Investigation of Trophic Transfer from Oyster Reefs to Predatory Fishes In

Home , Mosquito Lagoon

Investigation of Trophic Transfer from Oyster Reefs to Predatory Fishes

in Southwest Florida

______

A Thesis

Presented to

The Faculty of the College of Arts and Sciences

Florida Gulf Coast University

In Partial Fulfillment

of the Requirement for the Degree of

Master of Science

______

Robert M. Wasno

2014 APPROVAL SHEET

This thesis is submitted in partial fulfillment

of the requirements for the degree of

Master of Science

______

Robert M. Wasno

Approved:______

______

Aswani Volety, Ph.D. Committee Chair

______

Edwin M. Everham III, Ph.D. Committee Member

______

Ronald Toll, Ph.D. Committee Member

______

S. Gregory Tolley, Ph.D. Committee Member

The final copy of this thesis has been examined by the signatories, and we find that both the content and the form meet acceptable presentation standards of scholarly work in the above mentioned discipline.

ACKNOWLEDGMENTS

Foremost, I am forever indebted to my parents, Gisele and the late Edward Wasno for their understanding, endless patience and encouragement when it was most required. Thank you!

I would like to express my sincere gratitude to my friend and Chair of my Thesis Advisory

Committee, Dr. Aswani Volety for guidance, council, and opportunities that will have changed my life. I am also fortunate to have had a truly remarkable Advisory Committee that has demonstrated unwavering patience and support for my research: Dr. Win Everham, Dr. Ron Toll and, Dr. Greg Tolley.

I would like to thank my dear friend, Dr. Tomma Barnes for her support throughout this long and arduous process.

In addition, this thesis would not have been possible without the guidance and the help of many individuals who in one way or another contributed and extended their valuable assistance in the preparation and completion of this study: Commercial fishermen Captain Lanny Sheffield and

Captain Ron LaPree, Captain Denis Grealish (Florida Marine Patrol-ret.), Chuck Listowski

(West Coast Inland Navigation District), Lesli Haynes, Dr. Steve Bortone, David Ceilley, Kieth

Kibbey, Danielle Rosenthal, Kevin Lollar, and Patricia Rice.

Finally, I would like to acknowledge a legion of friends and colleagues that provided a source of inspiration and motivation to keep this research and thesis moving forward: John Stevely, Don

Sweat, Dr. Rob Loflin, Ray, Kristen, and Kal Judah, Dick Foster, Dr. Tom Dolan, ii

Dr. Loren Coen, Glen Kitner, Dr. Michael Spranger, Don Hood, Dr. Richard Soderburg, Patrick

Pantano, Norm and Nancy Vester, Eric Rieseberg, Dr. Darren Rumbold, Eve Haverfield, and Dr.

Chuck Adams.

Financial support was provided by Florida South Water Management District, West Coast Inland

Navigation District, Florida Gulf Coast University, and University of Florida Sea Grant Program.

iii

ABSTRACT

Reefs formed by the eastern oyster Crassostrea virginica are ecologically and economically important in the estuaries along the East and Gulf coasts of the United States.

Crassostrea virginica is a sessile benthic organism that plays a vital role in improving water quality in estuaries by filtering nutrients, sedimentary fines (microscopic sand particles), phytoplankton and pollutants. The resulting increase of sunlight penetration into the water column also helps promote seagrass growth. However, environmental value increases further when oysters and the reefs they create provide feeding stations for many species of predatory fish. These reef structures provide refugia for mobile benthic organisms that utilize the reef’s interstitial spaces for protection, feeding and reproductive activities. These organisms are important as a food source for higher trophic level organisms, such as recreationally and commercially important fishes, that use reefs as feeding stations.

Previous studies have shown that unique organisms are associated with specific types of benthic habitats, such as oyster reefs, seagrass meadows, mangrove root structure systems and mudflats. Habitats for particular organisms encompass certain characteristics such as physical structure, provision of food, substrate, hydrodynamics and hydrology that, together, determine their utilization by organisms. For example, species of mud crabs in southwest Florida belonging to the family Xanthidae are found predominantly on oyster reefs because of their ability to find protection inside the interstitial spaces between and beneath oyster valves, where they can endure the harsh environment created by inter-tidal exposure, and wave energy. For each of the benthic habitats previously mentioned, there are unique parameters that allow certain organisms to

iv thrive, while others may struggle to survive. Unique organisms that have evolved to exist in a particular environment as their primary residence are usually found in the greatest numbers in those habitats. This presence makes them an indicator species for specific benthic habitats.

However, many of these same organisms can be found in lesser numbers in several types of habitat as they could transition between habitats via tidal currents, swimming or hitching a ride on floating algae.

This project investigated the link between oyster reef communities and the trophic transfer of biomass to tertiary-level predator fishes that were captured in proximity to isolated reef structures. A previous study using stable isotopes (Abeels et al. 2012), demonstrated trophic transfer of biomass from nutrients in the water column through oysters and several organisms that reside on the oyster reefs. By examining gut contents and identifying prey items classified as oyster reef indicator species, this extension of the trophic link can be established.

From January 2006 through September 2006, sampling of fishes around oyster reefs was conducted using an entanglement net (also referred to as a gill net). A total of 294 fishes were captured for analysis of stomach contents. Of those fishes, 106 stomachs contained identifiable prey items. Within the gut contents, a total of 26 different prey item categories were identified.

These prey items were then characterized using the Lima-Junior and Goitein (2001) Importance

Index method of analysis. This method serves to rank predator diet composition of stomach contents to community prey assemblages of oyster reefs and of those from other benthic habitats.

These fishes were captured in the Horseshoe Keys area of Estero Bay, Lee County, Florida from

v a specified area measuring 4 km2. This site was chosen because of the nearly complete isolation of oyster reef habitat from that of other habitats, such as seagrass.

Results showed that prey items indicative of oyster reef residency belonging to the family

Xanthidae (mudcrabs) occurred in the greatest number of stomachs (44%). Xanthids found in the stomachs of predator fish include Panopeus spp. and Eurypanopeus depressus. Other prey items deemed to be indicator species of oyster reefs, including Palaemonetes pugio (daggerblade grass shrimp), Alpheus heterochaelis (big claw snapping shrimp), Petrolisthes armatus (green porcelain crab), Opsanus beta (gulf toad fish) and Gobiesox strumosus (skillet fish), occurred in the majority of stomachs, contributing 53% of the overall Importance Index (AI). These indicator species contributed 48% of the dry season diet and 58% of the wet season diet for cumulative prey items of all predators. Results suggest that while the diversity of predatory fish caught in wet and dry seasons did vary, the diets of those fish did not differ significantly.

These results demonstrate that several key prey items identified as oyster reef indicator species and found in the stomachs of predatory fishes contribute to oyster reef biomass transfer.

Therefore these results identify an important ecological service provided by oyster reefs as feeding sites for a variety of transient fishes. Further studies could show that expanded oyster reef restoration efforts can lead directly to enhanced fisheries production and, peripherally with clearer bay water, to greater production of seagrass meadows. This, in turn, could greatly enhance the overall ecological production of estuaries such as Estero Bay.

TABLE OF CONTENTS

ACKNOWLEDGEMENTS i

ABSTRACT iii

TABLE OF CONTENTS vi

LIST OF TABLES vii

LIST OF FIGURES viii

INTRODUCTION 1

METHODS 8

RESULTS 27

DISCUSSION 46

CONCLUSION 52

LITERATURE CITED 56

vii

LIST OF TABLES

Table 1. Standard Weight (SW) Table. Weight range table, as recorded in grams, for ascribing points for all stomachs with contents based on total weight. 24

Table 2. Determining the distribution of points based on total weight of stomach contents. 25

Table 3. The relative abundances of predator fish and those with stomach contents, sampled by season. 30

Table 4. Relative abundances of stomach content prey organisms by season. 33

Table 5. Importance Index for Dry season prey items with values > 3. 34

Table 6. Importance Index for Wet season prey items with values > 3. 35

Table 7. Cumulative Importance Index for Dry and Wet seasons. 36

Table 8. Percentage of indicator prey consumption by predator fishes. 37

viii

LIST OF FIGURES

Figure 1 Estero Bay watershed. Map depicts regional flow. 10

Figure 2. Study area in northern Estero Bay. 12

Figure 3. Detailed image of oyster reefs sampling sites for this study. 13

Figure 4. Map showing Lee County Environmental Laboratory EB-13 Water Quality Station site. 14

Figure 5. 2006 Estero Bay water temperature as reported by EB-13 site for sampling period and annual mean. 28

Figure 6. Estero Bay rainfall as reported by EB-13 site for 2006 sampling period and 1991- 2004 annual mean. 28

Figure 7. Estero Bay 2006 monthly average and 1991- 2004 annual means for salinity recordings by Lee County Environmental Laboratory, Station EB-13. 29

Figure 8. Importance Index of all prey items consumed by 13 Centropomus undecimalis sampled containing stomach contents. 38

Figure 9. Importance Index of all prey items consumed by 37 Ariopsis felis sampled containing stomach contents. 39

Figure 10. Importance Index of all prey items consumed by 14 Elops saurus sampled with stomach contents. 40

Figure 11. Importance Index of all prey items consumed by six Caranx hippos sampled with stomach contents. 41

Figure 12. Importance Index of all prey items consumed by 22 Lutjanus griseus sampled with stomach contents. 42

Figure 13. Importance Index of all prey items consumed by seven Archosargus probatocephalus sampled with stomach contents. 43

Figure 14. Importance Index of prey for three Eugerres plumieri sampled. 44

Figure 15. Importance Index of all prey items consumed by four Sciaenops ocellatus sampled with stomach contents. 45

INTRODUCTION

This goal of this study is to identify the relative importance of oysters and the reef structures they communally create, in trophic energy transfer to higher levels as utilized by

Estero Bay fishes. The recognition of this important link serves to emphasize the dependence of fishes on habitats that serve as feeding stations and their contribution to fisheries stocks. This trophic transfer should be considered in the overall management of these habitats and associated fisheries (Turner et al. 1999).

