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.     

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.     

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.     

Effects of roads and crabbing pressures on diamondback terrapin populations in coastal Georgia

Human activities, including the harvesting of natural resources and land development, place substantial pressure on wildlife. The diamondback terrapin (Malaclemys terrapin) is a small, estuarine species of emydid turtle in decline and at risk due to a suite of human activities. Vehicle-induced mortality from increasing coastal traffic and bycatch mortality in crab pots have been recognized as 2 of the primary conservation concerns for terrapins. We used mark-recapture estimates of terrapin density and sex ratio from repeated seining samples of 29 randomly stratified selected tidal creeks to evaluate the current relationships between road and crabbing pressures and the abundance, sex ratio, and size distribution of terrapin populations along the Georgia coast. We obtained 2005 captures of 1,547 individual terrapins among 29 tidal creeks sampled. Population density estimates ranged from 0 to 1,040 terrapins/km among tidal creeks with a median density of 65 terrapins/km. Among all sites, terrapin density declined with increasing crabbing activity within the creek, but was not related to proximity to roads. Sex ratios did not vary significantly with crabbing activity or proximity to roads; however, we found a significantly larger proportion of smaller-sized terrapins in creeks with no crabbing activity. Although roads may have significant localized effects on terrapin populations, we found no measurable association between proximity to roads and current variation in terrapin density along the Georgia coast. However, we did find that terrapin density and the proportion of smaller sized individuals within the population were negatively associated with crabbing activities. Bycatch from commercial and recreational activities threaten many species. We add to a growing body of research showing crabbing activities are affecting diamondback terrapin populations across much of the species' range. States committed to the conservation of terrapins and coastal species should focus on reducing bycatch risk; for example by regulating soak times and locations, requiring the use of bycatch reduction devices, and removing abandoned or lost crab pots from coastal habitats. © 2011 The Wildlife Society.     

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.     

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).     

Genetic effects of eelgrass restoration efforts by fishers' seeding to recover seagrass beds as an important natural capital for coastal ecosystem services

The reestablishment of seagrass vegetation is a vital part of recovering coastal marine ecosystem services. Historically the Hinase area was a famous for the fishing by coastal pound netting in eelgrass beds, but this practice was progressively displaced with oyster farming due to an enormous decline in seagrass vegetation. For several decades, the local fishers' cooperative has worked to restore eelgrass beds by a seeding method. Through these efforts, seagrass vegetation in their fishing area has increased to about half of their previous area. This study examined the effect of long-term seeding by fishers on the recovery of eelgrass beds in the Hinase area, based on analysis of eelgrass genetic structure using microsatellite markers. Specimens for the DNA analysis were collected from each of all eelgrass meadows that the fishers conducted sowing eelgrass seeds as well as from the source sites where they collected the seeds. The results found that restored beds in the study area have high genetic diversity comparable to natural ones. The multiple regression analysis revealed that a combined model of seedling intensity and geographic distance (R² = .457) better explained genetic structure across our sampling sites than models of seedling intensity (R² = .092) or geographic distance only (R² = .344). This supports that the eelgrass seeds they sowed did not disturb the genetic structure but rather supplemented natural dispersal, suggesting that the fishers' seeding did not develop nonnatural seagrass meadows but certainly contributed to the recovery of natural seagrass meadows.     

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.     

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.     

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.     

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.     

Innovative Techniques for Large‐scale Seagrass Restoration Using Zostera marina (eelgrass) Seeds

The use of Zostera marina (eelgrass) seeds for seagrass restoration is increasingly recognized as an alternative to transplanting shoots as losses of seagrass habitat generate interest in large‐scale restoration. We explored new techniques for efficient large‐scale restoration of Z. marina using seeds by addressing the factors limiting seed collection, processing, survival, and distribution. We tested an existing mechanical harvesting system for expanding the scale of seed collections, and developed and evaluated two new experimental systems. A seeding technique using buoys holding reproductive shoots at restoration sites to eliminate seed storage was tested along with new techniques for reducing seed‐processing labor. A series of experiments evaluated storage conditions that maintain viability of seeds during summer storage for fall planting. Finally, a new mechanical seed‐planting technique appropriate for large scales was developed and tested. Mechanical harvesting was an effective approach for collecting seeds, and impacts on donor beds were low. Deploying seed‐bearing shoots in buoys produced fewer seedlings and required more effort than isolating, storing, and hand‐broadcasting seeds in the fall. We show that viable seeds can be separated from grass wrack based on seed fall velocity and that seed survival during storage can be high (92–95% survival over 3 months). Mechanical seed‐planting did not enhance seedling establishment at our sites, but may be a useful tool for evaluating restoration sites. Our work demonstrates the potential for expanding the scale of seed‐based Z. marina restoration but the limiting factor remains the low rate of initial seedling establishment from broadcast seeds.     

