Evaluating uncertainty to improve a common monitoring method and guide management decisions for diamond-backed terrapins

Designing monitoring with adequate certainty to evaluate management actions can be challenging, especially for elusive species in relatively inaccessible habitats. The diamond-backed terrapin (Malaclemys terrapin) is considered a high priority species for management in all states within its range. Among key threats to terrapin populations is bycatch mortality in crab pots, prompting states throughout the species' range to consider crabbing regulations and creating a need for a monitoring approach able to evaluate the success of any new crabbing regulations to benefit terrapins. Because terrapins occupy extensive and often difficult to access estuarine habitat, it is hard to collect sufficient data to estimate population responses accurately and precisely for management. To assist state managers with decisions regarding monitoring bycatch reduction regulations, we modeled 12 years of terrapin capture-recapture data. We used estimates from those models to simulate capture-recapture data pre- and post-implementation of bycatch reduction that resulted in a 0.20 absolute increase in mean apparent survival probability. Results indicated weak reliability of a monitoring approach using only manual seining of tidal creeks to detect a real management effect, with a positive management effect detected at the 95% certainty level only 34% of the time. When we considered 85% and 75% certainty thresholds, we detected a positive effect on survival among 61% and 75% of simulations, respectively. Low within-year recapture probability and the effect of tide amplitude on terrapin availability indicate there is low feasibility of improving monitoring precision at a single site, requiring monitoring of more sites to improve confidence in the detection of the management effect. The number of sites monitored depends on the acceptable level of certainty. We recommend that researchers and management entities that use seining assess the level of certainty they require to evaluate management actions and increase the number of sites sampled to meet that level of certainty. Additionally, the use of multiple monitoring methods and integrated models should be explored to reduce uncertainty and to allow for easier monitoring of more populations over broader spatial scales.     

Mitigating by-catch of diamondback terrapins in crab pots

Chronic by-catch of diamondback terrapins (Malaclemys terrapin) in blue crab (Callinectes sapidus) pots is a concern for terrapin conservation along the United States Atlantic and Gulf of Mexico coasts. Despite the availability of by-catch reduction devices (BRDs) for crab pots, adoption of BRDs has not been mandated and by-catch of terrapins continues. We conducted experimental fishing studies in North Carolina's year-round blue crab fishery from 2000 to 2004 to evaluate the ability of various BRDs to reduce terrapin by-catch without a concomitant reduction in the catch of blue crabs. In 4,822 crab pot days fished, we recorded only 21 terrapin captures. Estimated capture rates were 0.003 terrapins/pot per day in hard crab experimental fishing and 0.008 terrapins/pot per day in peeler experimental fishing. All terrapin captures occurred from April to mid-May within 321.4 m of the shoreline. Longer soak times produced more dead terrapins, with 4 live and 4 dead during hard crab experimental fishing and 11 live and 2 dead during peeler experimental fishing. The 4.0-cm BRDs in fall and 4.5-cm and 5.0-cm BRDs in spring reduced the catch of legal-sized male hard crabs by 26.6%, 21.2%, and 5.7%, respectively. Only the 5.0-cm BRDs did not significantly affect the catch of legal-sized hard male crabs. However, BRDs had no measurable effect on catch of target crabs in the peeler crab fishery. Our results identify 3 complementary and economically feasible tools for blue crab fishery managers to exclude terrapins from commercially fished crab pots in North Carolina: 1) gear modifications (e.g., BRDs); 2) distance-to-shore restrictions; and 3) time-of-year regulations. These measures combined could provide a reduction in terrapin by-catch of up to 95% without a significant reduction in target crab catch. © 2011 The Wildlife Society.     

