Ozobranchus jantseanus (Clitellata: Ozobranchidae) from Reeve’s Turtle,Mauremys reevesii: New Annelid Fauna in Korea

Turtle leeches have not been recorded in Korea, although they occur in geographically adjacent countries including China and Japan. This study describes a turtle leech, Ozobranchus jantseanus (Clitellata: Ozobranchidae), found from Reeve’s turtle (Mauremys reevesii) in Korea. Of the 143 Reeve’s turtles collected from the freshwater reservoir in Jinju City, Gyeongsangnam-do, Korea, 95 unidentified leeches were found in 8 (5.6%) individuals. The leeches had 22 somites with 11 pairs of externally exposed branchiae, body-sized posterior suckers, and spines on the dorsal surface. We identified these leeches as Ozobranchus jantseanus Oka, 1912 (Clitellata: Ozobranchidae). This species of turtle leeches found in Korea may fill the gap in the biodiversity of East Asian annulus.     

Characterization and cross-species amplification of microsatellites from the endangered Hawksbill turtle (Eretmochelys imbricate)

Twelve novel polymorphic microsatellites were isolated from the endangered Hawksbill turtle (Eretmochelys imbricate). Eight of 12 markers were used to study genetic diversity of two sea turtle species: E. imbricate and green sea turtle (C. mydas). In E. imbricate, the average allele number of the eight microsatellites was 6.25/locus with a range of 3–13. The average expected and observed heterozygosity was 0.66 and 0.63 respectively. In C. mydas, the average allele number of the eight markers was 11.63/locus. The observed heterozyosity (0.68) was lower than the expected heterozyosity (0.79). Most of 12 microsatellites amplified specific and polymorphic PCR products in other six turtle species. Hence, the developed microsatellites would facilitate studies on genetic diversity and population structure of E. imbricate and other marine turtle species.     

Observations on Haemogregarina balli sp. n. from the Common Snapping Turtle,Chelydra serpentina*

SYNOPSIS. Haemogregarina balli sp. n. is described from the blood and organs of the common snapping turtle Chelydra serpentina serpentina and from the gastric and intestinal ceca of the presumed invertebrate hosts, the leeches Placobdella parasitica and Placobdella ornata. In the peripheral blood of the turtle, male and female gametocytes and immature erythrocytic schizonts are found within erythrocytes. The maturation of erythrocytic schizonts containing 6–8 merozoites is recorded from liver imprints. Schizonts with 13–25 merozoites are found in various cells of the liver, lung and spleen. In the gastric ceca of the leeches the host erythrocytes are digested, releasing the gametocytes and immature erythrocytic schizonts. Immature erythrocytic schizonts degenerate. Association of the gametocytes occurs in the intestinal ceca. The microgametocyte apparently gives rise to 4 nonmotile microgametes, one of which fertilizes the macrogamete while the other remain as condensed, residual nuclei on the periphery of the developing oocyst. The oocyst increases in size with maturity. A mature oocyst produces 8 sporozoites from a single germinal center. Sporozoites liberated from the oocyst are found in the tissues of the leech. Transovarial transmission of the parasite does not occur in the turtle. Attempts at experimental transmission failed. Previously unfed (control) leeches were negative for the parasite. Haemogregarina balli is compared with other haemogregarines described from C. serpentina. Features of species of Haemogregarina and Hepatozoon as well as the taxonomy of these genera are discussed.     

Nuclear markers reveal a complex introgression pattern among marine turtle species on the Brazilian coast

