Of Sea and Shore website, Sale Shell, Seashell, Land Snail,

Kleptoparasitic thieves are everywhere,
guard your food!

Erika V. Iyengar

Biology Department, Muhlenberg College, 2400 W. Chew St., Allentown, PA 18104
*Email: iyengar@muhlenberg.edu

You are watching the marine snail Trichotropis cancellata. Initially, the snail is extending from its shell. You can see the black eyespot at the base of its tentacle, and its psuedoproboscis (lower lip) in relaxed position. Then the camera shot changes so you can watch the snail suspension feeding. The small yellow balls entering the mantle cavity are brine shrimp cysts, about 200 micrometers in diameter. The cysts and other food particles are drawn into the mantle cavity through the action of cilia beating on the gill. The single gill hangs from the roof of the mantle cavity. As water travels through the gill, mucus on the gill traps food particles. This food-laden mucus is then moved to ciliated tracts in the base of the mantle cavity. You can see as the cord of mucus is moved to within close proximity of the snail’s mouth, and the snail uses its pseudoproboscis to lick up the mucus cord. When the camera zooms in, you might be able to see the radula manipulating the food particles in the mouth.

Next, the video changes to Trichotropis cancellata on Serpula columbiana, a tube-dwelling polychaete worm with a hard, calcareous, white tube and a plume of feeding tentacles that are red at the base and white distally. The snail approaches the opening of the worm tube and uses its tentacles to probe between the tentacles of the worm. The snail then extends its pseudoproboscis and inserts it into the mouth of the worm, at the center of the worm’s plume of feeding tentacles. Notice how the worm does not react while the snail is inserting its pseudoproboscis. If you look closely, you can see a small black piece of food traveling up the ciliated groove in the snail’s pseudoproboscis and entering the snail’s mouth before the camera shot changes. Finally, the video shows a close-up (shot through a dissecting microscope) of a snail stealing food. At the left, you can see the white shell of the snail sitting atop the white tube of the worm. The pseudoproboscis, with an obvious groove, extends from the snail, over the worm tube, and into the worm’s mouth, while touching the base of one of the worm’s feeding tentacles (red). The snail then begins stealing cells of Dunaliella marina (a green alga, cell diameter about 6 micometers) that the worm has collected on its feeding tentacles and moved down to its mouth. After I add brine shrimp cysts to the suspension (the image jiggles a bit when I do so), the worm begins feeding on those and you can see the snail steal the cysts (white balls traveling up the pseudoproboscis) as well as the Dunaliella.

When contemplating future careers, few people consider whether it would be more profitable to steal rather than to work for a living, much less what sort of a thief they would be. Yet theft is rampant throughout the animal kingdom, despite attempts to protect resources by those who have them. I am fond of food, so the thieves that strike me as the most insidious, yet the most practical and marvelous, are those who steal food, called kleptoparasites. Kleptoparasitism is a special form of parasitism where the parasite steals food from the host, but does not injure the host in any other direct way.

Imagine you order your favorite dinner at a nice restaurant. As the steaming platters approach, an arm shoots out from beneath your table and the food suddenly disappears. After a few more failed attempts to obtain a meal, you leave the restaurant, hungry and frustrated. You are the unwitting host of a kleptoparasite. You may leave the kleptoparasite behind as you return home. If you are not so lucky, upon opening your refrigerator door, you realize the kleptoparasite is still with you. If you are supremely unlucky, you will not even be able to leave the restaurant's seat. Instead, you will be doomed to a life of culinary delights ordered but never received, sister to the dehydrated soul in Dante’s Inferno who is always near water but unable to drink. Relegated to snatching small morsels from the cornucopia of food you procure, you watch the lion's share go to a pesky kleptoparasite you cannot evict. This is the plight of some tube-dwelling worms in the ocean waters of the Pacific Northwest, plagued by a small, innocent-looking snail (Trichotropis cancellata) that remains next to the opening of the worm tube. The worms are not able to leave their tube and their feathery feeding tentacles are apparently unable to dislodge the snails from the worm’s tube.