The overall trend of the production of the world’s fisheries has been one of decline. The oceans are under increasing pressure due to: 1) commercial fishing exploitation (Botsford et al.

1997, Pauly et al. 2003, Hilborn et al. 2004, Mullen et al. 2005); 2) a decrease in overall water quality (Botsford et al.1997); 3) marine biodiversity loss (Walters et al. 1997, Worm et al.

2006); 4) impacts from climate change that decrease the availability of fisheries-dependent habitat (Walther et al. 2002, FAO 2009); and 5) impacts from recreational fishing (Post et al.

2002, Cooke and Cowx 2004).

Decreasing water quality and loss of fisheries-dependent habitat are the most widely acknowledged contributions to world-wide fisheries collapse. A large percentage of fisheries are directly dependent on coastal and estuarine regions for reproduction or rely on these areas to support their prey. Several studies relating estuarine dependence by fisheries species report that

68% to 90% of commercially important species of marine fish and shellfish and 70% to 80% of recreationally important species are dependent on estuaries for their survival as areas for spawning, nurseries, and feeding areas (Lindall et al. 1979, Lellis-Dibble et al. 2008).

The United States has increased efforts to mitigate the decline of fisheries within its coastal exclusive economic zone. The Magnuson-Stevens Fishery Conservation and

Management Act was first enacted in 1976 and is the primary law governing marine fisheries in

U.S. waters. With amendments added in 1996, the focus of the revised act was the development of a domestic commercial fishing industry, the rebuilding of exploited fisheries, the protection of essential fish habitat and the reduction of by-catch.

Since 2001, the number of over fished populations has decreased in the U.S. Initial reports show that 80% of the wild commercial marine fish stocks have been improving or are being maintained at sustainable levels; however, approximately 20% have declined or are now labeled as overfished (Dorsett 2007).

In southwest Florida’s Estero Bay, suitable habitat for sustainable fisheries continues to be impacted by pollution and degradation of water quality from human population influx into the coastal region (Estero Bay Agency on Bay Management 1997). Although little information is available on commercial fishing in Estero Bay, the commercial fishing industry in all of Lee

County represents an important component of the Florida commercial seafood industry. In 2010, dockside value of commercial saltwater landings of finfish and shellfish in Lee County was

$10,252,968 (FWC-FMRI 2009). These fishes were most likely caught offshore or in locations other than Estero Bay, but many of the species fished commercially are estuarine dependent and reside in estuaries as juveniles before moving offshore. The United States commercial fish landings in 2004 amounted to $3.65 billion, of which 68% represented estuarine dependent species (Lellis-Dibble et al. 2008).

Recreational sport fishing in Estero Bay has long been an attraction to the area. Many anglers fish for common snook (Centropomus undecimalis), red drum (Sciaenops occelatus), spotted seatrout (Cynoscion nebulosus), tarpon (Megalops atlanticus) and several other sport species. Over the past few decades, there has been a decline in the overall quality of fishing in the bay (Estero Bay Agency on Bay Management 1997). From 1996 through 2002, landings for many fish species have shown a downward trend in all of Lee County (Estero Bay Agency on

Bay Management 2004). This decline in fishing seems to be a result of an increase in residential development, boat traffic, urban run-off and the subsequent decrease in water quality (Estero

Bay Agency on Bay Management 1997).

A common bottleneck for potential rebuilding and growth of all fisheries is the decrease in suitable habitat. From deep sea species, to coastal species, and inshore species, all fish are dependent on critical habitat to maintain sustainable populations. The primary location for much of the sustainable growth of fisheries is within proximity to coastal estuarine ecosystems.

However, patterns of fishery use of estuaries are complex because of factors such as salinity gradients, geography, seasonality and life histories (Able 2005). Habitats such as oyster reefs within estuaries can enhance growth and production for many species of fish. These habitat impacts can be far reaching.

Oyster Reefs as Valued Ecosystem Components

On a global scale, oysters had once been the dominant organism in many estuarine bays and coastal rivers (Beck et al. 2011). Oysters serve to maintain water clarity and water quality at levels required for many fish species to flourish, including estuarine waters in southwest Florida estuaries (see Volety et al. 2014). Additional ecological services of oysters include sequestering

4 atmospheric carbon in the form of calcium carbonate during the formation of their shells (Hargis and Haven 1999), stabilization of sediment and shoreline structures, and creation of three- dimensional habitat. More than 300 different organisms have been documented to use oyster reef structure for safe haven, reproduction and foraging (Wells 1961, Crabtree and Dean 1982,

Wenner et al. 1996, Coen et al. 1999, Tolley and Volety 2005, Abeels et al. 2012). Many of these species are prey for higher trophic levels.

For the past 200 years, excessive harvest and anthropogenic disturbance of oyster reefs have brought them to the point of being functionally extinct, meaning they lack any significant ecological role. It is estimated that 85% of world-wide oyster reefs have been lost (Beck et al.

2011).

Throughout the United States, oysters are highly sought as a food source and provide for substantial positive economic impact to local coastal communities where they are harvested. In

2011, 1,406 metric tons of oysters were harvested in Florida at a value of about $8.8 million

(FWC-FMRI 2013). In southwest Florida, oyster reefs have great ecological importance but no commercial value because of high concentrations of pollutants in local waters probably as a result of urbanization of surrounding coastal watersheds. However, where a thriving community of oysters exists, their ecological value is significant. Oysters provide many valuable ecological services. As filter feeders, they remove pollutants, assimilate nutrients, phytoplankton, and fine particulates, thus clarifying the surrounding water (Kellogg et al. 2013). Through this filtration process, oysters contribute to reducing turbidity that will increase the depth of the photic zone, thereby enhancing the growth of submerged aquatic vegetation such as seagrasses (Grabowski et al. 2005, Peterson and Heck 1999, Volety et al. 2014).

Many benthic organisms such as decapods of family Xanthidae rely on oysters for food, growth and propagation. Some of these organisms feed on larval oysters settling on the reef. In addition, oysters can provide nutrients by the production of fecal and pseudofecal pellets derived from the intake of food from the water column. This is an important supplemental food resource for many benthic organisms residing on the reef.

Studies have looked at reef communities along the Gulf and Atlantic coasts and have indicated that they can provide for large numbers of species, including some not found on adjacent benthic habitats such as mud flats or seagrasses (Zimmerman 1989, Posey et al. 1999,

Coen et al. 1999). The focus of this study is the organisms that use and reside within the interstitial spaces of the three-dimensional structure of these oyster reefs and the transient fishes that prey on them. Oyster restoration projects across the globe are testament to the importance of these ecologically and economically important shellfish and the reef structures that provide habitat for important prey species for higher trophic-levels. Large, viable oyster habitats relate directly to greater estuarine production of fisheries of commercial and recreational importance

(Luckenbach et al. 1997).

Trophic Transfer

Oysters serve an important role as the catalyst for energy and nutrient provision to organisms residing on oyster reef structure. Benthic organisms such as polycheate worms and amphipods consume decaying plants, animal detritus, and nutrients in sands by grazing

(Fauchald and Jumars 1979). Shrimp and crabs consume juvenile oysters, eggs deposited within the valves, and will also graze on epibenthic algae and nutrients deposited by oysters. Individual oysters can siphon five liters of water per hour, straining phytoplankton from the water column

6 while providing themselves with nutrients. Approximately 70% of ingested materials are assimilated into the oyster (Newell 1988). The remaining material is discharged as pelletized fecal matter (feces and pseudofeces) into the detritus (Coen et al. 1999). The fecal pellets and their derived nutrients provide for grazing benthic organisms that would otherwise not be able to obtain dissolved nutrients found in the water column (Harding and Mann 2001). A laboratory study determined that a 1-acre plot of oysters could deposit 7.58 metric tons of fecal material every 11 days (689 kg per day) or more than 254 metric tons per year (Lund 1957). In addition, oyster reefs can increase the surface area of an otherwise flat plain 50-fold (Lund 1957). These interstitial spaces on oyster reefs provide areas for many benthic organisms to live and reproduce, and the energy-rich fecal pellets help support a large population of organisms. These

2 bio-deposits have a caloric value of 1545 kcal/ m that is an important nutritional substrate.

