THE ASIAN INVASIVE FRESHWATER CLAM CORBICULA FLUMINEA AS PREY OF TWO NATIVE WATERBIRDS IN SOUTH-EASTERN BRAZIL

The invasive Asiatic freshwater bivalve Corbicula fluminea is regarded as a pest in several countries including Brazil. Two water birds native to South America, the limpkin Aramus guarauna and the common gallinule Gallinula galeata, are herein recorded preying on C. fluminea in a pond of an urban park in South-eastern Brazil. The exotic clam is becoming increasingly common in the diet of both these water birds. This trend is likely due to its increasing population and the consequent rarity of the habitual prey (apple snails and native clams) for the mollusc-specialised limpkin, besides being an accessible animal protein source for the omnivorous gallinule.

The freshwater bivalve Corbicula fluminea (O.F. Müller, 1774), Corbiculidae, underwent a global expansion from its native Asia to North America, South America, and Europe, and is still expanding its range in these countries (ARAUJO et al. 1993, KAMBURSKA et al. 2009, MANSUR et al. 2012, MACKIEWICZ 2013).The so called Asian or basket clam is regarded as one of the 100 worst invasive species in Europe (DAISIE 2008), being a source of serious environmental and economic damage (ISOM 1986, DARRIGAN 2002, SOUSA et al. 2008, 2009, MANSUR et al. 2012).The basket clam is the most common and widespread of the four recorded species of the genus Corbicula in Brazil (MANSUR et al. 2012).
Corbicula fluminea is preyed on by vertebrates, including fishes in North and South America (ROBIN- SON & WELLBORN 1988, OLIVEIRA et al. 2010), and turtles and ducks in North America (HOPPE et al. 1988, WILHELM & PLUMMER 2012).Herein we report on two native water birds, the limpkin Aramus guarauna (Linnaeus, 1766) (Aramidae) and the com-mon gallinule Gallinula galeata (Lichtenstein, 1818) (Rallidae) preying on C. fluminea at an urban park in South-eastern Brazil.The limpkin is a specialised mollusc-eater, whereas the gallinule is an omnivore feeding on both aquatic vegetation and invertebrates (HOYO et al. 1996, CORBO et al. 2013).
The study site is the Parque Ecológico Prof. Hermógenes de Freitas Leitão Filho (22°48'42"S, 47°04'21"W), Campinas, São Paulo, South-eastern Brazil.This park has a total area of 13.4 ha, of which about 75% is occupied by a pond surrounded by trees, bushes and grass patches.The foraging birds were observed with the naked eye and through 10×50 binoculars, and recorded with a 70-300 telephoto zoom lens mounted on a SLR camera from a distance of 4-20 m.Throughout the observational sessions we mostly used "focal-animal" and "sequence" samplings (ALTMANN 1974), both of which are adequate for opportunistic records.Sizes of preyed clams were measured directly from shells taken at limpkins' processing places (see below), or estimated against the bill size of the photographed birds holding their prey, and checked against actual clam shells and museum specimens of birds.C. fluminea shells taken at limpkins' processing places are housed as vouchers at the bivalve collection of the Museu de Zoologia da Universidade Estadual de Campinas (accession number ZUEC BIV 3981).Shells retrieved at such places have small chips on the edges of the valves (see SNYDER & SNYDER 1969 for similar, small damage done to clams by limpkins).
The limpkin waded while foraging for the Asian clam and picked this prey with its bill tip (Fig. 1).The bird carried the clams to the pond bank, anchored the prey hinge down in the wet ground and extracted the soft parts using its specialised bill (see detailed description in SNYDER & SNYDER 1969).Clams up to 4 cm were favoured over the smaller ones (likely due to cost-benefits of foraging on large versus small clams) and opened to extract the soft parts.Small clams (up to 2 cm) were sometimes taken and swallowed whole.The limpkin often used the same bank portions to open the clams, thus creating a sort of processing places full of empty shells (Fig. 2).The limpkin was recorded preying on this clam since 2007, although at that time it preyed mostly on large native molluscs, the channelled apple snail Pomacea canaliculata (Lamarck, 1819) (Ampullariidae) and the also native plate clam Anodontites trapesialis (Lamarck, 1819) (Mycetopodidae).The large plate clam was the favoured prey of the limpkin until its visible decrease at the study site from 2007 on, and becoming increasingly rare among the molluscs taken by the bird.
Foraging of gallinules on Asian clams was noticed in 2013 at a particular site, and appeared to spread through family groups composed of an adult couple and their grown chicks able to dive.While foraging for clams the gallinule swam over a site within radius limited to about 10 m, peered intently into the water and dove after the prey (Fig. 3).This water bird picked only small clams (up to 2 cm) and swallowed them whole (Fig. 4).Currently the gallinules forage at the clam bank regularly and this prey likely became an important part of their omnivorous diets.We recorded other sites at which the gallinules foraged for clams, but the one described above was the most favoured site.
Possibly influenced by an increase of C. fluminea populations in the studied pond (as noticed from some spots of massive mortality), Pomacea canaliculata and Anodontites trapesialis populations began to visibly  HOPPE et al. 1986).
As Corbicula fluminea is still expanding its range in Brazil (MANSUR et al. 2012), we suggest that it will be reported elsewhere as prey of the limpkin, the gallinule, and possibly other water birds such as ducks able to handle this invasive bivalve as food.

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Figs 1-4.Asian clam (Corbicula fluminea) preyed on by native water birds in Brazil: 1 -carrying a clam in its bill, a limpkin (Aramus guarauna) wades towards the pond bank to open the shell; 2 -several empty shells of the Asian clam and one of the apple snail Pomacea canaliculata on the bank portion where a limpkin opened the clams and extracted the soft parts; 3 -its feet still visible on the water surface, a young common gallinule (Gallinula galeata) dives to pick a clam from the bottom of the pond; 4 -upon surfacing, the young gallinule holds a small clam in the middle of its bill