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Dangling Shells and Dangerous Spiders: Malacophagy and Mimicry in Terrestrial Gastropods

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Dangling Shells and Dangerous Spiders: Malacophagy and Mimicry in Terrestrial Gastropods Folia conchyliologica , n°7 , Février 2011 Dangling shells and dangerous spiders: malacophagy and mimicry in terrestrial gastropods 2 par Abraham S.H. BREURE Abstract . ─ Shells dangling on lines attached to a substratum may be either empty shell in use by spiders, or gastropods in hibernation. Previous data on dangling gastropods and malacophagy by spiders and harvestmen are summarized and discussed. Some new observations on dangling shells are reported from various localities in the West Indies. Keywords . ─ Gastropoda, Annulariidae, Cyclophoridae, Araneae, Opiliones, malacophagy, mimicry, Malaysia, West Indies. Résumé . – Les coquilles suspendues par des fils attachés à un substrat peuvent être soit des coquilles vides utilisées par les araignées, soit des gastéropodes en hivernation. Les données antérieures sur les gastéropodes suspendus et la malacophagie par les araignées et les opilions sont résumées et discutées. Quelques nouvelles observations sur les coquilles suspendues sont signalées dans diverses localités des Antilles. Mots clés . ─ Gastropoda, Annulariidae, Cyclophoridae, Araneae, Opiliones, malacophagie, mimétisme, Malaysie, Antilles. Introduction Recently DEELEMAN -REINHOLD (2009) published an observation that she, as an arachnologist, made some years ago when collecting spiders in rainforests in Borneo. She observed shells of Alycaeus (Cyclophoridae), dangling on lines attached to limestone slabs. This behaviour was cursorily reported by SCHILTHUIZEN et al . (1999). However, as Deeleman-Reinhold found eight spiderlings inside the 22 shells observed, behind the operculum, she suggested that the shells were possibly used for shelter or deposition of eggs. More generally, observations on spider-gastropod interaction are usually limited to prey-predator relationships. Although spiders have been reported in entomological literature to predate on gastropods (for a review, see NYFELLER & S YMONDSON , 2001; see also ACOSTA & M ACHADO , 2007), this is hardly reported in malacological literature (DU PREEZ , 2001; POLLARD & J ACKSON , 2004). The aim of the present paper is to briefly review some recent work on malacophagy in spiders and harvestmen published in non-malacological literature. At the same time I like to draw attention to 'mimicrous' behaviour in certain groups of molluscs that may have confused some observers and that still remains poorly documented. Malacophagy in spiders and harvestmen Two arachnid orders, spiders (Araneae) and harvestmen (Opiliones), may play an important role in the food webs of terrestrial ecosystems (NYFFELER et al ., 1994, WISE , 1995). Both groups have a very different predating style. Spiders can only cope with liquid food and use digestive enzymes to liquify the tissues of the prey (i.c. gastropods). Prey is caught with venoms or silk webs. Harvestmen have no venom or silk glands and their feeding apparatus (stomotheca) allows to take chunks of food. While spiders feed mainly on insects and other arthropods, the diet of harvestman is more diverse. NYFFELER & S YMONDSON (2001: 618) state that the first reported observation of an arachnid predating a gastropod was JOHNSON (1863). However, Johnson only described a new spider from Madeira and made an observation on the colouration of another species; land snails are only mentioned in the text as an example of a speciose group and not related to these spiders. The oldest report of malacophagy thus seem to be VERHOEFF (1900), who based his observations on species held in captivity. In their review of malacophagy in arachnids, NYFFELER & S YMONDSON (2001) list 53 reported observations of predation on snails and slugs, covering 12 families of Araneae and three families of Opiliones. 2 Netherlands Centre for Biodiversity Naturalis, P.O. Box 9517, 2300 RA Leiden, Netherlands. 7 Folia conchyliologica , n°7 , Février 2011 More recent papers include SMITHERS (2005), and FOUNTAIN et al . (2009). These papers add to the observation that malacophagy is little studied and field data are mainly occcasionally published or - as a side-line - during experimental settings with the focus on other groups than molluscs. Spider-gastropod interaction can also occur when empty shells are used for shelter or nesting sites. This is reported for several spider families, notably in semi-arid environments (GESS & GESS , 1999; MORENO -RUEDA et al. , 2008), where this behaviour is associated with low temperatures. I have found no previous records from tropical rainforests where spiders used shells, until DEELEMAN -REINHOLD (2009) published her observation. This behaviour can cause confusion to the casual observer, since it may not be clear