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Crustacean Symbionts of the Sea Anemone Telmatactis at Madeira

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Crustacean Symbionts of the Sea Anemone Telmatactis at Madeira J. Zool, Lond. (1997) 242, 799-811 Crustacean symbionts of the sea anemone Telmatactis cricoides at Madeira and the Canary Islands* PETER WIRTZ « Centro de Ciencias Biologicas e Geologicas, Universidade da Madeira, Largo do Colegio, P-9000 Funchal, Portugal (Accepted 12 September 1996) (With 2 figures in the text) The crustacean symbionts of the club-tipped sea anemone Telmatactis cricoides (Duchassaing, 1850) were studied at Madeira (« = 81 anemones) and the Canary Islands (n = 124 anemones). Of all anemones, 86% had crustacean symbionts. Nineteen species of crustaceans were encountered in association with Telmatactis cricoides. There were up to 18 individuals of up to four crustacean species associated with the same anemone. Anemone size and number of crustacean symbionts were positively correlated (P< 0.001) but only weakly so (r= +0.27). The most common crustacean symbiont was the shrimp Thor amboinensis, encountered with 65% of all anemones. Frequency and type of association with Telmatactis cricoides is described for each of the crustacean symbionts, Thor amboinensis, Lysmata grabhami, Lysmata seticaudata, Eualus occultus, Brachy- carpus biunguiculatus, Stenorhynchus lanceolatus, Homola barbata, Pilumnus villosissimus, Cnatho- phyllum elegans, Inachus phalangium, Heteromysis sp. nov., Palaemonella atlantica, Herbstia condyliata, Stenopus spinosus, Athanas nitescens, Dromia personata, Xantho incisus, Galathea sp., Liocarcinus sp. The shrimp Lysmata grabhami appears to live in stable pairs of two simultaneous hermaphrodites, a social structure not previously described for any crustacean species. Introduction Symbioses are common in the marine environment. Some taxa appear to be particularly likely to be involved in associations. It is the crustaceans that probably form more associations with other classes than any other marine animals (Ross, 1983). Crustacean-cnidarian associations are particularly common (e.g. Balss, 1956-57; Patton, 1967). The club-tipped anemone Telmatactis cricoides (Duchassaing, 1850) is the largest and most conspicuous sea anemone in the eastern Atlantic. The species occurs throughout the tropical Atlantic and in the eastern and central Mediterranean Sea; animals at Madeira and the Canary Islands are larger than in the rest of the distributional range, but no other morphological characters that would justify the recognition of a separate species have as yet been found (den Hartog, 1995). Telmatactis cricoides is variable in colour (cf. Wirtz, 1995) and is known to harbour crustacean symbionts that live either among the tentacles or on the column of the anemone or within a distance of only a few centimetres from the tips of the tentacles (Criales, 1979, 1984; Perez Sanchez & Moreno Batet, 1991; Wirtz, 1991, 1995). Three symbiotic complexes of sea anemones and crustaceans have so far been described in detail. Herrnkind, Stanton & Conklin (1976) characterized the Caribbean sea anemones Lebrunia danae and Bartholomea annulata and their associates. Six crustaceans, an ophiuroid and a fish were found with * Dedicated to Prof. Dr Wolfgang Wickler on the occasion of his 65th birthday 799 © 1997 The Zoological Society of London 800 P. WIRTZ Lebrunia danae\ nine crustaceans were found with Bartholomea annulata. Abel (1961) and Diesel and Wirtz (In prep.) characterized the community living with the Mediterranean sea anemone Anemonia sulcata; 40 crustaceans and one fish species were recorded with Anemonia sulcata. In a comparative study, the eastern Atlantic anemone Telmatactis cricoides and its crustacean symbionts were studied at Madeira and the Canary Islands. For data on the biology of Telmatactis cricoides see Wirtz (In press). The crustacean symbionts and their relation to the anemone are here described. Material and methods While SCUBA diving in a depth range of 1-62 m on approximately 400 dives during July 1993-August 1995,1 examined every individual of Telmatactis cricoides that appeared larger than 3 cm in diameter. On an underwater writing board, that had a scale of 15 cm marked on it, I noted: the depth of the anemone and the presence of any crustaceans visible on or among the tentacles and within less than 5 cm distance from the tentacles. I then pinched one of the tentacle tips, which caused the anemone to contract. Additional crustaceans now visible on the column of the anemone were recorded. Small transparent shrimps of the genera Eualus and Palaemonella as well as tiny mysidaceans may have been overlooked on occasion; the other species are conspicuous enough to make this unlikely. With the scale on the writing board, the diameter of the column was measured along the longest axis of the ellipsoidal ly contracted animal. The number of anemones surveyed at Madeira plus Porto Santo was 78 plus 3. The number of anemones surveyed at Tenerife (Playa Paraiso, south-western coast) was 100, at El