Metazoan parasite communities and diet of the velvet belly lantern shark Etmopterus spinax (Squaliformes: Etmopteridae): a comparison of two deep‐sea ecosystems

By combining an examination of stomach contents yielding a snapshot of the most recent trophic niche and the structure of parasite communities reflecting a long‐term feeding niche, this study aimed at gaining more comprehensive information on the role of the small‐sized deep‐water velvet belly lantern shark Etmopterus spinax in the local food webs of the Galicia Bank and the canyon and valley system of the Avilés Canyon, which have been both proposed for inclusion in the Natura 2000 network of protected areas. As far as is known, this study provides the first comparative parasite infracommunity data for a deep‐sea shark species. Component parasite communities in E. spinax were relatively rich, whereas the infracommunities were rather depauperate, with similar low diversity at both localities. The significant differences in the composition and structure of both parasite communities and prey assemblages indicate differential effects of the two deep‐sea ecosystems on both long‐term and most recent trophic niches of E. spinax. These results underline the importance of the use of multivariate analyses for the assessment of geographical variation in shark populations based on parasites and diet data.     

Life history of a wide‐ranging deepwater lantern shark in the north‐east Atlantic,Etmopterus spinax (Chondrichthyes: Etmopteridae), with implications for conservation

In this paper, the population biology of the velvet belly lanternshark Etmopterus spinax was studied and life‐history coefficients determined. Age was estimated from sections of the second dorsal spine and validated by marginal increment analysis. Males attained a maximum age of 8 years while 11 year‐old females were found. Several growth models were fitted and compared for both size‐at‐age and mass‐at‐age data, showing that even though this is a small‐sized species, it has a relatively slow growth rate. This species matures late, specifically at 49·6 and 42·5% of the maximum observed ages for males and females, respectively. It has a low fecundity, with a mean ovarian fecundity of 9·94 oocytes and a mean uterine fecundity of 7·59 embryos per reproductive cycle. This species seems to have a long reproductive cycle, and even though no conclusive data were obtained, a 2–3 year cycle is possible. The estimated coefficients indicate that this species has a vulnerable life cycle, typical of deepwater squalid sharks. Given the high fishing pressures that it is suffering in the north‐east Atlantic, this fish may already be facing severe declines or in risk of facing them in the near future.     

In the intimacy of the darkness: Genetic polyandry in deep-sea luminescent lanternsharks Etmopterus spinax and Etmopterus molleri (Squaliformes,Etmopteridae)

Multiple paternity seems common within elasmobranchs. Focusing on two deep-sea shark species, the velvet belly lanternshark (Etmopterus spinax) and the slendertail lanternshark (Etmopterus molleri) we inferred the paternity in 31 E. spinax litters from Norway (three to 18 embryos per litter) and six E. molleri litters from Japan (three to six embryos), using 21 and 10 specific microsatellites, respectively. At least two E. spinax litters were sired from multiple fathers each, with highly variable paternal skew (1:1 to 9:1). Conversely, no clear signal of genetic polyandry was found in E. molleri.     

Comparing external and internal dorsal-spine bands to interpret the age and growth of the giant lantern shark, Etmopterus baxteri (Squaliformes: Etmopteridae)

The giant lantern shark, Etmopterus baxteri, is taken as bycatch of commercial fisheries that operate in deepwater off southeastern Australia. Bands on the second dorsal spine were used to obtain age estimates. The number of bands on the external surface of the spine and within the inner dentine layer increased with animal length. Most spines had more bands on the external surface, and the rate of band formation was significantly different between the external surface and the inner dentine layer. Females had a maximum of 57 external bands and 26 internal bands, while males had up to 48 external bands and 22 internal bands. Age estimates from external bands suggest maturity (A ₅₀) at 20 years for males and 30 years for females. Internal band age estimates suggest maturity at 10.5 years for males and 11.5 years for females. Although there is a large discrepancy between these two preliminary (i.e., unvalidated) age estimates, they both suggest that E. baxteri is a long-lived and late maturing species that is likely to be susceptible to over fishing.     