Surprisingly, a high frequency of interspecific sea turtle hybrids has been previously recorded in a nesting site along a short stretch of the Brazilian coast. Mitochondrial DNA data indicated that as much as 43% of the females identified as Eretmochelys imbricata are hybrids in this area (Bahia State of Brazil). It is a remarkable find, because most of the nesting sites surveyed worldwide, including some in northern Brazil, presents no hybrids, and rare Caribbean sites present no more than 2% of hybrids. Thus, a detailed understanding of the hybridization process is needed to evaluate natural or anthropogenic causes of this regional phenomenon in Brazil, which could be an important factor affecting the conservation of this population. We analysed a set of 12 nuclear markers to investigate the pattern of hybridization involving three species of sea turtles: hawksbill (E. imbricata), loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea). Our data indicate that most of the individuals in the crossings L. olivacea × E. imbricata and L. olivacea × C. caretta are F1 hybrids, whereas C. caretta × E. imbricata crossings present F1 and backcrosses with both parental species. In addition, the C. caretta × E. imbricata hybridization seems to be gender and species biased, and we also found one individual with evidence of multispecies hybridization among C. caretta × E. imbricata × Chelonia mydas. The overall results also indicate that hybridization in this area is a recent phenomenon, spanning at least two generations or ～40 years.     

Tetranucleotide markers from the loggerhead sea turtle (Caretta caretta) and their cross-amplification in other marine turtle species

The loggerhead sea turtle (Caretta caretta) is a federally threatened species and listed as endangered by the World Conservation Union (IUCN). We describe primers and polymerase chain reaction (PCR) conditions to amplify 11 novel tetranucleotide microsatellite loci from the loggerhead sea turtle. We tested primers using samples from 22 females that nested at Melbourne Beach, Florida (USA). Primer pairs yielded an average of 11.2 alleles per locus (range of 4–24), an average observed heterozygosity of 0.83 (range 0.59–0.96), and an average polymorphic information content of 0.80 (range 0.62–0.94). We also demonstrate the utility of these primers, in addition to primers for 15 loci previously described, for amplifying microsatellite loci in four additional species representing the two extant marine turtle families: olive ridley (Lepidochelys olivacea), hawksbill (Eretmochelys imbricata), green turtle (Chelonia mydas), and leatherback (Dermochelys coriacea).     

Predicted distributions and abundances of the sea turtle ‘lost years’ in the western North Atlantic Ocean

Oceanic dispersal characterizes the early juvenile life-stages of numerous marine species of conservation concern. This early stage may be a ‘critical period’ for many species, playing an overriding role in population dynamics. Often, relatively little information is available on their distribution during this period, limiting the effectiveness of efforts to understand environmental and anthropogenic impacts on these species. Here we present a simple model to predict annual variation in the distribution and abundance of oceanic-stage juvenile sea turtles based on species’ reproductive output, movement and mortality. We simulated dispersal of 25 cohorts (1993–2017) of oceanic-stage juveniles by tracking the movements of virtual hatchling sea turtles released in a hindcast ocean circulation model. We then used estimates of annual hatchling production from Kemp's ridley Lepidochelys kempii (n = 3), green Chelonia mydas (n = 8) and loggerhead Caretta caretta (n = 5) nesting areas in the northwestern Atlantic (inclusive of the Gulf of Mexico, Caribbean Sea and eastern seaboard of the U.S.) and their stage-specific mortality rates to weight dispersal predictions. The model's predictions indicate spatial heterogeneity in turtle distribution across their marine range, identify locations of increasing turtle abundance (notably along the U.S. coast), and provide valuable context for temporal variation in the stranding of young sea turtles across the Gulf of Mexico. Further effort to collect demographic, distribution and behavioral data that refine, complement and extend the utility of this modeling approach for sea turtles and other dispersive marine taxa is warranted. Finally, generating these spatially-explicit predictions of turtle abundance required extensive international collaboration among scientists; our findings indicate that continued conservation of these sea turtle populations and the management of the numerous anthropogenic activities that operate in the northwestern Atlantic Ocean will require similar international coordination.     

