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Gastropoda, Capulidae) 1 2 3 SUSPENSION FEEDING AND KLEPTOPARASITISM WITHIN THE 4 GENUS TRICHOTROPIS (GASTROPODA, CAPULIDAE) 5 6 ERIKA V. IYENGAR 7 Department of Biology, Muhlenberg College, 2400 W. Chew St., Allentown, PA 18104, USA. 8 9 10 RUNNING HEAD: SUSPENSION FEEDING & KLEPTOPARASITISM IN TRICHOTROPIS 11 12 Telephone, fax, email: 13 Correspondence: E.V. Iyengar; e-mail: [email protected] 14 15 phone: (484) 664-3731; FAX: (484) 664-3002 16 17 Suspension feeding and kleptoparasitism in Trichotropis 1 ABSTRACT 2 The marine gastropod Trichotropis cancellata is a facultative kleptoparasite, either 3 suspension feeding or parasitically stealing food from tube-dwelling polychaete worms. To 4 determine whether conclusions drawn from long-term studies in the San Juan Islands, 5 Washington, about the relative importance of suspension feeding and kleptoparasitism can be 6 applied generally to T. cancellata across its biogeographic range, I expanded earlier studies to 7 various locales in Alaska and British Columbia. Kleptoparasitism is pervasive throughout T. 8 cancellata 's range, occurring with equal frequency throughout the areas studied. The average 9 density and size of worm hosts are relatively constant across this range. Snail and worm densities 10 are not significantly correlated at the larger scale of site (averaged over nearby sampling 11 locations clustered around a city), but are correlated at the smaller local scale (within a sampling 12 location). Larger worms do not support more snails. The abundance of uninfected worm hosts is 13 usually not limiting, except potentially in some sampling locations in southwest Alaska where 14 the use of a novel host (a sea cucumber) may be the result of low densities of uninfected worms. 15 Additionally, I documented the feeding behaviors of other trichotropid species in these regions. 16 Trichotropis conica is the second confirmed kleptoparasite within the genus Trichotropis, with 17 kleptoparasitism as frequent in this species as in T. cancellata. Like T. cancellata, all sizes 18 observed of T. conica are kleptoparasites. On the other hand, Trichotropis insignis is an obligate 19 suspension feeder. Further studies are needed to determine exactly how many times this 20 behavior has arisen and how many times species have evolutionarily reverted and lost the 21 behavior, but kleptoparasitism evolved multiple times within this clade. 22 23 Keywords: feeding strategies, biogeographic studies, marine snails, symbiosis p. 2 Suspension feeding and kleptoparasitism in Trichotropis 1 INTRODUCTION 2 The pressure to maximize resources, including food, can drive evolutionary innovations 3 (Stearns, 1992; Halanych, 1993). Determining the relative importance of various trophic 4 strategies, such as kleptoparasitism compared with suspension feeding, can reveal some of the 5 selection pressures driving the evolution of a species or larger taxon. Suspension feeders 6 dominate sublittoral, rocky, benthic communities and are responsible for a large portion of the 7 energy flow from the pelagic to the benthic system (Gili & Coma, 1998). Some suspension 8 feeding snails are evolutionarily successful, both in terms of abundance and species longevity 9 (e.g., Turritellidae; Allmon, 1988). However, suspension feeding is largely confined to a few 10 families within the gastropods, despite evolving multiple times (Owen, 1966; Hickman, 1983) 11 and despite the dominance of this feeding mode in the closely related bivalves. Suspension 12 feeding gastropods that use their gill to capture food possess a distinctive set of ctendial and 13 mantle cavity traits (Declerck, 1995). Little is known about the factors promoting the evolution 14 of suspension feeding in snails, but investigations of facultative suspension feeders may shed 15 light on this topic. 16 The marine snail Trichotropis cancellata HINDS, 1843 can either suspension feed 17 independently or kleptoparasitically steal food from a host (Pernet & Kohn, 1998; Iyengar, 18 2002). Previous long-term studies in the San Juan Islands, Washington, USA, demonstrated that, 19 in the summer, the majority of snails in all size classes of T. cancellata are positioned at the 20 opening of worm tubes (Iyengar, 2005) and grow significantly more quickly as kleptoparasites 21 than suspension feeding snails (Pernet & Kohn, 1998; Iyengar, 2002, 2004). Therefore, this 22 feeding mode is likely important to the evolutionary ecology of this snail. However, the 23 frequency of feeding modes utilized by this species outside of the San Juan Islands is unknown, p. 3 Suspension feeding and kleptoparasitism in Trichotropis 1 as are the feeding mechanisms utilized by other species within the genus. Whether 2 kleptoparasitism is an alternative feeding strategy that is utilized