Small benthic organisms such as polycheate worms, juvenile crabs, amphipods, isopods, and shrimp ingest and/or graze on these pellets (Bernard 2011).These invertebrates are subsequently consumed by fish that hunt for food along the reef (Harding and Mann 2001). Thus, trophic transfer of food energy, derived from the water column and provided by oysters to community benthic organisms (prey) continues up to the next-higher trophic level such as predatory fishes. It is through these transfers of biomass that oyster reefs become important feeding stations for predator fish. This relationship between reef resident prey species and higher trophic level predators has been documented in the Chesapeake Bay (Grabowski et al. 2008), and many studies have been conducted on similar relationships between prey species in seagrass, salt marshes or mudflats, but there is a void of similar information in other regions (Coen et al.

1999), particularly southwest Florida.

Indicator Organism Community on Oyster Reefs

In a bay system that has several types of habitat, there are particular niches within each habitat that allow certain benthic species to thrive. Each type of habitat has unique characteristics: salinity, water flow, wave energy, depth, food sources, and turbidity can all contribute to where certain species thrive. In addition, organisms with different physical attributes, such as armor (exoskeleton), the ability to osmoregulate, camouflage, resistance to desiccation, avoidance of predation by burrowing, will most often be found in specific habitats such as seagrasses, mudflats, mangrove fringes or oyster reefs. The organisms that are commonly found in a specific habitat, but only rarely found over other types of habitat, can be classified as indicator species for that particular habitat. This is the definition used in this study.

Oyster reefs are particularly harsh environments, with high wave energy (not absorbed or reflected), intertidal exposure (desiccation) with extreme heat or cold temperatures, and a wide range of salinities. Organisms residing on oyster reef habitat have evolved to be able to withstand these environmental extremes. Several studies have shown organisms qualifying as indicator species on oyster reefs to include several species of residential fish, crabs and shrimp (McDonald

1982, Wilson et al. 1982, Lardies et al. 1998, Glancy et al. 2003, Tolley et al. 2005, Duci et al.

2009, and Abeels et al. 2012). Fish that reside on oyster reefs include the naked goby Gobiosoma bosc, Florida blenny Chasmodes saburrae, skillet fish Gobiesox strumosus, and oyster toadfish

Opsanus beta (Tolley and Volety 2005, Abeels et al. 2012). Species of decapod crustaceans that use oyster bars include green porcelain crab Petrolisthes armatus, mud crabs Panopeus spp., flatback mud crab Eurypanopeus depressus, Florida stone crab Menippe mercenaria, bigclaw

8 snapping shrimp Alpheus heterochaelis and daggerblade grass shrimp Palaemonetes pugio

(Tolley and Volety 2005, Abeels et al. 2012).

A study conducted by Abeels et al (2012), in Estero Bay using stable isotope analysis determined that trophic relationships were present within the oyster reef community. This analysis was based on stable isotopes of carbon and nitrogen from benthic organisms collected directly from oyster reefs and compared to sediment and secondary predators for similarity trends. The research presented here compliments that study by examining the fate of this biomass and how it is transferred to higher trophic levels and off the reef, via identification of predator and prey items consumed.

This research examines the trophic transfer on oyster reefs to higher trophic levels, such as recreationally and economically important fishes, by examining prey items consumed by predator fishes collected in proximity to oyster reefs in Estero Bay, Florida and identifying the relative importance of organisms identified as oyster reef indicator species. In addition, this study will reveal the relationship between seasonal variation (dry and wet season) of predator fishes sampled and their stomach contents.

METHODS

Study Area

Estero Bay, located in Lee County along the coast of Southwest Florida, is a long, narrow, and very shallow estuary. Situated approximately 24 km south of Fort Myers, the bay is bordered on the northwest by Bowditch Point on Estero Island and to the south by Bonita Beach

9 and is separated from the Gulf of Mexico by a string of barrier islands: Estero Island, Black

Island, Long Key, Lover’s Key, and Big Hickory Island. Five tributaries flow into the bay:

Mullock Creek, Hendry Creek, Estero River, Spring Creek, and the Imperial River. Gulf waters enter and exit the Bay through Matanzas Pass, Big Carlos Pass, New Pass, and Big Hickory Pass.

Although the bay itself has a surface area of only about 38 km2, its watershed encompasses approximately 1,441 km2 and extends throughout the southern part of Lee County into parts of

Hendry and Collier Counties (FDEP 2013) (Fig. 1). It is a well-mixed estuary due to its shallow depth and many passes to the Gulf of Mexico. Shorelines, where undeveloped, and many of the bay’s islands are lined with mangroves and oyster reefs. In 1966, the northern half of Estero Bay was designated as the state’s first aquatic preserve. In 1983, the southern half of the bay down to the Lee County line was added (FDEP 2013).

Figure 1. 1,441 km2 Estero Bay watershed. Map depicts regional flow (Byrne and Gabaldon 2008).

Estero Bay is tidally dominated and receives relatively little freshwater inflow from any of its five tributaries during most of the year. During the wet (or rainy) season, substantial upland run off can occur (Byrne and Gabaldon 2008). It should also be noted that during times of heavy flooding from storm water runoff, Wiggins Pass, 8.25 km south of Big Hickory Pass, alleviates much of the flood waters from the southern part of the bay (Bob Wasno, personal observation).

These tributaries are small, generally short, and have no outlet channels (channels suddenly end upon entering the bay). These are characteristics of generally low discharge rivers or tributaries.

Salinity gradients throughout the bay are controlled by the many small islands, the maze of oyster reefs and mud bars, precipitation, tides and wind (Byrne and Gabaldon 2008).

Estero Bay Oyster Reef Sampling Area

Oyster reefs form a unique substratum and significant habitat in Estero Bay. Oysters are common along the mouths of tributaries, especially in the northern part of the bay (Fig. 2). Based on 2011 data, there are 26 hectares of oyster bars in Estero Bay (FDEP 2013).

The study area is centered approximately 1.5 kilometers north of Mound Key (Fig. 3). It is approximately 4 km2 and centered at 810 52.60’W and 260 26.25’N. This area, known as

Decibels Rocks, was chosen because of its high density of oyster reefs and relative spatial isolation from other habitats such as seagrass meadows and mudflats. This isolation does not serve as a corral limiting fish feeding activity exclusively on oyster reefs, but serves to demonstrate the preference of oyster reefs as a feeding station. The bay bottom in this area is mostly hard, shelly sand that supports a maze of oyster reefs. The oyster reefs can vary from

Figure 2. Study area in northern Estero Bay (Byrne and Gabaldon 2008). Sampling area of approximately 4 km2, situated 1.5 km north of Mound Key. A total of 40 net deployments were conducted within this area.

wide (8 meters) and long (100+ meters) with heights up to 1 meter, to narrow and short. In addition to these established reef areas, much of the surrounding bay bottom contains numerous small cluster oyster reefs less than 1m2. Extreme tidal fluctuations ranged from +0.46 m at Little

Hickory Pass to -0.69 m NGVD at extreme low. Total difference in tide range is 1.06 m

(Suboceanics Consultants 1978).

Figure 3. Detailed image of oyster reefs sampling sites for this study. Circle indicates the sampling area (Image credit: Google Earth)

Estero Bay is a well-mixed, lagoon-type embayment with an average depth of 0.9m.

Combined with a relatively large watershed draining into the bay through five tributaries, the many hydrodynamic barriers (oyster reefs, mud flats and mangrove islands) create many different sub-basins within the bay that each exhibit its own salinity ranges (Byrne and Gabaldon

2008).

With these dynamic tidal confluences, sub-basin salinity ranges, and length of sampling gear (160 m entanglement net) encompassing large areas for each set, it is believed that using a controlled site and standard water quality recording device would offer the best information over the course of time during this study. Salinity and water temperature measurements used for this

14 study were collected by Lee County Environmental Laboratory’s (LCEL) Station EB-13:

81˚52’21.76” W and 26˚ 26’01.71” N. Depth at this site is 0.76 m. The water quality monitoring station is located approximately 1,300 m north of Mound Key on the southern perimeter of the sample area. Sample area and water quality monitoring station are depicted in Figs. 3 and 4.

