Sea Spider Species Research Articles

Ultrastructure of the female pedal gonad in Phoxichilidium femoratum (Chelicerata, Pycnogonida)

Phoxichilidium femoratum is a common species of sea spiders – a small and unique group of chelicerates with unusual adult anatomy. In particular, substantial parts of the reproductive system in pycnogonids (unlike euchelicerates) are located in the appendages. Existing studies of pycnogonid gonads are often limited to light-microscopic level, cover a small range of species, and focus on the contents of the gonad diverticula. Ultrastructural data are rare and contradictory, and the organisation of the gonad wall and the gonoducts is unknown. Here we present a detailed light and transmission electron microscopy-based examination of the pedal portion of the adult female reproductive system in Phoxichilidium femoratum Rathke, 1799. We describe its gross anatomy and the ultrastructure of the gonad diverticulum, oviduct and gonopore, as well as development of the oocytes. Each gonad diverticulum is enclosed in the extracellular matrix of the horizontal septum and bears some internal cellular lining. However, neither the gonad lining, nor the septum sheath cells, ever form a continuous epithelial layer. Oocytes, which undergo maturation in the diverticulum, remain, until very late in the process, attached to the gonad wall though specialised stalk cells. Interestingly, stalk cells do not participate in egg envelope or yolk formation: both are synthesized endogenously in the oocytes. The oviduct is supplied with musculature, which assists in egg transport to the gonopore, whereas the gonopore itself is surrounded by specialised glands.

New sea spider species (Pycnogonida: Austrodecidae) from a submarine cave in Japan

Abstract We describe a new sea spider species, Pantopipetta hosodai sp. nov., based on one juvenile female collected from a submarine cave (‘Akumanoyakata’ Cave) in Shimojijima Island, Miyako Island Group, Ryukyu Islands, southwestern Japan. It was collected from the second slope zone of the cave, 80–100 m from the entrance, no light, low salinity and with rocky substrate. This is the first record globally of a Pantopipetta species from a submarine cave and anchialine environment. Pantopipetta hosodai sp. nov. resembles Pantopipetta auxiliata, Pantopipetta lenis and Pantopipetta oculata in having auxiliary claws, but differs from them in having a palp with three short distal articles, lateral processes without dorsodistal tubercles, coxae 1 and 3 of legs 1–3 each with one long dorsal tubercle and one dorsodistal tubercle bearing a seta on each femur. Features of the palp appear to delineate two species groups in Pantopipetta, i.e. (1) those having four small distal articles, and a small, basal palp article between the lateral cephalon process and longest palp article (eight-articulate palp) and (2) those having three small distal articles, and lacking the small basal article (six-articulate palp), but further detail examination of the described species is needed. We discuss the diagnostic characters separating Pantopipetta and Austrodecus and the generic affiliation of Austrodecus aconae. Few pycnogonids from marine or anchialine caves have been identified to species, and it is generally unknown whether cave-dwelling pycnogonids tend to be troglobites.

Sea spiders (Arthropoda: Pycnogonida) collected during the Madibenthos Expedition from Martinique shallow waters

This study presents the inventory of sea spiders (Pycnogonida) sampled during the Madibenthos Expedition in Martinique (West Indies). Species were discriminated leaning on morphological and molecular data. A total of 761 specimens are classified in 72 species, 16 genera and nine families. Thirteen new species are described: Ammothella dirbergi sp. nov., A. krappi sp. nov., Tanystylum boucheti sp. nov., T. ingrallis sp. nov., Ascorhynchus iguanarum sp. nov., Eurycyde kaiouti sp. nov., Nymphon dorlis sp. nov., N. ludovici sp. nov., N. martinicum sp. nov., N. timons sp. nov., Anoplodactylus madibenthos sp. nov., Pycnogonum cesairei sp. nov. and Rhynchothorax sidereus sp. nov. We describe a neotype for Anoplodactylus micros Bourdillon, 1955 from the type locality. Martinique now includes 79 species of sea spiders, mostly endemic to the Tropical Northwestern Atlantic, cosmopolitan or shared with the South America Atlantic coast. Some species are potentially introduced. However, our knowledge of the distribution of species found in Martinique is probably biased by the scarcity of diagnostic morphological characters. Also, nine potentially cryptic species (discriminated on genetic data alone), are identified, shedding light on the overlooked diversity of sea spiders in the Tropical Northwestern Atlantic. Therefore, we call for a more widespread use of barcoding in sea spiders.

