Predation on freshwater bryozoans by invasive apple snails Timothy S. Wood1, Patana Anurakpongsatorn2 and Jukkrit Mahujchariyawong2 1Department of Biological Sciences, Wright State University, Dayton, Ohio 45435, USA. Email: [email protected] 2Department of Environmental Technology and Management, Kasetsart University, Chatujak, Bangkok 10903, Thailand. Email: [email protected], [email protected] Abstract Freshwater bryozoans in much of southern Asia are under assault from invasive apple snails (Pomacea canaliculata and perhaps P. maculata). In lakes and ponds where the snails are present the normal bryozoan populations are sharply reduced or absent. Laboratory feeding trials on inert substrata show that the snails readily consume sessile bryozoans in apparent preference over other organic material. Bryozoans in the family Plumatellidae appear to be most vulnerable to predation; the much smaller Hislopia species largely escape damage from snail grazing. In laboratory feeding trials other snail species native to Thailand, similar in size to the apple snails, ignore bryozoans completely. Other invertebrate species, as well as fish, are known to graze occasionally on bryozoans, but not as thoroughly as apple snails. Among the 42 bryozoan species living within the current invaded range of the apple snails, 24 are considered rare and 17 are known only from preserved specimens. Additional keywords: Ampullariidae, Asia, Bryozoa, Mollusca, Phylactolaemata, Pomacea Introduction Most studies on the invasive character of introduced apple snails, primarily Pomacea canaliculata but also P. maculata, have focused on the damage inflicted on economically important food crops (e.g. Cowie, 2002). This is not surprising. The destruction is considerable, immediate and easily quantified. In many areas around the world invasive 63 apple snails affect the lives of farmers, alter the local economy, change local habitats and raise serious issues of pesticide use (e.g. Naylor, 1996; Carlsson et al., 2004). Whether invasive apple snails also suppress local snail populations has long been suspected (Halwart, 1994), but solid evidence remains elusive. Populations of local snails have been reported to decline as the density of apple snails increases, but whether this is due to competition for limited resources or to human or environmental factors is unclear. Nonetheless, Pomacea canaliculata is known to prey on other snail species (Cazzaniga, 1990; Kwong et al., 2009) and so at least their carnivory is established. However, there is no question about the devastating effects of apple snails on populations of plumatellid bryozoans (Wood et al., 2006a). Since 2001 we have studied freshwater bryozoans in Thailand. From the first week of a nationwide survey it was apparent that where non-native apple snails were abundant we could not expect to find bryozoans. This observation, repeated at dozens of lakes and ponds, led to a suspicion that was confirmed in the laboratory (Wood et al., 2006a). Apple snails target bryozoans and graze on them systematically and thoroughly. The effect is to limit the substrata on Fig. 1. Morphology of plumatellid bryozoans. A: Plumatella javanica on bamboo pulled from the water; scale bar, 1 cm. B: Plumatella vaihiriae colony showing zooids with extended lophophores; scale bar, 3 mm. C: closer view of P. vaihiriae; scale bar, 1 mm. 64 BIOLOGY AND MANAGEMENT OF INVASIVE APPLE SNAILS which bryozoans can grow, and in many cases to eliminate bryozoan populations from an entire region. What are bryozoans? Bryozoans are commonly known as “moss animals” because many species look like moss. Usually brown or green, they are always attached to a submerged object, such as a stick of wood, macrophyte or an article of trash (Fig. 1a). They are abundant, widely distributed and second only to molluscs as the most important filter-feeding invertebrates in fresh waters (Wood & Okamura, 2005). The bryozoan species most vulnerable to grazing by apple snails are in the family Plumatellidae (Wood et al., 2006b). All are composed of branching tubules that spread like thin roots across the substratum (Fig. 1a, b). Sometimes the branches form dense patches with shrubby, upright growths. Apple snails also graze on gelatinous bryozoan species, such as Asajirella spp. (Lophopodidae), that grow as globular forms from the size of a pea to structures measuring >10 cm across. The only bryozoans that routinely escape apple snail predation are Hislopia spp. (Hislopiidae), which are very small and flat with a tough outer cuticle (Wood et al., 2006b). Bryozoans are modular animals. That is, they grow as colonies composed of multiple, identical units, called zooids. Each zooid is capable of carrying out basic life functions such as food gathering, digestion, respiration and reproduction. In tubular bryozoans the zooids are located at intervals along the tubes. To gather suspended particles of food they use ciliated tentacles organized in an organ called a lophophore (Fig. 1c). The particles are passed down to a large stomach located