Is a life of crime the only option?
The common name for Trichotropis cancellata is the “hairy shell” snail, due to the long, flexible projections that cover the shell. This snail was originally described as a suspension feeder (Yonge 1962), working for its food and feeding on small algae and other organic material floating in the water. Covering the gill, thousands of cilia (small, finger-like projections) beat to create a water current, drawing seawater into the mantle cavity (the cavern between the fleshy body of the snail and its shell). The water travels through the mesh lattice of the gill which acts as a sieve, trapping food particles in the mucus covering the gill. The snail then moves the food-ladened mucus over its right "shoulder" towards its mouth and uses its pseudoproboscis, a long lower lip, to collect and ingest the mucus (Yonge 1962). While mucus may not sound like an appetizing base constituent of human meals, it is commonly used among marine organisms to capture food or move it to an intended location. Suspension feeding is a common feeding strategy in aquatic systems (especially in the ocean), performed by some worms, anemones, oysters, clams, sponges, ascidians (sea squirts), and fish. Suspension feeding has evolved numerous times within marine snails (DeClerck 1995), but remains restricted to a few groups. On the other hand, within the bivalves (a group closely related to snails which includes clams and scallops) suspension feeding dominates. Why there are not more suspension feeding snails when it is such a successful way of feeding for other groups is puzzling. There must be as-yet-undiscovered limitations to this way of feeding for aquatic snails in general.

In addition to suspension feeding, Trichotropis can feed in an alternate way. As a parasite, the snail resides on a host, most often a bottom-dwelling tube worm, for long periods of time. The worms are also suspension feeders and pass water through a feathery crown of feeding tentacles. Particles caught on the tentacles are conveyed towards the mouth, at the base of the tentacular crown. Perched next to the opening of the tube-worm, the snails have close access to a feeding worm’s mouth. To steal food, the snail extends its pseudoproboscis (lower lip) between the host's feeding tentacles and into its mouth. Using cilia on the pseudoproboscis, the snail diverts food from the host’s mouth into its own. No host observed so far displays any overt behavioral reaction to the parasite, either while the snail is beginning a bout of parasitism (i.e., probing the host’s feeding tentacles) or while the snail is actively stealing.

Despite the apparent lack of response by the worm host, infected worms suffer a huge cost: they grow more slowly than uninfected worms (Iyengar 2002). In laboratory observations, an individual snail can steal up to 100% of particles ingested by a host (Pernet and Kohn 1998). However, empty tubes of these worm hosts do not commonly occur in nature, which suggests that the snails do not starve their hosts to death. For their part, Trichotropis snails (small and large ones) grow more quickly when on a worm host than when restricted to suspension feeding. When these snails work for a living, they barely grow at all (Iyengar 2002). Perhaps because of this growth benefit, most Trichotropis in Puget Sound, Washington, are found on worm tubes during much of the year. Most of the snails leave their worm hosts in winter to mate, but even at that time the smallest snails (which are sexually immature) remain on worms (Iyengar 2005). These snails are apparently struggling to make a living as suspension feeders and have evolved a new way of feeding: stealing food!

Marine kleptoparasites
Are these sneaky snail thieves unique? Not at all. Selection favors foraging strategies that minimize the costs of obtaining food, so many thieves attempt to grab cheap meals (Barnard 1984, Vollrath 1984). Scavenging animals often steal food from each other (Curio 1976) and animals that store food or are slow eaters are often the victims of kleptoparasites (Sivinski et al. 1999). Many marine suspension-feeders are rooted in place, collect food on outstretched projections, and then transport it to their mouths (e.g., anemones, bryozoans, hydroids, barnacles, and tube-dwelling worms). Thus these animals are potentially exploitable by kleptoparasites because they are reliably in the same place and a certain amount of time passes before the captured food is digested. Kleptoparasites occur in many different groups of animals.

Close relatives of Trichotropis also steal food. Theft is a family trait! The snail Capulus ungaricus (in the same taxonomic family as Trichotropis) is self-sufficient in food-rich waters, but a thief in food-poor waters, stealing food from bivalves, suspension feeding snails, tube worms and brachiopods (Orton 1949, Sharman 1956, Orr 1962, Thorson 1965). While the hairy shell snail seems to be merely exploiting an opportunity, C. ungaricus has developed skills for theft—similar to a good safe-cracker. To easily access food that is held on a clam’s gill, C. ungaricus rasps a crescent hole along the edge of the host's shell. Then even when the clam is shut tight, the kleptoparasitic snail can insert its lip and access the food (Orton 1949, Sharman 1956). This rasping is taken to a further extreme by related snails in the same genus which drill through the central portion of the shell and through the mantle (underlying tissue) of scallops to steal food from where it is most concentrated—from the scallop's lips and food-gathering tracts (Orr 1962, Matsukuma 1978, Hayami and Kanie 1980). Some carnivorous snails drill prey and consume the soft flesh inside, but these capulids do not eat the host’s flesh, they merely steal food. The parasites remain attached to the living host, with continuous access to the host’s food, for so long that the parasite’s shell grows to mirror the shape of the host’s shell.

