ANOPLODACTYLUS PETIOLATUS (PYCNOGONIDA) AND HYDRACTINIA ECHINATA (HYDROZOA) -OBSERVATIONS ON GALLS, FEEDING BEHAVIOUR AND THE HOST’S DEFENCE Martin Heß, Roland Melzer

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Martin Heß, Roland Melzer. ANOPLODACTYLUS PETIOLATUS (PYCNOGONIDA) AND HY- DRACTINIA ECHINATA (HYDROZOA) -OBSERVATIONS ON GALLS, FEEDING BEHAVIOUR AND THE HOST’S DEFENCE. Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, 2003, pp.135-138. ￿hal-03205151￿

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HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. VIE ET MILIEU, 2003, 53 (2-3) : 135-138

ANOPLODACTYLUS PETIOLATUS (PYCNOGONIDA) AND HYDRACTINIA ECHINATA (HYDROZOA) – OBSERVATIONS ON GALLS, FEEDING BEHAVIOUR AND THE HOST’S DEFENCE

Martin HEß1, Roland R. MELZER2,* 1Bioimaging Zentrum der LMU, Am Klopferspitz 19, 82152 München, Germany 2Zoologische Staatssammlung, Münchhausenstr. 21, 81247 München, Germany *address for correspondence

ALIMENTATION RÉSUMÉ. – Des observations et des expériences sur les relations entre Anoplodac- DÉFENSE tylus petiolatus et sa proie, Hydractinia echinata sont exposées. L’accent est mis FORMATION DE GALLES sur l’alimentation, les mouvements et la protection contre la défense de la colonie RELATIONS PANTOPODES-HYDRAIRES ANOPLODACTYLUS PETIOLATUS de polypes. Des éléments actifs (utilisation de la proboscis et de l’allure) et une PYCNOGONIDA sorte d’immunité sont pris en considération. Même après avoir été engloutis, les Anoplodactylus réussissent à s’extraire de la cavité gastro-vasculaire du polype sans blessure sérieuse. En outre, les larves d’Anoplodactylus qui vivent en parasite dans des polypes de l’Hydraire transformés en « galles » sont évoquées.

FEEDING ABSTRACT. – Observations and experiments are reported on the relationships bet- DEFENCE ween Anoplodactylus petiolatus and its prey, Hydractinia echinata, with special re- GALLING ference to feeding, movement and avoidance of the colony’s defence. The latter PYCNOGONID-HYDROZOAN RELATIONSHIPS includes active elements (usage of proboscis and legs) as well as a kind of immuni- ANOPLODACTYLUS PETIOLATUS ty: Even after having been engorged, Anoplodactylus can succesfully withdraw PYCNOGONIDA from the gastric cavity without serious bleeding. In addition, we have documented living Anoplodactylus larvae within polyps transformed to “gallzooids”.

INTRODUCTION Staples & Watson 1987, Chinery & Spooner 2001, Genzano 2002). Here we report on laboratory observations and A few members of the Pycnogonida, an an- experiments on the relationships between the cient group of marine arthropods, have been pycnogonid, A. petiolatus (Kröyer, 1844), and the found to feed on or encyst larvae in cnidarian hydrozoan, H. echinata Fleming, 1823, including polyps (see reviews in Helfer & Schlottke 1935, the pycnogonid’s feeding and the polyps’ defence Wyer & King 1974, Staples & Watson 1987), i.e. behaviour. Hydractinia polyps and Anoplodactylus animals that in their nematocysts possess a pycnogonids (and Phoxichilidiidae or Anoplo- highly effective defence system which compara- dactylidae in general) are classics of a sort as some tively few animals are able to overcome, whether of the first observations on pycnogonid-hydrozoan to use the colonies only as hiding places, e.g. relationships were made on representatives of these clownfish and anemone shrimps, or to prey on taxa, e.g. Allman (1860), Wright (1863), Hallez them, e.g. turbellarians, opisthobranch molluscs (1905), Cole (1906), and Dogiel (1911). In these – and some pycnogonids. early studies, the facts of “feeding and galling” are The latter use their proboscis, jaws and pharyn- presented, but descriptions of what happens while A. geal pumps to suck polyps. In addition, the petiolatus visits H. echinata colonies are lacking. protonymphon larvae of a few species are released We therefore describe how Anoplodactylus and from the ovigera of the adult males close to their Hydactinia behave during such foraging trips. In ad- hosts and, after they become attached, induce the dition, we investigate colonies under the influence formation of galls in which the larvae grow until of A. petiolatus using microscopical techniques, they leave the hosts again for their predatory e.g., we show A. petiolatus larvae nested inside liv- postlarval life that may occur on the previous ing polyps. A survey of A. petiolatus feedingonani- “nursing colony” (e.g., Helfer & Schlottke 1935, mals other than Cnidaria is given in Lotz (1968). 136 HEß M., MELZER R.R.

