Silvana Burela

Insights from an Integrated View of the Biology of Apple Snails (Caenogastropoda: Ampullariidae)

ABSTRACT Apple snails (Ampullariidae) are among the largest and most ecologically important freshwater snails. The introduction of multiple species has reinvigorated the field and spurred a burgeoning body of research since the early 1990s, particularly regarding two species introduced to Asian wetlands and elsewhere, where they have become serious agricultural pests. This review places these recent advances in the context of previous work, across diverse fields ranging from phylogenetics and biogeography through ecology and developmental biology, and the more applied areas of environmental health and human disease. The review does not deal with the role of ampullariids as pests, nor their control and management, as this has been substantially reviewed elsewhere. Despite this large and diverse body of research, significant gaps in knowledge of these important snails remain, particularly in a comparative framework. The great majority of the work to date concerns a single species, Pomacea canaliculata, which we see as having the potential to become a model organism in a wide range of fields. However, additional comparative data are essential for understanding this diverse and potentially informative group. With the rapid advances in genomic technologies, many questions, seemingly intractable two decades ago, can be addressed, and ampullariids will provide valuable insights to our understanding across diverse fields in integrative biology.

Nuptial Feeding In the Freshwater Snail Pomacea canaliculata (Gastropoda: Ampullariidae)

The males of the freshwater snail Pomacea canaliculata have a copulatory apparatus consisting in a delicate penis running through a muscular channeled sheath bearing three different glands. The outer gland is the most conspicuous one and often secrets a sticky drop of mucus during copula. However, its function is enigmatic because it opens toward the exterior of the pallial cavity. During laboratory trials performed to register copula duration and mating behaviour, we observed that females of P. canaliculata eat this secretion with approximately two deglutition events on average during the copula. This behaviour can be interpreted as a nuptial feeding, possibly functioning as an additional male mating effort to entice the female to remain in copula for long periods. To our best knowledge, there are no previously registered cases of nuptial feeding in gastropods.

SEQUENTIAL PATHWAYS IN THE MATING BEHAVIOR OF THE APPLE SNAIL POMACEA CANALICULATA (CAENOGASTROPODA: AMPULLARIIDAE)

Pomacea canaliculata is the most studied ampullarid in many aspects of reproductive biology, such as environmental factors triggering reproduction (Albrecht et al., 1999, 2005), functional properties of eggs (Heras et al., 2007), reproductive strategy and effort (Estebenet & Cazzaniga, 1993; Estoy et al., 2002b), and size and age at which maturity is reached (Estoy et al., 2002a; Tamburi & Martín, 2009). Surprisingly, though, the current knowledge on the details of mating behavior is scarce. Males of Pomacea canaliculata have a complex copulatory apparatus of pallial origin. It comprises a bulky and muscular penis sheath with a deep channel on its inner face, along which a slender penis runs during copula (Andrews, 1964; Gamarra-Luques et al., 2006). Knowledge on mating behavior of P. canaliculata comes mostly from non-systematic observations: matings are long lasting (up to 20 h), occur under water at any time of the day or night, and females can crawl freely but the males cannot and therefore depend on the females’ movements to reach the water surface and ventilate their lungs (Andrews, 1964; Albrecht et al., 1996; Burela & Martin, 2007). During mating, the male habitually secrets mucus from the outer gland of the penis sheath, and the female feeds on it, a phenomenon that was interpreted as a nuptial feeding (Burela & Martín, 2007). At least under laboratory conditions, both males and females show a multiple mating behavior (Albrecht et al., 1996). Several authors observed the mating behavior in other ampullarids (Guimarães, 1981; Bahl, 1928; Nono & Mane, 1931; Demian & Ibrahim, 1971; Berthold, 1989, 1991). All of the descriptions agree on the basic pattern. Matings are subaquatic, and the male’s foot adheres to the right side of the last whorl, while gripping the rim of the female’s shell with the penis sheath. MALACOLOGIA, 2009, 51(1): 157 164