Hierro (La Restinga, southern tip) 5, at Gran Canaria (El Cabron, eastern coast) 10, and at Lanzarote (Puerto del Carmen, southern coast) 9, giving a total of 205 anemones surveyed. Voucher specimens of the crustacean species have been deposited at the Nationaal Natuurhistorisch Museum at Leiden, Netherlands (RMNH) and at the Museu Municipal do Funchal (Historia Natural) at Madeira (MMF). Colour photos of most of these species can be found in Wirtz (1995). One subset of the data can be analysed for the frequency of co-occurrence of the symbiotic species (the other data sets are too small or were collected at locations too far apart from each other): 68 Telmatactis cricoides were surveyed along a shoreline of a few hundred metres in the area 'Playa Paraiso' at the south-western coast of Tenerife in July 1994. The expected values of co-occurrence of any 2 species are calculated as follows: if species A is encountered at 50% of all anemones and species B at 10% of all anemones, the expected value of co- occurrence is 0.5 x 0.1 = 0.05, i.e. 5% of all anemones. Expected and observed frequencies were then compared by chi-square test. Results Frequency of association and number of associates Of the 205 anemones, 86% had crustacean symbionts. The percentage was not significantly different at the Canary Islands and at Madeira (90% vs. 81%, x2 = 2.37, P = 0.13; Table I). Figure 1 shows the group-size frequency of symbionts, irrespective of species. The most common group size was one, but up to 18 individuals were recorded on an anemone and in the area directly around it. Average number of associates was 1.7. Associated crustaceans frequently belonged to more than one species: 45% of the anemones with symbionts harboured two to four species at the same time. Anemone size, anemone depth, and number of associates All anemones larger than 12 cm diameter (n = 47) had crustacean symbionts. The number of associated crustaceans correlated weakly with anemone size, both at Madeira and the Canary Islands CRUSTACEAN SYMBIONTS OF TELMATACTIS CRICOIDES 801 FIG. 1. Number of crustaceans per anemone (n = 205 anemones at least 3 cm in diameter). (Madeira r = + 0.47, P<0.001; Canary Islands r = + 0.20, P = 0.02; total sample: r = + 0.27, P<0.001). The shrimp Thor amboinensis frequently stayed on the substratum close to the anemone but without directly contacting it. Excluding this species, i.e. considering only the species that usually are in direct contact with either the column or the oral disk of the anemone, a much stronger correlation between anemone size and number of associated crustaceans can be detected at the Canary Islands (r= +0.56, P< 0.0001), but not at Madeira (r = + 0.31, P<0.005). The number of associated crustaceans did not correlate with the depth of the anemone (r = + 0.12, P>0.07). Species accounts Table I lists the most commonly associated species and the percentage of anemones harbouring them at Madeira and the Canary Islands. (a) Thor amboinensis Of the 205 Telmatactis cricoides, 59% had one or more Thor amboinensis associated with them. The incidence of this species at Madeira (67%) and at the Canaries (54%) did not differ significantly (X2 = 3.15, P = 0.07). Figure 2 shows the group-size frequency of Thor amboinensis (n = 123 anemones). Average group size was 2.3 Thor amboinensis per Telmatactis cricoides. Groups usually contained adult and much smaller individuals. Group size of Thor amboinensis associated with Telmatactis cricoides was unstable: during re-counts of the associates of the same anemones at intervals of a few days to a few weeks, the numbers of Thor amboinensis were never the same as recorded during the previous check. Thor amboinensis were seen on the substratum in the immediate vicinity of the tentacles of the anemone, on the column of the anemone and occasionally even on the tentacles and on the oral disk of the anemone (cf. photo on page 104 in Wirtz, 1995). Contact between the shrimp and the tentacles did not elicit feeding reactions of the anemone. At Madeira, Thor amboinensis can also be found associated with the snakelocks anemone Anemonia sulcata (Wirtz, unpubl.) and in small cracks in the rock face without cnidarian symbionts. Thor amboinensis is a circumtropical species that has been recorded with 13 different genera of sea 802 P. WIRTZ TABLE I • Associated species and the percentage of anemones with which they were found No. anemones , Madeira (%) Canary Islands (%) Species (« = 81) (n= 124) Thor amboinensis 67 54 Lysmata grabhami 15 33 Lysmata seticaudata 12 26 Eualus occultus and Palaemonella atlantica 12 7 Stenorhynchus lanceolatus 4 14 Brachycarpus biunguiculatus 4 9 Homo la barbata 5 2 Pilumnus sp. 4 1 Inachus phalangium 1 0 Stenopus spinosus 0 1 Gnathophyllum elegans 1 0 Herbstia condyliata 1 1 Xantho incisus 0 1 Athanas nitescens 0 1 Galathea sp. 1 0 Liocarcinus sp. 0 1 All species 81 90 anemones (Fransen, 1989). Criales (1984) recorded the occasional association of western Atlantic Thor amboinensis and Telmatactis cricoides (using the synonym Telmatactis rufa).
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