Survival rates of two nesting aggregations of diamondback terrapins at neighboring sites in New York City

The diamondback terrapin (Malaclemys terrapin) is a charismatic and long-lived species of the United States eastern coast, and the only North American turtle that exclusively inhabits coastal brackish waters. Many terrapin populations are declining, and these declines have been largely linked to human activities; however, few studies have documented human and natural factors affecting terrapin population demography. Jamaica Bay, an urban estuary located in southern New York City, USA, is home to 2 nesting aggregations of terrapins, located at Ruler's Bar Hassock (RBH) and John F. Kennedy Airport (JFK). We analyzed mark-recapture data for RBH from 2003–2018 and JFK from 2011–2018 to estimate annual survivorship of female diamondback terrapins and test the effects of 3 factors (a hurricane, water quality represented by nitrogen concentration, and injuries) on survival. The initial estimated annual survival was high (0.93) at RBH but declined to 0.89, while survival remained constant at JFK (0.92). Models examining the effect of Hurricane Sandy (2012) indicated a significant decline in survival in the 2 years following the hurricane in the RBH nesting aggregation but no change at JFK. Water quality did not influence trends in either aggregation, but the presence of major injuries (caused by boat collisions, predators, and the hurricane) significantly reduced annual survival at RBH. We propose increasing terrapin survivorship through mitigation of boat traffic, reducing populations of northern raccoons (Procyon lotor) to reduce injury to female terrapins and decrease egg and hatchling mortality, and increased law enforcement to reduce on-going poaching and capture as illegal by-catch.     

Sex-biased dispersal and natal philopatry in the diamondback terrapin, Malaclemys terrapin

Nesting ecology and population studies indicate that diamondback terrapins (Malaclemys terrapin) exhibit nest site fidelity and high habitat fidelity. However, genetic studies indicate high levels of gene flow. Because dispersal affects the genetics and population dynamics of a species, we used six highly polymorphic microsatellite markers to investigate sex-biased dispersal and natal philopatry of M. terrapin in Barnegat Bay, NJ. We compared results of spatial autocorrelation analysis, assignment methods and Wright's F(ST) estimators to a mark-recapture analysis. Mark-recapture analysis over a 4-year period indicated that most individuals have relatively small home ranges (<2 km), with mature females displaying greater home ranges than males. Goodness of fit analysis of our mark-recapture study indicated that some juvenile males were likely transient individuals moving through our study location. Mean assignment indices and first-generation migrant tests indicated that mature males were more prone to disperse than mature females, but first-generation migrant tests indicated that per capita there are more female than male dispersers. Thus, the relative importance of males and females on gene flow in terrapin populations may change in relation to population sex ratios. Spatial autocorrelation analysis indicated that mature females exhibited natal philopatry to nesting beaches, but first-generation migrant tests indicated that a small number of females failed to nest on natal beaches. Finally, we discuss the important conservation implications of male-biased dispersal and natal philopatry in the diamondback terrapin.     

Recreational Boats and Turtles: Behavioral Mismatches Result in High Rates of Injury

Recreational boats are a dominant feature of estuarine waters in the United States. Boat strike injury and mortality may have a detrimental effect on populations of diamondback terrapins (Malaclemys terrapin), a keystone species in estuarine ecosystems. In Barnegat Bay, New Jersey, 11% of terrapins (n = 2,644) have scars consistent with injuries from boats. Conservative estimates of injury rates from boats increased from 2006 to 2011. When exposed to playback recordings of approaching boat engines of varying sizes and speeds in situ, terrapins did not significantly change their behavior in response to sounds of boat engines of different sizes. The lack of behavioral response of terrapins to boat sounds helps explain high rates of injury and mortality of terrapins and may threaten the viability of terrapin populations. Boater education courses that discuss impacts of boats to wildlife, combined with closure of areas of high terrapin densities to boating, are necessary to protect terrapins and other aquatic species from injury and mortality caused by motorized boats.     

Evidence of Eelgrass (Zostera marina) Seed Dispersal by Northern Diamondback Terrapin (Malaclemys terrapin terrapin) in Lower Chesapeake Bay

