The Natural History Journal of Chulalongkorn University 6(1): 31-36, May 2006 ©2006 by Chulalongkorn University

Heavy Predation on Freshwater Bryozoans by the Golden Apple , canaliculata Lamarck, 1822 ()

TIMOTHY S. WOOD*, PATANA ANURAKPONGSATORN, RATCHA CHAICHANA, JUKKRIT MAHUJCHARIYAWONG AND TUNLAWIT SATAPANAJARU

Department of Environmental Sciences, Kasetsart University, P. O. Box 1072 Chatuchak, Bangkok 10900

ABSTRACT.– Laboratory feeding observations confirm that the golden apple snail (Pomacea canaliculata Lamarck, 1822) is a voracious predator of phylactolaemate bryozoans. An invasive in since the early 1980s, the snail now occupies most freshwater ponds, lakes, and rivers throughout the region. Despite the absence of baseline data, it appears that the snail has had a profound effect on the freshwater bryozoan community, including both tubular and globular colonies. The common gymnolaemate, Hislopia, is less affected. From repeated feeding trials it appears that indigenous apple ( spp.) do not graze on bryozoans; nor does the large indigenous Cipangopaludina chinensis.

KEY WORDS: , Phylactolaemata, Pomacea canaliculata, predation

Golden apple snails (called cherry snails in INTRODUCTION Thailand) were deliberately introduced from Argentina to Taiwan in 1979-80 (Mochida, In small lakes, ponds, and canals of 1991). It was thought that a cottage industry of Thailand, the presence of the golden apple snail culturing the snails for human consumption (Pomacea canaliculata Lamark, 1822) almost would provide income for impoverished always indicates the absence of freshwater farmers. Within several years cherry snails had bryozoans. This observation came to light shown up in Japan, , mainland during our survey of over 140 aquatic sites that China, Korea, Malaysia, and Thailand. While began in 2002. Subsequent work has reinforced local people found the snails unpalatable, the the possibility of massive and widespread snails discovered conditions in tropical Asia disappearance of bryozoans due to heavy that were close to ideal. According to Cowie grazing by the invasive apple snail known (2002) adult females can lay their eggs at primarily for its destructive herbivory. In this weekly intervals throughout the year, depositing paper we document predation by these snails on them in pink masses above the water level. bryozoans and discuss the impact on the After hatching, the young reach sexual maturity bryozoan community. within 2-3 months. With both gills and an air- breathing organ, the snails thrive even in water *Corresponding author: with low dissolved oxygen. During the dry Tel: (0011)-937-775-2542 season they burrow deeply into the mud of Fax: (0011)-937-775-3320 swamps and paddies and aestivate for Email: [email protected] several months (Mochida, 1991). Dispersing 36 NAT. HIST. J. CHULALONGKORN UNIV. 6(1), MAY 2006 with flowing water and even crawling overland, (Halwart, 1994). the cherry snail has spread rapidly and now Legitimate agricultural concerns have occupies most of Southern Asia. overshadowed the role of the cherry snail as a The agricultural impact of the snail has been possible predator in the freshwater community. thoroughly reviewed by Cowie (2002). Our particular interest is in bryozoans, among Attention in Southeast Asia has focused mainly the most common benthic suspension feeding on the extensive damage to rice crops (Oya et in fresh waters. Bryozoans are al., 1986; Yamanaka et al., 1988; Basilio, coelomate invertebrates with a modular growth 1991; Naylor, 1996). Lotus, water chestnut, structure (Wood, 2001, 2004). Appearing as (in Hawaii) and other economic plants also branching tubules or gelatinous mounds, they are affected. The application of chemical form colonies of identical zooids which grow pesticides is costly and takes a heavy toll on on aquatic macrophytes as well as submerged nontarget species. The consequent chemical wood, plastic, glass, and other firm substrata risk to human health is a serious concern, both (Fig. 1). About 80 species are known for the farmer and for the consumer of worldwide, although until recently bryozoans potentially contaminated food. For poorer have received little attention in Southeast Asia. farmers there is a heavy labor cost to removing Nearly all freshwater bryozoans are placed in snails, destroying their egg clusters, and the Class Phylactolaemata; a few genera, such replanting damaged fields. Anecdotal evidence as Hislopia and Victorella, belong to the Class links the spread of the cherry snail (and use of Gymnolaemata which is otherwise mostly molluscicides) to the near disappearance of marine. local edible snails (Pila spp.) in many regions

FIGURE 1. Prey and predator. (a) Bryozoan colony (Plumatella bombayensis) growing on a plastic panel; scale bar = 1 cm. (b) Female cherry snail (Pomacea canaliculata) laying a clutch of pink eggs above the water line; scale bar = 3 cm. WOOD ET AL. –PREDATION ON BRYOZOANS BY GOLDEN APPLE SNAIL 35