Almost all kleptoparasitic molluscs are snails. One wentletrap species sits in the mouth slit of an anemone and extends its lip into the anemone's gastric cavity (“stomach”) to feed (Den Hartog 1987). The snail responds quickly to food—within 15 minutes after an anemone has eaten, the snail is positioned at the host's mouth, even if the snail first has to climb up the side from the base of the anemone. That is motivated movement from an animal that is stereotypically slow as molasses! Other snails appear to weigh the risks and benefits of kleptoparasitism, waiting until hosts are indisposed or too busy feeding to prevent small amounts of theft. Some whelks steal food from sea stars that could potentially kill them, but the snails wait until the sea star has really tucked into its meal before coming in to steal food from an angle that is safe from the sea star’s stomach (Rochette et al. 1995, Morissette and Himmelman 2000). Sea stars do not just lose food to snails, some are plagued by other sea stars that help themselves to the dinner plate (Wobber 1975, Morissette and Himmelman 2000). Juveniles of one brittle star live in the bursae (breathing cavities) of adults of another brittle star species and steal food from their protector (Hendler et al. 1999).

Other groups of animals also contain kleptoparasites. Copepods living in the branchial chambers of ascidians (sea squirts) feed on particles brought in by the host (Caullery 1952). Clinging to the moving food string of the ascidian, the copepods gently pluck food particles from the mucus and slowly inch upwards, remaining always just in front of the host’s stomach opening (Gotto 1957). You may be able to find kleptoparasites in the seafood section of your local grocery store. Pea crabs, or pinnotherids, usually infect bivalves (such as mussels or oysters), but may also plague snails, tube worms, sea cucumbers and sea squirts (Misra and Ghatak 1983). These crabs feed on food particles trapped in the mucus on their bivalve host and sometimes inflict damage to the host gill. This damage to the host qualifies the pea crabs as parasites. Whether they sometimes eat part of the host’s gill and thus qualify as “true parasites,” in addition to their food-stealing kleptoparasitic behavior, is unclear (Street 1974). The pea crab-host relationship is long term. After sexual maturity, females are too large to leave and therefore are eternally trapped in that one host, relying on the miniature males to move around and come calling during the mating season.

Terrestrial kleptoparasites
Ornithologists point out that kleptoparasitism is most commonly seen among birds, particularly seabirds (Brockmann and Barnard 1979, Furness 1987). Piracy among predatory birds is frequent and nearly all raptors occasionally rob each other of food. Most commonly, avian kleptoparasites chase birds carrying food (either in their bill or their stomach) and force them to drop or regurgitate it (Curio 1976). Carbone et al. (1997) posit that kleptoparasitism may have contributed to the evolution of sociality in African large predatory mammals. Predators may have banded together in family units to prevent other carnivores from stealing hard-won prey. All large African carnivores except one at least occasionally steal meat. Cheetahs are the one exception, probably because their high prey capture success rate makes theft more costly than kills (Curio 1976, Barnard 1984).

Among the arthropods, kleptoparasitism is prevalent and most well-studied in the arachnids (spiders) and hymenopterans (ants, bees and wasps). Many spiders in one genus (Argyrodes) are kleptoparasitic specialists, with morphological and behavioral adaptations for this foraging strategy (Tso and Severinghaus 1998). In addition to stealing prey items from the webs of other spiders, some arachnid kleptoparasites also eat the host’s web material. Web material contains physiologically important compounds and represents a considerable portion of a spider's total energy reserves (Higgins and Buskirk 1998, Tso and Severinghaus 1998), so web theft is also a form of kleptoparasitism. Stingless bees pillage other bees' nests, stealing pollen, honey and building materials (Wille 1983). Ironically, some ants will invite harm into their nest, actively seeking certain kleptoparasitic beetle larvae and returning with them. The beetle larva secretes aromatic ethers which the ants ingest. But because the secretions contain no nutrition, the food and care the ants lavish on the beetle represent a loss of energy for the ants (Caullery 1952). Thus the beetle’s ability to essentially create drug-addicted hosts promotes the success of its kleptoparasitic lifestyle.