Daily water temperature and salinity averages were recorded from January 2006 through

December 2006 from LCEL Station EB-13.

Figure 4. Map showing Lee County Environmental Laboratory EB-13 Water Quality Station site. (Photo Credit: Google Earth)

Field Methods

Two methods were employed for the capture of predator species of fishes on oyster reef habitat: hook-and-line and entanglement net (also referred to as gill net). To assist in the identification of sampling sites, several local fishing experts (professional fishing guides, commercial back-water fishermen and local expert fishermen from the area), recommended locations of productive oyster reef fishing spots, discussed local fishing methods, and provided historical perspectives. Studies have shown this to be a valid method to optimize success in gathering information (Grant and Berkes 2006).

Hook-and-Line Gear

During the initial sampling phase using hook-and-line, both artificial and live bait were used. This sampling method accounted for 24 fish of four different species. Of the fish captured with this technique, only a scant amount of gut contents were collected in four fish, and the other

20 had empty stomachs. It was assumed that only hungry fish were being captured, while fish that had just fed were not as aggressive or perhaps had regurgitated their gut contents during the ensuing stressful fight (Marshall 1958, Fore and Schmidt 1973). As a result, the method used for capturing fish was changed and data collected using this sampling method was discarded.

Entanglement/Gill Net

A gill net was then used to sample fishes along the waterways in proximity to oyster reefs. The gill net measured 160 m by 3 m deep. The mesh size was 6 cm between knot mesh,

16 stretched. Once prospective sampling sites were determined, the gill net was deployed off the transom of a mullet skiff specifically designed for setting this type of gear. The gill net was deployed and allowed to soak (remain in water) for 60 minutes. The use of an entanglement net encompassing an oyster reef site is an unbiased method of capturing all fish within a particular size range within that area. This is selective gear, which means as a fish of a particular size range swims into the net, its goes through the mesh and the net tightens around the body of the fish, stopping forward progress. As the fish tries to back out, the operculum, or gill cover, hooks the netting so the fish cannot back out thus remains entangled. Smaller fish would simply swim through the netting, and the heads of larger fish would not fit through the net, but would simply bounce off and swim away. There were several other ways that fish were able to avoid capture.

Larger fish such as tarpon, for example, simply tore through the net, and small sharks bit through the mesh. On days when the water was clear, some fish demonstrated clear avoidance of the net by breaching over the top. The fish captured by the entanglement method provide a snapshot of the fishes utilizing oyster reefs during the time of sampling.

While the net was soaking, all participants walked the inside perimeter, flushing fish into the netting. As the net was retrieved, fish were removed and immediately placed on ice. Mounted on this skiff was a 160-cubic foot ice box that accommodated all fish captured. Total time from net deployment to complete retrieval was approximately 2 ½ hours. The gill net method was employed during various times of the day (6:00 am, noon, 6:00 pm and midnight) during both dry season (March−June) and wet season (July−September). On each occasion, the gill net was deployed five (5) times, 20 times per season. A total of 40 net deployments took place during the course of this study encompassing a cumulative total area of approximately 10.5 ha.

All locations at which the net was deployed were recorded with a hand-held GPS device.

Data collected included longitude/latitude of capture location, and water temperature, date, time, and salinity as recorded by Lee County Environmental Laboratory Monitoring Station EB-13.

A total of 11 species of fishes were captured by entanglement net in Estero Bay during wet and dry seasons (January to September 2006). Fish captured included red drum (Sciaenops ocellatus), common snook (Centropomus undecimalis), ladyfish (Elops saurus), sheepshead

(Archosargus probatocephalus), hardhead catfish (Ariopsis felis), crevalle jack (Caranx hippos), grey snapper (Lutjanus griseus), striped mojarra (Eugerres plumieri), black drum (Pogonias cromis), and bluefish (Pomatomus saltatrix). A single species of the herbivorous striped mullet

(Mugil cephalus) was also captured. Striped mullet were not included in any data set.

Laboratory Methods

The captured fish were stored on ice and processed within 24 hours of collection. All data were recorded on individual fish data sheets.

Gut Content Analysis

All collected fish were identified. Each fish was measured as standard length to the closest 0.5 centimeter and weighed using a calibrated scale (OHAUS model CS 5000) to the closest gram. Fish stomachs were removed intact by cutting at the pyloric sphincter and just behind the pharynx. Connective tissue was trimmed, and each stomach was placed in a plastic bag with corresponding fish record number. A small amount of seawater was added to the bag that was placed in a freezer and stored for subsequent analysis.

To identify the composition of the stomach contents, stomachs were removed from the freezer and allowed to thaw to room temperature. Once the stomachs became pliable, scissors were used to cut them open longitudinally, and the entire contents were washed out onto a sorting tray with distilled water. Contents were inspected using a dissecting scope at appropriate magnification. All materials deemed to be of animal origin or of significant interest, such as fishing gear or human related debris, were placed in an individual glass jar and preserved in 5% formalin and seawater to be considered for further study. All stomachs containing anything less than an identifiable organism or debris such as bits of shell, algal or seagrass material, and in one instance a small fishing jig, were also recorded.

For analysis, the gut contents were rinsed, transferred to new glass jars containing 70% isopropanol alcohol. Emptied stomachs were placed in a voucher container for each event date.

Empty stomachs or those containing only vegetative matter (seagrass and/or algae) were also placed in a voucher container for that event date. All voucher containers were returned to the freezer for storage. A total of 106 of the 294 fish stomachs contained the remains of animals, while 188 were completely empty or contained only vegetative contents.

Identification of Contents

Contents were identified by use of taxonomic keys, field guides and by expert colleagues

(Abele and Kim 1986, Ruppert and Fox 1988, Leslie Haynes, personal communication). Some food items were digested or macerated beyond positive identification. Items found to have parts attributed to teleosts, such as cranium or fins, were classified as Unidentified (UID) Teleost. Any other material that could not be identified, but was clearly of animal origin, was placed in the

19 category UID Organism. Hard parts, such as crab claws, chitinous shell, or fish otoliths, were omitted as they have longer evacuation times and do not necessarily reflect prey items taken during a recent feeding event (Joyce et al. 2002). When analyzing fish stomach contents, there are other mitigating circumstances that need to be considered. Stomach evacuation rate in fishes varies based on the species, size, how quickly different preys types are digested, and ambient water temperature (Adams et al. 2008).

All prey items were identified to the lowest practical taxon based on degree of digestion and body parts indicative of a specific species. For example, positive identification of the flatback mud crab (Eurypanopeus depressus) or mud crabs (Panopeus spp.) was based on whether or not a scoop claw, an orange spot on the 3rd maxilliped or carapace spines were evident. If not, this mud crab would be counted UID Xanthidae. Members of the Penaeidae were treated similarly. Other prey item categories included microgastropods, unknown fish eggs, and, in one case, a grasshopper (Order Orthoptera). Each of these received its own prey item category.

There were several instances where prey items were secondarily ingested, i.e., prey items contained within prey items. Examples included small shrimp, snails and fish eggs; however, the numbers and mass of these items were negligible. In this case, separate items were not categorized but were included with mass measurements as whole prey item in the analysis. A total of 26 prey item categories was established.

After stomach contents were identified and recorded, prey items for each stomach sample were separated by category. These items were then blotted with absorbent paper to remove excess water, left to dry for 20 seconds and then weighed on a digital scale. Values were

20 recorded to the nearest 0.01 gram. All prey items were returned to their individual glass jars and stored as vouchers.

Statistical Analysis

Hyslop (1980) reviewed methodologies developed over the past century that quantify fish feeding habits or stomach content analysis. Examples include determining stomach fullness, wet weight for large samples, and estimation of gut content proportions amongst prey items. Many of these methods are based on Ivlev’s Electivity Index (IEI) (Ivlev 1961) and have shown that the IEI is markedly influenced by the abundance of prey in the natural environment.

Another alternative was considered, the Feeding Importance Degree method proposed by

Andrade and Braga (2005). This method is a useful index when dealing with several fish species with different feeding habitats. However, this method can only be considered when using fish stomachs that are full. While removing stomach contents for this study, it was observed that there were several stomachs that had large volumes of contents present, but each of those was of great volume because of a single prey item such as a large herring or large shrimp that were most likely used as bait. In addition, because of the multitude of species and range of total lengths, determining stomach fullness would be subjective at best. While many of the other stomachs contained multiple organisms, they did not have volumes close to those with single large prey items. There were no stomachs of predator fish sampled in this study that could be deemed full.