Analyzing drivers of speciation in the Southern Ocean using the sea spider species complex Colossendeis megalonyx as a test case

Colossendeis megalonyx Hoek, 1881 has the broadest distribution of all sea spiders in the Southern Ocean. Previous studies have detected several evolutionarily young lineages within this taxon and interpreted them as a result of allopatric speciation in a few shelf refuges during glacial maxima. However, alternative scenarios such as ecological speciation in sympatry have rarely been considered or tested. Here, we generated the most extensive genomic and morphometric data set on the C. megalonyx species complex to (i) comprehensively describe species diversity, (ii) explore intraspecific connectivity between populations located around Antarctica, and (iii) systematically test for positive selection indicative of adaptive speciation. We successfully applied a target hybrid enrichment approach and recovered all 1607 genes targeted. Phylogenomic analysis was consistent with previous findings and, moreover, increased the resolution of branching within lineages. We found specimens of phylogenetically well-separated lineages occurring in sympatry to be genetically distinct from each other and gene flow between geographically separated populations of the same lineages to be restricted. Evidence for positive selection was found for four genes associated with structural and neuronal functions. Hence, there is an indication for positive selection in the C. megalonyx species complex, yet its specific contribution to the speciation process remains to be explored further. Finally, morphometric analyses revealed multiple significant differences between lineages, but a clear separation proved difficult. Our study highlights the relevance of positive selection as a potential driver for speciation in the Southern Ocean.

Postembryonic development of Nymphon australe Hodgson, 1902 (Pycnogonida, Nymphonidae) from Antarctica

Developmental modes in pycnogonids are variable, even between congeneric species. Most of our previous knowledge of pycnogonid life history stages is based on morphological descriptions of the larval and those postlarval instars still retained on male ovigers, whereas the free-living instars are largely unknown. In this paper, a combination of morphological and molecular tools is used in order to link those postlarval instars retained on male ovigers to free-living specimens representing putatively later stages in the postembryonic development of a sea spider species. Male specimens of Nymphon australe carrying postembryonic instars were collected from localities off the South Shetland Islands, the Weddell Sea, the Drake Passage, the Bransfield Strait, and the Ross Sea. Three subsequent free-living instars were collected from Drake Passage. Nymphon australe hatch as a postlarval instar with two-articled palps and limb buds of the two first-walking legs. Postlarval instars 1 and 2 (both carried on the ovigers of males), postlarval instars 3 and 4, and a juvenile (all three free living) are all described and illustrated. A molecular phylogenetic based on the cox1 gene links all free-living stages to N. australe populations from the Antarctic Peninsula. The postlarval development of N. australe is discussed here and compared with those known from other pycnogonid species with similar development pathways.

Combining morphological and genomic evidence to resolve species diversity and study speciation processes of the Pallenopsis patagonica (Pycnogonida) species complex

BackgroundPallenopsis patagonica (Hoek, 1881) is a morphologically and genetically variable sea spider species whose taxonomic classification is challenging. Currently, it is considered as a species complex including several genetic lineages, many of which have not been formally described as species. Members of this species complex occur on the Patagonian and Antarctic continental shelves as well as around sub-Antarctic islands. These habitats have been strongly influenced by historical large-scale glaciations and previous studies suggested that communities were limited to very few refugia during glacial maxima. Therefore, allopatric speciation in these independent refugia is regarded as a common mechanism leading to high biodiversity of marine benthic taxa in the high-latitude Southern Hemisphere. However, other mechanisms such as ecological speciation have rarely been considered or tested. Therefore, we conducted an integrative morphological and genetic study on the P. patagonica species complex to i) resolve species diversity using a target hybrid enrichment approach to obtain multiple genomic markers, ii) find morphological characters and analyze morphometric measurements to distinguish species, and iii) investigate the speciation processes that led to multiple lineages within the species complex.ResultsPhylogenomic results support most of the previously reported lineages within the P. patagonica species complex and morphological data show that several lineages are distinct species with diagnostic characters. Two lineages are proposed as new species, P. aulaeturcarum sp. nov. Dömel & Melzer, 2019 and P. obstaculumsuperavit sp. nov. Dömel, 2019, respectively. However, not all lineages could be distinguished morphologically and thus likely represent cryptic species that can only be identified with genetic tools. Further, morphometric data of 135 measurements showed a high amount of variability within and between species without clear support of adaptive divergence in sympatry.ConclusionsWe generated an unprecedented molecular data set for members of the P. patagonica sea spider species complex with a target hybrid enrichment approach, which we combined with extensive morphological and morphometric analyses to investigate the taxonomy, phylogeny and biogeography of this group. The extensive data set enabled us to delineate species boundaries, on the basis of which we formally described two new species. No consistent evidence for positive selection was found, rendering speciation in allopatric glacial refugia as the most likely model of speciation.