MATERIALS AND METHODS RESULTS

To obtain bryozoans colonies, glass plates Pomacea canaliculata: After roaming the 19 cm square were suspended horizontally in a test chamber for several minutes, the snails fish culture pond on the Bang Khen campus of mounted the underside of the glass plate and Kasetsart University in Bangkok. Within four began feeding immediately on the bryozoans. weeks the undersides of the plates were nearly They moved in the direction where bryozoan covered with several bryozoans species. About density was greatest, then returned to graze on 80% of the plate was occupied by Plumatella the less heavily populated regions of the glass bombayensis Annandale, Plumatella vorstmani plate. After only one hour the phylactolaemate Toriumi and Hislopia malayensis Annandale; bryozoans were completely gone, but many of the remaining space was taken by P. casmiana the Hislopia colonies remained alive and only Oka and an unnamed plumatellid species. In slightly damaged. Figure 2 shows similar many places the plumatellid colonies had results using a petri plate rather than flat glass. overgrown Hislopia malayensis. Small sponges Cipangopaludina chinensis: After roaming also were present. the test chamber for several minutes, the snails To observe snail feeding behavior we used mounted the underside of the glass plate and an open polyethylene test chamber measuring began feeding immediately, but not on 16 x 26 x 6 cm submerged in a pan of pond bryozoans. Instead they scraped debris from the water with the glass plate of bryozoans placed plate, working around the bryozoans, feeding across the top, bryozoan side down. The entire immediately adjacent to the colonies and even apparatus was placed under a dissection in narrow crevices between lines of zooids. The microscope so that the observer could focus snail radula made a flicking motion that directly on the bryozoans at magnification of scooped up only loose detritus. Some damage to 10-40x. young plumatellid colonies did occur, but after For comparative purposes, snails used in the four hours the plate was polished clean and study included Pomacea canaliculata,as well as nearly all bryozoans remained intact and alive indigenous Thai snails: Pila pesmei (Morelet, (Fig. 3). 1889), Pila ampullaceal (Linné, 1758), Pila Pila spp.: These snails roamed the test polita (Deshayes, 1830), and Cipangopaludina chamber for several hours, spending most of chinensis (Reeve, 1863). The Pila species were their time on or near the bottom. Sprints across identified according to the morphological the glass plate were brief and rapid. The snails criteria described by Keawjam (1986) and glided over the bryozoan colonies but displayed matched with reference specimens at Kasetsart no interest whatever. Thai residents familiar University. Cipangopaludina and Pomacea with Pila tell us that the snails normally live were collected from ponds at Kasetsart and feed in pond and wetland sediments. We University; the Pila species came from Bann could find no published information to support Teoy, Wang Hin Subdistrict (Tambon), None- these reports. Thong District, Nakhon Ratchasima Province. Separate tests were run with cherry snails as All snails measured 3-4 cm in their largest small as 6 mm. Results of their predation were diameter. Pairs of freshly collected snails were exactly the same as with large adults. We also introduced to the chamber and allowed to roam confirmed cherry snail predation on freely. Observations were made continuously Lophopodella carteri, a globular, gelatinous for about 30 minutes, then periodically over the colony very different in structure from the next several hours. Cipangopaludina chinensis branching tubular plumatellids. Lophopodella were left in the apparatus for eight hours. carteri (Hyatt, 1866) has been shown to be Digital video footage was taken of feeding highly toxic to fish (Tenney & Wollcott, 1964), behavior. but it had no apparent effect on the snails. 36 NAT. HIST. J. CHULALONGKORN UNIV. 6(1), MAY 2006

FIGURE 2. Effects of cherry snail predation; scale bar = 2 cm. (a) Petri dish with colony growths of Plumatella bombayensis, Plumatella vorstmani, and Hislopia malayensis. (b) Same dish after one hour of feeding by a single 4 cm diameter cherry snail. Most of the remaining material is living colonies of Hislopia.

FIGURE 3. Effects of feeding by indigenous apple snail, Pila pesmei (Morlet, 1889); scale bar = 1 cm. (a) Glass plate with colonies of Plumatella vorstmani Toriumi (b) Same plate after 8 hour exposure to Pila pesmei, showing a much cleaner glass plate and relatively undamaged colonies.

