaining large populations as well as contributes to the patchy spatial distribution of damselfish throughout suitable areas of resource consumption in the reef habitat (Sale 1991).

Herbivorous fish

As discussed previously, marine grazers have been shown to be a major factor impacting the benthic community structure of coral reefs (Ogden and Lobel 1978,

Hatcher 1981, Sammarco 1983, Sale 1991, Sluka and Miller 2001). Fish, as key grazers, affect community stability; extinction of large herbivores can lead to coextinction of many other species (Sole and Montoya 2001). Surgeonfishes (Family Acanthuridae), rabbitfishes (Family Siganidae), parrotfishes (Family Scaridae), and damselfishes

(Family Pomacentridae) are the predominant consumers of benthic algae as well as numerically, the most important families of herbivorous fishes on coral reefs (Choat

1991). These families, along with sea urchins, also have the greatest impact on algal community structure due to the denuding and scraping methods of eating behavior

(Steneck 1988). Feeding intensity of these herbivores, however, is not uniform along reef depths and is generally favored in shallow reef slopes where high relief coral contours allow herbivores to seek shelter from predators. Lower rates of herbivory are found in deep sand plains, lagoons, and reef flats that have lower relief coral contours (Hay 1991).

The heavily grazed area between high and low relief habitats forms a barren region or

“halo” (Ogden and Lobel 1978, Glynn 1990). In areas where grazing is generally

favored, damselfish competitors are both excluded from territories (Ohman et al. 1998,

Risk 1998) and left undisturbed (Gutierrez 1998).

Larger grazing fishes and potential egg predators are excluded from damselfish

gardens through territorial aggression; hence, territoriality from aggressive damselfish

affects the local distribution of these species (Thresher 1976, Brawley and Adey 1977,

Itzkowitz 1977, Lassuy 1980, Montgomery 1980, Hixon and Brostoff 1983, Sammarco

1983, Steneck 1988, Klumpp and Polunin 1989, Jones and Andrew 1990, Itzkowitz and

Slocum 1995, Hixon and Brostoff 1996). A correlation exists between interspecific

aggression and overlap in resource use (Bay et al. 2001). Therefore, aggressive behavior

is directed primarily towards herbivorous grazing fishes such as parrotfishes (Family

Scaridae), rabbitfishes (Family Siganidae), and surgeonfishes (Family Acanthuridae)

affecting their distribution (Robertson et al. 1981, Hourigan 1986), while carnivores are

generally ignored (Myberg and Thresher 1974, Potts 1977). Distribution of other fish

such as the ocean surgeonfish (Acanthurus bahianus) are effected by reduction the

settlement and post-settlement survival by presence of some species of damselfish, such

as the beaugregory damselfish (Stegastes leucostictus) (Risk 1998).

Because algal lawns are attractive to herbivorous organisms, many herbivores have developed behavior strategies that facilitate penetration into damselfish territories.

Herbivorous striped parrotfish (Scarus croicenis) penetrate the protected territories of damselfish through a behavior known as mass-marauding. This behavior is described as an “overpowering raid of fish into one algal lawn after another overwhelming each territorial damselfish and feeding on its algae.” Although one attack does not completely

34 destroy the algal lawn, a collapse of dead staghorn coral is often visible. Algal lawns of damselfish (Family Pomacentridae) and those of surgeonfishes (Family Acanthuridae) are attacked most frequently (Kaufman 1977). Marauding fish feed at higher rates and are attacked less than nonschooling, nonterritorials. Their actions also create a diversion allowing other teleost species, benthic browsing omnivores, and herbivores to feed on organisms disturbed by the feeding school without being subject to aggression from damselfish (Robertson et al. 1976). In addition, some species of wrasses (Family

Labridae) prey on the eggs of Caribbean damselfish by means of mass-marauding behavior (Kaufman 1977). This method of territory penetration may partially negate efforts of territorial defense demonstrated by the damselfish. The overall success of the mass-marauding depends on factors such as geographic zone in which the damselfish reside as well as the number of schooling fish in the area.

An interesting deviation in the behavior of damselfish occurs with the surgeonfish and some juvenile species enhancing multi-species coexistence in a shared space.

Damselfish and some species of territorial surgeonfishes (Acanthurus lineatus, and A. leucosternon) have similar diets, feeding therefore in the same areas. Although both families are considered competitors, the shared defense of territory imparts a metabolic advantage for each and prevents either damselfish or surgeonfishes from excluding the other (Robertson and Polunin 1981). Damselfish territories also function as important recruitment sites for some reef fishes despite their ecological role as adults. The dense algal mats offer recruiting fishes shelter from predation and food in the form of algae or small invertebrates (Ceccarelli et al. 2001). Some juvenile fish, labroid fishes and

35 parrotfish, are significantly more abundant in damselfish territories (Green 1992, 1996,

1998).

Herbivorous urchins and seastars

Within the past few decades, the long-spined sea urchin (Diadema antillarum) has received considerable attention in the Caribbean due to an epizootic die off in 1983. The long-spined sea urchin was a major herbivore in the Caribbean before the mass mortality of the species (93-99%) (Lesios 1988), caused by a waterborne pathogen first noted in

Panama and which subsequently spread throughout the Caribbean. The die off of these species has resulted in dramatic effects on the area, including the encouragement of a phase shift from a coral dominated to an algae dominated ecosystem (Brown 1997), the transition from sea urchins to fishes as dominant herbivores, and the decrease in populations of fishes that feed on these urchins (Hay 1984). Urchin recovery has been minimal since the die off (Sluka and Miller 2001).