Evidence of counter‐gradient growth in western pond turtles (Actinemys marmorata) across thermal gradients

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A matter of size: the population structure of the smallest known living shark,Etmopterus perryi (Springer & Burgess, 1985), from deep waters off the Colombian Caribbean coast

The dwarf lanternshark (Etmopterus perryi) is the smallest known described shark, and practically no information has been available on this species since first described in the mid-1980s. Therefore, the aim of this work is to describe, for the first time, the population structure regarding dwarf lanternshark in the Colombian Caribbean Sea. During deep-water research surveys conducted along the Colombian Caribbean coast, 87 stations were sampled using the swept area method. A total of 153 dwarf lanternshark individuals were caught in depths ranging from 230 to 530 m. This information was used to describe the size structures, morphological measurements including length-at-weight relationship, length at maturity in females and the spatial distribution of mean length and biomass of the species. The lengths of individuals ranged from 78.02 to 289.00 mm total length (TL), which is a new record of maximum length for this species. The spatial distribution of mean lengths and biomass distributions show high abundances and high relative mean lengths in the northeast area off Santa Marta and the area northwest of Riohacha. The mean biomass density in the whole prospected area was 5.52 kg km⁻². Length at 50% maturity in females was estimated in 203 mm TL (95% C.I. : 190–214 mm). Deep-water elasmobranch species, such as the dwarf lantern shark, are expected to show extremely low resilience to fishing exploitation, even when they are not targeted by commercial fishing. Therefore, the information reported in this study can serve as a baseline upon which management measurements can be proposed for the conservation of this shark species.     

Feeding of the megamouth shark (Pisces: Lamniformes: Megachasmidae) predicted by its hyoid arch: A biomechanical approach

Studies of the megamouth shark, one of three planktivorous sharks, can provide information about their evolutionary history. Megamouth shark feeding has never been observed in life animals, but two alternative hypotheses on biomechanics suggest either feeding, i.e., ram feeding or suction feeding. In this study, the second moment of area of the ceratohyal cartilages, which is an indicator of the flexural stiffness of the cartilages, is calculated for 21 species of ram‐ and suction‐feeding sharks using computed tomography. The results indicate that suction‐feeding sharks have ceratohyal cartilages with a larger second moment of area than ram‐feeding sharks. The result also indicates that the ram–suction index, which is an indicator of relative contribution of ram and suction behavior, is also correlated with the second moment of area of the ceratohyal. Considering that large bending stresses are expected to be applied to the ceratohyal cartilage during suction, the larger second moment of area of the ceratohyal of suction‐feeding sharks can be interpreted as an adaptation for suction feeding. Based on the small second moment of area of the ceratohyal cartilage of the megamouth shark, the feeding mode of the megamouth shark is considered to be ram feeding, similar to the planktivorous basking shark. From these results, an evolutionary scenario of feeding mechanics of three species of planktivorous sharks can be suggested. In this scenario, the planktivorous whale shark evolved ram feeding from a benthic suction‐feeding ancestor. Ram feeding in the planktivorous megamouth shark and the basking shark evolved from ram feeding swimming‐type ancestors and that both developed their unique filtering system to capture small‐sized prey. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Dental structure of the Giant lantern shark <Emphasis Type="Italic">Etmopterus baxteri</Emphasis> (Chondrichthyes: Squaliformes) and its taxonomic implications

Dogfish sharks (Squaliformes) are a highly diverse group of neoselachians occurring in a wide range of marine environments and are common members of deep-sea faunas. The order Squaliformes comprises six families with approximately 98 extant species. The dentition of most squaliforms is characterized by a strong dignathic heterodonty and dental variation yielding a suite of potential tooth characters that could be used for taxonomic and systematic purposes. So far, no detailed study has been carried out to analyse the use of tooth morphologies in reconstructing the phylogeny of squaliforms. Also, the degree of characteristics of intraspecific variability of tooth morphologies is still unclear. Here, we analysed the dental differences between juveniles and adults and between the sexes of the Giant lantern shark, Etmopterus baxteri, and tested these dental characters for taxonomic purposes employing different statistical procedures. The results show that upper teeth of adult females and males differ morphologically in that those of females are bigger and display a lanceolate central cusp, whereas male specimens have thin and needle-like central cusps. Upper teeth of males have a higher number and a more pronounced variability of lateral cusplets than those of females. Moreover, an ontogenetic heterodonty might be developed in male specimens with sexually immature males displaying similar dental morphologies to those of adult females. Lower teeth, conversely, do not differ morphologically between the sexes. Results indicate that tooth morphologies of squaliform sharks bear high potential for phylogenetic purposes if tooth variations are considered, but have to be treated with care, if no variation is analysed.     

