Class or suphylum Pycnogonida
(by Claudia Arango)
The Pycnogonida (Gr. pyknos = crowded + gony = knee), commonly named sea spiders, are a distinct group of marine arthropods of uncertain affinities, frequently linked to the Chelicerata (see review in Dunlop & Arango 2005), but quite controversial due to their unique and very conspicuous characters including an external proboscis, a ventral pair of appendages (called ovigers), and the reduction of the abdomen to a peg-shaped vestige(1987). DNA data have shown discrepancies among different analyses with the Pycnogonida appearing as sister group of the chelicerates or as the most primitive of all living arthropods (Giribet & Ribera 2000; Giribet et al. 2001). Recent interpretations of neuroanatomical data proposed a homology between chelifores of sea spiders and the "great appendages" of Cambrian arthropods supporting the basal position of Pycnogonida (Maxmen et al. 2005), but more recent hox gene expression data is supprting the homology of chelifores and chelicerae (Jager et al. 2006; Manuel et al. 2006; Edgecombe et al. 2000). There are more 1300 species of pycnogonids described and it is believed there are many more species to be discovered mainly from remote deep-sea habitats. The known species are traditionally distributed in 80 genera and eight or nine families as they are: Ammotheidae, Austrodecidae, Callipallenidae, Colossendeidae, Nymphonidae, Phoxichilidiidae, Pycnogonidae, Rhynchothoracidae, and Endeididae a monogeneric family sometimes included in Phoxichilidiidae, but phylogenetic studies are challenging the monophyly of these families (Arango & Wheeler in press). Ecologically, sea spiders are essentially marine benthic dwellers that occur from the shoreline to abyssal depths in all the seas around the world. They range in size from tiny midgets having leg spans of only 2 mm, to deep-sea giants with leg spans of up to 75 cm; the larger species are usually found at deeper habitats. Sea spiders are mostly epibenthic and carnivorous, some species have been described in parasitic associations with hydroids, molluscs and echinoderms (Arnaud & Bamber 1987). Taxonomic descriptions of new species are still the most common type of publication on sea spiders. Monographs on pycnogonids started to appear in the late 1800s and have covered most of the regions of the world. Biological and ecological work related to feeding and reproductive traits has also been carried out, however this has been done mainly on temperate or polar species (Fry 1965; De Haro 1978; Davenport et al. 1987; see review in Arnaud & Bamber 1987).
The body of the sea spiders is always very reduced and sometimes appears to be only a connector between each pair of legs; thus, the digestive and reproductive organs have migrated to the legs. Most species have four body segments, each of them bearing a pair of walking legs. However, some deep-sea species can have five or six body segments and ten or twelve legs respectively ('polymerous forms' in Hedgpeth, 1947), which is a very unusual phenomenon in arthropods, and yet to be explained. The first segment or cephalon bears the ocular tubercle housing four simple eyes (typically pigmented), the proboscis, the first pair of walking legs and three other pairs of appendages: the chelifores above the proboscis, the palps laterally, and the ovigers ventrally. The most prominent external feature of pycnogonids is the proboscis. It is a moveable organ and shows wide variation in size and shape among families. The shape and internal structure has been related to specialised feeding habits, sometimes specific to a particular host among parasitic species (Fry 1965; Staples & Watson 1987). The ocular tubercle can be a tall, pointed protuberance or a low tubercle situated dorsally on the midline of the cephalon. Some species lack the ocular tubercle (especially abyssal and psammophilic species). The chelifores consist of the scape or proximal part, and the chela, which has a fixed finger and a moveable finger articulated on the palm. In some species the fingers are robust and denticulate, in others they are very feeble. Chelifores are present in all the larval stages and juveniles known so far, but in some taxa, the chelifores disappear with the last moult before adulthood. The palps, presumed to be homologues of arachnid pedipalps, are multi-segmented and seem to have sensory, cleaning and feeding functions (see review in Arnaud & Bamber 1987). However, there are three families in which palps are completely absent. Additionally, the ovigers are another pair of appendages joined to the cephalon on its ventral surface. The males use these appendages to carry the eggs until hatching; in some species they also carry the larvae after hatching. Ovigers have a very particular configuration with a sickle-shaped