The initial discovery in May 2009 of eelgrass (Zostera marina) seeds in fecal samples of wild-caught northern diamondback terrapins (Malaclemys terrapin terrapin) was the first field evidence of eelgrass seed ingestion in this species. This finding suggested the potential of terrapins as seed dispersers in eelgrass beds, which we sampled for two additional years (2010 and 2011). Seeds were only found in feces of terrapins captured prior to June 8 in all three years, coinciding with eelgrass seed maturation and release. Numbers of seeds in terrapin feces varied annually and decreased greatly in 2011 after an eelgrass die off in late 2010. The condition of seeds in terrapin feces was viable-mature, germinated, damaged, or immature. Of terrapins captured during time of seed release, 97% were males and juvenile females, both of which had head widths <30 mm. The fraction of individuals with ingested seeds was 33% for males, 35% for small females, and only 6% for large (mature) females. Probability of seed ingestion decreased exponentially with increasing terrapin head width; only males and small females (head width <30 mm) were likely to be vectors of seed dispersal. The characteristic that diamondback terrapins have well-defined home ranges allowed us to estimate the number of terrapins potentially dispersing eelgrass seeds annually. In seagrass beds of the Goodwin Islands region (lower York River, Virginia), there were 559 to 799 terrapins, which could disperse between 1,341 and 1,677 eelgrass seeds annually. These would represent a small proportion of total seed production within a single seagrass bed. However, based on probable home range distances, terrapins can easily traverse eelgrass meadow boundaries, thereby dispersing seeds beyond the bed of origin. Given the relatively short dispersion distance of eelgrass seeds, the diamondback terrapin may be a major source of inter-bed seed dispersal and genetic diversity.     

Introduced delicacy or native species? A natural origin of Bermudian terrapins supported by fossil and genetic data

Humans have greatly altered the natural distribution of species, making it difficult to distinguish between natural and introduced populations. This is a problem for conservation efforts because native or introduced status can determine whether a species is afforded protection or persecuted as an invasive pest. Holocene colonization events are especially difficult to discern, particularly when the species in question is a naturally good disperser and widely transported by people. In this study, we test the origin of such a species, the diamondback terrapin (Malaclemys terrapin), on Bermuda using a combination of palaeontologic (fossil, radiometric and palaeoenvironmental) and genetic data. These lines of evidence support the hypothesis that terrapins are relatively recent (between 3000 and 400 years ago) natural colonizers of Bermuda. The tiny population of Bermudian terrapins represents the second naturally occurring non-marine reptile that still survives on one of the most densely populated and heavily developed oceanic islands in the world. We recommend that they should be given protection as a native species.     

Isolation of Fecal Coliform Bacteria from the Diamondback Terrapin (Malaclemys terrapin centrata)

Total and fecal coliform bacteria were isolated from the cloaca and feces of the estuarine diamondback terrapin. The majority of samples contained fecal coliforms. Escherichia coli was the predominant fecal coliform species isolated, and members of the genus Salmonella were isolated from 2 of 39 terrapins. Fecal coliform numbers are used to regulate shellfish harvests, and diamondback terrapins inhabit the brackish-water habitats where oyster beds are found; therefore, these findings have implications for the efficacy of current regulatory parameters in shellfishing waters.     

Regional differentiation among populations of the Diamondback terrapin (Malaclemys terrapin)

The Diamondback terrapin (Malaclemys terrapin) is a brackish-water turtle species whose populations have been fragmented due to anthropogenic activity such as development of coastal habitat and entrapment in commercial blue crab (Callinectes sapidus) fishing gear. Genetic analyses can improve conservation efforts for the long-term protection of the species. We used microsatellite DNA analysis to investigate levels of gene flow among and genetic variability within 21 geographically separate collections of the species distributed from Massachusetts to Texas. Quantified levels of genetic variability (allelic diversity, genotypic frequencies, and heterozygosity) revealed three zones of genetic discontinuity, resulting in four discrete populations: Northeast Atlantic, Coastal Mid-Atlantic, Florida and Texas/Louisiana. The average number of alleles and expected heterozygosity for the four genetic clusters were N_A = 6.54 and H_E = 0.050, respectively. However, the geographic boundaries of the populations did not correspond to accepted terrapin subspecies limits. Our results illuminate not only the need to sample terrapins in additional sites, specifically in the southeast, but also the necessity for allowing uninterrupted gene flow among population groupings to preserve current levels of genetic diversity.     

