INTRODUCTION
Associations between amphipods and sea anemones are probably not all that rare, but few have been recorded hitherto. Specimens of a small amphipod found commonly among the tentacles and on the mouth-field of the sea anemone Antholoba achates near Coquimbo, Chile, by Professor Martin Thiel (Coquimbo) were forwarded by him to the authors and turned out to belong to a hitherto undescribed species of the genus Parametopella (Amphipoda: Stenothoidae), a genus hitherto only known from boreal and temperate waters on both coasts of North America. The new species is described here, and the authors have also taken this opportunity to provide a short survey of what is known about amphipod–sea anemone associations. As the present species lives in very shallow water and seems to be common, it will be probably easily accessible to future studies of its biology.
Abbreviations
A1, 2, antennae 1, 2; art, article; Cx, coxa; Gn1, 2, gnathopods 1, 2; Md, mandible; Mx1, 2, maxillae 1, 2; Mxp, maxilliped; P 3–7, peraeopods 3–7; U1–3, uropods 1–3.
Fig. 1. Parametopella antholobae sitting inside the sea anemone Antholoba achates.
Fig. 2. Parametopella antholobae: habitus male, antennae, mouthparts and Gn1 female.
Fig. 3. Parametopella antholobae Gn1 male, Gn2 male and female.
Fig. 4. Parametopella antholobae P4–7 and urosome with U1–3.
Fig. 5. Parametopa alaskensis (Holmes) Gn2 male and P7.
DIAGNOSTIC CHARACTERS
A1 with or without nasiform process on art1. Acc flag present or absent. Palp of Md lacking. Palp of Mx1 1-articulate. Inner plate of Mx2 ordinary (tandem-position). Inner plates of Mxp partially fused together. Gn1, 2 different in size and shape. Gn1 simple, merus more or less lobate, carpus elongate, propodus narrow. Gn2 enlarged, carpus triangular, short, palm oblique. P5–7 similar to P3, 4, with slender rectolinear basis. Cx4 ovoid, covering most peraeopods. Pereonites ordinary, free. Urosomite 2+3 can be fused. Telson horizontally thickened.
REMARKS
This genus shares the one-articulate palp of Mx1 and the simple Gn1 with Metopa, the lack of Md palp with Stenothoe. It belongs to the stenothoids with strongly broadened Cx4, hiding most of the peraeopods and developing nasiform antennal processes, having their main distribution in the Arctic region like Hardametopa, Zaikometopa, Vonimetopa, Metopella and Metopelloides (called ‘mesometopids’ in Krapp-Schickel & Koenemann, Reference Krapp-Schickel and Koenemann2006, not belonging to the Thaumatelsonidae like Raumahara, Prothaumatelson, Thaumatelson, Antatelson, Parathaumatelson and Pseudothaumatelson etc., having their distribution in the Antarctic).
Holotype: male 3.0 mm, from sea anemone Antholoba achates, collected in seagrass bed Heterozostera tasmanica. Shallow subtidal, 1 m depth, Puerto Aldea (Bahia Tongoy), about 50 km south of Coquimbo, Chile. 14 December 2004 (collected by M. Thiel). Slide deposited at the Museo Civico di Storia Naturale Verona (Italy).
Paratypes: 9 males, females 3 mm, 2 juveniles, same locality, deposited at the same museum.
DIAGNOSIS
Antenna 1 peduncle without nasiform process. Gn2 powerful, male propodus palm with wide semicircular excavation.
DESCRIPTION
Length: 3.0 mm.
Head small, eyes rounded, lateral cephalic lobes rounded.
Antennae: A1 about 1/3 body length. A1 < A2; A1 peduncle art1 subequal art2, art3 subequal to first flagellar art; flagellum with 9 arts. Art1 of peduncle wider than art2. A2: peduncle much longer than that of A1, art4 > art5, flagellum with 3–4 arts.
Mouthparts: Md palp lacking but place of insertion indicated by a triangular hump; molar triturative. Mxp outer plate totally lacking.
Gnathopods: Cx1 small; Gn1 basis unexpanded, carpus longer and wider than propodus which has about 4/5 of carpus length, widest proximally, posterior margin straight, palmar corner absent. Cx2 deeper than wide, not covered by Cx4. Gn2 basis subequal to length of propodus + carpus; carpus triangular, cup-shaped; merus posterodistally rounded; propodus about 1.5 times as long as wide, palmar corner about rectangular, at about 1/2 length of propodus; palm deeply excavated; dactylus shorter than palm.