A new record of the genus Trygaeus Dohrn, 1881 and species Trygaeus communis Dohrn, 1881 (Arthropoda, Pycnogonida) from Turkey (Eastern Mediteranean)

Sampling studies in the Turkish Aegean Sea revealed the occurrence of the sea spider species, Trygaeus communis Dohrn, 1881. The genus Trygaeus and species Trygaeus communis Dohrn, 1881 are recorded for the first time from Turkey. The genus and species are also recorded for the second time from the Eastern Mediterranean Sea. Distribution map of the species in the Eastern Mediterranean Sea is provided, together with photographs and line drawing of the species. This record further extends the known distribution of the species to Turkey in the Eastern Mediterranean.

Predatory behavior of giant Antarctic sea spiders (Colossendeis) in nearshore environments

AbstractPycnogonids in the genus Colossendeis are found in the deep sea and Southern Ocean. Although the genus contains the largest and most conspicuous species of sea spiders, little is known about their ecology or behavior. We documented two species feeding on a variety of benthic and pelagic invertebrates during three diving field seasons at McMurdo Station, Antarctica. Individuals of one species, Colossendeis megalonyx, fed on a variety of pelagic organisms, particularly the pteropod Clione antarctica. We used video to document rapid capture of individuals of C. antarctica by captive specimens of C. megalonyx in the laboratory, and we suggest that, at least in the nearshore environment, pelagic invertebrates are an important food source for this and potentially other pycnogonid species.

Genetic signature of Last Glacial Maximum regional refugia in a circum-Antarctic sea spider.

The evolutionary history of Antarctic organisms is becoming increasingly important to understand and manage population trajectories under rapid environmental change. The Antarctic sea spider Nymphon australe, with an apparently large population size compared with other sea spider species, is an ideal target to look for molecular signatures of past climatic events. We analysed mitochondrial DNA of specimens collected from the Antarctic continent and two Antarctic islands (AI) to infer past population processes and understand current genetic structure. Demographic history analyses suggest populations survived in refugia during the Last Glacial Maximum. The high genetic diversity found in the Antarctic Peninsula and East Antarctic (EA) seems related to multiple demographic contraction–expansion events associated with deep-sea refugia, while the low genetic diversity in the Weddell Sea points to a more recent expansion from a shelf refugium. We suggest the genetic structure of N. australe from AI reflects recent colonization from the continent. At a local level, EA populations reveal generally low genetic differentiation, geographically and bathymetrically, suggesting limited restrictions to dispersal. Results highlight regional differences in demographic histories and how these relate to the variation in intensity of glaciation–deglaciation events around Antarctica, critical for the study of local evolutionary processes. These are valuable data for understanding the remarkable success of Antarctic pycnogonids, and how environmental changes have shaped the evolution and diversification of Southern Ocean benthic biodiversity.