Historical perspectives on population genetics and conservation of three marine turtle species

Considerable phylogeographic and population genetic research has been conducted on marine turtles. Less attention, however, has been paid to the historical patterns and processes that have led to present patterns of genetic structure, and particularly, how these populations have responded to major climatic changes in the past. To address these questions, we analyzed previously published mitochondrial haplotype data independently for three marine turtle species, the loggerhead (Caretta caretta), hawksbill (Eretmochelys imbricata), and green turtle (Chelonia mydas). Considering all three species, we conducted analyses on a total of 657 individuals from 36 nesting beaches in the Atlantic and Mediterranean. Our results suggest that much of the contemporary genetic structure has been significantly affected by complex patterns of historical population subdivision, long-distance dispersal, and restricted geneflow. These inferences also imply that the climatic and sea level fluctuations during the Pleistocene may have had contrasting effects on genetic structure (e.g., fragmenting versus homogenizing) and on population sizes. Estimates of historical and current effective population sizes further highlight differential demographic responses across species to historical climatic cycles. Collectively, our results provide evidence for the occurrence of historical refugia through climatic cycles and complex historical metapopulation dynamics, and identify common and unique patterns of metapopulation structure across species. These historical patterns provide a basis for predictive estimates of metapopulation responses to habitat loss, population extirpation, and global climatic change.     

Heavy Metal Accumulation in Four Species of Sea Turtles from the Baja California Peninsula, Mexico

Heavy metals were assessed in four species of sea turtles from the Baja California Peninsula, Mexico, representing the first report of heavy metal concentrations in tissues of post-yearling sea turtles from the Eastern Pacific. Concentrations of Cd measured in C. mydas kidney (653 μg/g dry wt) were the highest ever reported for any sea turtle species. Cd accumulated preferentially in kidney and the ratios of kidney to liver Cd in Baja California turtles were among the highest reported for sea turtles globally. Zn, Ni, and Mn concentrations were also significantly higher in kidney than other tissues, while Cu and Fe were greatest in liver, and all metals were lowest in muscle. With the exception of one value (69.9 μg/g in kidney of C. caretta), Pb was low in all tissues from Baja California. In comparisons across species, kidney of C. mydas had greater Zn and Ni concentrations as compared to other species, although there was no difference in liver metal levels among the species. Positive correlations were detected in the concentrations of Cd, Cu and Ni with the straight carapace length of C. caretta.     

Impacts of a geotextile container dune core on marine turtle nesting in Juno Beach,Florida, United States

Hard armoring technologies (e.g. rock revetments and seawalls), which are installed to protect homes from beach erosion, can diminish the aesthetics and amenity of the beach. Over time, these structures cause beach narrowing and often prevent marine turtle access to nesting habitat altogether. An alternative armoring technology, known as geotextile dune core systems (or geocores), has been developed and implemented to protect inland infrastructure from beach erosion, yet there remains an absence of research on possible effects on marine turtles. In this study, we examined the impacts of a geocore installed on Juno Beach, Florida, United States in February 2014 on loggerhead (Caretta caretta) and green turtle (Chelonia mydas) nesting success, hatching success, and emergence success. A before‐after‐control‐impact paired series design evaluated the difference in nesting success per week for the impact and control sites 4 years before (2010–2013) and 4 years after (2014–2017) the installation of the geocore. Neither loggerhead nor green turtle nesting success was significantly different after the installation of the geocore; however, when analyzing loggerhead crawls that came to within 5 m of the geotextile bags, nesting success decreased. Neither hatching nor emergence success was significantly different after the installation of the geocore for either species. Our results suggest that geocores may minimally affect loggerhead and green turtles and provide a suitable restoration technique for homeowners facing beach erosion.     

Twelve new polymorphic microsatellite markers from the loggerhead sea turtle (Caretta caretta) and cross-species amplification on other marine turtle species

We describe 12 new polymorphic dinucleotide microsatellite loci and multiplex Polymerase Chain Reaction conditions from the loggerhead sea turtle Caretta caretta. Levels of polymorphism were assessed in 50 individuals from the nesting population of the Cape Verde Islands. Number of alleles ranged from 3 to 13 (average of 7.33) and the values of observed heterozygosities from 0.32 to 0.80 (average of 0.61). Cross-species amplification on three other marine turtles, Chelonia mydas, Eretmochelys imbricata and Dermochelys coriacea, revealed polymorphism and variability at eight, eleven and three loci, respectively.     