Long-spined sea urchins (D. antillarum) are non-selective feeders and feed at higher rates than herbivorous fishes (Foster 1987); therefore, grazing from these urchins leads to communities with lower algal biomass than communities grazed by herbivorous fish (Carpenter 1986). This principle was supported by a caging experiment in a backreef area, and demonstrated that grazing by herbivorous fishes had a minor effect on algal biomass in comparison to grazing by D. antillarum (Foster 1987). Effects of grazing habits of sea urchins are seen through patterns of algae growth. Halos are found surrounding patch reef areas due to the migratory patterns of sea urchins that move between the coral heads during the day and the protective cover of the seagrass at night.

As they travel, urchins will graze on the way to each habitat. Due to the reduced effect of

36 algal biomass caused by the sea urchin, damselfish exclude many large herbivorous or predatory invertebrates from their territories through defensive action to protect remaining food supplies (Sammarco and Williams 1982, Eakin 1987, Glynn and Colgan

1988). Damselfish are known to expend massive effort defending their lawns from invading urchins. A damselfish was reported removing an urchin 195 cm out of its lawn by carrying in its mouth (Eakin 1987).

Threespot damselfish are responsible for stabilization of competitive interactions and a reduction of potential competitive exclusion of several urchin species (Williams

1980). In the Caribbean, the long-spined urchin (Diadema antillarum) and the reef urchin (Echinometra viridis) are treated as potential competitors and are attacked and excluded from territories of damselfish, including the threespot damselfish

(Eupomacentrus planifrons), (Williams 1979, 1980, 1981, Sammarco and Williams

1982). Although the threespot damselfish attacks both species of urchins, they are more tolerant of the reef urchin (Echinometra viridis) and thus contribute to the spatial partitioning of and coexistence of these urchin species (Branch et al. 1992). These behaviors of differential exclusion are factors primarily attributed to predatory keystone species, supporting damselfish in this role (Williams 1980).

F. Overview

Review of existing research shows that a common role of the various species of territorial damselfishes is their effect in influencing the distribution and abundance of algae, coral, cryptofauna, and other competitive species in their surrounding coral reef communities. Insights from previous studies illuminate the many ecological contributions of damselfish, and provide evidence for their role as “keystone species.”

While past studies have focused on a specific functional group, the designation of a species as “keystone” cannot be made without an overall analysis of integrated functional groups. My thesis objective is to not only synthesize existing data and analyses, but also to utilize this information in conjunction with my own study of the threespot damselfish

(Stegastes planifrons) at a specific patch reef near Andros Island to determine if this species functions as a keystone species in this coral reef community.

III. MATERIALS AND METHODS

To determine if the threespot damselfish (Stegastes planifrons), could be considered a keystone species in a patch reef near Andros Island, I measured the aggressive behavior of this fish at different population densities as well as surveyed four aspects of the community which served as a measure of biodiversity.

A. Study area

The profile of Caribbean barrier reefs is typically divided into three zones: fore reef, reef crest, and the back reef, which is sometimes called the shore zone. Three

Sister’s Patch Reef is located in the shore zone approximately halfway between Rat and

Calabash Cays at approximately 24°57.700N and 77°55.790W (Figure 3.1). This patch reef was chosen as the study location because of the abundance of the threespot damselfish (Stegastes planifrons): damselfish territories cover approximately 80% of the reef substratum (personal observation). Many of these territories are completely separated from each other while others apparently overlap. Water depth ranges from approximately two to three meters. A bed of seagrass surrounds the entire patch reef area. Because it is located in the shore zone, its waters are characteristically calm. The reef substratum is composed primarily of mounds of finger coral (Porites porites) and boulder star coral (Montastrea annularis) with sand between coral heads. This patch reef contains low levels of Microdictyon algal biomass, contrasting with the outlying barrier reef where Microdictyon appeared to cover 75% of the coral substratum (personal observation).

B. Experimental sites

Sampling was conducted between July 28, 2002 and August 9, 2002 to survey

Three Sister’s Patch Reef. Forty-nine sites were haphazardly chosen based on the relative populations of threespot damselfish (Stegastes planifrons). Nearly the entire patch reef was surveyed. Sixteen sites were assayed outside damselfish territories, eleven sites that had a threespot damselfish density of one, ten sites that had the overlapping area of two damselfish territories, and twelve sites that had the overlapping area of three damselfish territories. Sites of overlapping territories were specifically selected to investigate if damselfish density and the shared defense of territory contributed to a difference in biodiversity. All sites were circular in shape with a one-meter radius centered around what was observably the core of the territories (one to three depending on density). Sites were visually assayed for biodiversity and local territorial behavior by two observers using snorkel and mask. Specific locations were recorded using a Global

Positioning System (figure 3.1).

Figure 3.1 Census plots on Three Sister’s Patch Reef. The legend describes the density of threespot damselfish at each plot.

C. Biodiversity

Biodiversity was quantified within and outside damselfish territories by assessing the abundance of different taxonomic variables within four functional groups: algae, coral, fish, and a combined group of sessile and slow moving organisms. Observations of variables were combined into functional groups allowing for observation of patterns and insight into the processes and mechanisms governing them (Steneck 1988). These four functional groups were chosen based on previously published research concerning damselfish affects on community dynamics. Although the interactions of damselfish and microfauna are included in the primary literature, they were not examined in this experiment due to their small size and the extensive time that an assessment of their population would have entailed. Blue-green algae was not evaluated. Identifications of

41 taxonomic variables in each functional group were determined using the following texts:

Kaplan 1982, Littler et al. 1989, Alevizon 1994, Humann and Deloach 1993, and Wood

& Wood 2000. All variables were assessed at each previously described site and recorded onto underwater slates. Sites were randomly sampled for density during daylight hours to control for variation of time of day.