terminal portion, with denticulate or simple spines. It is suggested the ovigers are important for grooming (Davenport et al. 1987), however, there might be some more important duties related to the mating and parenting behaviour, since it has been observed that legs can also clean the body, in both sea spiders with ovigers and those without. Females of some taxa lack ovigers, and these structures are completely absent in both sexes of some Pycnogonum species. The legs of pycnogonids have generally eight segments, and a main distal claw, and many species have auxiliary claws placed dorsolaterally to the main claw. Males possess cement glands on the femora that secrete the substance used to wrap the eggs and attach them to the ovigers. The outlet can be a long duct, a short tube, a single pore, or a number of tiny pores located dorsally or ventrally on the femur. Males and females can be easily differentiated by the absence of ovigers in females of the families Phoxichilidiidae and most Pycnogonidae species, otherwise the presence of cement glands on the femora indicates a male individual [although hermaphrodite specimens are known for some species (see Miyazaki & Makioka 1993)]. The fertilisation of the eggs is known to be external, the female releases the eggs and the male fertilises and attaches them to the ovigers in a single mass. The process has been observed in Phoxichilidim femoratum, Endeis species (see 1973), Pycnogonum litorale (Jarvis & King 1972) (Tomaschko & B�ckmann 1997), and mating behaviour has also been recorded in Propallene longiceps (Nakamura & Sekiguchi 1980). Regarding reproduction and development, the best-known species is Pycnogonum litorale, a common species of the north Atlantic that shows specific associations with a hydroid and a sea anemone (Jarvis & King 1972; Behrens 1984; Wilhelm et al. 1997; Tomaschko & Bueckmann 1997). Reproductive biology has also been studied in Endeis laevis (Jarvis & King 1975), Nymphon species (King & Jarvis 1970) and Parapallene famelica from the east coast of Australia (Hooper 1981), among few others. Pycnogonids do not have a planktonic stage in their life cycle, and this is believed to have implications for the patterns of distribution and a possible high rate of speciation. In species of callipallenids and nymphonids the larvae stay attached to the parent's ovigers until they reach a well-developed stage (after the fourth instar) (Nakamura 1981). Pycnogonid protonymphs resemble a nauplius larva of the crustaceans, but they have a proboscis, bear chelifores with strong pincers, and have two other pairs of appendages with a single terminal claw. There is little information to date on morphological characters of larvae and juvenile stages.
Taxonomy and Systematics
The taxonomy of Pycnogonida is principally based on the presence and the characteristics of the appendages on the cephalic segment. Characters of chelifores, palps and ovigers (presence, number of segments, configuration) define the artificial classification of families currently in use. Characters of the propodus and the cement glands are useful for identification at genus and species levels. Some of the most relevant publications on the taxonomy of the Pycnogonida are early monographs (Hoek 1881; Loman 1908 and others) and more recently the series of works by J. Hedgpeth (1947, 1954), J. H. Stock (1975, 1994) and C. A. Child (between 1982 and 1998). The group has been reviewed by Helfer and Schlottke (1935), Fage (1949), King (1973) and Arnaud and Bamber (1987) with comprehensive reports on species from specific locations (Gordon 1944; Hedgpeth 1948; 1949; Stock 1954; Fry & Hedgpeth 1969 among others). Taxonomy and some aspects of general biology have been the concern of most of the published works, however novel information on the ecology of some species has been produced more recently (Mercier & Hamel 1994; Arango & Brodie 2003; Sheerwood et al. 1998; Arango 2001). The phylogeny of the Pycnogonida has been little studied. Hedgpeth (1947) established a system of classification based on traditional morphological distinctions. This classification is currently accepted and followed by most of the students of the group, with few changes made along the time. A hypothesis of a reduction series of the number of segments as an evolutionary trend towards the loss of appendages, has been behind this traditional classification (Hedgpeth 1947; Stock 1994). This has been a simple explanation accepted to describe the phylogeny of the group, but it is important to provide the tools to be able to test this taxonomic hypothesis. The current methods available for the analysis of morphological and molecular data provide an opportunity to confront the hypothesis of a gradual reduction and present alternatives about the evolutionary history of the sea spiders.
