Anomalies in the Diets of Malaclemys terrapin, the Northern Diamondback Terrapin, in the Bays of Long Island, NY: The Impact of Urbanization on Unusual Diet Prey Item PFO (Percent Frequency of Occurrence)

 

Introduction

Nesting female diamondback terrapin


Beside the mudflats of Jamaica Bay, underneath the willow trees, I immediately took cover, disguising myself with the local American beach grass. While the tall tips of the beach grass tickled my dirtied face and deer flies constantly attacked my vulnerable lower legs, I didn’t dare move for I was on a mission: to observe and record nature’s ultimate gift. There she sat, the female diamondback terrapin, diligently digging through the rocky ground of Jamaica Bay in order to lay her precious eggs. What a sight. For a moment, the annoying tickle and the bites did not seem to bother me. In fact, at this moment, nothing bothered me; the pressures and expectations of school, family, friends, and society all vanished for a transient moment. I was awestruck at the clumsy tap dance of the female, attempting to cover up her eggs with her awkward webbed feet. 

From this moment on, I was captivated by the estuaries of New York, their ecological structure, and the complexities of life they nurture. I was especially passionate about the northern diamondback terrapin, which would always charm me with its lifestyle and behaviors. As a result, I started to volunteer with a local conservation group in the Jamaica Bay Wildlife Refuge, protecting terrapin eggs and helping to restore the bay.

During the summer of 2013, I had the opportunity to use my passion for terrapins; with the help of the Jamaica Bay Terrapin Research and Conservation Group, I was able to conduct a full diet analysis study of the adult diamondback terrapins of Long Island. I spent most of my time doing what I do best: stalking the female terrapins that surface to lay their eggs and capturing them for data samples. I consider this experience the most valuable of my life. This opportunity not only peaked my curiosity and passion but also instilled in me the dream of becoming a wildlife veterinarian.

My curiosity about the terrapins propelled my research goals. I wanted to examine the ecological niche on Long Island that terrapins filled, and the impact of urbanization on them, which might be hindering them. As a result, I came up with the proper research question: What prey species do local terrapin diets consist of, and how has urbanization impacted their diet? Interested in finding the answer for myself, I began to investigate, collect, and study the fecal samples of urban terrapin populations. By conducting a fecal analysis, I could gain a holistic picture of the terrapins and their aquatic environment.

 

Background

Malaclemys terrapin terrapin, the northern diamondback terrapin, is a species of Emydid turtle native to brackish coastal waters of the eastern U.S., ranging from Cape Cod to Cape Hatteras along the Atlantic Coast (Ernst et al.). Research revealed that terrapins are found in a variety of estuarine environments, including coastal marshlands, coves, tidal rivers, and the lagoons behind barrier beaches (Ernst et al.).

The northern diamondback terrapin


The Malaclemys terrapin terrapin is a commonly studied species of turtle. Studies have uncovered many aspects of its behavior and life patterns, including nesting behavior (Roosenburg et al.), hibernation, hatchling behavior (King), population density (Simoes), and diet (King). These studies conclude that terrapins are dietary generalists who consume a variety of crustaceans, bivalves, fish, and gastropods.

Few studies, however, have investigated the diet of terrapin populations in urban areas such as Long Island. In New York State, the diamondback terrapin is a species under heavy threat. Due to overhunting, habitat loss, increasing predatory raccoon populations, highly polluted waters, and urbanization since the 1900’s, New York terrapin populations have  diminished significantly (Burke). As a result, dietary, behavioral, and ecological data and research are required for proper conservation management (Burke).

In this study, I hypothesized that the terrapin populations in Jamaica Bay would have a diet similar to the terrapin populations in Oyster Bay because both bays have similar ecosystems (Burke). By examining the terrapins’ diet, I could create a holistic picture of the terrapins and their interactions in aquatic environments and be able to evaluate the impact of urbanization on their diet.