inside the tube (Fig. 1c). While ingested particles are thoroughly churned about in the stomach most of them appear to remain intact. There is evidence that bryozoan nutrition is derived from bacteria captured along with the particles of detritus (Richelle et al., 1994). After variable time in the stomach the particulate material is packed into a so-called intestine, where it is infused with mucus and eventually discharged through the anus as a faecal pellet (Fig. 1c). Faecal pellets accumulating in the sediments are a rich source of food for annelids, insect larvae and other benthic invertebrates. When threatened or alarmed the bryozoan can withdraw its delicate lophophore into the tube. There are no other behavioural, structural or chemical defence mechanisms that would protect the bryozoan colony from a grazing apple snail. The food value of a colony would include muscle tissue and gut contents. However, there is even more energy to PREDATION ON FRESHWATER BRYOZOANS BY INVASIVE APPLE SNAILS 65 be derived from dormant, lipid-filled capsules called statoblasts that often occur in the tubules. Whether statoblasts can be processed by the snail digestive system is not known. Statoblasts are a primary means of dispersal. Each is about the size of a full stop (period) on this page. Many hundreds or thousands of them are normally released into the water by a bryozoan colony. With a natural buoyancy they are widely distributed during the flooding season and can also be carried to new sites on the feet and feathers of waterfowl. Statoblasts tolerate desiccation and other unfavourable conditions, and after a period of dormancy they are able to germinate to produce a new colony. All non-gelatinous bryozoans are attached permanently to the substrate. Although the lophophore can move in and out of the tubes, the colonies as a whole are fixed in place. Fish sometimes nibble at overgrown colonies; various snails, flatworms and immature insects also feed on bryozoans (Wood & Okamura, 2005). However, nothing compares to the wholesale, systematic destruction of entire colonies caused by apple snails. Further information on these and other aspects of the biology of freshwater bryozoans can be found in the publications of Wood & Okamura (2005), Wood (2009) and Wood et al. (2010). What is the evidence for apple snail grazing on bryozoans? The indirect evidence is compelling: bryozoans are common residents of lakes and ponds throughout Thailand, except at those sites where apple snails are abundant. In those instances the bryozoans are either missing entirely or else surviving in places inaccessible to snails, such as dangling rope or floating buoys. We have encountered small refugee colonies hidden in deep crevices of floating logs. Sometimes they thrive on the spiny underside of lotus leaves, which apple snails tend to avoid. In general we have learned that whenever we see pink clusters of apple snails eggs we can expect to find very few bryozoans. More direct evidence of grazing comes from experimental feeding trials in the laboratory. To prepare for these tests we suspended 19 cm x 19 cm glass plates in a pond on the campus of Kasetsart University in Bangkok. After four weeks in the water the plates were covered with a wide variety of organisms, including protozoans, rotifers, flatworms and nematodes. There were also numerous bryozoan colonies, a natural combination of Plumatella bombayensis, P. vorstmani, P. vaihiriae and Hislopia malayensis. In the laboratory these plates were cleaned on one side and inverted (clean side up) into a basin of pond water with a single snail. The snails quickly located the 66 BIOLOGY AND MANAGEMENT OF INVASIVE APPLE SNAILS Fig. 2. Photos from a video file showing an apple snail feeding on a plumatellid bryozoan. The animals were on one side of a glass plate and the photos were taken from the opposite side of the plate. A: snail foot is in the upper right, head and mouth are to the left; the bryozoan colony appears as a central hub with 5 branches. B: several seconds later most of the colony is gone, represented here by white dotted lines. Scale bar, 5 mm. bryozoans and began feeding immediately. If the colony was a single long branch the snail would follow the branch, ignoring the flocculent material on either side and specifically targeting the bryozoans (Fig. 2). The trials were repeated five times, each time with a different snail, and each time giving the same result. All the plumatellid bryozoans were readily consumed; only the very small hislopiid colonies escaped with little apparent damage. In subsequent tests we found apple snails as small as 6 mm shell diameter capable of destroying plumatellid bryozoan colonies. Are bryozoans affected by native snails? Our laboratory tests were repeated using native Thai snails: Pila pesmei, Pila ampullacea, Pila virescens (often referred to incorrectly as Pila polita; see Cowie, 2015) (Ampullariidae) and Cipangopaludina chinensis (Viviparidae). The C. chinensis came from the Bangkhen campus of Kasetsart University; the Pila spp.