Australia and New Zealand
Arango, C. P. 2001. Sea spiders (Pycnogonida) from the Great Barrier Reef, Australia, feed on fire corals and zoanthids. Memoirs of the Queensland Museum 46: 656.
Arango, C. P. & Brodie, G. D. 2003. Observations of predation on the tropical nudibranch Okenia sp. by the sea spider Anoplodactylus longiceps Williams (Pycnogonida, Arthropoda). The Veliger 46: 99-101.
Arango, C. P. & Wheeler, W. C. in press. Phylogeny of the sea spiders (Arthropoda; Pycnogonida) based on direct optimization of six loci and morphology. Cladistics. International Journal of the Willi Hennig Society.
Arnaud, F. & Bamber, R. N. 1987. The biology of Pycnogonida. Advances in Marine Biology 24: 1-95.
Ax, P. 1987. The phylogenetic system: the systematization of organisms on the basis of their phylogenesis. UK: John Wiley & Sons.
Behrens, W. B. 1984. Larvenentwicklung und Metamorphose von Pycnogonum litorale (Chelicerata, Pantopoda). Zoomorphology 104: 266-279.
Davenport, J., Blacstock, N., Davies, D. A. & Yarrington, M. 1987. Observations on the physiology and integumentary structure of the Antarctic pycnogonid Decolopoda australis . Journal of Zoology, London 211: 451-465.
De Haro, A. 1978. Ecological distribution of pycnogonids on the Catalan coast. Zoological Journal of the Linnean Society (London) 63: 181-196.
Dunlop, J. A. & Arango, C. P. 2005. Pycnogonid affinities: a review. Journal of Zoology, Systematics and Evolutionary Research 43: 8-21.
Edgecombe, G. D., Wilson, G. D. F., Colgan, D. J., Gray, M. R. & Cassis, G. 2000. Arthropod Cladistics: Combined analysis of histone H3 and U2 snRNA sequences and morphology. Cladistics. International Journal of the Willi Hennig Society 16: 155-203.
Fage, L. 1949. Classe de Pycnogonides. In Grasse, P. P. (Ed) Traite de Zoologie (pp. 906-941).
Fry, W. G. 1965. The feeding mechanisms and preferred foods of three species of Pycnogonida. Bulletin of the British Museum of Natural History, Zoology 12: 195-233.
Fry, W. G. & Hedgpeth, J. W. 1969. Pycnogonida: Colossendeidae, Pycnogonidae, Endeidae, Ammotheidae. New Zealand Department of Scientific and Industrial Research Bulletin Part 7: 1-139.
Giribet, G., Edgecombe, G. D. & Wheeler, W. C. 2001. Arthropod phylogeny based on eight molecular loci and morphology. Nature 413: 157-161.
Giribet, G. & Ribera, C. 2000. A review of arthropod phylogeny: New data based on ribosomal DNA sequences and direct character optimization. Cladistics. International Journal of the Willi Hennig Society 16: 204-231.
Gordon, I. 1944. Pycnogonida. British and New Zealand Antarctic Research Expeditions. (pp. 1-72).
Hedgpeth, J. W. 1947. On the evolutionary significance of the Pycnogonida. Smithsonian Miscellaneous Collection 106: 1-53.
Hedgpeth, J. W. 1948. The Pycnogonida of the Western North Atlantic and the Caribbean. Proceedings of the US National Museum 98: 157-342.
Hedgpeth, J. W. 1949. Report on the Pycnogonida collected by the Albatross in Japanese waters. Proceedings of the US National Museum 97: 233-321.