 

Study Sites

Geographical locations of study sites. (Site A: Jamaica Bay, New York; Site B: Oyster Bay, New York)

Click to enlarge


This study collected dietary data from the terrapins in Jamaica Bay and compared that data to past data from terrapins in Oyster Bay, because the largest populations of terrapins on Long Island are found in those two bays (Burke).

Characterization of the current and past availability of potential prey items in study sites is crucial to understanding the diets of terrapins (King). 

 

Site A: Jamaica Bay. Polyhaline embayment at the southwestern end of Long Island.

Specific Site: Jamaica Bay Wildlife Refuge

Over the past three centuries, Jamaica Bay has lost 90% of its salt marshes and 95% of its freshwater wetlands. Northern quahogs, soft-shell clams, Atlantic ribbed mussels, eastern mud snails, and common slipper snails are abundant in Jamaica Bay’s mudflats, tidal zones, and deep waters (King).

 

Site B: Oyster Bay. Oyster Bay Harbor, located on the north shore of Long Island.

Specific Site: Mill Neck Creek

The Oyster Bay creeks and mudflats support soft-shell clams, Atlantic ribbed mussels, oysters, annelids, snails, and crustaceans such as crab and shrimp (Petrochic).

Study sites: Mill Neck Creek in Oyster Bay (left), Terrapin nesting ground Oyster Bay (right)

Study sites: Mill Neck Creek in Oyster Bay (left), Terrapin nesting ground Oyster Bay (right)



Materials and Methods

Proper handling of diamondback terrapins


Female terrapin trying to escape from the cooler


Jamaica Bay fecal samples stored in vials.


Fecal Sample Collection

Field research took place during the nesting season of female diamondback terrapins, in early June to early August 2013. After the female terrapins had surfaced and nested in each of the study sites of Jamaica Bay and Oyster Bay, they were collected inside individual coolers with approximately 25 liters of freshwater each, allowing for full coverage of their carapaces without drowning the animals. Each of the terrapins was soaked for three to four days until they defecated. Evaporated water was replaced inside the coolers daily, and the terrapins were released back to their habitats immediately after defecation.

The feces were filtered and stored by pouring the water inside the coolers into a sieve and preserving any solid material in formalin (later preserved in ethanol for safety). The filtered fecal samples were collected in numbered vials that recorded the date of collection, study site, and tag number. (Note that each terrapin had its own individual vial.)

Fecal Analysis

In order to identify the prey remains inside the fecal samples, common terrapin prey items in Jamaica Bay and Oyster Bay were collected from each of the sites and crushed into the sizes of the matter found in terrapin feces. For this study I collected and smashed the desiccated shells of most commonly found invertebrates: Atlantic blue crab, rough periwinkle, bay scallop, Atlantic ribbed mussel, American oyster, amethyst gem clam, periwinkle, eastern mud snail, common slipper snail, and soft-shell clam. The crushed prey items were then used as standards to identify the unknown prey pieces found in the fecal samples.

Crushed Atlantic ribbed mussel standards (left), Atlantic ribbed mussel found in fecal sample (right)

Crushed Atlantic ribbed mussel standards (left), Atlantic ribbed mussel found in fecal sample (right)


The fecal samples were placed on petri dishes and examined through a dissecting microscope. Undeterminable prey pieces were separated out using forceps and compared to the prepared standard prey items. Prey items were classified into the following categories: Algae (sea lettuce and other algae-like material); Plantae (leaves, stem, grass, and seeds); Bivalvia (soft-shell clam, Atlantic ribbed mussel, and amethyst gem clam); Gastropoda (eastern mud snail, slipper snail, and periwinkle); Crustacea (crabs); Insecta; Annelids; and Unidentifiable Animal Tissue. This study ultimately calculated the percent frequency of occurrence (PFO) by summing up the number of times each prey item was identified in the fecal samples and dividing that number by the total number of terrapins collected in the particular study site. (This study did not measure the proportions of prey items in fecal matter; only the presence of prey items was checked off for each of the fecal samples.)

Chang Won examining fecal sample using a dissecting microscope (left). Undeterminable prey pieces were separated out (right).

Chang Won examining fecal sample using a dissecting microscope (left). Undeterminable prey pieces were separated out (right).


