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Status of the Nemertea As Predators in Marine Ecosystems

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Status of the Nemertea As Predators in Marine Ecosystems Hydrobiologia 456: 21–32, 2001. Juan Junoy, Pedro Garc´ıa-Corrales & Martin Thiel (eds), 5th International Conference on Nemertean Biology. 21 © 2001 Kluwer Academic Publishers. Printed in the Netherlands. Status of the Nemertea as predators in marine ecosystems Martin Thiel1 & Inken Kruse2 1Facultad Ciencias del Mar, Universidad Cat´olica del Norte, Larrondo 1281, Coquimbo, Chile E-mail: [email protected] 2Wattenmeerstation Sylt, Alfred-Wegener-Institut für Polar- und Meeresforschung, D-25992 List/Sylt, Germany Key words: nemertean, foraging, feeding rate, predation, prey selection, benthos Abstract The ecology of nemertean predators in marine ecosystems is reviewed. Nemerteans occur in most marine environ- ments although usually in low abundances. Some species, particularly in intertidal habitats, may reach locally high densities. During specific time periods appropriate for hunting, nemerteans roam about in search of prey. Upon receiving a stimulus (usually chemical cues), many nemertean species actively pursue their prey and follow them into their dwellings or in their tracks. Other species (many hoplonemerteans) adopt a sit-and-wait strategy, awaiting prey items in strategic locations. Nemerteans possess potent neurotoxins, killing even highly mobile prey species within a few seconds and within the activity range of its attacker. Most nemertean species prey on live marine invertebrates, but some also gather on recently dead organisms to feed on them. Heteronemerteans preferentially feed on polychaetes, while most hoplonemerteans prey on small crustaceans. The species examined to date show strong preferences for selected prey species, but will attack a variety of alternative prey organisms when deprived of their favourite species. Ontogenetic changes in prey selection appear to occur, but no further information about, e.g. size selection, is available. Feeding rates as revealed from short-term laboratory experiments range on the order of 1–5 prey items d−1. These values apparently are overestimates, since long-term experiments report substantially lower values (0.05–0.3 prey items d−1). Nemerteans have been reported to exert a strong impact on the population size of their prey organisms through their predation activity. Considering low predation rates, these effects may primarily be a result of indirect and additive interactions. We propose future investigations on these interactive effects in combination with other predators. Another main avenue of nemertean ecological research appears to be the examination of their role in highly structured habitats such as intertidal rocky shore and coral reef environments. Introduction (1970) on the intertidal hoplonemertean Paranemertes peregrina (Coe, 1901). Thereafter, several other stud- Nemerteans are common predators in a wide variety ies on the food and feeding biology, primarily of of marine habitats. Benthic nemerteans prey on many intertidal nemertean species, have been conducted different prey organisms, primarily polychaetes and (Bartsch, 1973, 1975, 1977; McDermott, 1976, 1988, crustaceans (McDermott & Roe, 1985), but some spe- 1993; Reise, 1985; Nordhausen, 1988; Thiel & Re- cies also scavenge on recently dead organisms (Heine ise, 1993; Kruse & Buhs, 2000). These studies have et al., 1991; Thiel, 1998). Pelagic nemerteans occur in revealed that most nemertean species are highly se- all major oceans but apart from recent studies on their lective with respect to their prey species. Reported reproductive biology and distribution pattern (Noren- feeding rates and the results of experimental studies burg & Roe, 1998; Roe & Norenburg, 1999) very little have indicated that nemertean predators have the ca- is known about their general ecology. In this present pacity to exert a significant impact on the populations review, we will primarily focus on benthic nemertean of their preferred prey organisms (McDermott, 1984, species with a strong bias towards nemerteans from 1988; Nordhausen, 1988; Rowell & Woo, 1990; Thiel shallow subtidal and intertidal habitats. & Reise, 1993; Kruse & Buhs, 2000). Modern studies focussing on the ecology of mar- Among marine predators, nemerteans are quite ine nemerteans started with the contribution by Roe unique in that they are very slow-moving primarily 22 relying on their rapidly everted proboscis and highly may be biased since these habitats allow easy access potent toxins. Furthermore, their chemosensory sys- to researchers. On the other hand, there is good indic- tem is strongly developed permitting them to remain ation that nemerteans have a relatively high foraging on the trail of a prey item once ‘smelled the rat’ success in intertidal and shallow subtidal habitats, and (Amerongen & Chia, 1982). It is for these unique fea- thus, these habitats may be most suitable to nemertean tures that nemerteans may play a crucial role in marine predators. Many studies on nemertean predators have habitats in which they occur in high abundance. been conducted in soft-bottom