Visual estimation of each site was initially determined by holding a one-meter long PVC pipe at the estimated center to indicate the radius of the given area. The size of each study site (one meter radius) and the technique of visual estimation were chosen based on protocols from a coral reef biodiversity study done by Sluka and Miller (2001).

The following chart lists the four functional groups, which taxonomic variables were chosen to represent these groups, what order they were assessed in, how they were assessed, and from what study they were derived (Table 3.1). Variables in the fish functional group were assessed last to allow time for fish that were previously startled by observer presence to return to the area.

Table 3.1 Taxonomic variables in each functional group, method and order of observation, as well as study from which they were derived.

Taxonomic variables Order Method of assessment Study derived from first red algae percent cover estimated Brawley and Adey 1981, Foster 1987, Branch et al. 1992 green filamentous algae percent cover estimated Brawley and Adey 1981, Foster 1987, Branch et al. 1992 green branching algae percent cover estimated Brawley and Adey 1981, Foster 1987, Branch et al. 1992 brown algae percent cover estimated Brawley and Adey 1981 second encrusting coral percent cover estimated Kaufman 1977, Sammarco and Carleton 1981, Wellington branching coral (live and dead) percent cover estimated 1982 Kaufman 1977, Sammarco and Carleton 1981, Wellington massive coral (live and dead) percent cover estimated 1982 third sponges percent cover estimated echinoderms counted Potts 1977, Lobel 1980 polychaetes counted Lobel 1980 gorgonians counted fourth butterflyfish (F. Chaetodontidae) counted within a five minute period sugeonfish (F. Acanthuridae) counted within a five minute period Lobel 1980, Hourigan 1986 parrotfish (F. Scaridae) counted within a five minute period Robertson et al. 1979, Lobel 1980, Hourigan 1986 sergeant majors (F. Pomacentridae) counted within a five minute period Lobel 1980 all other fish counted within a five minute period

D. Aggression

Within each site occupied by damselfish, the degree of territorial defense was determined through focal-animal sampling (Altmann 1974). This observation period was conducted after the biodiversity census. One individual damselfish was observed at each site for five minutes, during which time the number of attacks and identification of attacked victims were recorded onto an underwater slate. Each damselfish was observed only one time. A five-minute period was chosen as the behavior time to avoid counting the same intruder multiple times. Juveniles were included in the study, as they displayed aggressive actions capable of chasing away intruders. Two attack behaviors, bites and charges, were used to quantify aggression. These measurements are similar to those used by Bay et al. (2001) in a study of damselfish behavior.

Aggression was analyzed in two ways: first, simply as aggression level, or raw number of attacks per five minute interval and, secondly, as aggression index, or measure of intensity determined by dividing attack rates into four different categories. These four categories were chosen based on the natural division of individual attack rates and were assigned as follows: zero attacks per five minutes designated aggression index zero, one through five attacks per five minutes designated aggression index one, six through ten attacks per five minutes designated aggression index two, and eleven or more attacks per five minutes designated aggression index three. Dividing aggression levels into four indexes was done for the purpose of testing a possible factor of whether a given range of aggression has more of an effect on biodiversity than individual attack rates.

E. Data analyses

To test the hypotheses that aggressive behavior and density of threespot damselfish influences biodiversity of coral reefs, two different types of analyses were performed using the statistical program JMP (SAS Institute 2002). Univariate analyses of variance (ANOVAs) were initially conducted to determine the effect of damselfish density on both aggression level and aggression index. Secondly, because the individual variables in each group could be correlated, multivariate analyses of variance

(MANOVAs) were conducted to determine if the main effects (damselfish density, aggression level, and aggression index) significantly correlated with variables in each functional group simultaneously. For each fixed factor significantly correlated to a functional group, univariate analyses of variance (ANOVAs) were then conducted to determine ways in which the fixed effect correlated to individual variables within the functional group. As total values are independent of individual variables, total values of algae cover, coral cover, and number of fish were tested univariately, separate from each

MANOVA procedure. MANOVAs were also performed to test if the combined pairwise interactions of density, aggression level, and aggression index significantly affected variables in individual functional groups. The resulting correlations between both aggressive behavior and threespot density and elements of biodiversity were then used both qualitatively and quantitatively to evaluate the interaction strengths of damselfish with their community members and thus speculate their status as a keystone species in patch reefs of the Bahamas.

IV. RESULTS

There was a significant effect of density of threespot damselfish on aggression level and aggression index (aggression level; F1, 46 = 19.03; P = 0.0001), (aggression index; F1, 46 = 44.79; P = 0.0001; Table 4.1). In addition, there were several significant effects of the main fixed variables (threespot density, aggression level, and aggression index) on functional groups as a whole as well as on individual variables within each functional group. Examinations of significant effects within each functional group

(algae, coral, fish and sessile or slow moving organisms) as well as the individual variables in each group are described below.

Despite the relationship between threespot density and both aggression level and aggression index, examination of combined pairs of density, aggression level, and aggression index and their effects on variables in each functional group revealed that only one MANOVA was significant: red algae coverage was significantly affected by the combined factors of density and aggression level (F1, 42 = 5.00; P = 0.0307), while there was no relationship between combined factors of density and either measure of aggression and all other variables measured (values ranged from F = 0.028 – 3.00; P =

0.091 - .840). This suggests that combined factors of density and aggression have less of an impact on variables in each group than each factor individually.

Table 4.1 Mean measures of aggression level and aggression index, as well as mean percent cover algae within each threespot density.