For the above reasons, the method selected for the current study is the Importance Index developed by Lima-Junior and Goitein (2001). This method takes into consideration the number of individual prey species, contributing weight, and frequency of occurrence of prey items. The

21 method serves to limit problems of distortion or bias revealed in other statistical approaches and, when applied, can be directly compared with future studies based on a Standard Weight established in this study. The Importance Index ranking of prey found in the stomach contents of transient fishes in Estero Bay will be used to determine whether trophic transfer occurs from oyster reefs to these transient fishes via benthic indicator species, and can be a continuing contribution to oyster reef research.

Importance Index

In order to reduce bias in analyzing fish dietary data, stomach content information was analyzed using an Importance Index based on methodology described by Lima-Junior and

Goitein (2001). This Index takes into consideration how common or rare a prey item is relative to other prey found in the stomach. This analysis was used only with fish with animal prey contents in their guts. Fish with empty stomachs or those containing only plant material were not used in this analysis.

The Importance Index uses a points method, a 3-step process that begins once all stomach content prey items are identified and weighed. To calculate the Importance Index, it was first necessary to compute Frequency of Occurrence and a Volumetric Analysis Index with all 26 prey item categories. The Volumetric Analysis Index is based on a constant that was calculated as the cumulative weight of all prey items from stomachs and divided by the total number of stomachs that contained prey, defining a Standard Weight scale.

Computation of Importance Index

Frequency of Occurrence was calculated for all 26 prey categories and represents that proportion of stomachs containing a particular prey item:

Fi = 100ni /n where

th Fi is the frequency of occurrence of the i prey item in the sample;

th ni is the number of stomachs in which the i item is found;

n is the number of stomachs with prey in the sample.

The Volumetric Analysis Index represents the relative abundance of a particular prey based on the mass of the prey item rather than just occurrence. This formula is based on a Standard

Weight (SW). The SW is calculated as the total weight of all stomach contents divided by the number of stomachs with organism contents:

SW= (∑Si )/ni where

SW is the mean weight for all stomach contents;

∑Si is the sum of all stomach content weights;

ni is the number of stomachs with contents.

Once SW has been determined, a table of ranges is produced that is used to ascribe points to each stomach based on its total weight. As per Lima-Junior and Goitein (2001), the stomach weight that is within the range of weights of the SW will be ascribed 4 points. The scale is then

23 broken down to proportional weight ranges that represent values of 0.5 point each. Points are then ascribed to each fish stomach content’s proportion of total content weight compared to SW.

Points as values should not differ from units of 0.5. Table1 identifies the weight ranges and points to be ascribed.

Table 1. Standard Weight (SW) Table. Weight range table, as recorded in grams, for ascribing points for all stomachs with contents based on total weight.

Standard Wet Weight (SW)

1.88

0.00 0.35 0.59 0.82 1.06 1.30 1.53 2.00 2.24 2.47 2.71 2.94 3.18 3.41 3.65 3.89 Weight 1.76 ------Range 1.99 0.34 0.58 0.82 1.05 1.29 1.53 1.76 2.23 2.46 2.70 2.93 3.17 3.40 3.64 3.88 4.11

Ascribed Points 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 4.5 5.0 5.5 6.0 6.5 7.0 7.5 8.0 8.5

When each stomach has been ascribed points based on total weight, those points are then distributed amongst the various prey items within based on their percentage of that weight.

Table 2. Determining the distribution of points based on total weight of stomach contents. The following is an example based on fish record number 052706-10, grey snapper, Lutjanus griseus. The total stomach weight equals 2.49 grams for 4 prey items. From S.W. Chart: 2.49 grams = 5.5 points

Prey items: E. depressus Panopeus spp. UID Xanthid C. sapidus

Weights (gr.): 0.3572 0.9104 0.0957 1.1272

% total weight 14% 37% 4% 45%

(% wt.) (5.5 pts.) = 0.77 2.03 0.22 2.47

Points distribution: 1 2 0 2.5

In this example, points were distributed based on the percentage of weight for each prey item. For UID Xanthid, no points are ascribed due to the small contribution of weight to the total.

Once all calculations are made and points are distributed to all prey items for all stomachs, points for each prey item are summed, and then an arithmetic mean is calculated.

The value of the proportional item after summing all points for each prey item is:

Mi= (∑i) / n where

Mi is the mean of the ascribed points for the ith prey item;

∑i is the sum of the ascribed points for the ith prey item;

n is the total number of stomachs with prey in the sample.

The Volumetric Analysis Index was then scaled by multiplying the value of Mi by 25 to provide for easier interpretation:

Vi = 25 Mi where

Vi is the Volumetric Analysis Index of the ith prey item in the sample;

Mi is the mean of the ascribed points for the ith prey item.

The Importance Index is used to determine how important a particular prey item is for the diet of predatory fish near oyster reefs in Estero Bay. The first Importance Index ranking was used to determine the difference in relative importance between wet and dry seasons. A second

Importance Index was calculated for all prey items, both seasons inclusive.

Importance Index calculation:

AIi = (Fi ) (Vi)

Where:

th AIi is the Importance Index of the i prey item in the sample;

Fi is the frequency of occurrence of the prey item;

Vi is the Volumetric Analysis Index of the prey item.

Importance Index calculations can then be ranked accordingly to determine the most important prey items for fishes in Estero Bay.

Wet and Dry Season Variation Comparison

To identify seasonal differences in the Importance Index of prey species to the overall fish community, a non-parametric 2 (season) by 7 (prey species) G-test of independence was conducted. The comparison was limited to the seven prey items that had Importance Index values greater than 1% for at least one season. Sixteen prey categories that were never rated higher than 1% were therefore excluded from this analysis.

RESULTS

Estero Bay Water Data

Temperature, rainfall and salinity values are within the normal range for the region’s climactic pattern (LCEL-2006 Annual Data).

Water Temperature

During the time period of this study (January through September), the water temperature was lowest January through February, but began to increase rapidly through April reflecting the seasonal change to summer. Temperature continued to gradually increase to its highest level in

August. Water temperature in the bay fluctuated from a low of 19.0o C in February 2006 to a high of 30.3o C in August 2006 (Fig. 5).

33 31

0 27 25 23

21 Temperature 19 17 15

Month 2006 Monthly Mean Annual Mean (1991- 2004)

Figure 5. 2006 Estero Bay water temperature as reported by EB-13 site for sampling period and annual mean. Temperatures recorded are within typical ranges for Estero Bay. (Lee County Environmental Laboratory, Station EB-13)

Rainfall

30 25 20 15 10

5 Rainfall Rainfall (Centimeters) 0

Month 2006 Monthly Mean

Figure 6. Estero Bay rainfall as reported by EB-13 site for 2006 sampling period and 1991- 2004 annual mean. Rainfall measurements recorded are within typical ranges for Estero Bay. (Lee County Environmental Laboratory, Station EB-13).

Salinity

An increase in salinity occurred from January through May to 36.6 ppt. A relatively drastic decrease occurred during July and August, reflecting the beginning of the rainy season.

During this decrease, appreciable rainfall occurred and was measured at 53.95 cm for these two months (Fig. 7).

25 Salinity Salinity (‰) 20

Month

2006 Monthly Average Monthly Mean (1991- 2004)

Figure 7. Estero Bay 2006 monthly average and 1991−2004 annual means for salinity recordings by Lee County Environmental Laboratory, Station EB-13. Salinity values are typical for Estero Bay (LCEL, EB- 13).

Seasonal Comparison of Captured Predatory Fish and Stomach Content Prey Items

A total of 294 fish representing eleven predator species were collected (Table 3). Of these fish, 106 had some stomach contents (36%). The shortest fish sampled for this study was a 17 cm

Lutjanus griseus. The longest fish was a 58-cm Sciaenops ocellatus. Average fish size was 36.97 cm.

Table 3. The relative abundances of predator fish and those with stomach contents, sampled by season. Predators By Season

Dry Season Wet Season

# with # with Predator Species # Sampled Stomach # Sampled Stomach Contents Contents

Ariopsis felis, hardhead catfish 45 27 14 10

Elops saurus, ladyfish 129 14 0 0

Lutjanus griseus, grey snapper 20 15 14 7

Mugil cephalus, striped mullet 6 0 5 0

Pogonias cromis, black drum 1 0 0 0

Sciaenops ocellatus, red drum 1 0 4 4

Centropomus undecimalis, common snook 13 7 10 6

Caranx hippos, crevalle jack 9 6 1 0

Eugerres plumieri, striped mojarra 1 1 2 2

Pomatomus saltatrix, bluefish 2 0 0 0

Archosargus probatocephalus, sheepshead 9 4 8 3

TOTALS 236 74 58 32

Of the eleven species collected, six were captured during both wet and dry seasons.

However, only five of those species captured during both seasons contained stomach contents.

Two other species had stomach contents only during the dry season, one other species only had stomach contents during the wet season, and three species had no stomach contents in either season.

Predator fish comparisons for dry and wet seasons

A total of 236 fish were caught during the dry season. Of these, 74 had 20 different prey categories in their stomachs. A total of seven of the 11 different fish species sampled had identifiable stomach contents. Dry season sampling yielded 80% of total predator fish sampled.