MATERIAL AND METHODS Undisturbed movement of A. petiolatus on the hydrozoan colonies and feeding

In an aquarium with H. echinata settling on shells of Mostly at night, A. petiolatus individuals left the gastropod, Buccinum undatum, provided by the their hiding places under and/or within the Biologische Anstalt Helgoland, A. petiolatus was found Buccinum shells and moved slowly onto the H. to be very abundant, both as larvae galling in H. echinata colonies. During this, polyps were not echinata polyps and as free juveniles and adults. The an- touched, i.e. the legs were set on the colony surface imals were kept in artificial sea water at about 12oC. H. between the polyps, thus avoiding nematocyst at- echinata was fed on brine shrimp larvae, Artemia salina. tacks, and the body was also kept away from the Pycnogonids were identified after King (1974) and colony’s surface (Fig. 1C, see also 1B). Elliot et al. (1990). Movement and feeding of about 30 A. petiolatus indi- Feeding took place in various locations on the viduals of different sizes were observed for about colony, but one third to half of feeding observa- 15 hours without any disturbance of the aquarium. tions were made at the tips of the spines standing Alltogether about 50 foraging trips were observed dur- between the normal trophozooids and nematozooids ing this period of time. In addition, pycnogonids were (Fig. 1A), thus corresponding well with the scars at seized with forceps and released from about 10 cm the tips of spines seen on SEM preparations. At- above the hydrozoan colonies in such a way that they tacks on “gallzooids” containing pycnogonid lar- landed with body and legs in random positions (n=16). vae were not seen. For feeding, the pycnogonid Pictures of “gallzooids” with pycnogonid larvae were bent down its forelegs and inserted the tip of the taken with a Zeiss Axioplan photomicroscope, surveys proboscis into the colony’s tissue. Afterwards it re- of A. petiolatus feeding on H. echinata with a conven- mained still for between 2 and 16 minutes while tional macro camera. SEM pictures were taken with a sucking the prey’s body fluid. Finally, it left the Leo 1430VP at 15 kV after fixation in AAF solution colony for its hiding place in the same stilted man- (85% ethanol, 10% acetic acid, 5% formalin; Anoplodactylus) or 4% Glutardialdehyde in 0.1M so- ner in which it had moved onto it. dium cacodylate buffer at pH 7.1 (Hydractinia), dehy- dration in a graded acetone series, CP-drying in a Polaron E 3000, and sputtering with gold in a Bio Rad Provoked contact between A. petiolatus SEM coating system. and H. echinata