Threespot Aggression Aggression green green density Level Index red filamentous branching brown total 0 0 0.00 8.93 10.67 9.47 1.33 30.40 1 2.64 1.00 8.45 18.27 4.45 8.55 39.73 2 4.90 1.30 8.00 22.80 11.50 17.80 59.30 3 11.33 1.83 30.7 27.00 7.17 7.83 70.17

To test the influences from the three main effects (threespot density, aggression

level, and aggression index) on the algae functional group as well as on individual

variables in this group, a series of univariate ANOVAs were performed (Table 4.3). Of

the main effects, only threespot density had an overall affect on the algae functional

group (F4,41 = 6.53; P = 0.0004). Specific variables within the algae functional group that

were found to be significantly correlated to threespot density were red algae coverage (F1,

44 = 12.98; P = 0.0008) and green filamentous algae coverage (F1, 44 = 7.60; P = 0.0085).

Total algae coverage was also significantly correlated to threespot density (F1, 46 = 21.47;

P = 0.0001; Figure 4.1). Although the mean percent cover of both green branching and

brown algae were consistently less than mean percent cover green filamentous algae

(Table 4.1), neither green branching nor brown algae variables were significantly

correlated to any of the main fixed variables.

100 90 80 70 red 60 gr filamentous 50 gr branching 40 30 brown 20 total 10 Average Percent Cover Algae 0 0123 Three-spot Population Density

Figure 4.1 Mean percent cover red, green filamentous, green branching, brown, and total algae within each threespot population density.

Overall variation in the coral functional group was significantly effected by each of the three main effects: threespot density (F5,42 = 3.01; P = 0.021), aggression level

(F5,42 = 3.46; P = 0.01), and aggression index (F5,42 = 3.57; P = 0.009). However, univariate analyses also revealed that only few of the individual variables within the coral functional group were significantly effected by the main effects. Percent cover encrusting coral, live massive coral, and dead branching coral were not influenced by the main effects. However, percent cover of dead massive coral was significantly correlated to aggression level (F1, 46 = 5.83; P = 0.0197; Figure 4.2; Table 4.2), and percent cover live branching coral was significantly correlated to aggression index (F1, 46 = 5.52; P =

0.0232; Figure 4.3; Table 4.2).

Table 4.2 Mean aggression level and aggression index as well as mean percent cover coral variables and total coverage within each threespot density. The symbol (l) denotes live coral and (d) denotes dead coral.

Threespot Aggression Aggression Encrusting Massive density level index coral (l) coral (l) 0.0 0.0 0.0 10.7 8.7 1.0 2.6 1.0 2.1 17.3 2.0 4.9 1.3 2.5 20.5 3.0 11.3 1.8 2.9 1.7 Branching Massive Branching Total coral (l) coral (d) coral (d) Total (l) (d) 29.0 28.3 19.3 48.3 47.7 9.9 33.6 34.5 29.3 68.2 3.5 45.5 17.7 26.5 63.2 13.1 36.7 33.3 17.7 70.0

90 80 70 60 50 dead massive coral 40 dead branching coral 30 20 10 0

Mean Percent Cover Dead Coral 0 2.6 5.0 11.7 Mean Aggression Level at Each Population Density

Figure 4.2 The effects of mean aggression level at each threespot population density (0,1,2,3) on percent cover dead coral.

50 live encrusting coral 40 live braching coral

30 live massive coral total live coral 20

10 Mean Percent Cover Live Coral 0 0123 Aggression Index

Figure 4.3 The effects of aggression index on percent cover live coral.

Total amount of live coral cover was significantly effected by all three main effects: threespot density (F1, 46 = 11.25; P = 0.0016; Figure 4.4), aggression level (F1, 46 =

7.41; P = 0.0091; Figure 4.5), and aggression index (F1, 46 = 13.20; P = 0.0007; Figure

4.6). Additionally, total amount of dead coral cover was significantly affected by

aggression level (F1, 46 = 4.95; P = 0.031; Figure 4.5) and aggression index (F1, 46 = 6.42;

P = 0.014; Figure 4.6).

120

100

80 total live coral 60 total dead coral 40

20 Mean Percent Cover Coral 0 0123 Three-spot Population Density

Figure 4.4 The effects of each threespot population density on mean percent cover total coral.

120

100

60 total live coral total dead coral 40

20 Mean Percent Cover Coral 0 0 2.6 5.0 11.7 Mean Aggression Level at Each Density

Figure 4.5 The effects of aggression level on total percent cover of live and dead coral.

120

100

80 total live coral 60 total dead coral 40

20 Mean Percent Cover Algae

0 0123 Aggression Index

Figure 4.6 The effects of aggression index on total percent cover live and dead coral.

Although both aggression level (F5,41 = 2.40; P = 0.05) and aggression index

(F5,41 = 3.56; P = 0.009) had overall affects on the fish functional group as a unit, density did not correlate with either the functional group or the individual variables of this functional group. Both aggression level (F5,41 = 5.15; P = 0.028) and aggression index

(F1, 45 = 6.53; P = 0.0141) explained a significant amount of variation on the number

sergeant majors. Aggression index also had a significant effect on the number of

auxiliary fish (F1, 45 = 8.18; P = 0.0064), as well as the total number fish (F1, 46 = 4.73; P

= 0.0348; Figure 4.7).

Finally, none of the main effects were correlated to any of the variables found in

the slow moving or sessile functional group (Table 4.3).

35 butterflyfish 30 surgeonfish 25 parrotfish sergeant majors 20 all other fish 15 total fish

Number Fish in Territory 10

0 0123 Aggression Index

Figure 4.7 The affects of aggression index on the number of fish in each territory.

Table 4.3 Results of the main effects on all functional groups and all taxa. Results in bold indicate those that were found to be significant.