 

Data/Results

Fifty-six fecal samples (n=56) were collected from individual terrapins in Jamaica Bay.

Figure 1 shows the Percent Frequency of Occurrence of major prey items in Jamaica Bay terrapin diets. Unusually high PFOs of algae (sea lettuce) and plant material were found during this study. In addition, the JB terrapins did not consume large amounts of marine gastropods unlike many other terrapin populations in Connecticut, Florida, and other states. (King 2007)


Figure 2 shows the overall PFOs of classified prey items. In Jamaica Bay, terrapin diets mostly consist of Bivalves (Mostly Soft-Shell Clams). Unusually high values of algae and plants were found, and gastropod PFOs were reported extremely low.


Fecal samples collected from individual terrapins in Oyster Bay (Petrochic).

Fecal samples were collected from individual terrapins in Oyster Bay (Petrochic, 2009)

Figure 3 shows the recalculated Percent Frequency of Occurrence of Major Prey Items in Oyster Bay from previous dietary data stated in (Petrochic 2009). Unlike JB terrapin diets, the Oyster Bay terrapins consumed a wide variety of prey items (the highest PFO being Eastern Mudsnails). Similar results were found, however; algae (sea lettuce) and plant material were found in abundance in Oyster Bay as well as Jamaica Bay.


Figure 4 shows that the Oyster Bay Terrapins consume a wide variety of prey items.


Interestingly, the terrapins’ main prey items in Oyster Bay were gastropods such as rough periwinkles and eastern mud snails, which was different from Jamaica Bay. However, both Oyster Bay and Jamaica Bay terrapin diets included high PFOs for algae and plant material.

  

Discussion

Algae found in fecal samples


Analyzing the data samples collected during my field research suggested that urbanization on Long Island has drastically increased the algae content in terrapin diets in both Jamaica Bay and Oyster Bay. In Jamaica Bay, nearly 39% of terrapin diets consisted of some species of algae or sea lettuce. In Oyster Bay, terrapin diets consisted of 21% algae. Diamondback terrapins are not known to consume any type of plant or algal species (Burke). Therefore, it is especially surprising that such high percentages were possible in both diets. Such high PFOs of algae and plant material may be correlated with the burying behavior of soft-shell clams and Atlantic ribbed mussels (Zwarts). While foraging through algae-filled mudflats for prey, terrapins may accidentally ingest large amounts of algal matter.

The high algae PFOs in their diet directly correlate with increasing algae density in Long Island. Because of urbanization and climate change, excess nitrogen loads, pollutants, rising sea levels, and warmer climates have lead to an overpopulation of algae and eutrophication in estuarine mudflats (Mackenzie, 2005). A major threat to conserving terrapin populations is the increasing algae population. Studies have shown that the expansion of sea lettuce may reduce the number of macroinvertebrates on sedimentary surfaces, and as a result significantly lower the presence of terrapin prey species. In addition, eutrophication and algal blooms may suffocate the smooth cordgrass marshlands that nurture millions of estuarine life forms, including the terrapin (Mackenzie, 2005).

Eastern mudsnail found in the fecal matter of an Oyster Bay terrapin


Although the diets of Oyster Bay and Jamaica Bay terrapins were similar in their high percentage of algae, they also differed significantly, despite the fact that the two bays are only 45 miles from each other. While Jamaica Bay terrapin diets consisted mostly of bivalves, Oyster Bay terrapin diets consisted of a variety of prey items, including gastropod species such as the eastern mud snail. Interestingly, studies show that the habitats of Oyster and Jamaica Bay have similar invertebrate communities (Burke). Although there is an abundance of gastropod populations in Jamaica Bay for the terrapins to feast on, the terrapins do not attempt to consume gastropods (extremely low PFO of 2%). Although not enough data was collected to draw a conclusion, the Jamaica Bay and Oyster Bay terrapins may have developed disparate evolutionary features. For example, eastern mud snails are a highly resilient species, requiring as much as 250 Newtons of force to crack open (Petrochic). The Oyster Bay terrapins may have more developed jaws to crack open the resilient mud snail shells. On the other hand, Jamaica Bay terrapins may be unable to crack open such tough prey or are simply reluctant to waste energy on a futile hunt.  