Nuptial Gifts in Pomacea canaliculata (Ampullariidae, Caenogastropoda): Experimental and Field Evidence about Their Function

ABSTRACT Pomacea canaliculata is a South American apple snail that shows a multiple mating behavior. The copulations are frequent and long lasting, and consequently the males have to face strong sperm competition. The outer gland at the base of the penis sheath secrets drops of mucus that females eat during copulation. These mucus drops are nuptial gifts, and the occurrence of them is the only known instance of this behavior in molluscs. We investigated three possible functions of the gift-giving behavior in P. canaliculata based on three hypotheses: prowler deterrence, male mating effort and paternal investment. We also quantified the frequency of nuptial gifts in two populations of P. canaliculata and its possible role in male competition. We found no aversive reaction neither in females nor in males, but females were attracted to the mucus secretion. The consumption of artificial nuptial gifts (homogenates of the outer sheath gland) had no effect on the copulation duration nor on the total number of eggs and egg masses laid by females. In the field, the frequency of nuptial gifts was almost ten times greater in the population with the highest density of snails, indicating a much higher rate of production of nuptial gifts. The proportion of couples with both nuptial gifts and a prowler males attached was significantly higher than expected by chance in the population with the highest population density. Even though our results give no support for the three hypothesized functions for the nuptial gifts in P. canaliculata, this study revealed a possible different role in male competition: the enticement of the female to remain in copulation when the other males are trying to gain access.

First description of egg masses, oviposition and copulation of a neglected apple snail endemic to the Iguazú and Alto Paraná Rivers

ABSTRACT The Ampullariidae have attracted persistent scientific interest, although this has been mostly concentrated on a few invasive species. Pomacea americanista (Von Ihering, 1919) new combination is a neglected species as there has been no published information about its anatomy and natural history since its description in 1919. Our aim was to describe its egg masses, oviposition and copulation to compare them with those of other Ampullariidae. We made observations on egg masses in the Iguazú River and tributaries and on snails reared in the laboratory. Pomacea americanista exhibited the same reproductive mode as other Pomacea species: aerial egg masses composed of hundreds (mean 186.12) of eggs with calcareous shells (mean 3.1 mm in diameter) that are deposited on emergent substrates, mostly rocks. The egg masses were a characteristic pale pink that distinguishes them from those of other species of Pomacea. Embryonic development took nearly 17 days at 26 °C. Hatchlings had a smooth shell with 1⅛ whorls (mean 2.6 mm in diameter) and began to breathe air and feed within a few hours. Copulation was subaquatic and long lasting (mean 16.13 h) and both sexes were highly promiscuous. The evidence gathered supports the hypothesis that P. americanista belongs to the genus Pomacea. http://zoobank.org/urn:lsid:zoobank.org:pub:6484308C-3128-4013-ACCA-A274176958DE

Life Table and Demographic Parameters of the Neotropical Apple Snail Asolene platae (Caenogastropoda, Ampullariidae)

Abstract: Apple snails are regarded as invasive or potentially problematic species but some species may be under threat. Life tables are a useful tool to understand the growth potential of freshwater snail populations. Our aim was to estimate the demographic parameters of the Neotropical apple snail Asolene platae (Maton, 1811) to allow a quantitative comparison with invasive apple snails like Pomacea canaliculata (Lamarck, 1822). Life tables were calculated for three laboratory cohorts bred at 25 °C. Life expectancy rises abruptly up to 32–37 months after a period of high post-hatching mortality of one month. The reproductive value peaked at 15–19 months for two cohorts and at 33 months in the other one. The net reproductive rates (R0), generation times (GT) and intrinsic rates of increase (r) were as 55.86 hatchlings, 25.7 months, and 0.188 individuals per individual per month on average, respectively. Among freshwater snails there is a clear inverse relationship between r and GT while R0 has a minor positive influence. The values of GT and r for A. platae are among the highest and lowest, respectively, calculated for freshwater snails at 24–26 °C. These low values of r under optimum conditions indicate a relatively low potential of A. platae populations to increase in new habitats or to recover from disturbances.