FUNCTIONAL GROUP density aggression level aggression index

ALGAE F4,41 = 6.53; P = 0.0004 F4,41 = 1.14; P = 0.353 F4,41 = 1.15; P = 0.347

red F1, 44 = 13.0; P = 0.0008 F1, 44 = 3.66; P = 0.062 F1, 44 = 3.10; P = 0.085

green branching F1, 44 = 0.016; P = 0.90 F1, 44 = 0.72; P = 0.402 F1, 44 = 0.284; P = 0.60

green filamentous F1, 44 = 7.60; P 0.0085 F1, 44 =0.35; P = 0.852 F1, 44 = 1.24; P = 0.27

brown F1, 44 = 1.98; P = 1.66 F1, 44 = 0.29; P = 0.59 F1, 44 = 0.43; P = 0.52

total F1, 46 = 21.5; P = 0.0001 F1, 46 =0.34; P = 0.57 F1, 46 = 3.03; P = 0.089

CORAL F5,42 = 3.01; P = 0.021 F5,42 = 3.46; P = 0.01 F5,42 = 3.57; P = 0.009

encrusting F1, 46 = 3.06; P = 0.086 F1, 46 = 0.72; P = 0.40 F1, 46 = 1.00; P = 0.32

live branching F1, 46 = 3.45; P = 0.07 F1, 46 = 2.71; P = 0.11 F1, 46 = 5.51; P = 0.023

dead branching F1, 46 = 0.47; P = 0.50 F1, 46 = 0.16; P = 0.69 F1, 46 = 0.06; P = 0.81

live massive F1, 46 = 0.47; P = 0.50 F1, 46 = 0.66; P = 0.42 F1, 46 =0.65; P = 0.42

dead massive F1, 46 = 0.84; P = 0.36 F1, 46 = 5.83; P = 0.02 F1, 46 = 3.56; P = 0.065

live total F1, 46 = 11.25; P = 0.002 F1, 46 = 7.41; P = 0.01 F1, 46 = 13.2; P = 0.0007

dead total F1, 46 = 3.80; P = 0.057 F1, 46 =4.95; P = 0.03 F1, 46 = 6.42; P = 0.014

FISH F5,41 = 1.43; P = 0.234 F5,41 = 2.40; P = 0.05 F5,41 = 3.56; P = 0.009

butterfly F1, 45 = 0.98; P = 0.33 F1, 45 = 2.34; P = 0.13 F1, 45 = 2.83; P = 0.10

surgenfish F1, 45 = 0.05; P = 0.826 F1, 45 = 3.59; P = 0.064 F1, 45 = 1.49; P = 0.23

parrotfish F1, 45 = 1.26; P 0.27 F1, 45 = 0.0056; P = 0.94 F1, 45 = 0.45; P = 0.51

sergeant majors F1, 45 = 3.03; P = 0.089 F1, 45 = 5.14; P 0.028 F1, 45 = 6.53; P = 0.014

all other fish F1, 45 = 3.76; P = 0.059 F1, 45 = 0.98; P = 0.33 F1, 45 =8.18; P = 0.006

total F1, 46 = 1.05; P = 0.31 F1, 46 = 3.40; P = 0.07 F1, 46 = 4.73; P = 0.035 SLOW OR SESSILE TAXA F4,43 = 1.17; P = 0.34 F4,43 = 1.56; P = 0.203 F4,43 = 1.55; P = 0.206

sponges F1, 46 = 2.04; P = 0.16 F1, 46 = 0.80; P = 0.376 F1, 46 = 0.87; P = 0.36

echinoderms F1, 46 = 0.36; P = 0.055 F1, 46 = 0.744; P = 0.39 F1, 46 = 1.12; P = 0.30

polychaetes F1, 46 = 1.26; P = 0.27 F1, 46 = 0.084; P = 0.77 F1, 46 = 0.44; P = 0.51

gorgonians F1, 46 = 0.54; P = 0.47 F1, 46 = 3.40; P = 0.07 F1, 46 = 2.14; P = 0.15

V. DISCUSSION

A. Functional groups

Threespot damselfish (Stegastes planifrons) have a dominating influence on the composition of Three Sister’s Patch Reef, suggesting they function as a keystone species for this community. Measures of both aggressive behavior and density of threespot damselfish were correlated with components of biodiversity, suggesting that there are several important interactions between damselfish and the other members of their community. However, there appears to be a limit to the amount of aggression and/or number of damselfish that are beneficial per unit area, which lends support to the intermediate disturbance hypothesis (Connell 1978).

Before beginning a detailed discussion of the results found in this study, an issue regarding correlation between the main fixed factors (damselfish density, aggression level, and aggression index) and functional groups as well as these factors with individual variables must first be explained. Although density of damselfish correlated with both aggression level and aggression index, correlation between density and a functional group or an individual variable does not necessarily result in a correlation between that functional group or other variables and a measure of aggression. This suggests that the presence of damselfish influences the community through a mechanisms other than their territorial behavior. This point is seen most clearly in the analysis of the total algae variable. Total percent cover of algae was positively correlated to threespot density, even though total percent cover of algae was not correlated to either measure of aggression.

Therefore, a behavior other than territorial aggression must explain the correlation between algae cover and density. One possibility is that the farming practices of the

54 damselfish such as weeding, preparing substratum, and fertilization function to increase algae cover rather than the aggressive territorial behavior reducing the number of herbivores. This particular result is consistent with other research showing that algal biomass is higher inside territories compared with adjacent undefended areas (Vine 1974,

Brawley and Adey 1977, Potts 1977, Ogden and Lobel 1978, Mahoney 1981, Sammarco and Carleton 1981, Sammarco 1983, Hixon 1996).