Nuclear and Mitochondrial Gene Data Support Recent Radiation within the Sea Spider Species Complex Pallenopsis patagonica

The climate history of the Antarctic continental shelf has formed a diverse benthic ecosystem over evolutionary time scales. The extent of faunal diversity has only recently been unveiled especially by using genetic data. In addition to newly reported species, known species of benthic invertebrates in the Southern Ocean turned out to be in fact species complexes representing genetically very distinct clades. Previous studies have shown that the sea spider Pallenopsis patagonica is such a species complex consisting of several mitochondrial clades. However, genetic analyses of another sea spider complex, Colossendeis megalonyx, showed that looking at one gene only can lead to overestimation of species number within a species complex. In this study we expand the current data set of P. patagonica by adding not only samples from Patagonia, the Subantarctic and the Eastern Weddell Sea, but also sequence data of the nuclear internal transcribed spacer region to obtain more information about the species complex. In fact, the number of clades is reduced when looking at nuclear data, but there are no cases of mito-nuclear discordance and hence no evidence for hybridization and speciation reversal events between divergent mitochondrial clades as has been reported for C. megalonyx. As patterns of genetic differences within P. patagonica and C. megalonyx are very similar when looking at the mitochondrial COI gene and also molecular dating of both species complexes suggest a recent separation of clades during the Pleistocene, different biological processes seem to have led to fast and stable species boundaries in P. patagonica as opposed to C. megalonyx where hybridization even across major mitochondrial lineages was still possible.

New records of Sea Spiders (Arthropoda: Pycnogonida) for continental Portugal and notes on species distribution

A sampling effort carried out in the Northern coast of Portugal revealed the presence of two species of sea spiders that are recorded for the first time in Portugal: Anoplodactylus angulatus and Ammothella longioculata. While A. angulatus is widespread along the North East Atlantic coast, A. longioculata is recorded for the first time outside of the Mediterranean Sea. Eight species were recorded in this survey, increasing the pycnogonid species list of Portugal to twenty-four. A species list of the Pycnogonids of continental Portugal including references and distribution is provided.

Larval stages of two deep sea pycnogonids

The larvae of two species of sea spiders in the archived collections of the Smithsonian Institution's National Museum of Natural History (NMNH) are described: the first three instars of Ammothea allopodes Fry et Hedgpeth 1969, and one late post-hatching stage of Nymphon tenellum (Sars, 1888). Ammothea allopodes larval stages are examples of a typical protonymphon larva. The single stage of N. tenellum does not fit into any of the five recognized larval developmental patterns; it displays characteristics of an attaching larva, an encysting larva and a typical protonymphon larva. These characteristics are: (1) 3-segmented larval appendages I, II and III; (2) underived buds of appendages IV-VI, walking legs 1, 2 and 3, present; (3) the digestive tract is incomplete, there is no proctodeum present; and (4) a large amount of yolk is present. A new developmental pattern is proposed for this larval stage. How to cite this article: Fornshell J.A.. 2015. Larval stages of two deep sea pycnogonids // Invertebratze Zoology. Vol.12. No.2. P.197-205. doi: 10.15298/invertzool.12.2.05

On the occurrence of Ascorhynchus castelli (Dohrn, 1881) (Arthropoda: Pycnogonida) in the Aegean Sea

Sampling studies in the Turkish Aegean Sea revealed the occurrence of a sea spider species, Ascorhynchus castelli (Dohrn, 1881). The presence of this species is reported for the first time from the Aegean Sea and the second time from the eastern Mediterranean Sea. This record further extends the known distribution of the species from the Turkish Mediterranean Sea to the Aegean Sea in the eastern Mediterranean. This is also the first record of the species from shallow waters in the eastern Mediterranean Sea (10 m).

Larval morphologies and potential developmental modes of eight sea spider species (Arthropoda: Pycnogonida) from the southern Oregon coast

Larvae of eight sea spiders from three families (Ammotheidae, Pycnogonidae and Phoxichilidiidae) are described for the first time. The external morphology of the first larval stage of each species is presented in detail using scanning electron microscopy photographs in order to determine the mode of postembryonic development. Three types of larval development are apparent in the species examined. The speciesAchelia gracilipes, Eurycyde spinosa, Pycnogonum rickettsiandPycnogonum stearnsi(families Ammotheidae and Pycnogonidae) have larval morphologies indicative of an ‘ectoparasitic’ development. Morphological characteristics ofAchelia simplissimaandAchelia chelata(family Ammotheidae) larvae suggest an ‘endoparasitic’ development, while larvae of the speciesAnoplodactylus viridintestinalis(family Phoxichilidiidae) have traits implying an ‘encysting’ postembryonic mode of development. Larvae of the speciesNymphopsis spinosissimahave unusual morphological characteristics that may be indicative of a new developmental mode.