Sometimes ants themselves are the kleptoparasites and this behavior has been carried to such an extreme in some species that the ants are no longer capable of feeding themselves. To establish a new colony, a kleptoparasitic queen will invade the nest of another ant species, smear herself with host secretions to mask her scent and kill the host queen. The invader becomes the new queen, laying her own eggs. The host species tends her and her offspring, regurgitating food for the workers of the invading species, oblivious to the duplicity of the invader queen (Caullery 1952). Not all slave-making ants move into the host’s home, some bring the hosts home with them. In one Amazonian slave-making ant species, the ants have no option of feeding themselves because their mandibles have no masticating edges. (Imagine yourself with no teeth, trying to eat a salad!) Instead, soldier ants capture the pupae of other ant species and bring them, unharmed, back to the nest. When the captured ants emerge from the pupae as adults, these slaves feed their masters and help them care for the nest (Caullery 1952, Read 1970).

Evolutionary importance of kleptoparasitism
Two of the highest priorities of most animals are finding and protecting food resources. Kleptoparasitism can have profound impacts on the morphology, behavior and life histories of both the kleptoparasite and the host as selection pressures can cause an escalating co-evolutionary arms race. Diet choice and searching behavior of the host may be influenced by the presence of kleptoparasites. Smaller prey that can be consumed rapidly before kleptoparasites intervene may suddenly become more profitable. Wild dogs, lapwings (birds), golden plovers (birds), and northern pike (fish) consume smaller prey in the presence of kleptoparasites (Barnard 1984, Carbone et al. 1997, Nilsson and Bronmark 1999). Lapwings and golden plovers may even toss large worms that they have found towards nearby gulls to avoid harassment by these kleptoparasites, even though they would eat these large food items if the kleptoparasites were absent. Especially because gulls are significantly larger birds and will likely win a tug-of-war, it is better for the smaller birds to minimize the loss and sooner search again for a small, quick meal than to waste a lot of time and energy tussling over a large food item. For animals already operating near their physiological limits, kleptoparasites can have devastating effects. Wild dog populations are negatively impacted by even low levels of spotted hyena kleptoparasitism. Because kleptoparasitism may have contributed to the extinction of one Serengeti wild dog population, managers now consider it when developing conservation plans for this species (Carbone et al. 1997, Gorman et al. 1998).

However, the prevalence of kleptoparasitism in different systems may often be underestimated because some kleptoparasites are facultative, able to feed as a kleptoparasite or using another strategy and switching between methods as the opportunities arise. Additionally, the extent of the negative impact exerted by the kleptoparasite can depend on the current condition and habits of each organism. This variation causes difficulties in assessing the prevalence and impacts of the interaction.

Facultative parasitic interactions, as in the Trichotropis snail-worm example have advantages as study systems. In obligate symbiotic interactions, the partners cannot live outside the association. However, experiments using facultative parasites can assess the performance of each participant within (as kleptoparasites) and outside (as independent feeders) the interaction and determine the relative costs and benefits of each feeding strategy. Experiments have demonstrated that Trichotropis cancellata is food-limited when suspension feeding and grows more quickly as a kleptoparasite and may provide insight as to the characteristics that have prevented the evolutionary success of suspension feeding in snails. At least for these snails, it turns out that it is far more lucrative to steal than to work for a living.

References cited
Barnard CJ. 1984. The evolution of food-scrounging strategies within and between species. Pages 95-126 in Barnard CJ, ed. Producers and scroungers: Strategies of exploitation and parasitism. London: Croom Helm.

Brockmann HJ, Barnard CJ. 1979. Kleptoparasitism in birds. Animal Behaviour 27: 487-514.

Carbone C, Du Toit JT, Gordon IJ. 1997. Feeding success in African wild dogs: Does kleptoparasitism by spotted hyenas influence hunting group size? Journal of Animal Ecology. 66: 318-326.

Caullery M. 1952. Parasitism and Symbiosis. London: Sidgwick and Jackson Limited.

Curio E. 1976. The ethology of predation. Berlin: Springer-Verlag.

Declerck CH. 1995. The evolution of suspension feeding in gastropods. Biological Reviews of the Cambridge Philosophical Society 70:549-569.

Den Hartog JC.1987. Observations on the wentletrap Epitonium clathratulum (Kanmacher, 1797) (Prosobranchia, Epitoniidae) and the sea anemone Bunodosoma biscayensis (Fischer, 1874) (Actinaria, Actiniidae). Basteria 51: 95-108.

