Predatory potential of freshwater animals on an invasive agricultural pest, the apple snail Pomacea canaliculata (Gastropoda: Ampullariidae), in southern Japan
Yoichi Yusa
1,*, Naoyuki Sugiura
2& Takashi Wada
National Agricultural Research Center for Kyushu Okinawa Region, Nishigoshi, Kumamoto 861-1192, Japan;
1Present address: Faculty of Science, Nara Women’s University, Kitauoya-Nishimachi, Nara 630-8506, Japan;
2Present address: Uki Agricultural Extension Services, Kumamoto Prefecture, Matsubase, Kumamoto 869- 0532, Japan;*Author for correspondence (e-mail: [email protected]; fax: +81-742-20-3424)
Received 31 January 2004; accepted in revised form 4 August 2004
Key words: alien species, biodiversity, biological control, natural enemy, paddy field, predation, rice Abstract
The apple snail Pomacea canaliculata is an invasive species and a serious pest of rice in many Asian countries. We studied predatory activities of various animals living in Japanese freshwater habitats, by keeping each individual of a potential predator species with 36 snails of various sizes for three days in the aquarium. Forty-six species were tested, and 26 in eight classes fed on small snails. A species of leech, crabs, the common carp, turtles, the mallard duck and the Norway rat attacked even adult snails of 20–30 mm in shell height. These findings will be helpful in identifying effective predators for biologi- cal control of the pest snail. In addition, most of the animals attacking snails are reported to be com- mon in rivers or ponds, but few live in modernized paddy fields having little connections with natural water systems. This may be a reason why this snail maintains large populations in paddy fields but not in other freshwater habitats.
Introduction
The apple snail Pomacea canaliculata is originat- ing from temperate to subtropical, or possibly to tropical South America (Cowie 2002). It was introduced into many countries mainly in Asia and also in North and Central Americas, either deliberately (as human food or aquarium pet) or accidentally (Halwart 1995; Naylor 1996; Perera and Walls 1996; Cowie 2002). Soon after intro- duction, the snails invaded local aquatic habitats such as rivers, ponds, canals or paddy fields. The snail damages paddy crops such as taro, lotus, and especially young rice. It has become one of the worst pests of rice in Asia (Naylor 1996; Co- wie 2002). The resulting economic loss, as well as environmental and health hazards are highly
problematic in introduced areas (Naylor 1996).
Many adjacent countries where people rely heav- ily on rice such as India or Bangladesh, or where the local ecosystems are characterized by high endemism such as Australia, are threatened with the snail’s invasions (Baker 1998).
In Japan, the snail was introduced as human food mainly in 1981, and after that the areas with snail infestation have been increasing (Wada 1999; Yusa and Wada 1999). In addition to the natural expansion of the distribution, artificial spreading of the snail still continues: although local governments prohibit, the snail has been introduced to new areas for paddy weeding, as it is an effective paddy weeding agent (Wada 1999).
In Korea, such weeding is becoming popular among organic farmers, and the snails were
Biological Invasions (2006) 8: 137–147 Springer 2006
DOI 10.1007/s10530-004-1790-4
released in ca. 2000 ha of paddy fields in 2002 for this purpose (Hwang 2002).
The apple snail appears to have life history traits suitable for colonization into new areas:
adaptability to broad environmental conditions, omnivorous feeding habit and early maturation together with a high fecundity under preferable conditions (Lach et al. 2000). For instance, the snails live in tropical, sub-tropical and temperate climates. They bury themselves in the mud dur- ing the dry season as well as at extreme tempera- tures in the field, which makes them more tolerable to these harsh conditions. The snails occur both in clean and polluted waters (Lach et al. 2000). They are also tolerable to starvation, without eating any visible food for 5 months in the water (Lach et al. 2000). In addition, they are omnivorous, eating various plants (Lach et al.
2000) as well as some animal material such as dead fishes (Cowie 2002). They reach sexual maturity in 2–3 months in good conditions, and a typical female can lay 2400–8700 eggs per breeding season under captivity (Miyahara et al.
1986). Initially, most of these characteristics were ideal for the aquaculture. However, the same characteristics might have allowed the snail to settle successfully in introduced areas, and to have major impacts on local ecosystems after successful colonization.
A species will actually become invasive when it is released from its natural enemies, when intro- duced into new areas (Mack et al. 2000). Several effective predators of P. canaliculata have been known in the native areas, including the snail kite,Rostrhamus sociabilisor the limpkin,Aramus guarauna (Perera and Walls 1996). On the other hand, few effective predators have been known in introduced areas (but see Yusa et al. 2000; Joshi 2001; Yusa 2001 for exceptions). However, rela- tively low densities of the snail in natural habitats such as rivers in Japan (Ichinose et al. 2000) sug- gest the presence of effective predators. The infor- mation on the effects of local predators is especially important for snail control, because pesticides are generally not effective to control the snails in paddy fields in the rainy season, and not allowed to apply in canals, ponds or rivers. Thus, natural enemies are expected as an effective con- trol agent in Japan, as well as other countries suffering from the snail infestation.
The purpose of this study was to investigate the predatory potential of animals living in Japa- nese freshwaters. We arbitrarily selected 46 ani- mal species, most of which are commonly observed in southern Japan, and tested their predatory activities on the apple snails of various sizes, from hatchlings to adults in the laboratory.
Materials and methods Animals used
We caught most potential predators in ponds, rivers, canals or paddy fields in Kumamoto Pre- fecture, Kyushu Island, southern Japan in 1997 and 1998. The other animals were purchased from pet shops (marked as ‘‘reared’’ in Appendix A). All the animals were acclimated for at least 1 day under the experimental conditions (25C and 14L:10D photoperiod). In some cases where the acclimation period lasted for several days, we fed them with artificial food pellets for carp (‘Swimmy’; Japan Pet Food Co., Tokyo) up to 1 day before the experiment.
Most snails were collected in paddy fields in Kumamoto, and kept in 60-l aquaria until use.
Carp food pellets were given to them as needed.
Some small snails <4 mm in shell height were collected from egg masses laid in the stock culture in the laboratory.
Experimental procedure
In each experiment, we introduced an individual of the potential predator and 36 snails in a 60-l plastic aquarium (59 cm length ·23 cm width, with 35 cm water depth) with a lid on it. No hiding or resting places were provided inside the aquarium.
We used six individuals ofP. canaliculatafor each of six size classes: <4 mm in shell height, <8 mm,
<12 mm, <16 mm, <20 mm, and 20–30 mm (the last category representing adults). The test animal and 36 snails were kept together for 3 days at 25C and 14L:10D. Blot-dry body weight and the maxi- mum length of the potential predator were mea- sured when elongated, mostly prior to the experiment, but sometimes after it to avoid the stress for the animal (mainly for fishes). No animals other than experimental snails were added in the 138