WOOD ET AL. –PREDATION ON BRYOZOANS BY GOLDEN APPLE SNAIL 35

DISCUSSION Among bryozoan species in Thailand, the two most common are Hislopia malayensis and Results confirmed our suspicion that cherry Plumatella bombayensis. Our results show that snails graze actively and selectively on Hislopia is seldom damaged by cherry snail freshwater bryozoans. Not merely accidental grazing, and so may actually benefit from predators, the snails follow the path of colony reduced competition for space by other branches, lingering over dense beds of zooids bryozoans. Plumatella bombayensis displays until they are completely consumed. This unusual speed in its growth and reproduction, behavior of the invasive snail is in stark and the zooids tend to be widely spaced. These contrast to that of indigenous snails of the same features may offer some protection from cherry large size, which do little damage to bryozoan snail predation, at least in areas where the snail colonies. Given the ubiquity of the cherry snail population is sparse. in Asia and the extensive freshwater habitat in Sponges often occur alongside bryozoans which bryozoans are not present, we conclude and would appear to be equally vulnerable to that we are witnessing an unprecedented loss of cherry snails. However, we have never bryozoans throughout the region. Moreover, observed snails grazing on sponges either in the this loss would be relatively recent, at least lab or in the field. The dense meshwork of since the introduction of the cherry snail in the sharp spicules and the probable low nutritional 1980s. value probably make sponges unpalatable to Missing, of course, is any reliable most grazers. information about bryozoan populations in The long term impact of cherry snails on Thailand prior to the appearance of cherry freshwater bryozoans in Southeast Asia is snails. Previous reports or descriptions of new difficult to assess because the situation is species from southern Asia include two from unprecedented. The affected area is enormous, the Philippines (Kraepelin, 1886, 1906), two well exceeding 3 million km2, not even from Indonesia (Vorstman, 1928a, b), and eight including China where the extent of Pomacea from India (Rao, 1992; Wood & Wood, 2000). canaliculata is yet unknown. In Europe and None of these includes notes on bryozoan North America bryozoans survive predation by ecology, abundance, or distribution. A pre-snail flatworms, various insect larvae, certain fish, inventory from India includes six species that crayfish, and snails (Wood & Okamura, 2005). have not been reported since, nor have they However, the effects of these are generally been found in post-snail Thailand. localized and highly seasonal, while Pomacea Thai bryozoans find apparent refuge from canaliculata is ubiquitous and maintains an the cherry snail on floating structures that have unremitting predation pressure. Moreover, little direct contact with the shore or bottom populations of bryozoan predators in temperate sediment, such as boats, buoys, and fish culture regions seldom achieve the high densities or the pens. In large lakes we find bryozoans growing mechanical feeding efficiencies comparable to on the undersides of leaves of the red water cherry snails. lily, (Nymphaea lotus Linné, 1753) which Another complicating factor in assessing appears to be avoided by the cherry snail; but long term impact is the lack of knowledge about on the lotus (Nelumbo nucifera Gaertn., 1788) freshwater bryozoans in Southeast Asia and in there are usually many cherry snails and very tropical habitats generally. Many species appear few bryozoan colonies. Finely divided to thrive and reproduce both sexually and substrata, such as exposed tree roots, frayed asexually throughout the year. Colony growth rope, and certain aquatic plants also appear to rates are often very high; dispersal with offer refuge to bryozoans, although they seem seasonal flood waters may be widespread and not to be ideal for vigorous colony growth. effective. All of these can be significant factors 36 NAT. HIST. J. CHULALONGKORN UNIV. 6(1), MAY 2006 in species survival against heavy predation, and Kraepelin, K. 1906. Eine Süsswasser Bryozoë yet no details are known. (Plumatella) aus Java. Mitteilungen aus dem For now our concern is with those bryozoan Naturhistorisches Museum in Hamburg, 23: 143- species already rare, many of which have yet to 146. Mochida, O. 1991. Spread of freshwater Pomacea be described. Although the diversity of Thai snails (Pilidae, ) from Argentina to species appears to be high, many species are Asia. Micronesia supplement, 3: 51-62. known only from single, isolated populations. Naylor, R. 1996. Invasions in agriculture: assessing It is very possible that a number of the cost of the golden apple snail in Asia. Ambio, phylactolaemate bryozoans will soon join 25: 443-448. legions of other species worldwide that have Oya, S., Hirai, Y. and Miyahara, Y. 1986. Injuring been lost through the innocent introduction of habits of the apple snail, Ampullarius insularus exotic predators. d’Orbigny, to the young rice seedlings. Proceedings of the Association of Plant Protection in Kyushu, 32: 92-95. ACKNOWLEDGEMENTS Rao, K.S. 1992. Fresh-water Ecology (Bryozoa). Anmol Publications: New Dehli. We are pleased to acknowledge special Tenney, W. R and W.S. Woolcott. 1964. A comparison of the responsews of some species of assistance in the field by Sayan Jiwjaratrong of fishes to the toxic effect of the bryozoan, Kasetsart University. Snails of the genus Pila Lophopodella carteri (Hyatt). Virginia Journal of were provided by Tippayachat Sanohlum and Science (new series) 15: 16-20. identified with assistance from Nitaya Vorstman, A. 1928a. Some freshwater Bryozoa from Laohachinda, Department of General Science at West Java. Treubia, 10: 1-14. Kasetsart University. This work was part of a Vorstman, A. 1928b. 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