Catch composition,reproductive biology and diet of the bramble shark Echinorhinus brucus (Squaliformes: Echinorhinidae) from the south‐eastern Arabian Sea

Fishery and biological data are presented for the poorly known bramble shark Echinorhinus brucus (Squaliformes: Echinorhinidae), from the deep waters of the south‐eastern Arabian Sea. A total of 5318 individuals from by‐catch landings of deep‐water bottom set longlines, gillnets and shrimp trawl fisheries operating at depths of 200–1200 m were recorded between January 2008 and December 2011 at the Kochi Fisheries Harbour (Kerala). A total of 431 individuals, from 46 to 318 cm total length (L_T) and 0·8 to 132 kg total mass (M_T), were examined to determine biological data for this species. The L_T at which 50% were mature (L_T50) for females and males was estimated at 189 and 187 cm L_T. Litter size ranged from 10 to 36 and size at birth was between 42 and 46 cm L_T. Dietary analysis of stomach contents revealed E. brucus feeds on a variety of prey including crustaceans (69% index of relative importance, I_RI), teleosts (25·8% I_RI), cephalopods (1·7% I_RI) and elasmobranchs (0·7% I_RI). This study provides the first detailed biological data for this species and also highlights the extent of the by‐catch fishery for this species in Indian waters.     

The Pillars of Hercules as a bathymetric barrier to gene flow promoting isolation in a global deep‐sea shark (Centroscymnus coelolepis)

Knowledge of the mechanisms limiting connectivity and gene flow in deep‐sea ecosystems is scarce, especially for deep‐sea sharks. The Portuguese dogfish (Centroscymnus coelolepis) is a globally distributed and near threatened deep‐sea shark. C. coelolepis population structure was studied using 11 nuclear microsatellite markers and a 497‐bp fragment from the mtDNA control region. High levels of genetic homogeneity across the Atlantic (Φ_ST = ?0.0091, F_ST = 0.0024, P > 0.05) were found suggesting one large population unit at this basin. The low levels of genetic divergence between Atlantic and Australia (Φ_ST = 0.0744, P < 0.01; F_ST = 0.0015, P > 0.05) further suggested that this species may be able to maintain some degree of genetic connectivity even across ocean basins. In contrast, sharks from the Mediterranean Sea exhibited marked genetic differentiation from all other localities studied (Φ_ST = 0.3808, F_ST = 0.1149, P < 0.001). This finding suggests that the shallow depth of the Strait of Gibraltar acts as a barrier to dispersal and that isolation and genetic drift may have had an important role shaping the Mediterranean shark population over time. Analyses of life history traits allowed the direct comparison among regions providing a complete characterization of this shark's populations. Sharks from the Mediterranean had markedly smaller adult body size and size at maturity compared to Atlantic and Pacific individuals. Together, these results suggest the existence of an isolated and unique population of C. coelolepis inhabiting the Mediterranean that most likely became separated from the Atlantic in the late Pleistocene.     

Origins of the Greenland shark (Somniosus microcephalus): Impacts of ice‐olation and introgression