 

Conclusion

This research showed that urbanization has directly impacted the diets of diamondback terrapins in both Jamaica Bay and Oyster Bay. Urbanization and climate change have led to an explosion of algal matter in the estuarine mudflats; therefore, the diamondback terrapins may be accidentally ingesting a large amount of algae. The increase in algae is a potential risk to both the terrapins and the estuarine environment. Algae may suffocate the prey items of terrapins as well as destroy the Spartina cordgrass plants that house many invertebrates. In addition, algal toxin may prove to be deleterious to the terrapins’ health as well.

This research also revealed that there are important disparities between the diets of Jamaica Bay and Oyster Bay terrapins. Thus, my original hypothesis is rejected. While Oyster Bay terrapins consumed a variety of prey items, mostly gastropods such as eastern mud snails, the Jamaica Bay terrapins consumed only bivalves such as soft-shell clams. Because both sites share similar invertebrate communities, the disparities may lie in the terrapins themselves. One population may have developed stronger jaw strength than the other population in order to adapt to the local environment. This finding further suggests that the two aquatic environments may be quite different as well.

 

Further Research

As a result of my diet studies at the two sites, I developed new questions based on the disparities between the diets of the two terrapin populations. In order to measure the possibly distinct evolutionary differences among local populations, I will measure terrapin bite force, scale mud snail shell strength/resistance, and conduct a population census on eastern mud snail populations in both Jamaica Bay and Oyster Bay during the summer of 2014. In addition, I will compare my results to terrapin populations in Georgia and Florida in order to have a holistic picture of the terrapins within their estuarine environments and to evaluate the impact of urbanization on them.

  

Bibliography

Burke, Russell L., Susan M. Felice, and Sabrina G. Sobel. “Changes in Raccoon (Procyon lotor) Predation Behavior Affects Turtle (Malaclemys terrapin) Nest Census.” Chelonian Conservation and Biology 8 (2009): 208-11. Print.

Ehret, Dana J., and Ralph E. Werner. “Malaclemys terrapin terrapin (northern diamondback terrapin) diet.” Herpetological Review 35 (2004): 265. Print.

Ernst, Carl H., Jeffery E. Lovich, and Roger William Barbour. Turtles of the United States and Canada. Washington D.C.: Smithsonian Institution, 1994. Print.

King, Thomas M. “The diet of hatchling Northern Diamondback Terrapins (Order Testudines; Malaclemys terrapin terrapin).” M.S. thesis., Long Island University, 2007. Print.

MacKenzie, C.L. “The Abundances of Small Invertebrates in Relation to Sea Lettuce, Ulva lactuca.” Bulletin of the New Jersey Academy of Science 45 (2000): 13-17. Print.

MacKenzie, C.L. “Removal of Sea Lettuce, Ulva spp., in Estuaries to Improve the Environments for Invertebrates, Fish, Wading Birds, and Eelgrass, Zostera marina.” Marine Fisheries Review 67 (2005): 1-8. Print.

Petrochic, Sara L. “Feeding ecology of the northern diamondback terrapin, Malaclemys terrapin terrapin.” M.S. thesis., Long Island University, 2009. Print.

Roosenburg, Willem M. “Nesting Habitat Requirements of the Diamondback Terrapin: A Geographic Comparison.” Wetland Journal 6.2 (1994): 8-11. Print.

Simoes, Jose C. and Randolph M. Chambers, “A Population Study of Diamondback Terrapins of Piermont Marsh, Hudson River, NY.” In J.R. Waldman and W.C. Nieder (eds.), Reports of the Tibor T. Polgar Fellowship Program, Hudson River Program, 1997. PDF.

Zwarts, L., and J. Wanink. “Siphon size and burying depth in deposit- and suspension-feeding benthic bivalves.” Marine Biology 100: 227-40. Print.