Factors affecting temperature variation and habitat use in free-ranging diamondback terrapins

Measuring the thermal conditions of aquatic reptiles with temperature dataloggers is a cost-effective way to study their behavior and habitat use. Temperature dataloggers are a particularly useful and informative approach to studying organisms such as the estuarine diamondback terrapin (Malaclemys terrapin) that inhabits a dynamic environment often inaccessible to researchers. We used carapace-mounted dataloggers to measure hourly carapace temperature (T_c) of free-ranging terrapins in South Carolina from October 2007 to 2008 to examine the effects of month, sex, creek site, and tide on T_c and to determine the effects of month, sex, and time of day on terrapin basking frequency. Simultaneous measurements of environmental temperatures (T_e; shallow mud, deep mud, water) allowed us to make inferences about terrapin microhabitat use. Terrapin T_c differed significantly among months and creek and between sexes. Terrapin microhabitat use also varied monthly, with shallow mud temperature being the best predictor of T_c November–March and water temperature being the best predictor of T_c April–October. Terrapins basked most frequently in spring and fall and males basked more frequently than females. Our study contributes to a fuller understanding of terrapin thermal biology and provides support for using dataloggers to investigate behavior and habitat use of aquatic ectotherms inhabiting dynamic environments.     

Population genetics of the diamondback terrapin (Malaclemys terrapin)

We examined the population genetic structure of the diamondback terrapins (Malaclemys terrapin), within and among estuaries. Based on mark-recapture studies, these estuarine turtles have high site fidelity that is likely to make them vulnerable to local extinctions. We tested if observed site fidelity of adults would be reflected in intraestuarine population genetic structure of six highly polymorphic microsatellite loci (five tetranucleotide and one dinucleotide). No evidence was found for population structuring within the Charleston estuary nor among three different estuaries in South Carolina. We then examined four other terrapin populations from North Carolina to New York, as well as from the Florida Keys and from Texas. With increasing geographical distance, genetic differentiation increased from South Carolina through New York, but overall values were low. The dinucleotide locus contributed significantly more to the genetic differentiation of some population comparisons than any of the other loci. Interestingly, terrapins from South Carolina to New York were much more genetically similar to those from Texas (rho = 0.154) than to those from Florida (rho = 0.357). We attribute this pattern to extensive translocations of terrapins during the early 20th century to replenish diminished populations and to provide turtle farms with stocks. Terrapins collected in Texas were especially sought for shipment to the northeastern US because of their larger size. Our study indicates no population structure within or among adjacent estuaries. Thus, the mark-recapture information from adult and subadult feeding locations is a poor predictor of population genetic structure. Additionally, it appears that past human activities may have drastically altered the genetics of current populations. Finally, our data suggest that translocation of eggs or head starting of terrapins within estuaries or among adjacent estuaries is acceptable from a genetic standpoint.     

Spatiotemporal analysis of gene flow in Chesapeake Bay Diamondback Terrapins (Malaclemys terrapin)

There is widespread concern regarding the impacts of anthropogenic activities on connectivity among populations of plants and animals, and understanding how contemporary and historical processes shape metapopulation dynamics is crucial for setting appropriate conservation targets. We used genetic data to identify population clusters and quantify gene flow over historical and contemporary time frames in the Diamondback Terrapin (Malaclemys terrapin). This species has a long and complicated history with humans, including commercial overharvesting and subsequent translocation events during the early twentieth century. Today, terrapins face threats from habitat loss and mortality in fisheries bycatch. To evaluate population structure and gene flow among Diamondback Terrapin populations in the Chesapeake Bay region, we sampled 617 individuals from 15 localities and screened individuals at 12 polymorphic microsatellite loci. Our goals were to demarcate metapopulation structure, quantify genetic diversity, estimate effective population sizes, and document temporal changes in gene flow. We found that terrapins in the Chesapeake Bay region harbour high levels of genetic diversity and form four populations. Effective population sizes were variable. Among most population comparisons, estimates of historical and contemporary terrapin gene flow were generally low (m ≈ 0.01). However, we detected a substantial increase in contemporary gene flow into Chesapeake Bay from populations outside the bay, as well as between two populations within Chesapeake Bay, possibly as a consequence of translocations during the early twentieth century. Our study shows that inferences across multiple time scales are needed to evaluate population connectivity, especially as recent changes may identify threats to population persistence.     

Microsatellite DNA loci from the Diamondback terrapin (Malaclemys terrapin)

We describe polymerase chain recation (PCR) primers and conditions to amplify one dinucleotide and five tetranucleotide microsatellite DNA loci isolated from the Diamondback terrapin (Malaclemys terrapin). The PCR primers were tested on 21 terrapins from Cape Romain, SC, USA. The microsatellite primers developed yielded a high number of alleles (8–14) and high observed heterozygosities (0.57–1.0).     