When pycnogonids were dropped onto H. echinata colonies, parts of the bodies of all tested RESULTS animals came into contact with polyps. This led to massive reactions by H. echinata: polyps in reach of an A. petiolatus started to move towards the pycnogonid’s body and legs and apparenly at- tacked it with nematocysts. Some polyps even tried General observations and “galling” to engorge legs or even whole pycnogonids (see of Hydractinia below). However, all tested pycnogonids managed to withdraw from the colonies without any appar- ent serious bleeding. Using the claws at the tips of In agreement with the above-cited earlier stud- their legs as hooks, they brought themselves back ies, our H. echinata colonies were food as well as to their normal upright walking position in a pro- larval habitat for A. petiolatus.SEMsurveysof cess that lasted between 1 and 10 minutes, and then parts of H. echinata colonies previously visited by moved on as described above. A. petiolatus allowed more detailed analysis of the effects of feeding (Fig. 1A): while trophozooids, dactylozooids and gonozooids showed no damage Is Anoplodactylus “inedible” for Hydractinia? after A. petiolatus visits, the tips of the “spines”, i.e. the structures for which H. echinata is named, showed scar-like grooves and wrinkles apparently Parts of the bodies of three of the smaller caused by pycnogonid probosces. The habitus of an pycnogonids released over the colonies were A. petiolatus individual mounted in foraging posi- engorged by polyps. Of one A. petiolatus only the tion is depicted in Fig. 1B. On the studied H. distal halves of two legs were left outside the echinata colonies we observed numerous polyps polyp, and the major part of the body was already transformed into long and slender “gallzooids” in the gastric cavity. Remarkably, however, all lacking tentacles, but having a swelling bearing a three were able to withdraw from the polyp’s stom- single A. petiolatus larva within the stomach cav- ach by moving the free legs back and forth until ity, as illustrated in the photographs showing vital they found a place to hook on with their claws and polyps and larvae (Fig. 1D, E). pull out the engorged part of the body. With the al- ANOPLODACTYLUS PETIOLATUS (PYCNODONIDA) AND HYDRACTINIA (HYDROZOA) 137