only by a few populations of T. 3 cancellata and not used by congeneric species is unknown. Such a restriction of kleptoparasitism 4 would suggest that environmental, morphological or host factors affect the relative benefit of 5 each feeding mode. The studies reported herein examined the frequency of these two feeding 6 strategies in T. cancellata throughout a significant part of its biogeographic range and compared 7 population characteristics of this snail and its hosts in different areas with those measured in the 8 San Juan Islands. I also documented the prevalence of feeding strategies used by other species in 9 the same genus and compared the importance of kleptoparasitism in these species with its 10 importance in T. cancellata. 11 As a suspension feeder, T. cancellata, and likely other suspension feeding species within 12 Trichotropis, beats cilia to draw seawater into the mantle cavity where food particles are trapped 13 in the mucus that covers the gill. The snail moves the food-ladened mucus to grooves in the base 14 of the mantle cavity, translocates the food to within close proximity of its mouth, and uses its 15 pseudoproboscis (a flexible, extensible lower lip) to collect and ingest the mucus (Yonge, 1962). 16 As a kleptoparasite, T. cancellata extends its pseudoproboscis between the feeding appendages 17 of its host, usually a tube-dwelling polychaete worm (Iyengar, 2005), and into the host’s mouth. 18 Cilia on the pseudoproboscis create a counter-current and divert food from the host's mouth to 19 the snail's mouth (Pernet & Kohn, 1998). The snail does not injure the host in any way other 20 than through nutrition deprivation. 21 Thompson (1998) emphasized that a population-level, rather than a species-level, approach 22 is needed to understand fully the dynamics of the coevolutionary process due to the potential for 23 the existence of selection mosaics among populations. Because few traits will be favorable in all p. 4 Suspension feeding and kleptoparasitism in Trichotropis 1 populations, few will be fixed for a species (Thompson, 1998). Trophic shifts and the process of 2 the evolution of feeding behaviors necessarily involve interactions with the surrounding biotic 3 and abiotic environments, even if the animals are not necessarily involved in strict co-evolution 4 (sensu Janzen, 1980). New feeding modes are not instantaneously pervasive across the species 5 range, nor will they necessarily ever become fixed, as the benefits of the new trophic strategy 6 may vary in different environments. Suspension feeding may be profitable for snails only in 7 certain restricted microhabitats, with alternative feeding modes selectively advantageous in other 8 situations. Thus, generalizations about a species based on studies performed in only one region 9 are fraught with uncertainty, as the amount of variation within the species across its entire 10 biogeographic range is unknown. 11 I intended to determine whether conclusions drawn from long-term studies in the San Juan 12 Islands, Washington, can be applied to T. cancellata in general, or whether the importance of 13 suspension feeding versus kleptoparasitism varies across the biogeographic range of this species: 14 Bering Sea to Oregon (Abbott & Dance, 1983). Therefore, I expanded earlier studies to various 15 locales in southeast and southwest Alaska and Vancouver Island, British Columbia. 16 Additionally, I searched for other trichotropid species (and found two: Trichotropis conica 17 MOLLER, 1842 and Trichotropis insignis MIDDENDORFF, 1849) and observed the feeding 18 behaviors utilized by these species. I wanted to consider these behaviors within a phylogenetic 19 context in an attempt to investigate the number of times that kleptoparasitism has arisen within 20 this clade, ostensibly driven by inefficient suspension feeding. Unfortunately, there is 21 uncertainty concerning the phylogeny of groups closely related to Trichotropis, and only a few 22 studies beyond the present report have explicitly examined the feeding modes of trichotropids. 23 These issues, for now, preclude an accurate assessment of the number of times that p. 5 Suspension feeding and kleptoparasitism in Trichotropis 1 kleptoparasitism has evolved and been lost within the trichotropids and their close relatives. The 2 trichotropids and capulids (the latter restricted to the genera Capulus and Hyalorisia) have 3 recently been assigned to the same family (Bouchet & Warén, 1993), within the superfamily 4 Capuloidea (Bouchet & Rocroi, 2005). Because other kleptoparasites have been found within 5 the clade Littorinimorpha (sensu Bouchet & Rocroi, 2005), a preliminary assessment of the 6 minimum number of times that kleptoparasitism has evolved within this clade is possible. 7 8 MATERIALS
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