Seasonal changes in thermal environment and metabolic enzyme activity in the diamondback terrapin (Malaclemys terrapin)

Diamondback terrapins experience broad fluctuations in temperature on both a daily and seasonal basis in their estuarine environment. We measured metabolic enzyme activity in terrapin muscle tissue to assess thermal dependence and the role of temperature in seasonal metabolic downregulation in this species. Activity of lactate dehydrogenase (LDH), pyruvate kinase (PK), citrate synthase (CS), and cytochrome c oxidase (CCO) was assayed at 10, 20, 30, and 40 °C for tissue collected during summer and winter. The Q(10) for enzyme activity varied between 1.31 and 2.11 within the temperature range at which terrapins were active (20-40 °C). The Q(10) for LDH, CS, and CCO varied between 1.39 and 1.76 and between 10 and 20 °C, but PK exhibited heightened thermal sensitivity within this lower temperature range, with a Q(10) of 2.90 for summer-collected tissue and 5.55 for winter-collected tissue. There was no significant effect of season on activity of LDH or PK, but activity of CS and CCO was significantly lower in winter-collected tissue compared with summer-collected tissue. Results indicate that temperature effects contribute to seasonal metabolic downregulation and dormancy in terrapins, but other environmental factors (i.e. oxygen availability), as well as seasonal shifts in blood biochemistry and circulating hormones may also play an important role.     

海草种子特性与海草床修复

海草床面积的急剧减少已引起人们对海草床生态修复的重视, 种子在海草床修复中具有较大的应用潜力。该文系统归纳了近年来有关海草种子的研究概况及其应用进展: 从种子生物学和生态学角度对海草种子的形态结构、发育、散布、休眠和萌发进行了归纳比较; 提出了在研究天然海草种子库的同时, 有必要建立人工海草种子库的观点, 并指出建立和完善人工海草种子库需基于种子生物学和生态学研究, 以指导种子的采集和保存; 对海草种子的播种方式和利用种子修复海草床的途径进行了阐述, 并指出了目前研究和应用中存在的一系列问题。最后对海草种子的研究和应用前景进行了展望, 提出海草种子生态学将成为今后的研究热点, 在应用方面, 仍然需要以提高种子萌发率和成苗率为研究重点, 并指出如果利用由种子获得的人工幼苗进行海草床修复, 需首先解决幼苗成活率低的难题。     

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.     

Seed rafting as a dispersal strategy for eelgrass (Zostera marina)

Using observations, experiments and model simulations we investigate the possibility and range of long-distance dispersal by seed rafting in eelgrass, Zostera marina, at the Swedish west coast. A field experiment showed that the breaking strength of post-flowering rhipidia decreased significantly over a 30-day period, indicating that ontogenetic changes of the morphology facilitate dislodgement of the rhipidia at the optimal time for dispersal. We recorded positive buoyancy of detached post-flowering rhipidia for at least 26 days. Finally, we found evidence for sexual reproduction via seeds in the study area. These results, together with field measurements of wind-driven surface-transport velocity of rhipidia and wind data from 7 years, allowed us to model a dispersal potential of up to 150 km in one season along the Swedish west coast, which corresponds well with published estimates of dispersal potential from both observational and genetic studies. The results add to evidence that rafting of seeds on floating reproductive shoots is an important dispersal strategy for eelgrass, allowing for colonisation of new areas and for recolonisation after die-back events.     

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.     

Drinking and water expulsion in the diamondback turtle Malaclemys terrapin

Postural and kinematic characteristics of the drinking behaviour in the diamondback turtle, Malaclemys terrapin (Latreille) were investigated by video and high-speed filming experiments. Head, jaw and throat movements in drinking cycles are described. Postures of neck and head were compared for three water depths (2, 10 and 30 mm). Water expulsion, occurring after the turtle was disturbed, is also kinematically described. Finally, a drinking mechanism in the turtle is proposed.     

Seed dispersal by pygmy chimpanzees (Pan paniscus): A preliminary report

The role in seed dispersal played by the pygmy chimpanzees (Pan paniscus) inhabiting Wamba, Republic of Zaïre, was studied. Germination was tested for seeds of 17 plant species recovered from the feces of pygmy chimpanzees at Wamba. The fecal seeds of 13 species germinated, and in six of the species the germination rate for the fecal seeds was higher than that of control seeds. Although five other species showed a higher germination rate in the control seeds than in the fecal seeds, the remaining two species revealed no difference in germination rate between the fecal and control seeds. There was no great difference in germination velocity between the fecal and control seeds of the same species. For comparison, seeds of four plant species collected from the feces of common chimpanzees (Pan troglodytes) and gibbons (Hylobates lar) in captivity in Okinawa were tested for their germinability. In this test, although the seeds had passed through the digestive tract, their germinability demonstrated little change. Based on the behavioral characteristics of the pygmy chimpanzee at Wamba and observations of the captive primates on Okinawa, it seems that pygmy chimpanzees may play an important role in the seed dispersal of fruit plant species at Wamba.