Fig. 1. – A, H. echinata “meadow”, the feeding ground of A. petiolatus (SEM); asterisks dactylozooids, arrowheads spines with scars; scale bar 300 µm. B, Habitus of A. petiolatus; scale bar 200 µm. C, An A. petiolatus moving carefully on a H. echinata colony; scale bar 500 µm. D, E, An A. petiolatus (arrowheads) in a “gallzooid” of H. echinata; scale bar 50 µm. most completely swallowed specimen this took 1987, Bain 1992, Lovely 1997, Chinery & Spooner about 2 hours, but was eventually successful. 2001, Genzano 2002). A detailed description of the life cycle of an ectoparasitic pycnogonid, Pycnogonum littorale, is given in Bueckmann & Tomaschko (1997) and Tomaschko & Bueckmann (1997), and DISCUSSION a comparison between ecto- and endoparasitic lar- val life cycles in Russel & Hedgpeth (1990). Of interest, however, are some new points to be The basic features of Anoplodyctylus-Hydractinia made regarding feeding behaviour and avoidance relationships observed here agree well with earlier of the polyps’ defence. First, our observations indi- descriptions (Allman 1860, Wright 1863, Hallez cate that – under the applied laboratory conditions 1905, Cole 1906, Dogiel 1911): H. echinata is A. – there seems to be a diurnal rhythm with a feeding petiolatus’ prey and nursing colony for the larvae peak at night and a resting and hiding phase during at the same time. In addition, galling results in typ- the day. It is, however, not clear whether this is ical modifications of the host zooids found in other also the pycnogonid’s behaviour in the natural hab- endoparasitic species as well (Staples & Watson itat. H. echinata only grows on shells of Buccinum 138 HEß M., MELZER R.R. gastropods inhabited by hermit crabs like Eupagurus Bueckmann WE, Tomaschko KH 1997. Life cycle and bernhardus. Hiding somewhere at or below the population dynamics of Pycnogonum litorale (Pycno- shell thus might help to avoid the loss of the prey gonida) in a natural habitat. Mar Biol 129: 601-606. colony when the crab actively moves around. Chinery M, Spooner B 2001. The galling of sea firs (Hy- drozoa) and other coelenterates by larval sea spiders Secondly, A. petiolatus shows indications of an (Pycnogonida). Cecidology 13: 24-27. active avoidance of the colony’s defences by walk- Cole LJ 1906. Feeding habits of the pycnogonid Anoplo- ing and sucking in a way that minimizes physical dactylus lentus. Zool Anz 29: 740-741. contact. Correspondingly, Pycnogonum sucks at Dogiel V 1911. A short account of work on Pycnogonida the body stalk of Metridium and other sea anemo- done during June, 1911, at Cullercoats, Northumber- nes, where it is not within direct reach of the tenta- land. Sea Fish Comm Rep Sci Invest 26: 27. cles (Helfer & Schlottke 1935). If contact is pro- Elliot P, King PE, Morgan CJ, Pugh PJA, Smith A, voked, however, it becomes evident that Hydractinia Wheeler SLA 1990. Chelicerata, Uniramia, Tardigra- would defend itself against Anoplodactylus attacks – da. In Hayward DJ, Ryland JS eds, The marine fauna if the pycnogonid triggered such reactions. Except of the British isles and NW Europe. Clarendon Press, for the above-described scars, it is not clear at the Oxford 1: 553-627. moment to what extent H. echinata colonies are Genzano GN 2002. Associations between pycnogonids damaged by the pycnogonids as described by and hydroids from the Buenos Aires littoral zone, with observations on the semi-parasitic life cycle of Mercier & Hamel (1994) for the sea anemone, Tanystylum orbiculare (Ammotheiidae). Sci Mar 66: Bartholomea. 83-92. Thirdly, our experiments indicate that A. Hallez P 1905. Observations sur le parasitisme des lar- petiolatus possesses a kind of immunity against ves de Phoxichilidium chez Bougainvillea. Arch Zool H. echinata defences, as the pycnogonids were able Exp Sér. 4.III: 133-144. to leave the colonies even after serious attacks. Helfer H, Schlottke E 1935. Pantopoda. In Bronns Klas- Most astonishing is the fact that they could even sen und Ordnungen des Tierreichs, Fünfter Band, IV. withdraw after being engorged. This might be con- Abt 2. Buch. Akad. Verlagsgesellschaft Leipzig, 314p. nected to the larval development also taking place King PE 1974. British Sea Spiders. Synopses of the Bri- inside polyps, and hence the requirement for the tish Fauna (New Series) 5. Linnean Society of Lon- don. larvae to move in and out of the polyp without be- Lotz G 1968. Nahrungsaufnahme und Beutefang bei ei- coming injured and staying inside for a longer pe- nem Pantopoden, Anoplodactylus petiolatus Kröyer. riod of time without being digested as seen in other Oecologia 1: 171-175. endoparasitic forms (e.g. Staples & Watson 1987, Lovely EC 1997. Evolution of larval parasitism in the Lovely 1997, Chinery & Spooner 2001). To make Pycnogonida. Amer Zool 37: 196. this point clear, comparisons with other arthropods Mercier A, Hamel JF 1994. Deleterious effects of a pyc- engorged by polyps are necessary, as well as stud- nogonid on the sea anemone Bartholomea annulata. ies on the nesting of protonymphons. Can J Zool 72: 1362-1364. In summary, A. petiolatus shows remarkable Russel DJ, Hedgpeth JW 1990. Host utilization during abilities to handle its host colonies relating to feed- ontogeny by two pycnogonid species Tanystylum duospinum and Ammothea hilgendorfi parasitic on the ing, active defence avoidance, as well as a kind of hydroid Eucopella everta Coelenterata Campanula- passive immunity that might have contributed to riidae. Bijdr Dierk 60: 215-224. the evolution of the unique galling of cnidarians by Staples DA, Watson JE 1987. Associations between pyc- the larvae. nogonids and hydroids. 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