Egg-feeding in the freshwater piscicolid leech Cystobranchus virginicus (Annelida, Hirudinea)

Abstract. Leeches are common terrestrial and aquatic annelids, parasitizing or feeding on a wide range of host taxa. Here we report evidence for an unusual feeding behavior of egg‐feeding in the piscicolid leech Cystobranchus virginicus. We identified distended specimens of C. virginicus in the nests of at least 4 different fish species: Campostoma anomalum, Moxostoma carinatum, Moxostoma sp. (either M. anisurum and/or M. breviceps), and Nocomis leptocephalus. We collected a total of 41 leeches from the nests of these host species and documented at least 1 leech in 19 of 55 nests (35%), with many sites containing multiple leeches. Individuals of C. virginicus were not identified feeding on any of the 41 adult specimens of Moxostoma spp. or the 635 adult specimens of Nocomis leptocephalus examined, and were never found in the absence of active host spawning (26 sites). These results are consistent with individuals of C. virginicus being an opportunistic or possibly even an obligate egg‐feeder, potentially timing their own reproductive activities with the spawning of their fish hosts. The current distribution of C. virginicus has been expanded to include North Carolina, South Carolina, and Tennessee. The potential for leech species to induce mortality in developing fish eggs could be a concern for fish conservation and merits further investigation.     

Early growth and development of morphological defenses in post-hatchling flatbacks (Natator depressus) and green turtles (Chelonia mydas)

Marine turtles produce hundreds of precocial offspring (“hatchlings”) that are virtually defenseless. Many are consumed by predators. Hatchlings improve their survival prospects by migrating to offshore “nursery” areas with lower predator densities and, as they grow, by developing morphological defenses. The flatback turtle (Natator depressus), however, remains in the predator-rich coastal waters of Australia. To gain insights into how they survive there, we compared patterns of early growth and morphological development in flatbacks to their closest relative, the green turtle (Chelonia mydas), which migrates offshore. We found that morphological structures likely to be used in defense are better developed in juvenile flatbacks than in juvenile green turtles. Those structures probably represent one of a suite of characters that enable young flatbacks to survive in coastal habitats where interactions with predators are likely to be more frequent.     

Leech removal is not the primary driver of basking behavior in a freshwater turtle

Leaving the water to bask (usually in the sun) is a common behavior for many freshwater turtles, with some species also engaging in “nocturnal basking.” Ectoparasite removal is an obvious hypothesis to explain nocturnal basking and has also been proposed as a key driver of diurnal basking. However, the efficacy of basking, day or night, to remove leeches has not been experimentally tested. Therefore, we examined the number of leeches that were removed from Krefft''s river turtles (Emydura macquarii krefftii) after experimentally making turtles bask at a range of times of day, durations, and temperatures. Turtles had high initial leech loads, with a mean of 32.1 leeches per turtle. Diurnal basking under a heat lamp for 3 hr at ~28°C significantly reduced numbers of leeches relative to controls. In diurnal trials, 90.9% of turtles lost leeches (mean loss of 7.1 leeches per turtle), whereas basking for 30 min under the same conditions was not effective (no turtles lost leeches, and all turtles were still visibly wet). Similarly, “nocturnal basking” at ~23°C for 3 hr was not effective at removing leeches. Only 18% of turtles lost leeches (one turtle lost one leech and another lost four leeches). Diurnal basking outdoors under direct sunlight for 20 min (mean temp = 34.5°C) resulted in a small reduction in leeches, with 50% of turtles losing leeches and an average loss of 0.7 leeches per turtle. These results indicate basking can remove leeches if temperatures are high or basking durations are long. However, it was only effective at unusually long basking durations in this system. Our data showed even the 20‐min period was longer than 70.1% of natural diurnal basking events, many of which took place at cooler temperatures. Therefore, leech removal does not appear to be the purpose of the majority of basking events.     