Although no clear trend in dominant algae type existed among all territory densities, green filamentous algae was dominant in territories with threespot population density 1-2, and red algae was dominate in territories with density equal to three, results similar to other studies that found these as the two prevailing types of algae in territories

(Vine 1974, Montgomery 1980, Lassuy 1980, Sammarco 1983, Klumpp and Polunin

1989, Branch et al. 1992). The dominance of these two types of algae, as well as their positive correlations with threespot density, suggests that they are either preferred food algae or preferred for their ability to harbor invertebrate that provide an important source of food protein. The percent cover green branching algae was consistently smaller than green filamentous algae at all densities, never exceeding 11.5% cover. This is not surprising given that damselfish are not capable of digesting robust green branching algae

(Branch et al. 1992), and suggests that this type of algae is not a preferred food. For these reasons, it can be inferred that green branching algae is probably “weeded” from territories by the damselfish. It was also interesting that despite a lack of correlation found between measures of aggression and the algae functional group, red algae appeared to have a trend with the two measures of aggression. This supports other results

55 indicating a strong influence from the threespot damselfish (S. planifrons) on the red algae variable.

Another method of measurement, which would have allowed for a less subjective analysis of farming behavior, is a preferred food algae experiment. This type of experiment allows for an analysis of feeding preference through artificial introduction of algal species into existing algal lawns to determine the percent impact of algal farming, and would have allowed for more complete analysis of overall impact of the damselfish on the reef community, and more specifically the algal percent composition.

Coral cover appears to be greatly influenced by the presence of threespot damselfish, as cover of the coral functional group correlated with each of the three main effects: threespot density, aggression level, and aggression index. The facts that percent cover of dead massive coral increased with aggression level, and live branching coral increased with aggression index suggest that areas with these conditions are favorable habitats for damselfish, and that highly aggressive threespot damselfish are more adept at acquiring them. It is not unrealistic to suggest this given the previously mentioned concept that these contours offer space for algal mat growth (Kaufman 1977, Potts 1977,

Lobel 1980, Robertson et al. 1981, Wellington 1982) as well as offer refuge from predators (Wellington 1982). These result suggest that damselfish are a factor to be considered among those in determining the distribution of corals, a conclusion also drawn by Kaufman (1977) and Wellington (1982) who further stated that for this reason damselfish can be considered keystone species.

Total amount of live coral cover decreased as all three main effects increased. In addition, total amount of dead coral cover increased with increase in aggression level and

56 aggression index. These results may be due to the large number of threespot damselfish in the patch reef with territories covering approximately 80% of the substratum (personal observation). An area with a high density of damselfish requires a greater amount of food algae than in an area with an intermediate density of damselfish. Therefore, damselfish kill a greater amount of coral to allow for growth of this algae. This does not suggest, however, that in the absence of damselfish the percentage cover of live coral would be larger. In the absence of grazing regulation, a concentrated number of herbivores can often completely denude the area of both algae and coral growth. It does suggest, however, that the benefits of damselfish to the community depend on the density of damselfish, with the ideal density for maximizing coral being intermediate.

As the number of auxiliary and total fish increased in territories, thus increasing grazing intensity, aggression index also significantly increased. This result is congruent with results found by Montgomery (1980) who also discovered a direct correlation between grazing intensity and number of fish excluded from territories. These areas may possibly have been more attractive to these herbivores, although there was no significant correlation found between algae cover and aggression index. Number of sergeant majors

(Abudefduf saxatilis) was also negatively correlated to aggression index. The relative absence of other territorial Caribbean damselfish, including the beaugregory (Stegastes leucostictus), the bicolor damselfish (Stegastes partitus), the yellowtail damselfish

(Microspathodon chrysurus), and the dusky damselfish (Stegastes fuscus) may indicate that the threespot damselfish is aggressively dominant over these related species causing competitive exclusion in their recruits. The absence of territorial damselfish other than the threespot (S. planifrons) at Three Sister’s Patch Reef could also be explained by

57 different habitat preferences of these related species. Finally, despite the fact that parrotfish were the single most common fish at all densities, no significant correlation existed between measures of aggression or density of damselfish and number of parrotfish.

It should also be noted that surgeonfish, parrotfish, and sergeant majors appeared to be the dominant grazers in this area. In addition, solitary grazers were more likely to be chased by the focal damselfish than individuals within a school. Furthermore, grazers traveling within a heterospecific school were also common targets of the damselfish.

These examples show the importance of schooling as a strategy to outmaneuver protective damselfish (Robertson et al. 1976, Brawley and Adey 1977), as well as confirm that solitary grazers are often excluded from territories (Doherty 1983, Ceccarelli et al. 2001). Although the fish assay and aggressive behavior observations were the last two measurements at each site, they were not conducted simultaneously, and therefore the presence or lack of a correlation between these two factors may be spurious. For example, fish that were intimidated by our presence during the fish assay may have felt safe enough to return to the territory during the aggression observation; therefore, the degree of influence the damselfish had on these species from the damselfish may have been underestimated.

A “bottle experiment” can be utilized to determine which species the damselfish is aggressive towards and the relative levels of this aggression. In these experiments, fishes of various species are individually placed in a bottle and introduced to the damselfish at varying distances to its territory. These distances as well as number of times the damselfish attacks the bottle provides a measure of aggression intensity. This

58 type of experiment would have allowed for a less ambiguous measurement of aggression than the measures used in the current study.