Helfer, H. & Schlottke, E. 1935. Pantopoda. In Bronn H. G. (Ed) Dr. H. G. Bronns Klassen und Ordnungen des Tierreichs (pp. 1-314). Leipzig: Akademische Verlagsgesellschaft m.b.H.
Hoek, P. P. C. 1881. Report on the Pycnogonida dredged by HMS Challenger 1873/76. Challenger Report Zoology 3: 1-167.
Hooper, J. N. A. 1981. Some aspects of the reproductive biology of Parapallene avida from northern New South Wales. Australian Zoologist 20: 395-411.
Jager, M., Murienne, J., Clabaut, C., Deutsch, J., Le Guyader, H. & Manuel, M. 2006. Homology of arthropod anterior appendages revealed by Hox gene expression in a sea spider. Nature 441: 506-508.
Jarvis, J. H. & King, P. E. 1972. Reproduction and development in Pycnogonum littorale. Marine Biology 13: 146-154.
Jarvis, J. H. & King, P. E. 1975. Egg development and reproductive cycle in Endeis laevis. Marine Biology 33: 331-339.
King, J. A. & Jarvis, J. H. 1970. Egg development in a littoral pycnogonid Nymphon gracile. Marine Biology 7: 294-304.
King, P. E. 1973. Pycnogonids. London: Hutchinson and Co.
Loman, J. C. C. 1908. Die Pantopoden der Siboga-Expedition. Siboga Expeditie Monographie 40: 1-88.
Manuel, M., Jager, M., Murienne, J., Clabaut, C. & Le Guyader, H. 2006. Hox genes in sea spiders (Pycnogonida) and the homology of arthropod head segments. Developmental Genes Evolution DOI 10.1007/s00427-006-0095-2.
Maxmen, A., Browne, W. E., Martindale, M. Q. & Giribet, G. 2005. Neuroanatomy of sea spiders implies an appendicular origin of the protocerebral segment. Nature 437: 1144-1148.
Mercier, A. & Hamel, J. F. 1994. Deleterious effects of a pycnogonid on the sea anemone Bartholomea annulata. Canadian Journal of Zoology 72: 1362-1364.
Miyazaki, K. & Makioka, T. 1993. A case of intersexuality in the sea spider, Cilunculus armatus. Zoological Science Tokyo 10: 127-132.
Nakamura, K. 1981. Post embryonic development of a pycnogonid, Propallene longiceps. Journal of Natural History 15: 49-62.
Nakamura, K. & Sekiguchi, K. 1980. Mating behaviour and oviposition in the pycnogonid Propallene longiceps. Marine Ecology Progress Series 2: 163-168.
Sheerwood, J., Walls, J. T. & Ritz, D. A. 1998. Amathamide alkaloids in the pycnogonid, Stylopallene longicauda, epizoic on the chemically defended bryozoan, Amathia wilsoni. Papers and Proceedings of the Royal Society of Tasmania 132: 65-70.
Staples, D. A. & Watson, J. E. 1987. Associations between pycnogonids and hydroids. In Bouillion, J. (Ed) Modern trends in the systematics, ecology and evolution of hydroids and hydromedusae (pp. 215-226). Oxford: Oxford University Press.
Stock, J. H. 1954. Papers from Dr. Mortensen's Pacific Exped. 1914-1916 LXXVII. Pycnogonida from the Indo-West Pacific, Australian, New Zealand waters. Videnskabelige Meddelelser fra Dansk naturhistorisk Foreningen 116: 1-168.
Stock, J. H. 1994. Indo-west pacific Pycnogonida collected by some major oceanographic expeditions. Beaufortia 44: 17-77.
Tomaschko, K. H. & B�ckmann, D. K. 1997. Growth and reproduction of Pycnogonum littorale under lab conditions. Marine Biology 129: 595-600.
Wilhelm, E., B�ckmann, D. K. & Tomaschko, K. H. 1997. Life cycle and population dynamics of Pycnogonum litorale (Pycnogonida) in a natural habitat. Marine Biology 129: :601-606.
Pycnogonida are also listed in the Australian Faunal Directory.