The majority of these fishes were schooling Elops saurus (ladyfish). Three other species were collected only during the dry season sampling: Pogonias cromis (black drum), Pomatomus saltatrix (bluefish), and Caranx hippos (crevalle jack). The fish sampled during the dry season accounted for 71% of the cumulative stomach content weight for both seasons.

A total of 58 fish were caught during the wet season. Of these, 32 had 21 different prey item categories in their stomachs. Six of the eight different fish species had identifiable stomach contents and accounted for 29% of the total stomach content weight of all fish for both seasons.

Prey Organisms

A total of 464 prey organisms were collected from 106 predator fish stomachs. These prey organisms represented 26 different prey item categories. A total of 20 different families and

20 different species were positively identified. Of the 26 prey categories, 6 were unidentified

(Table 4). These categories represented organisms that could be identified to family, but because of extreme digestion and/or maceration could not be identified to species.

Importance Index: Dry Season Prey

A total of 305 individual prey organisms, representing 20 different prey item categories, were identified from the stomachs of fishes caught during the dry season. The cumulative

Importance Index (AI) for all dry season prey was 965.86 (Table 5).

Dry season indicator species

For all dry season predator stomach contents, six prey categories were identified as indicator species: Eurypanopeus depressus, Panopeus spp., UID Xanthidae, Alpheus heterochaelis, Petrolisthes armatus and, Opsanus beta. When based on overall percentage for all

23 dry season prey categories, UID Xanthidae accounted for 23% of the total value.

Eurypanopeus depressus accounted for 20%. Alpheus heterochaelis accounted for 4%,

Petrolisthes armatus accounted for 2%, and the remaining indicator prey categories Panopeus spp. and Opsanus beta represented < 1% each. For prey items deemed indicator species, cumulative percentage of total AI for dry season was 50%.

Table 4. Relative abundances of stomach content prey organisms by season.

# # Sampled Sampled Species Common Name DRY WET Season Season Eurypanopeus depressus flatback mud crab 42 17 Panopeus spp. mud crabs 2 1 UID xanthid crabs UID xanthid crabs 37 12 Callinectes sapidus blue crab 2 0 Farfantepenaeus duorarum commercial pink shrimp 12 3 Palaemonetes pugio daggerblade grass shrimp 2 1 UID penaeidae UID penaeid 22 13 Alpheus hetrochaelis big claw snapping shrimp 13 2 Petrolisthes armatus green porcelain crab 7 30 Lagodon rhomboides pinfish 1 0 Opsanus beta Gulf toad-fish 1 0 Lophogobius cyprinoides crested goby 2 0 Eucinsostomus gula silver jenny 0 1 Opisthonema oglinum Atlantic thread herring 1 1 Gobiesox strumosus Skillet-fish 0 1 UID Teleost UID teleost 36 20 UID Other UID other 9 5 UID Fish eggs UID fish eggs 8 0 Amphipoda amphipods 5 3 Polychaeta polycheate worms 13 9 Syngnathidae pipefish 6 5 Sabellidae tube worms 100 1 Orthoptera grasshopper 0 1 Trematoda trematodes 0 25 Myrophis punctatus speckled worm eels 0 3 UID Snails UID snails 0 5 Total individuals collected 305 159

Table 5. Importance Index for Dry season prey items with values > 3. For 12 prey items with values < 3, values were summed and placed within Others category for table clarity. Prey items depicted in bold type are indicator species.

Species Dry Season Importance Index (AI)

Eurypanopeus depressus 190.90 Panopeus spp. 4.34 UID xanthid crabs 225.84 Alpheus heterochaelis 41.94 Opsanus beta 3.34 Petrolisthes armatus 18.36 Farfantepenaeus duorarum 29.70 UID Penaeidae 33.26 Opisthonema oglinum 16.69 UID Teleost 358.11 UID Organism 22.03 UID Fish Eggs 6.67 Polychaeta 8.57 Others 6.12

Total AI for Dry Season 965.86

Importance Index: Wet Season Prey

A total of 159 individual prey items, representing 21 different prey categories, were identified within the gut contents of fishes caught during the wet season. The cumulative

Importance Index value for all wet season prey was 448.33 (Table 6).

Table 6. Importance Index for Wet season prey items with values > 3, with the exception of indicator species. For 12 prey items with values < 3, values were summed and placed within “Other” category for table clarity. Prey items depicted in bold type are indicator species.

Species Wet Season Importance Index (AI)

Eurypanopeus depressus 104.13 Panopeus spp. 0.67 UID Xanthidae 116.14 Alpheus heterochaelis 7.23 Petrolisthes armatus 35.49 UID Penaeidae 49.17 Opisthonema oglinum 12.68 UID Teleost 112.92 Other 9.79

Total AI for Wet Season 448.22

There were five prey items identified as indicator species: Eurypanopeus depressus,

Panopeus spp., UID Xanthidae, Alpheus heterochaelis, and Petrolisthes armatus.

UID Xanthidae accounted for 26% of the total wet season value for all 23 prey item categories. Eurypanopeus depressus accounted for 23%, Petrolisthes armatus contributed 8% ,

Alpheus heterochaelis accounted for 2% and, Panopeus spp. represented <1%. The cumulative

AI for the remaining 17 prey items was 186 (41%). For the indicator species, cumulative percentage of total AI for the wet season was 59%.

Importance Index: Combined Dry and Wet Season Prey Totals

A total of 464 individual prey items, representing 26 different prey categories were counted within the total gut contents of both wet and dry season fish caught. The cumulative

Importance Index (AI) value for dry and wet season prey items was 1414.20 (Table 7).

Table 7. Cumulative Importance Index for Dry and Wet seasons. For 10 prey items with values < 1, values were summed and placed within Other category for table clarity. Prey items depicted in bold type are indicator species. Species Importance Index

Eurypanopeus depressus 295.03 Panopeus spp. 5.01 UID Xanthidae 341.98 Alpheus heterochaelis 49.17 Petrolisthes armatus 53.84 Opsanus beta 3.34 Callinectes sapidus 2.22 Farfantepenaeus duorarum 31.04 UID Penaeidae 82.44 Lagodon rhomboides 1.00 Opisthonema oglinum 29.37 UID Teleost 471.03 UID Organism 24.47 UID Fish Eggs 6.67 Polychaeta 10.90 Syngnathidae 4.67 Other 2.01

Total 1414.20

Of the 6 prey categories representing oyster reef residents, the cumulative total AI was

748.37 or 53% of overall Importance Index. UID Xanthidae accounted for 24% of the overall

37 value for all 26 prey item categories. Eurypanopeus depressus accounted for 21%, Alpheus heterochaelis accounted for 3%, and Petrolisthes armatus accounted for 4%. Panopeus spp. and

Opsanus beta accounted for less than 1% each. The cumulative AI of the remaining 20 prey categories was 665.83 or 47% of the overall Importance Index.

Predator Consumption of Prey Items

For 11 species of predator fishes sampled, only six had oyster reef indicator species within the stomach contents (Table 8).

Table 8. Percentage of indicator prey consumption by predator fishes.

Predator fishes Indicator Prey Species

Eurypanopeus Panopeus UID Palaemonetes Alpheus Petrolisthes Opsanus depressus spp. Xanthid pugio heterochaelis armatus beta

Archosargus 6% 9% probatocephalus 53% 73% 57% 38% 18% Ariopsis felis Centropomus 8% 100% undecimalis 4% 1% 35% 100% Elops saurus 22% 27% 4% 18% 61% Lutjanus griseus Sciaenops 22% 25% 9% 11% ocellatus

Stomach content inventory for all fishes containing prey

The following figures represent the prey contained within stomach contents for all fishes sampled. For each prey item, scales are represented as Importance Index values based on each predator species.

Centropomus undecimalis- Common snook

A total of 23 snook were sampled, of which 13 had stomach contents. The percent of the total Importance Index for all prey consumed by snook was 23%. For indicator species only, the total Importance Index percent was 2% (Fig. 8).

300 251.65

250

200

150

100 Importance Index Importance 50 29.04 28.92 12.68 1.33 0.22 1.00 0.11 0

Prey

Centropomus undecimalis- Importance Index of Prey

Figure 8. Importance Index of all prey items consumed by 13 Centropomus undecimalis sampled containing stomach contents.

Ariopsis felis- Hardhead catfish

A total of 59 Ariopsis felis were sampled, of which 37 had stomach contents. The percent of the total Importance Index for all prey consumed by Ariopsis felis was 32%. For indicator species, the total Importance Index percent was 27% (Fig. 9). For Ariopsis felis’ diet, 83% was attributable to oyster reef indicator prey species.