Even though a significant correlation was not found between any of the main factors and the slow or sessile taxa functional group, two individual taxa showed trends with the main factors suggesting a slight influence imparted by the damselfish. Number of gorgonians increased with aggression level possibly due to the increased substrate available from a larger amount of dead massive coral. In addition, even though a conspicuous halo ring indicating the presence of echinoderms was not found around the patch reef, there was a relationship between density of damselfish and echinoderms. It is possible that the limited number of long-spined sea urchins (Diadema antillarum) at

Three Sister’s Patch Reef prevented the detection of a significant relationship. Because long-spined sea urchin (D. antillarum) recovery has been minimal since the die off in

1983 (Sluka and Miller 2001), their existence in this area suggests that patch reefs are important for maintaining this species. Populations of long-spined sea urchins, as well as populations of Queen conch (Strombus gigas), a threatened species observed between coral heads at Three Sister’s, should be studied further in patch reefs of the Bahamas as possible critical habitats of these species.

B. Biodiversity

Most studies classifying damselfish as keystone species have focused either on algae, coral, or urchins. However, my study was more extensive, taking into account three components of biodiversity: algae, coral, and herbivorous fish. Consideration of all three groups facilitated the determination of the role of damselfish as a keystone species, i.e., a species whose presence is essential to the diversity of life for a given ecosystem

(Sole and Montoya 2001). The large amount of data made the comparisons more complex. Therefore, I provide a quantitative analysis as well as a qualitative model in assessing whether the threespot damselfish (Stegastes planifrons) meets the definition of a keystone species.

Changes in two components of biodiversity, algae and coral, in relation to density of threespot damselfish supports the hypothesis of a keystone species. Algal cover was greatest at high damselfish densities and lowest in the absence of damselfish. Coral cover is inversely related to algal cover. Note that the evenness of algal and coral cover occurs at intermediate densities of threespot damselfish (figure 5.1).

Similarly, a qualitative model of reef biodiversity may be constructed by examination of the changes in functional coverage in response to variation in damselfish density, and aggression index. Simultaneous examination of all functional groups showed that the evenness was greatest at intermediate values for damselfish activities.

That is, at high damselfish density or aggression, or in the absence of damselfish, one functional group tends to predominate.

Results of the quantitative analysis and the qualitative model suggest that there is a minimum and maximum density and/or aggression threshold that when exceeded leads to the dominance of only one functional group. The analyses also suggest that between these thresholds, there is an intermediate damselfish density and/or aggression index in which damselfish are keystone species. Therefore, the threespot damselfish (Stegastes planifrons) are keystone species only at intermediate densities and/or disturbance levels.

These analyses are insightful in that they set a limit in determining damselfish as a

60 positive influence as a keystone species: extreme densities and/or amounts of aggression may cause proliferation of one taxa thereby creating exclusion of others.

60 50 algae 40 coral 30

20 Total Percent Cover 10

0 0123 Threespot Damselfish Density

Figure 5.1 A comparison of the algae and coral functional groups at different damselfish densities.

Supplementary assessments of damselfish as a keystone species in the Bahamas may perhaps include comparisons with a variety of other species of damselfish (Family

Pomacentridae) along with behavior comparisons between threespot damselfish and other

Pomacentrids that may provide insight into the relative contribution of aggression versus other farming behaviors. Research in other zones and patch reefs will help shed light on habitat preferences of damselfish as well as their role in contributing to the diversity of these environments. Damselfish interactions with additional variables may also be considered.

C. Research applications

A primary goal of ecologist and management experts is to explain the patterns of biodiversity distribution. While it is apparent that damselfish directly influence some groups more than others, the dynamic interconnectedness of coral reef ecosystems offers

61 little doubt that these influences have indirect effects on all other aspects of the ecosystem. The degree of this influence varies across time and space. Therefore, one way to increase the practical application of research on damselfish to marine management systems throughout the world would be to formulate a database based on several key factors, including the presence and/or absence of damselfish. This database will allow for further refinement and continued input from scientists of ongoing research in various geographic locations and including numerous variables within the ecosystems themselves.

Geographical location would be the initial factor entered into the database to generate information relevant to the region. Atlantic and IndoPacific regions, have distinct differences in species richness, diversity, and composition (Ogden 1997) that result from conditions of temperature, environmental stability, and geological processes

(see Appendix A). These large-scale regional differences, as well as numerous other geographical differences such as latitude and longitude differences in marine ecosystems, are the primary factors in initiating management inquiry (Birkeland 1997). Within these biogeographic realms, local assemblages are created through competition, predation, recruitment, disturbances, and immigration (Mora et al. 2003). Data from scientific research pertaining to these factors can be entered within biogeographic locations to find significant correlations for conditions relevant to a given location. Other factors to be considered in a possible compilation database include the size of adjacent land mass

(Ogden 1997), season (Hatcher 1981), water depth (Meekan et al. 1995) and corresponding trends in tidal exposure, wave action (Brawley and Adey 1977), shelter availability, algal abundance, and fish distribution. Amount of anthropogenic influence

62 must also be considered. The immense number of variables to be considered along with the number of variables within the ecosystem itself requires a software system capable of compiling and correlating data from around the world in order to achieve valid results from these findings. Utilization of this data compilation will allow management programs to analyze patterns in species of damselfish, density of damselfish, or aggressiveness by damselfish. This data may then be utilized in management systems where existing conditions could be entered into a database and ideal treatment recommendations made through correlated data.

Utilization of the damselfish as a management tool in maintaining biodiversity in coral reef systems has many possibilities. Random introduction must be done with caution however. Some scientists warn that while patterns can be useful to managers, generalizations are not a good idea and should be used with caution, especially when altering the abundance of any inhabitant (Hixon 1996). In addition, using damselfish as indicator species may be counter-intuitive because territories may have both positive and negative effects from human perspective: sites with high algal productivity and dense herbivore populations also have reduced coral growth and weakened framework.