Herein, we use genetic data from 277 sleeper sharks to perform coalescent‐based modeling to test the hypothesis of early Quaternary emergence of the Greenland shark (Somniosus microcephalus) from ancestral sleeper sharks in the Canadian Arctic‐Subarctic region. Our results show that morphologically cryptic somniosids S. microcephalus and Somniosus pacificus can be genetically distinguished using combined mitochondrial and nuclear DNA markers. Our data confirm the presence of genetically admixed individuals in the Canadian Arctic and sub‐Arctic, and temperate Eastern Atlantic regions, suggesting introgressive hybridization upon secondary contact following the initial species divergence. Conservative substitution rates fitted to an Isolation with Migration (IM) model indicate a likely species divergence time of 2.34 Ma, using the mitochondrial sequence DNA, which in conjunction with the geographic distribution of admixtures and Pacific signatures likely indicates speciation associated with processes other than the closing of the Isthmus of Panama. This time span coincides with further planetary cooling in the early Quaternary period followed by the onset of oscillating glacial‐interglacial cycles. We propose that the initial S. microcephalus–S. pacificus split, and subsequent hybridization events, were likely associated with the onset of Pleistocene glacial oscillations, whereby fluctuating sea levels constrained connectivity among Arctic oceanic basins, Arctic marginal seas, and the North Atlantic Ocean. Our data demonstrates support for the evolutionary consequences of oscillatory vicariance via transient oceanic isolation with subsequent secondary contact associated with fluctuating sea levels throughout the Quaternary period—which may serve as a model for the origins of Arctic marine fauna on a broad taxonomic scale.     

Huffmanela selachii n. sp. (Nematoda: Trichosomoididae: Huffmanelinae): A new species infecting the skin of the great hammerhead shark (Sphyrna mokarran) and the blacktip reef shark (Carcharhinus melanopterus) in the Arabian Gulf,off-shore Saudi Arabia

From January 2017 - December 2019, 75 out of 850 (8.8 %) great hammerhead sharks from the Arabian Gulf had skin lesions of black irregular discolorations on the ventral surface of the head. The lesions consisted of pencil-like lineations often advancing forward by about 2 mm in back-and-forth looped scribbles often forming a relatively linear bands of about 5–7 cm wide. Similar lesions were also found in the blacktip reef shark from the same area within the same period, and consisted of straight to irregular black lines, extended indiscriminately across the skin of the sharks. Microscopic examination of the skin revealed the presence of dark-brown eggs exhibiting the spindle or ellipsoidal eggs characteristic of Huffmanela sp. The morphometrics of eggs from both hosts were similar (62.9–89.9 μm long and 29.3–56.1 μm wide). The eggshells were smooth with polar plugs protruding or not, with an abruptly truncated crown-like or shoulder-like collar surrounding the plug. The eggs were only found in the epidermal layer of the skin. Based on the unique morphometrics of the eggs, we report a new species, named: Huffmanela selachii n. sp.. This appears to be the first report of Huffmanela from either the great hammerhead shark or the blacktip reef shark, and the third reported Huffmanela in sharks from the Arabian Gulf. It is also one of few species reported from connecting waters of the greater Indian Ocean. This new finding contributes to our understanding of the diversity and ubiquity of Huffmanela sp. in marine creatures.     

Determination of counter‐ions in synthetic peptides by ion chromatography,capillary isotachophoresis and capillary electrophoresis

The utility of three various analytical techniques [ion chromatography (IC), capillary electrophoresis (CE) and isotachophoresis (ITP)] was tested in the determination of counter‐ions in synthetic peptides. The analyzed ions were acetates, trifluoroacetates and chlorides. IC provided the best results; CE, except limit of detection and limit of quantification, exhibited the comparable results. ITP was classified as the less useful because of the problem with the determination of the chloride ions. Nevertheless, all the three techniques were able to analyze trifluoroacetates and acetates ions with satisfactory results. Except analytical methods, three procedures using hydrochloric acid (HCl) (at two different concentrations) and acetic acid as sample solvents processed by lyophilization were tested. It has been found that the lyophilization not only by HCl but also by acetic acid is a simple and cheap procedure for removal of toxic trifluoroacetic counter‐ions from peptides on satisfactory levels. Copyright © 2012 European Peptide Society and John Wiley & Sons, Ltd.     

Phylogeography of the whelk genus Cominella (Gastropoda: Buccinidae) suggests long‐distance counter‐current dispersal of a direct developer

The gastropod genus Cominella Gray, 1850 consists of approximately 20 species that inhabit a wide range of marine environments in New Zealand and Australia, including its external territory, the geographically isolated Norfolk Island. This distribution is puzzling, however, with apparently closely‐related species occurring either side of the Tasman Sea, even though all species are considered to have limited dispersal abilities. To determine how Cominella attained its current distribution, we derived a dated molecular phylogeny, which revealed a clade comprising all the Australian and Norfolk Island species nested within four clades of solely New Zealand species. This Australian clade diverged well after the vicariant separation of New Zealand from Australia, and implies two long‐distance dispersal events: a counter‐current movement across the Tasman Sea from New Zealand to Australia, occurring at the origination of the clade, followed by the colonization of Norfolk Island. The biology of Cominella suggests that the most likely method of long‐distance dispersal is rafting as egg capsules. Our robust phylogeny also means that the current Cominella classification requires revision. We propose that our clades be recognized as subgenera: Cominella (s.s.), Cominista, Josepha, Cominula, and Eucominia, with each subgenus comprising only of New Zealand or Australian species. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 315–332.     