Peraeopods: Cx3 rhomboid shaped, partly covered by very enlarged, ovoid shaped Cx4. P3, 4 slender, basis similar to P5, 6. P5–7 merus posterodistally somewhat lengthened but not widened; P7 basis a bit wider than that of P5, 6, but distally narrowing; all other articles very similar.
Uropods: U1, 2 peduncle longer than rami; U1 peduncle and outer ramus with short robust setae. U1, 2 rami somewhat unequal. U3 ramus with two arts, together longer than length of peduncle, though each art shorter than peduncle.
Telson: naked, partly fused with urosome, distally U-shaped.
Ovigerous females 3.0 mm. Gn2 propodus without palmar excavation, palmar corner rounded.
ETYMOLOGY
Antholobae, a noun in genitive form, for the host sea anemone, Antholoba achates.
DISCUSSION
The genus is known as pan-North-American warm temperate. The first species described was P. cypris (Holmes, Reference Holmes1904–1905), which has been reported until now from Cape Cod to northern Florida. In Reference Gurjanova1948 Gurjanova described P. stelleri from the Bering Sea, in 1962 Barnard P. ninis from southern California, 1976 Watling P. inquilinus from Delaware Bay and finally Reference McKinney, Kalke and Holland1978 McKinney et al. P. texensis from the Gulf of Mexico.
The known species are reported as found together with hydroids, ectoprocts, sponges and in oyster beds, furthermore their morphology is rather similar; most Parametopella species are reported as ‘rare’, which of course may be correlated with the difficulty of collecting.
The present species was sitting among the tentacles and on the mouthfield of the sea anemone (Figure 1). It shares the excavate palm on Gn2 with P. inquilinus and P. texensis, but these two species have half of the palm dentate and not excavate, while in the new species the excavation starts right after the dactylus insertion.
KEY TO ALL PARAMETOPELLA SPECIES
1. A1 art1 of peduncle with nasiform process… … … … … … … … … … … … … … … . .P. stelleri (Bering Sea)
- A1 art1 of peduncle lacking nasiform process… … . 2
2. Telson marginally with robust setae……… … … … … … … … . … … … … … … … . . P. ninis (California)
- Telson smooth . . … … … … … … … … … … .3
3. A2 peduncle art4, 5 about similar length of A1 peduncle art1… … … … … … … … … … … … … … … . . … …P. cypris (Atlantic Ocean from Cape Cod to Florida)
- A2 peduncle art4, 5 clearly longer than length of A1 peduncle art1… … … … … … … … … … … … . .4
4. Gn2 propodus palm regularly semicircularly excavated… … … … … .P. antholobae sp. nov. (Pacific Ocean, Chile)
- Gn2 propodus palm distal half dentate, proximal half excavated… … … … … … … … … … … … … . . 5
5. Gn1 propodus palm straight, carpus with parallel margins; U3 ramus art1 = subequal art2… … … … … … … … … … … … … . P. inquilina (Atlantic Ocean, Delaware)
- Gn1 propodus palm, rounded, widened, carpus also posteriorly widened, rounded; U3 ramus art1 much shorter than art2… … … … … … … … P. texensis (Gulf of Mexico)
We checked the holotype of Parametopa alaskensis (Holmes) (one half specimen, USNM 86805 from St Paul I., Pribilof Ids. = fur seal Ids. = Kotovi, south-western Alaska, under Stenothoe alaskensis), as a lot of striking similarities to the genus Parametopella are reported. The head is missing in this specimen, P3–6 are similarly slender, but P7 is much more rectangularly widened than illustrated by Gurjanova Reference Gurjanova1951 for her material (see Figure 5), while the urosome of the specimen of Holmes seems to match the drawings of Gurjanova. Gn2 of this male (only one is present) is similar to Parametopa alaskensis figured by Gurjanova Reference Gurjanova1951 and to Parametopella inquilina Watling Reference Watling1976, but has a second hump in the middle of the palm (see Figure 5).