Of mudsnails,terrapins, and flukes: Use of trematodes as a field‐based project in parasitology research

We present an exercise for counting trematode cysts on mudsnails that can be implemented as a field‐based project in course work by students or by volunteers. The exercise involves the digenetic trematode Pleurogonius malaclemys, which infects diamondback terrapins (Malaclemys terrapin) as its definitive host, and eastern mudsnails (Tritia obsoleta) as its intermediate host. The trematode forms macroscopic metacercarial cysts on the shells and opercula of the mudsnails, and the life cycle is completed when terrapins ingest the intermediate hosts with cysts. Previous research has suggested that quantifying cysts on mudsnails can be a relatively simple method to estimate terrapin population sizes where terrapins co‐occur with mudsnails. Three non‐professional scientist groups (including students and volunteers) were tested in their estimates of prevalence and intensity data compared to verified cyst counts. Prevalence data were relatively accurate (~76–78%) and reliable (68–89%) across the groups. The intensity of cysts (on shells and opercula of mudsnails) were mostly within 12% of the verified counts (total mean intensity of 1.81–2.97 cysts/parasitized mudsnail) but varied significantly in two cases due to false positives (likely due to sand grains or debris scored as cysts) or negatives (likely due to missed cysts behind the operculum). The exercise can be completed as a lab or series of labs in courses, and data from such projects could be used in terrapin conservation efforts, particularly in helping scientists determine where terrapins occur. We discuss modification of the exercise for other trematode species in regions around the world and hope this expands recognition by the public of the important role of parasites in ecosystems.     

Maximum standard metabolic rate corresponds with the salinity of maximum growth in hatchlings of the estuarine northern diamondback terrapin (Malaclemys terrapin terrapin): Implications for habitat conservation

I evaluated standard metabolic rates (SMR) of hatchling northern diamondback terrapins (Malaclemys terrapin terrapin) across a range of salinities (salinity = 1.5, 4, 8, 12, and 16 psu) that they may encounter in brackish habitats such as those in the Maryland portion of the Chesapeake Bay, U.S.A. Consumption of O₂ and production of CO₂ by resting, unfed animals served as estimates of SMR. A peak in SMR occurred at 8 psu which corresponds closely with the salinity at which hatchling growth was previously shown to be maximized (salinity ∼ 9 psu). It appears that SMR is influenced by growth, perhaps reflecting investments in catabolic pathways that fuel anabolism. This ecophysiological information can inform environmental conservation and management activities by identifying portions of the estuary that are bioenergetically optimal for growth of hatchling terrapins. I suggest that conservation and restoration efforts to protect terrapin populations in oligo-to mesohaline habitats should prioritize protection or creation of habitats in regions where average salinity is near 8 psu and energetic investments in growth appear to be maximized.     

Hermit crabs, humans and Mozambique mangroves

There is a complex interrelationship between upper shore hermit crabs (such as Coenobita sp. and Clibanarius sp.), coastal human populations and mangrove forests in Mozambique. The abundance, activity, shell selection and behaviour of three species of hermit crab are related to the level of mangrove cover. With increased density of mangrove trees, the study species of hermit crab changed in abundance, tended to become diurnal, spent more time feeding and were clustered in larger groups when doing so, and selected longer spired shells. All five of the same variables are also linked to the proximity and activity of humans through both direct and indirect actions. Direct effects included a tendency to nocturnal activity with proximity to human activity; indirect effects included increased and more clumped food supplies, and shell middens from intertidal harvesting and deforestation. Mangroves are important to local human populations as well as to hermit crabs, for a wide variety of (similar) reasons. Mangroves provide storm shelter, fisheries and fishery nursery grounds for adjacent human settlements, but they also harbour mosquito populations and their removal provides valuable building materials and fuel. Hermit crabs may be useful (indirectly) to coastal human populations by being a source of food to certain commercial species, and by quickly consuming rotting/discarded food and faeces (thereby reducing disease and pests). They can also cause minor problems to coastal human populations because they use shells of (fisheries) target mollusc species and can be more abundant than the living molluscs, thereby slowing down effective hand collection through confusion over identification. The mixture of positive and negative attributes that the three groups impart to each other in the Quirimba Archipelago, northern Mozambique, is discussed.     