Complexity of these effects may limit the ability to predict accurately effects of any particular species let alone multiple species (Hixon 1996).

D. Direct conservation efforts at Three Sister’s Patch Reef

There are few historical scientific studies documenting how the Andros Island

Barrier Reef has changed over the last few decades; however, anecdotal observations suggests that the condition of the reef has deteriorated over the last 30 years, as shown primarily through algal overgrowth (Andros Conservancy and Trust 1999). Possible

63 causes of the algal growth on Andros’ Barrier Reef at present are destructive fishing practices (Andros Conservancy and Trust 1999), a reduced population of long-spined sea urchins (Diadema antillarum), and conditions caused by El Nino Southern Oscillation.

The fact that reduced population of herbivores has played a role in the increase of algal growth was confirmed during our preliminary research on the barrier reef, where there was a high coverage of Microdictyon algae and low densities of herbivorous fishes. An area displaying signs of more even biodiversity was Three Sister’s Patch Reef. Upon entering the habitat at Three Sister’s Patch Reef, a considerably smaller amount of

Microdictyon algae was present, probably due to the high density of grazers in the area.

As this location displayed better health than the forereef, it is an important area to conserve. The high density of threespot damselfish and relative absence of other territorial damselfish at Three Sister’s Patch Reef also makes this site a prime location for further studying the ecological role of the threespot damselfish. This area is also valuable as a habitat as it facilitates movement of fish and other organisms between the barrier reef and mangrove swamps. This movement is important to promote species dispersal and to prevent sink populations. A final argument for the protection of this area is the shelter it gives for marine organisms in protection from the elements.

The present time offers a prime opportunity to protect Three Sister’s Patch Reef by its incorporation into the reserve design of Central Andros National Park. Local

Andros residents and organizations along with the Bahamas National Trust have recently

(April 2002) succeeded in convincing the Bahamas Government to establish a diverse network of protected habitat types on Andros Island called the Central Andros National

Park. Five main areas of the Park, totaling approximately 288,000 acres, encompass the

64 highest concentration of blue holes, two portions of Andros’ Barrier Reef, a Land crab management area, a Creek and Mangrove System Protection and Management Area

(Andros Conservancy and Trust 2002), and three Scientific Monitoring Zones (Andros

Conservancy and Trust 1999). The two portions of the barrier reef extend inland to the east coast of the Island and are termed Marine and Coastal Park Areas, or Marine

Replenishment Zones (Figure 5.1; Andros Conservancy and Trust 1999). In these Zones, only non-consumptive uses will be permitted. In addition, three small reef areas within

Area 1 will be designated Scientific Monitoring Zones: two patch reef areas (Porites

North and South). Specific objectives of the Scientific Monitoring Zones are to provide sites away from all uses (including diving, snorkeling, fishing, etc.) for scientific monitoring including the assessment of reef health and the effects of establishing the park

(Bahamas National Trust 2001). It is my thought that Three Sister’s Patch Reef area should be considered a Scientific Monitoring Zone for the aforementioned reasons. This designation would not be difficult if it were established as an extension of Marine

Replenishment Area 2 because of its close proximity, 2.796 nautical miles north of Area

2’s northern boundary.

Figure 5.2 Marine Replenishment Zones and Scientific Monitoring Zones in Central Andros National Park (Bahamas National Trust 2001).

Currently, only .25% of the Earth’s oceans are offered some level of protection, and a recommended 20% must be preserved to ensure population viability (Murray et al.

1999). Unfortunately, most coral reefs are often found in less developed countries where budgets are limited. Because it is expensive to gather information such as catch, effort, and populations of fishes needed for scientific fisheries management, future management systems must carefully balance socioeconomic demands with population viability factors, as well as promote education and awareness throughout the public in order to sustain fish populations for the future.

Many of the Caribbean coral reef fauna that allowed reef communities to escape collapse in the past are declining today in response to anthropogenic disturbances, suggesting that Caribbean reef communities may be less resilient in the future to respond to ongoing environmental perturbations (Johnson et al. 1995). As human population and habitat degradation continues to escalate, identifying and understanding the complexity of highly interactive keystone species will allow scientists to discover ways to assist coral reef ecosystem in maintaining its own balance through regulation and protection of habitats in which keystone species live.

The identification of damselfish as keystone species has already been established in many areas throughout the world. This definition for the species in the waters surrounding the Bahamas, however, is yet to be determined. The Three Sister’s Patch

Reef damselfish (Stegastes planifrons) directly effects its territories through its aggressive behavior and algal farming practices by altering the distribution and abundance of algae, coral, cryptofauna, and many species of herbivores. In the Three

Sister’s Patch Reef specifically, the threespot damselfish appears to be a keystone species based on the analysis of their impacts on the chosen functional groups. The biodiversity of this patch reef and the critical role that the threespot damselfish play here provides evidence that this patch reef is a unique area that must be protected to explore implications this species may have for improved biodiversity in other reef areas.

“In the end, we will conserve only what we love. We will only love what we understand.” -Baba Dioum, Senegalese naturalist and poet

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APPENDIX

A. Differences in coral reefs in different geographic regions

On the western coast of continents some coral communities receive concentrated nutrient input from the upwelling of deep waters. Along the eastern coast of continents, coral reefs receive sediment and nutrients from terrestrial runoff. The coral reefs of atolls in central oceanic regions receive nutrients at lower rates and lower concentrations than those along the coast. Differences in nutrient input among geographic regions create differences in the dominance of different organisms and differences in ecological processes (Birkeland 1997).