250

193.57

200 156.19 150

100

Importance Index Importance 50 35.49 18.80 9.79 17.13 10.90 3.67 1.45 0.22 6.67 2.67 0.22 0.22 0

Prey

Ariopsis felis- Importance Index of Prey

Figure 9. Importance Index of all prey items consumed by 37 Ariopsis felis sampled containing stomach contents.

Elops saurus- ladyfish

A total of 129 Elops saurus were sampled, of which 14 had stomach contents. The percent of the total Importance Index for all prey consumed by Elops saurus was 5%. For indicator species, the total Importance Index percent was 3% (Fig. 10). For Elops saurus stomach contents, 41% were oyster reef indicator species.

35 29.04 30 25 19.02 20 17.35

15 11.57 10 5 3.23 3.34

Importance Index Importance 1.22 0

Prey

Elops saurus- Importance Index of Prey

Figure 10. Importance Index of all prey items consumed by 14 Elops saurus sampled with stomach contents.

Caranx hippos- crevalle jack

A total of 10 Caranx hippos were sampled, of which six had stomach contents. The percent of the total Importance Index for all prey consumed by Caranx hippos was 9%. There were no stomach content prey items deemed indicator species (Fig. 11).

70 61.30

40 30.37 30

20 16.69 ImportanceIndex 10.68 10 1.33 0 Farfantepenaeus UID Penaeidae Opisthonema UID Teleost Syngnathidae duorarum oglinum

Prey

Caranx hippos- Importance Index

Figure 11. Importance Index of all prey items consumed by six Caranx hippos sampled with stomach contents.

Lutjanus griseus- grey snapper

A total of 34 Lutjanus griseus were sampled, of which 22 had stomach contents. The percent of the total Importance Index for all prey consumed by Lutjanus griseus was 15%. For indicator species, the total Importance Index percent was 8% (Fig. 12). For Lutjanus griseus,

56% of total stomach contents were due to oyster reef indicator species.

100 87.11 90

70 63.63 60 50 40 33.04 30 20 12.90 Importance Index Importance 8.68 4.34 10 1.33 1.11 1.22 0.67 0.22 0

Prey Lutjanus griseus- Importance Index of Prey

Figure 12. Importance Index of all prey items consumed by 22 Lutjanus griseus sampled with stomach contents.

Archosargus probatocephalus- Sheepshead

A total of 17 Archosargus probatocephalus were sampled, of which seven had stomach contents. The percent of the total Importance Index for all prey consumed by Archosargus probatocephalus was 2%. For indicator species, the total Importance Index percent was 1.7%

(Fig. 13). For Archosargus probatocephalus, 56% of total stomach contents were due to oyster reef indicator species.

20 19.36

10 Importance Index Importance

4.89 4.89 5

1.11 0 UID Xanthidae Callinectes sapidus Petrolisthes armatus UID Organism Prey

Archosargus probatocephalus- Importance Index of Prey

Figure 13. Importance Index of all prey items consumed by seven Archosargus probatocephalus sampled with stomach contents.

Eugerres plumieri- striped mojarra

A total of three Eugerres plumieri were sampled, all of which had stomach contents. The percent of the total Importance Index for all prey consumed by Eugerres plumieri was 3%. Stomach contents did not contain any indicator species. The overall total Importance Index percent was

<1% (Fig. 14).

3.5 3.23 3

2.5 2 1.5 1 0.44

0.5 0.33 Importance Index Importance 0 UID Teleost Sabellariidae UID Snails

Prey

Eugerres plumieri- Importance Index of Prey

Figure 14. Importance Index of prey for three Eugerres plumieri sampled.

Sciaenops ocellatus- red drum

A total of five Sciaenops ocellatus were sampled, of which four had stomach contents.

The percent of the total Importance Index for all prey consumed by Sciaenops ocellatus was

13%. For indicator species, the total Importance Index percent was 11% (Fig.15). For Sciaenops ocellatus, 88% of total stomach contents represented oyster reef indicator species.

90 83.88 80

70 63.63 60 50 40 30 17.35 Importance Index Importance 20 10 4.34 6.12 3.23 0 Eurypanopeus UID Xanthidae UID Penaeidae Alpheus Petrolisthes UID Teleost depressus heterochaelis armatus Prey

Figure 15. Importance Index of all prey items consumed by four Sciaenops ocellatus sampled with stomach contents.

DISCUSSION

The specific objectives of this study were to: 1) develop a quantitative description of the diet of predatory fish caught on or near oyster reefs; and 2) determine the contribution of oyster- reef indicator species to the diets of transient fishes sampled on or near oyster reefs in Estero

Bay, Florida. By examining and identifying stomach contents, a quantitative inventory has been derived from fishes captured in proximity to oyster reefs. A total of 26 different prey item categories were established. A total of 6 of those different categories represented organisms that make oyster reefs their primary residence, or oyster reef indicator species as defined in this study.

Results show that for the combined wet and dry season Importance Index, 53% of predator stomach prey items collected can be attributed to organisms that primarily reside on oyster reefs. For prey items found within the gut contents of predators sampled during the dry season, these prey items contributed to 48% of the predator diet as measured using the

Importance Index. During the wet season, the percentage of AI due to oyster community organisms was 58%. This study serves as an extension of the research by Abeels et al (2012) that demonstrated, through stable isotope analysis, the multilevel trophic relationship from organic sources through oyster reef-resident community organisms. This study has demonstrated that energy and biomass are being transferred to higher trophic levels via the indicator prey organisms that reside on reefs to predators, such as fish. Establishing this link has further elevated the value of oysters and the structured reefs they build as important fish habitat, when utilized as feeding stations by predator fish.

The importance of oysters and reef structures in terms of contributing to ecologically and economically important fish species in comparison to other complex habitats such as seagrass meadows and marshes is underappreciated (Coen et al. 1999). Many studies have shown that oyster reef resident species are highly diverse and include numerous species that are rare or non- existent in nearby habitats such as seagrass and mudflats (Zimmerman 1989, Glancy et al. 2003,

Wasno et al., unpublished results). In addition, Peterson et al. (2003) showed that there is a direct correlation between oyster reef production and fisheries production. This study has quantified how important oyster reefs are to supporting fisheries in Estero Bay and, subsequently, through association with offshore pelagic fish, the Gulf of Mexico.

The results of this study show that 53% of the total Important Index prey items consumed by predatory fish were indicator species. For both the dry and wet seasons, specific indicator species prey items ranked consistently among the highest Importance Index totals. Xanthidae,

Alpheus heterochaelis, and Petrolisthes armatus were the most popular prey of multiple predator species.

1. Biological factors

The study site, Decibels Rocks in Estero Bay, was chosen because of its nearly-isolated location to other benthic habitats such as seagrass and mud bottoms. When researching fish and oyster reef community structures to include interactions (i.e., predator-prey trophic coupling), many variables need to be considered. Peterson et al. (2003) showed that many factors contribute to fish and decapod behavior such as oyster reef height, proximity to other habitat types and water depth. Polis et al. (1997) identified factors such as water currents that would influence community structure, particularly at inter-tidal reef sites where foraging predator fish would need

48 to relocate as ebb tide waters receded. Also, it should be noted that numerous studies have shown that reefs made up of older, dead oysters with many of the valves disarticulated will not support same densities of associated organisms as reefs made of living and/or articulated valves (Tolley and Volety 2005, Boudreaux et al. 2006). Another factor determining organism population on a specific habitat is the delicate balance of available resources for organisms (prey) and the number of predators (Abrams 1982).

2. Oyster reef indicator species

The oyster reef indicator species Eurypanopeus depressus, Panopeus spp., Alpheus heterochaelis, Opsanus beta, Petrolisthes armatus, and unidentified Xanthidae have previously been shown to be abundant on oyster reefs in Estero Bay (Tolley et al. 2005, Abeels et al., 2012).

These indicator species have evolved to successfully grow and reproduce on oyster reef habitat.

This established presence can also translate to greater populations than other organisms that primarily reside on other habitat types or are transient across oyster reefs. However, several researchers have demonstrated that the populations of these indicator species can vary, atleast temporarily, from site to site due to several conditional factors. Tolley et al. (2012) showed that decapod larvae will have reduced abundances near reefs due to wet season transport away from tidal creeks and greater abundances during dry months. Other examples of conditions that can limit populations include chlorophyll-a for the Harris mud crab (Rhithropanopeus harrisii)

(Beck 2006) and local hydrology due to reef structure and complexity (Humphries 2010,

Grabowski 2004, and Grabowski et al. 2008).

3. Indicator species are more accessible than many other species of benthic organisms on reefs.

When looking at the stomach contents for each predator species, it is apparent that each predator species has specific target prey when foraging. Each predator has unique feeding behaviors due to its evolution. Predators can be classified in several categories such as lie-in- wait, where fish may lie concealed until prey comes within reach to be engulfed, or grazers, which exhibit continual browsing while drawing in plankton or straining the bay floor searching for small organisms. All of these predators have specialized adaptions that allow them to hunt over specific habitat for their prey.