Furness RW. 1987. Kleptoparasitism in seabirds. Pages 77-100 in Croxall J.P, ed. Seabirds:
feeding ecology and role in marine ecosystems. Cambridge: Cambridge University Press.

Gorman ML, Mills MG, Raath JP, Speakman JR. 1998. High hunting costs make African wild dogs vulnerable to kleptoparasitism by hyaenas. Nature. 391: 479-481.

Gotto RV. 1957. The biology of a commensal copepod, Ascidicola rosea Thorell, in the ascidian Corella parallelogramma (Muller). Journal of the Marine Biological Association U.K. 36: 281-290.

Hayami I, Kanie Y. 1980. Mode of life of a giant capulid gastropod from the Upper Cretaceous of Saghalien and Japan. Paleontology (London) 23: 689-698.

Higgins LE, Buskirk RE. 1998. Spider-web kleptoparasites as a model for studying producer-consumer interactions. Behavioral Ecology, 9: 384-387.

Iyengar EV. 2002. Sneaky snails and wasted worms: kleptoparasitism by Trichotropis cancellata (Mollusca, Gastropoda) on Serpula columbiana (Annelida, Polychaeta). Marine Ecology Progress Series. 244: 153-162.

Iyengar EV. 2005. Seasonal feeding-mode changes in the marine facultative kleptoparasite Trichotropis cancellata (Gastropoda, Capulidae): trade-offs between trophic strategy and reproduction. Canadian Journal of Zoology 83: 1097-1111.

Matsukuma A. 1978. Fossil boreholes made by shell-boring predators or commensals. I. Boreholes of capulid gastropods. Japanese Journal of Malacology Venus. 37: 29-45.

Misra A, Ghatak SS. 1983. On some symbiotic associations between different species of marine animals. Pages 117-134 in Tikader BK, ed. Host as an environment: proceedings of the Symposium on Host as an Environment. Zoological Survey of India. Calcutta: Bani Press.

Morissette S, Himmelman JH. 2000. Subtidal food thieves: Interactions of four invertebrate kleptoparasites with the sea star Leptasterias polaris. Animal Behaviour. 60: 531-543.

Nilsson PA, Bronmark C. 1999. Foraging among cannibals and kleptoparasites: Effects of prey size on pike behavior. Behavioral Ecology. 10: 557-566.

Orr V. 1962. The drilling habit of Capulus danieli (Crosse) (Mollusca: Gastropoda). The Veliger 5: 63-67.

Orton JH. 1949. Notes on the feeding habit of Capulus ungaricus. Reports Marine Biological Station Pt Erin 61:29-30.

Pernet B, Kohn AJ. 1998. Size-related obligate and facultative parasitism in the marine gastropod Trichotropis cancellata. Biological Bulletin 195: 349-356.

Read CP. 1970. Parasitism and Symbiology. New York: The Ronald Press Company.

Rochette R, Morissette S, Himmelman JH. 1995. A flexible response to a major predator provides the whelk Buccinum undatum L. with nutritional gains. Journal of Experimental Marine Biology and Ecology. 185: 167-180.

Sharman M. 1956. Note on Capulus ungaricus (L.) Journal Marine Biological Association U.K. 35: 445-450.

Sivinski J, Marshall S, Petersson E. 1999. Kleptoparasitism and phoresy in the diptera. Florida Entomologist. 82: 179-197.

Street P. 1974. Animal Partners and Parasites. Newton: David and Charles.

Thorson G. 1965. A neotenous dwarf-form of Capulus ungaricus (L.) (Gastropoda, Prosobranchia) commensalistic on Turritella communis Risso. Ophelia 2: 175-210.

Tso IM, Severinghaus LL. 1998. Silk stealing by Argyrodes lanyuensis (Araneae: Theiriidae): A unique form of kleptoparasitism. Animal Behaviour 56: 219-225.

Vollrath F. 1984. Kleptobiotic interactions in invertebrates. Pages 61-94 in Barnard CJ, ed. Producers and scroungers: Strategies of exploitation and parasitism. London: Croom Helm.

Wille A. 1983. Biology of the stingless bees. Ann Reviews of Entomology 28: 41-64.

Wobber DR. 1975. Agonism in asteroids. Biological Bulletin (Woods Hole) 148: 483-496.

Yonge CM. 1962. On the biology of the mesogastropod Trichotropis cancellata Hinds, a benthic indicator species. Biological Bulletin (Woods Hole) 122: 160-181.