Effects of salinity and flooding on seedlings of cabbage palm (Sabal palmetto)

Sabal palmetto (Walt.) Lodd. ex Schultes (cabbage palm) dominates the coastal limit of many forests in North Florida and Georgia, United States. Changes in saltwater flooding due to sea level rise have been credicted with pushing the coastal limit of cabbage palms inland, eliminating regeneration before causing death of mature trees. Localized freshwater discharge along the coast causes different forest stands to experience tidal flooding with waters that differ in salinity. To elucidate the effect of such variation on regeneration failure under tidal flooding, we examined relative effects of flooding and salinity on the performance of cabbage palm seedlings. We examined the relationship between seedling establishment and degree of tidal inundation in the field, compared the ability of seedlings to withstand tidal flooding at two coastal sites that differed in tidal water salinity, and investigated the physiological responses of cabbage palm seedlings to salinity and flooding in a factorial greenhouse experiment. Seedling survival was inversely correlated with depth and frequency of tidal flooding. Survival of seedlings at a coastal site flooded by waters low in salinity [c. 3 parts per thousand (ppt)] was greater than that at a site flooded by waters higher in salinity (up to 23 ppt). Greenhouse experiments revealed that leaves of seedlings in pots flushed twice daily with salt solutions of 0 ppt and 8 ppt exhibited little difference in midmorning net CO₂ assimilation rates; those flushed with solutions of 15 ppt and 22 ppt, in contrast, had such low rates that they could not be detected. Net CO₂ assimilation rates also declined with increasing salinity for seedlings in pots that were continuously inundated. Continuous root zone inundation appeared to ameliorate effects of salinity on photosynthesis, presumably due to increased salt concentrations and possibly water deficits in periodically flushed pots. Such problems associated with periodic flushing by salt water may play a role in the mortality of cabbage palm seedlings in the field. The salinity range in which plant performance plummeted in the greenhouse was consistent with the salinity difference found between our two coastal study sites, suggesting that variation in tidal water salinity along the coast plays an important role in the ability of cabbage palm seedlings to withstand tidal flooding.     

Egg masses on the move: corixid oviposition on terrapin shells

In a very dry year, when aquatic habitats were scarce, we observed exceptionally massive corixid oviposition on terrapin shells in Doñana National Park, southwestern Spain. Most terrapins inhabiting a large pond devoid of aquatic vegetation exhibited a dense cover of corixid eggs, whilst terrapins from vegetated ponds had no egg cover. Corixid oviposition had also been observed on terrapin shells in previous periods of severe drought. Considering that terrapins frequently alternate between aquatic and terrestrial environments, we experimentally assessed the viability of corixid eggs in varying degrees of dry-exposure. A significant proportion of corixid eggs did not hatch when they were occasionally dried under sun exposure, but egg mortality was lower when they were dried in the shade. The massive oviposition on terrapin shells was probably a consequence of the limited availability of adequate oviposition sites, and it might increase the odds of egg survival when terrapins migrate to other ponds.     

Genetic Population Structure of Local Populations of the Endangered Saltmarsh Sesarmid Crab Clistocoeloma sinense in Japan

During recent decades, over 40% of Japanese estuarine tidal flats have been lost due to coastal developments. Local populations of the saltmarsh sesarmid crab Clistocoeloma sinense, designated as an endangered species due to the limited suitable saltmarsh habitat available, have decreased accordingly, being now represented as small remnant populations. Several such populations in Tokyo Bay, have been recognised as representing distributional limits of the species. To clarify the genetic diversity and connectivity among local coastal populations of Japanese Clistocoeloma sinense, including those in Tokyo Bay, mitochondrial DNA analyses were conducted in the hope of providing fundamental information for future conservation studies and an understanding of metapopulation dynamics through larval dispersal among local populations. All of the populations sampled indicated low levels of genetic diversity, which may have resulted from recent population bottlenecks or founder events. However, the results also revealed clear genetic differentiation between two enclosed-water populations in Tokyo Bay and Ise-Mikawa Bay, suggesting the existence of a barrier to larval transport between these two water bodies. Since the maintenance of genetic connectivity is a requirement of local population stability, the preservation of extant habitats and restoration of saltmarshes along the coast of Japan may be the most effective measures for conservation of this endangered species.