There are several reasons for the amount of access predators have to prey over oyster reef habitat that are unique amongst other types of habitat. This amount of access equates to the amount of success predators have when hunting over oyster reefs. Oyster reef structure, such as height, size or area covered, majority of live or vacant valves and overall production of oysters is based partly on the physical and water quality parameters of the site itself. Water quality and salinity, wave action created by vessel traffic, weather or tides and bay bottom that allows oysters to successfully settle are the governing forces that create the maze of reefs in the bay. In addition, quantity and quality of nutrients for food and salinity regime will dictate the growth of oyster reefs.

Prey that is classified as indicator species will use specific areas of a reef over other areas based on several factors including: 1) live oysters versus vacant oyster shells and whether they are articulated or loose valves, 2) tidal currents and their access to food within the water column, and 3) exposure to the elements during low-tide. Predators foraging success or failure can be based on an inherent instinct for survival by prey over distinct areas on the reef.

Predator Fish Sampled

A total of 11 species of fish were sampled during this study. Of these species, eight were captured during both dry and wet seasons. These eight species, Centropomus undecimalis,

Sciaenops occelatus, Archosargus probatocephalus, Caranx hippos, Eugerres plumieri, Lutjanus griseus, Ariopsis felis and Mugil cephalus, are typically found year round in Estero Bay. Three species were caught during the dry season only. Of these, only Pogonias cromis maintains a year round presence in Estero Bay. The other two species, Pomatomus saltatrix and Elops saurus migrate between the open Gulf of Mexico and the bay and would be least likely to be caught during the wet season.

It is speculated that more fish were caught during the dry season due to the uniform salinity and relatively constant temperature gradients throughout the bay that allowed greater range of grazing for fish over bay habitats. During the wet season, salinity and water temperature gradients vary greatly between bay waters and open passes to the Gulf of Mexico (Byrne 2003).

In contrast, a fisheries-independent monitoring study was conducted in Estero Bay in 2005 by the Florida Fish and Wildlife Research Institute and determined that monthly catch totals were greatest in August and lowest in December. They did not speculate as to why this had occurred

(FWC-FMRI 2005).

For fisher-folk in Estero Bay, locating target species can be frustrating. Successful professional fishing guides that are working several days a week in Estero Bay will follow schools of fish traversing throughout the water body. As many professional fishing guides know,

“90% of the sport fish are found in 10% of Estero Bay” (Captain Eric Davis, personal communication). In other words, predator fish will move throughout the shallow bay based on

51 water condition factors most likely caused by weather. These factors include winds that cause turbid water thus making feeding more difficult, rain and the associated freshwater runoff that cause salinity gradients, and clouds or lack of clouds that will create temperature fluctuations over the flats or shallow depths.

Prey Item importance to predators

Other results in this study provide a quantitative listing or inventory of prey organisms found on oyster reefs that had been ingested by predatory fishes. Studies have shown community residents of more than 300 different organisms residing on oyster reefs (Wells 1961). The results of this study focus on 19 identifiable species that were eaten by predator fish. The Importance

Index provides a value for those organisms based solely on prey captured and eaten by predators and not by nutritional value that some fish may inherently use for selectivity. A unique study on freshwater brown trout (Salmo trutta) showed wild trout used net energy maximization by cost minimization. Effectively, trout would spend 86% of their time in lie-in-wait feeding mode in areas where energy costs were minimal (Bachman 1984). It could be speculated that some species of fish may duplicate these efforts by looking for the easy prey with maximum nutritional value, while expending as little energy as possible. Predatory fishes can also demonstrate a preference for a particular food item based on learned or instinctive knowledge of its nutritional value. Blue-fish (Pomatomus saltatrix), for example, grow much faster when they consume fish than crustaceans (Juanes and Conover 1994). Future studies may also relate nutritional value to different prey species when using an Importance Index. For this study, the

Importance Index calculations only determined the relative ingestion of the food item but did not

52 provide information or relative nutritional dietary requirements. These variables were not included in the current analysis.

In addition, the basic morphological structure of the predator’s mouth will dictate success for capturing a different array of prey. Many predator fish utilize special morphology and behaviors to capture prey. Oyster reefs could provide unique hiding places that limit success of predatory fish with particular body shapes and feeding styles (Moyle and Cech, 2004). For example, this study has shown the greatest consumer of Xanthidae was the hardhead catfish,

Ariopsis felis. Ariopsis felis has evolved a mouth that can extract mudcrabs from small nooks that would be virtually impossible for some of the other fish that had no decapods in their gut contents.

A third case is made that some fish may choose habitat that has small numbers of prey that are nonetheless easily consumed as opposed to habitat that has larger numbers of prey that, because of the reef’s structural complexity, are not easily accessed (Crowder and Cooper 1982).

Other examples would include complex structures such as mangrove overhangs or bridge fender systems, as opposed to open waters.

CONCLUSION

The characterization of the diets of predatory fish on oyster reefs cannot depend wholly on oyster reef habitat. The organisms contained within the stomachs of these predatory fish are mobile and can spend time between benthic habitats facilitated by tidal currents, drift algae, or active swimming or crawling. The numbers of organisms found on different habitats can vary, but it is apparent that certain prey species of decapods and fishes can be found in greater

53 numbers on oyster reefs. Predators could be selecting prey independent of habitat type in which food resources can be found. However, predator fish will use oyster reefs for feeding, but based on benthic organism inventories for other benthic habitats such as seagrass and mudflats, there is not enough evidence that reefs are exclusive sites for feeding, nor is this likely. Most likely predators will forage in several types of habitat.

This study is unique to Estero Bay in that it uses a Standard Weight for analysis based on predator fish stomach contents of those fishes captured around isolated oyster reefs. In addition, the methodology of Lima-Junior and Goitein (2001) has not been used in this region. The analysis method described by Lima-Junior and Goitein (2001) was used because it allowed for the analysis of a unique data set (multiple fish species, multiple class sizes, and variation of habitat functionality) that can then be used for duplicating this project in similar water bodies using the Standard Weight developed in this study. As similar Florida estuaries are compared using a matrix of studies and analyses based on water quality, supporting habitat, anthropogenic influences, etc., use of a comparative Importance Index based on the Standard Weight developed in this report for prey items may contribute to a Habitat Suitability Index important for maintaining and enhancing sustainable fisheries.

Environmental Value Derived From This Study

Whenever an environmental system is studied, whether it is a small home aquarium or an isolated island, the overall production of the system is based on an established carrying capacity.

The carrying capacity as it relates to the overall health, sustainability and productivity of a system for a particular area or volume depends on three basic attributes: 1) a clean and healthy environment, 2) adequate food and nutrition, and 3) removal of wastes. Oysters and the reefs

54 they engineer provide these three attributes by filtering pollution and absorbing excessive particulate or dissolved organic matterin the water column, thus providing for greater water quality and clarity. The enhanced photic zone in the water column is important to peripheral seagrass meadows. The aquatic vegetation will thrive and, in turn, continue to reduce turbidity by stabilizing the sediment maintaining good water quality essential for a healthy environment.

Oysters provide food and nutrition. Many benthic organisms prey on juvenile oysters and feed on their biodeposits. Through the engineering of structured reefs, oysters provide many benthic inhabitants with refugia that, as revealed in this study, support upper trophic level organisms.

Oysters are unique in this ability to provide many life-supporting benefits that can increase the carrying capacity for estuaries that have adequate oyster assemblages. As a shallow, low energy system such as Estero Bay, water quality parameters can fluctuate rapidly as wet season storm events wash upland pollutants into the bay. It has been estimated that the first inch of storm water run-off contains 90% of the overall impact of the pollutants being washed into the bay (Livingston and McCarron 1988). This influx of chemical and biological pollutants can have a devastating effect on the flora and fauna that make up the coastal environment. A healthy population of oysters as part of a living reef can dampen the effects of this pollution and increase the overall carrying capacity for embayments such as Estero Bay. Because the oyster is the keystone species described by Kennedy et al. (1996), the demise of the oyster and associate reef formations will have trophic consequences that will radiate upward and potentially influence the diet and habitat choices of predators.

This study demonstrates that ecosystem services provided by oyster reefs may have historically been underestimated and that habitat provided by the reefs play an important part in

55 overall estuarine productivity through trophic transfer of biomass to higher level predator species.

When considering the year-round existence of reefs versus the seasonality of marsh-edge and seagrass habitats, and the low productivity of mud flats, the importance of reefs as food resource providers is exponentially greater. The results of this study demonstrate that prey items associated with oyster reefs are an essential component of the diets of predatory fish using these reefs as feeding stations.

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