Genetic differentiation in the circum—Antarctic sea spider Nymphon australe (Pycnogonida; Nymphonidae)

Nymphon australe Hodgson 1902 is the most abundant species of sea spiders in the Southern Ocean. The species is recognised as highly morphologically variable, circumpolar and eurybathic—which is surprising given that sea spiders lack a planktonic stage; the fertilised eggs and larvae remain attached to the ovigers of the father, and consequently have limited dispersal capacity. In this study, we investigate the genetic structure of N. australe populations around Antarctica, confronting the apparent limited dispersal ability with its recognised circumpolarity. Here we analyse mitochondrial DNA of specimens from Antarctic Peninsula, Weddell Sea and East Antarctica to determine if they represent populations of the widespread N. australe — or instead we can recognise cryptic species – and how genetically different they are. Both CO1 and 16S sequence data produced single haplotype networks for N. australe from all three Antarctic locations without indication of cryptic speciation. However, we found strong phylogeographic structure among the three Antarctic locations based on CO1 data. There was only a single shared haplotype between the Antarctic Peninsula and the East Antarctica locations, and all three regions were significantly subdivided from each other ( F ST =0.28, p<0.01). Furthermore, within the Antarctic Peninsula and East Antarctic locations, we found evidence of genetic subdivision between populations of N. australe separated by 10–100 s of km ( F ST =0.07–0.22, p<0.05), consistent with sea spiders life history traits indicating a limited dispersal capability. We conclude N. australe represents a single circum-Antarctic species that, despite its limited dispersal abilities, has successfully colonised large parts of the Antarctic marine ecosystem through geological history. However, clear genetic differences among and within locations indicate contemporary gene flow is limited, and that populations of N. australe around Antarctica are effectively isolated.

Postembryonic development of Nymphon unguiculatum Hodgson 1915 (Pycnogonida, Nymphonidae) from the South Shetland Islands (Antarctica)

Male specimens of the sea spider species Nymphon unguiculatum, carrying eggs, larvae and postlarvae in various stages of development, were collected off the South Shetland Island at water depths between 112 and 472 m in austral summer 2006/2007. Here, we describe the external morphology of four postembryonic stages (protonymphon, instar 1, instar 2, and instar 3) carried by these specimens. We found that (1) protonymphon larvae hatch from the eggs; (2) larvae and postlarval stages have yolk reserves and are characterized by a relatively large size (average body lengths of 0.46, 0.55, 0.65 and 0.73 mm in the successive stages); (3) postlarvae remain on the ovigerous legs of males during several moults; (4) a spinning apparatus is present; (5) the development of walking legs is sequential. The larval and postlarval development of N. unguiculatum is compared with that known from other pycnogonid species.

Polygynandry and sexual size dimorphism in the sea spiderAmmothea hilgendorfi(Pycnogonida: Ammotheidae), a marine arthropod with brood‐carrying males

Species that exhibit uniparental postzygotic investment by males are potentially good systems for investigating the interplay of sexual selection, parental care and mating systems. In all species of sea spiders (Class Pycnogonida), males exclusively provide postzygotic care by carrying fertilized eggs until they hatch. However, the mating systems of sea spiders are poorly known. Here we describe the genetic mating system of the sea spider Ammothea hilgendorfi by assaying nearly 1400 embryos from a total of 13 egg-carrying males across four microsatellite markers. We also determine the extent of sexual dimorphism in trunk and leg size, and assess how reproductive success in males varies with these morphological traits. We detected instances of multiple mating by both sexes, indicating that this species has a polygynandrous mating system. Genotypic assays also showed that: males do not mix eggs from different females in the same clusters; eggs from the same female are often partitioned into several clusters along a male's oviger; and clusters are laid chronologically from proximal to distal along ovigers. Females were on average larger than males with respect to leg length and width and trunk length, whereas males had wider trunks. Among the genotyped egg-carrying males, neither the number of eggs carried nor the number of mates was correlated with body-size traits. Nevertheless, the high variance in mating success, genetically documented, suggests that males differ in their ability to acquire mates, so future studies are needed to determine what traits are the targets of sexual selection in this species. In addition to providing the first description of the mating system in a sea spider, our study illustrates the potential uses of this group for testing hypotheses from parental investment and sexual selection theories.