A molecular and ecological study of Grillotia (Cestoda: Trypanorhyncha) larval infection in small to mid‐sized benthonic sharks in the Gulf of Naples,Mediterranean Sea

AimTrypanorhyncha cestodes comprise a wide range of heteroxenous parasites infecting elasmobranchs as definitive hosts. Limited data exist on the larval infection of these cestodes and the role of intermediate and paratenic hosts in the life cycle of these parasites. We investigated the factors that determine the occurrence and the level of infection of Grillotia plerocerci in the skeletal muscles of various benthonic sharks and analyzed the parasites through an integrative taxonomic approach.LocationMediterranean Sea.MethodsSharks obtained as bycatch of commercial trawling activities (i.e., Etmopterus spinax, Galeus melastomus, and Scyliorhinus canicula) were used in this study. Data from a limited number of Dalatias licha and Scyliorhinus stellaris were also included. Grillotia plerocerci were molecularly characterized using the partial 28S large subunit rDNA. Boosted regression trees were used to model the relationship between the abundance of infection with both morphological and physiological predictors in each host.ResultsPlerocerci of Grillotia were detected in all shark species except S. stellaris. Host species significantly differed in terms of parasite abundance, with the highest and lowest prevalence and abundance of infection detected in G. melastomus and E. spinax, respectively. The relative influence of the traits involved in explaining the parasite abundance was related to the host size in G. melastomus, while both morphology‐ and physiology‐related traits explained the patterns observed in E. spinax and S. canicula. The 28S rDNA sequences shared an identity of ∼99.40% with a Grillotia species previously found in the Mediterranean Sea. At intraspecific level, two different genotypes were found. A first type was retrieved only from D. licha, whereas a second type was found in G. melastomus, E. spinax, and S. canicula.Main conclusionsPresent results suggest that the two genotypes could be involved in different consumer‐resource systems and confirm most of the examined shark species as transport hosts of Grillotia species for unknown larger top predators.     

Neural development in Onychophora (velvet worms) suggests a step-wise evolution of segmentation in the nervous system of Panarthropoda

A fundamental question in biology is how animal segmentation arose during evolution. One particular challenge is to clarify whether segmental ganglia of the nervous system evolved once, twice, or several times within the Bilateria. As close relatives of arthropods, Onychophora play an important role in this debate since their nervous system displays a mixture of both segmental and non-segmental features. We present evidence that the onychophoran “ventral organs,” previously interpreted as segmental anlagen of the nervous system, do not contribute to nerve cord formation and therefore cannot be regarded as vestiges of segmental ganglia. The early axonal pathways in the central nervous system arise by an anterior-to-posterior cascade of axonogenesis from neuronal cell bodies, which are distributed irregularly along each presumptive ventral cord. This pattern contrasts with the strictly segmental neuromeres present in arthropod embryos and makes the assumption of a secondary loss of segmentation in the nervous system during the evolution of the Onychophora less plausible. We discuss the implications of these findings for the evolution of neural segmentation in the Panarthropoda (Arthropoda + Onychophora + Tardigrada). Our data best support the hypothesis that the ancestral panarthropod had only a partially segmented nervous system, which evolved progressively into the segmental chain of ganglia seen in extant tardigrades and arthropods.     

Observations on the biological traits of the rare shark Oxynotus centrina (Chondrichthyes: Oxynotidae) in the Hellenic Seas

New records of the rare angular rough shark Oxynotus centrina from the Hellenic Seas are presented. Its occurrence is reported for the first time in the Corinthian Gulf. Some aspects of the species' biology are described and compared with previous studies.