Life cycle of Pomacea americanista, a poorly known apple snail endemic to the Iguazú and Alto Paraná Rivers, southern South America

The Ampullariidae (apple snails) are freshwater snails of tropical and subtropical regions. Recent research has concentrated on a few species that are invasive or potential biocontrol agents, but the basic life history traits of most species remain unknown. One such poorly known species is Pomacea americanista, endemic to the Alto Paraná and Iguazú Rivers in southern South America, which may be vulnerable to environmental degradation. We studied the growth, survivorship, maturation and reproductive activity of P. americanista to help evaluate its resilience under different scenarios of environmental change. Fifty snails that hatched in the laboratory from two egg masses collected in San Francisco Stream (Misiones Province, Argentina) were reared under controlled conditions until their natural death. Shell growth was almost linear up to the 20th week of life, subsequently decreasing smoothly. Growth rate, asymptotic sizes, time to reach asymptotic size and age at maturity were greater for females than males. Mortality patterns were similar for both sexes, with no deaths up to 38 weeks and steady mortality thereafter, the maximum longevity being 143 weeks. The fecundity of P. americanista is lower than that of other apple snails under similar conditions. Under laboratory conditions males and females underwent a single extended reproductive period, but under the seasonal climate in their natural habitats their life cycle would probably extend for more than 3 years, with two or more reproductive periods. The low fecundity and the late maturity of P. americanista indicate slow population growth and low resilience relative to invasive apple snails. These traits, combined with a restricted geographical range and an association with hard substrates in swiftly flowing waters, suggest that P. americanista could be vulnerable.

First record of colour polymorphism in the Neotropical apple snail Asolene platae: inheritance mechanism and evidence for multiple paternity

ABSTRACT Asolene platae (Ampullariidae) is a dioecious freshwater snail with subaquatic gelatinous egg masses that dwells in the Río de la Plata basin (Argentina). The aim of this study was to describe the inheritance mechanism of the colour variations of the shell and soft parts of this snail, and to study their potential use as a genetic marker. The wild-type phenotype presents dark pigments in the soft parts and in shell bands, whereas the yellow phenotype lacks dark pigments in the soft parts and also most dark bands in the shell, except for a subsutural and a periumbilical band. The data showed that the lack of pigments in A. platae is a recessive homozygotic condition with a simple Mendelian inheritance mechanism. Females of the wild-type phenotype had a higher number of bands than the males. The pigment of the bands of both phenotypes is located in the calcareous matrix of the shell. Using the lack of pigments as a genetic marker we demonstrated the existence of biparental egg masses in A. platae, hitherto known in only one species within the Ampullariidae.

The influence of energy, nutritional value and noxiousness of prey in sex- and size-biased predation by Snail Kites in southern South America

ABSTRACT Snail Kites (Rostrhamus sociabilis) feed almost exclusively on Apple Snails (Pomacea spp.). While field observations indicate they discard the noxious albumen gland (AG) when feeding on female snails, there is no information on the energy lost by this behaviour, the gland composition, or whether there are associated snail sex preferences. We addressed, for the first time, these aspects for Snail Kites foraging on Pomacea canaliculata in southern South America. The whole snail’s biochemical composition exhibited significant differences between sexes. Proteins and carbohydrates were the major energy-providing components. Soft parts provide ~2.91 ± 0.16 and 2.50 ± 0.14 Kcal g−1 dry weight (dw) for male and female without the AG, respectively, while the AG accounts for 15% of available energy. The size and sex of prey consumed, determined at foraging perches sampled monthly, showed that Snail Kites preferentially fed on the largest snails available throughout the sampling period. Even though the remains of the female body without the AG have less energy than males, sex preferential predation towards females was observed. Our study demonstrates, for the first time, the optimal foraging trade-off between prey size/sex and nutrition/energy in Snail Kites. After discarding the AG, male and female snails of equivalent size provide different nutrients and energy, though Snail Kite foraging is generally biased towards females mostly as a result of their larger size, suggesting that Snail Kites are unable to distinguish between the sexes.