Microscopic anatomy of pycnogonida: II. Digestive system. III. Excretory system

The digestive system of several species of sea spiders (Pycnogonida, Arthropoda) was studied by electron microscopy. It is composed of the foregut inside a long proboscis, a midgut and a hindgut. Lips near the three jaws at the tip of the proboscis receive several hundred ductules originating from salivary glands. These previously undetected glands open on the lips, a fluted, projecting ridge at the external hinge line of the jaws, i.e., to the outside of the mouth. This disposition suggests affinities to the chelicerate line. The trigonal esophagus within the proboscis contains a complex, setose filter device, operated by dedicated muscles, that serves to reduce ingested food to subcellular dimensions. The midgut has diverticula into the bases of all legs. Its cells differentiate from the basal layer and contain a bewildering array of secretion droplets, lysosomes and phagosomes. In the absence of a hepatopancreas, the midgut serves both digestive and absorptive functions. The cuticle-lined hindgut lies in the highly reduced, peg-like abdomen. Traditionally, pycnogonids have been claimed to have no excretory organ at all. Such a structure, however, has been located in at least one ammotheid, Nymphopsis spinosissima, in which a simple, but standard, excretory gland has been found in the scape of the chelifore. It consists of an end sac, a straight proximal tubule, a short distal tubule, and a raised nephropore. The end sac is a thin-walled and polygonal chamber, about 150 microm in cross section, suspended in the hemocoel of the appendage, its edges radially tethered to the cuticle at more than half a dozen locations. This wall consists of a filtration basement membrane, 1-4 microm thick, facing the hemocoel, and internally of a continuous carpet of podocytes and their pedicels. The podocytes, measuring maximally 10 by 15 microm, have complex contents, of which a labyrinthine system of connected intracellular channels stands out. These coated cisternae open into a central vacuole that often rivals the nucleus in size. The design of the organ closely approximates that of the primitive crustacean Hutchinsoniella macracantha.

Larvae of three sea spider species of the genus Nymphon (Arthropoda: Pycnogonida) from the White Sea

Larvae of three Nymphon species are described. For Nymphon brevirostre Hodge, 1863 and Nymphon micronyx Sars, 1888 protonymphon larvae are examined, larvae of N. micronyx have been studied for the first time. The fine external morphology of larvae is studied in detail using SEM methods; the internal structure of N. brevirostre protonymphon is additionally described. SEM data on external morphology and fine surface structures are given for several postembryonic stages of Nymphon grossipes Fabricius, 1780. Different types of postembryonic development are revealed in examined Nymphon species. N. brevirostre and N. micronyx have a “typical protonymphon” developmental pathway. A special developmental pathway named “lecithotrophic protonymphon” is suggested for N. grossipes and other Nymphonidae having large yolky eggs.

Deep-sea pycnogonids from the North Atlantic and their distribution in the World Ocean

The information on the composition and distribution of present-day pycnogonids in different regions of the World Ocean and, especially, in the northern part of the Atlantic Ocean acquired during the past decades allowed us to perform a biogeographical analysis of these animals, which represent a permanent component of bottom communities. For 34 species of sea spiders (Pycnogonida) found in the North Atlantic deeper than 2 km, ten types of geographical distribution were recognized. Half of the species identified represent Atlantic forms, and 41% of them are endemic forms with West-Atlantic, East-Atlantic, amphi-Atlantic, and central-Atlantic distributions. The other half of the deep-sea Atlantic species have broad geographical ranges. Among them, 11.7% are Atlantic-Pacific species, 14.7% dwell in the Atlantic and West Pacific, 8.9% are low-latitudinal panocaanic species, and 14.7% are panoceanic species able to penetrate to higher latitudes. The zoogeographical species composition shows a significant independence of this fauna in the northern Atlantic Ocean and its relation to the Pacific and Indian oceans. At present, these relations are probably maintained via the temperate latitudes of the Southern Hemisphere and via the Drake Passage; meanwhile, it seems that, previously, they were realized possibly via the ancient Tethys Ocean.