habitats. Undoubtedly The main objective of this review, is to synthes- nemerteans play an important role as predators in these ise the information on the ecology of nemerteans that environments and there is no reason to believe that has been accumulated during the past three decades. they are of less importance in (intertidal) hard-bottom Rather than providing a detailed overview summar- habitats. ising all the information available, we attempted to put Several nemertean species apparently have distinct together the pieces and direct attention to points that preferences for microhabitats such as mussel clumps still require further research attention. or sea-grass patches on intertidal soft-bottoms, the underside of boulders or even polychaete burrows (Bartsch, 1977; McDermott, 1988; Roe, 1993; Thiel Results and discussion & Reise, 1993; Table 1). While pursuing prey, they may leave their shelters, but, following a foraging trip, Habitats nemerteans apparently retreat into these microhabitats. Various nemerteans also live symbiotically on, or Nemerteans occur in almost all marine habitats from in other organisms. Nemertean egg predators and their the benthos to the pelagial, from the tropics to the impacts on the host’s reproductive success are well polar seas, and from the shallow intertidal zone to known (Shields & Kuris, 1988; Kuris, 1993). Other the deep sea. However, most studies that report ne- nemerteans inhabit the interior parts of bivalves (Gib- merteans as important predators have been conducted son & Jennings, 1969; Gibson & Junoy, 1991), or in benthic habitats of temperate and polar regions ascidians (Dalby, 1996), microhabitats which they (e.g. Paranemertes peregrina, Nipponemertes pulcher share with a variety of potential prey organisms. (Johnston, 1837), Lineus viridis (Müller, 1774), Am- Malacobdella grossa (Müller, 1776) feeds both com- phiporus lactifloreus (Johnston, 1827–28), Micrura mensally with its bivalve hosts and as a predator on lactea (Hubrecht, 1879) and Parborlasia corrugatus ◦ small crustacean larvae entering the mantle cavity of (McIntosh, 1887), all from latitudes >40 NorS), their hosts (Gibson & Jennings, 1969). Other ne- yet they are not restricted to these higher latitudes. mertean species in these symbiont-assemblages may The nemertean P. peregrina is also a common pred- also pursue a predatory habit foraging on parasites of ator in the rocky intertidal of California (Roe, 1979). their hosts. Multiple infestation of, e.g., bivalves with Recently, Christy et al. (1998) reported a new species various metazoan species, is not uncommon (Cáceres- that was frequently observed to prey on fiddler crabs Martínez & Vásquez-Yeomans, 1999). Possibly dis- from Panama. Nemerteans appear to be most abundant tinct interactions occur between different associate in intertidal and shallow subtidal habitats. This result species as had earlier been suggested for the hoplone- Table 1. Particular microhabitats reported for some nemertean species Nemertine species Microhabitat Refs. Tetrastemma melanocephalum burrows of Nereis diversicolor Bartsch, 1977 Tetrastemma fozensis Scrobicularia plana Gibson & Junoy, 1991 Gononemertes australiensis Pyura stolonifera Dalby, 1996 Amphiporus lactifloreus mussel clumps Thiel & Reise, 1993 Lineus viridis mussel clumps Thiel & Reise, 1993 Cephalotrix linearis holdfasts of Laminaria spp. Gibson, 1994 23 Table 2 Abundances of nemerteans (Nemertea spp.) reported from various marine environments (Sb soft-bottoms; Hb hard-bottoms) Habitat Location Water depth Abundance Ref. − [m below MLW] [ind.m 2] Sb 37.01 S/174.49 E 0 ∼60 Hewitt et al., 1997 Sb 37.02 S/174.41 E 0 ∼630 Thrush et al., 1992 Sb 43.56 N/69.35 W 0 ∼300 Thiel & Watling, 1998 Sb 36.30 N/6.10 W 0 15–80 Arias & Drake, 1994 Sb 28.00 N/48.00 E 0 ∼6 Prena, 1996 Sb 40.35 N/0.40 E 3 16–56 Palac´ın et al., 1991 Sb 30.00 N/90.00 W ∼5? 105 Gaston et al., 1997 Sb 69.42 N/18.50 E 20 403 (max.) Oug, 1998 Sb 42.45 N/9.00 W ∼20? 50–200 Lopez-Jamar´ & Mejuto, 1986 Sb 42.35 N/8.50 W ∼20? 20–100 Lopez-Jamar´ & Mejuto, 1986 Sb 54.10 N/11.28 E 23 0–3 Prena et al. 1997 Sb 62.05 S/58.28 W 30 70 Jazdzewski et al., 1986 Sb 59.40 N/10.35 E 60 ∼50 Olsgard, 1999 Sb 36.45 S/73.10 W 8–65 8–64 Carrasco et al., 1988 Sb 36.40 S/73.05 W 11–61 ∼2 Carrasco et al., 1988 Sb 58.18 N/6.10 E 50–170 ∼300 Olsgard & Hasle, 1993 Sb 62.43 S/60.30 W 32–421 4.4 Saiz-Salinas et al., 1998 Sb 64.00 S/61.00 W 42–671 5.5 Saiz-Salinas et al., 1997 Sb 67.30 N/6.00 W 1200–1500 1.2 Romero-Wetzel & Gerlach, 1991 Sb 55.58 N/12.41 E 27 122 McDermott, 1984 Sb 20.30 N/18.30 W 1590–2040 111 Cosson et al., 1997 Sb (mesotrophic) 18.30 N/21.02 W 3095–3128 10 Cosson et al., 1997 Sb (oligotrophic) 21.04 N/31.10 W 4580–4647 2.4 Cosson et al., 1997 Hb 32.18 S/28.50 E 0 ∼45 Lasiak & Field, 1995 Hb 40.55 N/140.50 E 0 ∼200 Tsuchiya & Nishihira, 1985 Hb 53.10 N/4.30 W 0 ∼16 000 Lintas & Seed, 1994 Hb 30.00 S/70.00 W 0 ∼10 000 (max.) Thiel & Ullrich, in press mertean Tetrastemma fozensis Gibson & Junoy (1991) pears relatively safe to assume that for most species and copepod parasites of its bivalve hosts (Thiel & the abundance does not exceed 10 individuals m−2 Francés-Zubillaga, 1998).
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