Diversity of features of the female reproductive system and other morphological characters in leeches (Citellata,Hirudinida) in phylogenetic conception

An epistemological–evolutionary conception of leeches (Hirudinida) based on features of the female reproductive system in combination with other morphological characters is presented in the spirit of the cladistic school of taxonomy. Characters relating to the structure of the ovary and the course of oogenesis in leeches were interpreted in this manner, for the first time. Each study was conducted on type species of higher taxonomic groups of true leeches. Results of analyses using features of the reproductive system only as well as in combination with other morphological characters show Piscicolidae and Glossiphoniidae as sister clades making Rhynchobdellida a monophyletic group. Also, Hirudiniformes and Erpobdelliformes appeared to be sister clades within Arhynchobdellida. The relationship between the outgroup specimens and leeches remained unresolved, because both Acanthobdella peledina and branchiobdellidans appeared to be in an equivocal relationship to hirudinidans. Characters concerning the structure of the female reproductive system and course of oogenesis thus appeared to be useful, although conservative, for reconstruction of leech phylogeny, and they well reflect phylogenetic relationships of Hirudinida at the family level.     

Validating the use of stereo‐video cameras to conduct remote measurements of sea turtles

Point 1: Stereo‐video camera systems (SVCSs) are a promising tool to remotely measure body size of wild animals without the need for animal handling. Here, we assessed the accuracy of SVCSs for measuring straight carapace length (SCL) of sea turtles.Point 2: To achieve this, we hand captured and measured 63 juvenile, subadult, and adult sea turtles across three species: greens, Chelonia mydas (n = 52); loggerheads, Caretta caretta (n = 8); and Kemp''s ridley, Lepidochelys kempii (n = 3) in the waters off Eleuthera, The Bahamas and Crystal River, Florida, USA, between May and November 2019. Upon release, we filmed these individuals with the SVCS. We performed photogrammetric analysis to extract stereo SCL measurements (eSCL), which were then compared to the (manual) capture measurements (mSCL).Point 3: mSCL ranged from 25.9 to 89.2 cm, while eSCL ranged from 24.7 to 91.4 cm. Mean percent bias of eSCL ranged from −0.61% (±0.11 SE) to −4.46% (±0.31 SE) across all species and locations. We statistically analyzed potential drivers of measurement error, including distance of the turtle to the SVCS, turtle angle, image quality, turtle size, capture location, and species.Point 4: Using a linear mixed effects model, we found that the distance between the turtle and the SVCS was the primary factor influencing measurement error. Our research suggests that stereo‐video technology enables high‐quality measurements of sea turtle body size collected in situ without the need for hand‐capturing individuals. This study contributes to the growing knowledge base that SVCS are accurate for body size measurements independent of taxonomic clade.     

Coexistence of <Emphasis Type="Italic">Placobdella costata</Emphasis> (Fr. Müller, 1846) (Hirudinida: Glossiphoniidae) and mud turtle <Emphasis Type="Italic">Emys orbicularis</Emphasis>

Emys orbicularis is receding from Europe, mainly due to anthropogenic habitat changes. Its parasite, Placobdella costata, is widely distributed within both the former and the present distribution range of the host. Though closely associated with the mud turtle, it may have other hosts (birds, amphibians, reptiles). Its reproductive period coincides with that of its host’s migration to the breeding grounds, thus facilitating dispersal of the parasite. Based on literature data we have analyzed the geographic spread of P. costata and mud turtle to observe the possible overlap of their habitats. Observations on the population of mud turtle and the associated leech species (P. costata) were carried out in eastern Poland — Podlasie Lowland. The studies were conducted in spring and summer in 1986–1993. The leeches were collected from the turtles caught in the water and on land. Observations showed that most leeches were found on turtles inhabiting the lake or moving to a breeding area. The greatest intensity of invasion was observed in June and July and that most leeches were observed in female E. orbicularis characterized by greater length of the carapace and weight, compared with males and juvenile individuals.     

Does body size difference in the leeches Glossiphonia complanata (L.) and Helobdella stagnalis (L.) contribute to co-existence?