As Gurjanova shows a rather bottle-shaped slender basis of P7, we hesitated if this species should not better belong to Parametopella (see also the similarly slender but rounded basis of P7 in the new species), and in fact be Parametopella inquilinus. But Holmes's type definitely does not belong to Parametopella, but fits very well Parametopa (thus the question mark in Barnard & Karaman, Reference Barnard and Karaman1991: 694 can be removed).
Associations between amphipods and sea anemones
Most stenothoid amphipods live among hydroids or similar epizoic growths, a few are also regularly found on sponges. Few associations with large individual invertebrates have hitherto been described, although it is probable that many have been overlooked. A few Metopa species live inside bivalve molluscs (see Tandberg et al., in preparation), while various stenothoids have been found on and even inside ascidians (Stebbing, Reference Stebbing1920; Pirlot, Reference Pirlot1933; Stephensen & Thorson, Reference Stephensen and Thorson1936). A few species, especially Metopelloides micropalpa (Shoemaker, 1930) and Stenula rubrovittata (G.O. Sars, 1883) have been found in association with hermit crabs (cf Besner, Reference Besner1976; McGrath, Reference McGrath1978), while Stenothoe symbiotica Shoemaker, Reference Shoemaker1956 lives on spider crabs (Shoemaker, Reference Shoemaker1956; Thomas & Cairns, Reference Thomas and Cairns1984).
Only two stenothoid amphipods, Metopa solsbergi and Stenothoe brevicornis, have hitherto been found as regular associates of sea anemones, but a number of such associations has been reported where the specific identity of the amphipod partner has not yet been determined (see Table 1). Both species live among the tentacles of their host, where apparently they may spend their entire life cycle (Vader & Krapp-Schickel, Reference Vader and Krapp-Schickel1996), and at least S. brevicornis feeds on its host's tissues (Moore et al., Reference Moore, Rainbow and Vader1994); in addition, the amphipods may feed commensally on the prey captured by the host sea anemone.
Table 1. A survey of published data on associations between stenothoid amphipods and sea anemones.
Quite a number of associations between representatives of other families of amphipods and sea anemones have been reported, although the literature is very scattered (cf Vader, Reference Vader1983; Vader & Krapp-Schickel, Reference Vader and Krapp-Schickel1996). In some cases, amphipods are specialized feeders on sea anemones; examples are Andaniexis lupus Berge & Vader, 1997 (Moore et al., Reference Moore, Rainbow and Vader1994), Maxilliphimedia longipes (Walker, 1906) (Coleman, Reference Coleman1989), and Parandania boecki (Stebbing, 1888) (Coleman, Reference Coleman1990). Acidostoma species live as ‘lice’ on the outside of the column of sea anemones and suck food with their specialized mouthparts (Dahl, Reference Dahl1964; Vader, Reference Vader1967; Ansell, Reference Ansell1969). Other amphipods live more or less permanently inside the coelenteron of their host, where they seem to be immune to the digestive enzymes of the sea anemone (Vader & Lønning, Reference Vader and Lønning1973), and feed at least in part on host tissue (Moore et al., Reference Moore, Rainbow and Vader1994). Onisimus species leave their host sea anemone as adults (Vader, Reference Vader1970), but the Pacific littoral species Orchomenella recondita (Stasek, Reference Stasek1958) spends its entire life-cycle inside its host, Anthopleura elegantissima (Brandt, 1835) (Stasek, Reference Stasek1958; De Broyer & Vader, Reference De Broyer and Vader1990).
In a number of other amphipod species the association with sea anemones seems to be a less permanent one, and more directly comparable with decapod–sea anemone associations, where the primary advantage for the crustacean partner seems to be the protection afforded by the nematocysts of the sea anemone, but none of the associations have been properly investigated as yet. Examples are the occurrence of Melita obtusata (Montagu, 1813) (partly cited under Abludomelita) (Hartnoll, Reference Hartnoll1971), Caprella acanthifera Leach, 1814 (Stroobants, Reference Stroobants1969), and Phtisica marina Slabber, 1769 (Vadon, Reference Vadon1984) on Anemonia sulcata (Pennant, 1766), and possibly also that of the little known Elasmopus calliactis (Edmondsson, Reference Edmondsson1951) on Calliactis armillatus Verrill, 1928 (Edmondsson, 1951).
ACKNOWLEDGEMENT
The authors are very grateful to Professor Martin Thiel for the opportunity to study this very interesting material.