at first sight whether the thread on which the shell dangles is made from silk or mucus. Dangling shells The observation by DEELEMAN -REINHOLD (2009) may seem logical from an arachnologist's point of view. Arthropods frequently use empty snail shells as shelter or nesting sites (MORENO -RUEDA et al. , 2008); see also fig. 1 . Thus shells dangling on threads could indeed be in use by spiders, having attached the shells by their silk lines to a substratum. I do believe, however, that the 'mimicrous behaviour' of dangling shells has a different cause and may be more often found than reported so far. This behaviour is different from real mimicry, in that it only accidentally does resemble spiders using an empty shell. Observations by malacologists in the West Indies show that this phenomenon may be rather wide-spread. At the same time, it was only found in the operculate land-snail family Annulariidae. GONZÁLEZ GUILLÉN (2008) reported it from Cuba, Prov. Pinar del Río, Sierra de los Órganos. Additional data (González Guillén, pers. commun.) show that dangling on mucus threads has been encountered in the following Cuban species: Blaesospira echinus infernalis (Torre & Bartsch, 1941), Chondropomora presasianum (Gundlach, 1863), Chondropometes magnum elisabethae Torre & Bartsch, 1938, Chondrothyretes sp. and Eutudora jimenoi (Arango in Pfeiffer, 1864) ( figs 2-7). In Prov. Holguín, Chondropoma sp . was found on very short threads ( figs 8-9). 0,5 mm Fig. 1 – Hamataliwa sp ., juvenile, inside the aperture of Alycaeus sp ., with snail excrements. Malaysia, Sarawak, Gunung Mulu © Photo courtesy by C. Deeleman-Reinhold New records for this behaviour are from Jamaica and Puerto Rico. Rosenberg (pers. commun.) observed several species of Annulariidae in Jamaica dangle from threads. Only one of these findings was documented. Three adults, one female and two males of Adamsiella cf. intermedia (C.B. Adams, 1849) were found close to a 8 Folia conchyliologica , n°7 , Février 2011 limestone wall north of Grants Bailey, St. Ann Parish, in a humid habitat. Robinson (pers. commun.) found Parachondria fascia (Wood, 1828) just east of Port Antonio, Portland Parish. Live specimens of this species were encountered dangling from mucus threads from the tips of the bark spines of Ceiba trees. Some adults were dangling in pairs. In areas where the canopy had been cut back, exposing the snails to direct sunlight, the snails were dead and still dangling on dried mucus threads. In Puerto Rico Chondropomoros riisei (L. Pfeiffer, 1852) ( fig. 10 ) was observed dangling in Bosque Estatal de Guajacata (Hovestadt, pers. commun.). The same species was found dangling on mucus threads in very humid conditions in the area of Aguas Buenas. At the same locality Parachondria conspecta (von Martens, 1883) was observed under similar conditions. Both species are typically living on limestone karst surfaces (Robinson, pers. commun.). Fig. 2 – Cuban annulariids showing dangling behaviour. Blaesospira echinus infernalis © Photo courtesy by A. González Guillén 9 Folia conchyliologica , n°7 , Février 2011 Figs 3-5 – Cuban annulariids showing dangling behaviour. 3-4, Chondropometes magnum elisabethae; 5, Eutudora jimenoi ; © Photo courtesy by A. González Guillén Figs 6-7 – Cuban annulariids showing dangling behaviour. 6, Chondropomora presasianum ; 7, Chondrothyretes sp. © Photo courtesy by A. González Guillén 10 Folia conchyliologica , n°7 , Février 2011 Figs 8-9 – Cuban annulariids showing dangling behaviour. Chondropoma sp. © Photo courtesy by A. González Guillén Fig. 10 – Puerto Rican Chondropomorus riisei ; in the background Brachypodella portoricensis © Photo courtesy by A. Hovestadt 11 Folia conchyliologica , n°7 , Février 2011 Discussion As the relatively limited literature shows, malacophagy is not so uncommon in arachnids as some might still believe it to be. Nevertheless, it is clear that harvestmen are more frequently found as gastropod predators than spiders; some species are even specialized in terrestrial gastropods as prey (MARTENS , 1978). What seemed only a cursorily observation of peculiar behaviour reported from Borneo (SCHILTHUIZEN et al. , 1999; DEELEMAN -REINHOLD , 2009), now seems to be just another case of convergent evolution with reports from different islands in the West Indies. In this region, this behaviour has been observed in operculate land-snails of the family Annulariidae only. The early observation of GUPPY (1866) on Adamsiella aripensis Guppy, 1864 from Trinidad (“It frequently suspends itself by two or three glutinous threads from branches on the under surface of leaves at a height of one or two feet from the earth”), remained unnoticed until recently Rutherford (pers. commun.) called my attention to it. Another early paper was by TRYON (1868), with an observation on Chondropoma dentatum Say, 1825 (“one of the figures represents this species
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