The effect of predator and prey body size on the feeding success of the British lake-dwelling leeches Glossiphonia complanata and Helobdella stagnalis was examined in the laboratory, and any involvement of size difference between the leeches in allowing coexistence in the field assessed. G. complanata breeds in advance of H. stagnalis and maintains a body size advantage throughout their annual life-cycle. In experiments, conducted at 14 °C and a photoperiod of 16 hrs L: 8 hrs D, three size classes of leeches of each species were each exposed to each of three size classes of each of five prey species, viz. Tubifex sp., Chironomus sp., Asellus aquaticus, Lymnaea peregra and Potamopyrgus jenkinsi. For each prey species, three different types of experiments were performed: one leech exposed to four prey individuals; four leeches of the same species with sixteen prey; and two leeches of each species with sixteen prey. In the first experiment, all sizes of G. complanata were capable of feeding on all sizes of the prey types offered; the same was true for H. stagnalis with exceptions of feeding on large A. aquaticus and large L. peregra. For both species, but especially for G. complanata, there was a trend within each size class of leech for decreasing proportions of fed leeches with increasing prey size, and within each size class of prey for an increasing proportion of fed leeches with increasing leech size; however there were several exceptions to these trends. Both leeches fed extensively on Tubifex sp. but there were significant differences in the proportions feeding on other prey types; G. complanata fed more on A. aquaticus and the two snail species, and less on Chironomus, than H. stagnalis. The effect of increasing the number of leech individuals from one to four individuals, of the same or mixed species, had little effect on the proportion of leeches which had fed. It is concluded that large G. complanata will have access to large individuals of certain prey taxa denied H. stagnalis, which may lessen the intensity of interspecific competition.     

Variation in reproductive output of marine turtles

Most marine turtle species are non-annual breeders and show variation in both the number of eggs laid per clutch and the number of clutches laid in a season. Large levels of inter-annual variation in the number of nesting females have been well documented in green turtle nesting populations and may be linked to environmental conditions. Other species of marine turtle exhibit less variation in nesting numbers. This inter-specific difference is thought to be linked to trophic status. To examine whether individual reproductive output is more variable in the herbivorous green turtle (Chelonia mydas Linneaeus 1758) than the carnivorous loggerhead (Caretta caretta Linneaeus 1758), we examined the nesting of both species in Cyprus over nine seasons. Green turtles showed slower annual growth rates (0.11 cm year⁻¹ curved carapace length (CCL) and 0.27 cm year⁻¹ curved carapace width (CCW)) than loggerhead turtles (0.36 cm year⁻¹ CCL, 0.51 cm year⁻¹ CCW). CCL was highly correlated to mean clutch size in both green (R²=0.51) and loggerhead turtles (R²=0.61) and maximal clutch size of green turtles (R²=0.58). Larger females did not lay a greater number of clutches or have a shorter remigration interval than smaller females of either species. On average, the size of green turtle clutches increased and that of loggerhead turtles decreased as the season progressed. Individual green turtles, however, produced more eggs per clutch through the season to a maximum in the third or fourth clutch. In loggerhead turtles, clutches 1-4 were very similar in size but the fifth clutch was 38% smaller than the first. No individuals of either species were recorded laying more than five clutches. Green turtles may not be able to achieve their maximum reproductive output with respect to clutch size throughout the season, whereas only loggerhead turtles laying five clutches (n=5) appear to become resource depleted. Green turtles nesting in years when large numbers of nests were recorded laid a greater number of clutches than females nesting in years with lower levels of nesting.     

A comparative study of the food niches of lake-dwelling triclads and leeches

The food niches of four species of triclads and three species of non-parasitic leeches living in the littoral zone of British lakes of different trophic status were investigated, over one year, using a serological technique. Antisera against ten potential prey groups were employed. The basic data were adjusted to compensate for differences in predator size and seasonal changes in field temperatures. Data on two of the leech species have been presented elsewhere, but comparisons of the diet of all seven predator species are made in this paper. Much overlap in diet between the various predator species occurs, but, with one exception, each of the genera has a major food resource. The Polycelis spp. feed extensively on oligochaetes, Dugesia polychroa on molluscs, Dendrocoelum lacteum on Asellus, Erpobdella octoculata on chironomids and Glossiphonia complanata on molluscs. Helobdella stagnalis is a generalist feeder. Problems of coexistence of the leech species, and of the leech and triclad species are discussed.