Pablo R. Martín

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.

Effects of food availability on reproductive output, offspring quality and reproductive efficiency in the apple snail Pomacea canaliculata

Phenotypic plasticity in life history traits favors the establishment of invaders and may magnify their ecological impacts. Pomacea canaliculata, the only freshwater snail listed among the 100 worst invaders worldwide, is able to complete its life cycle within a wide range of conditions, a capacity attributed to its life history plasticity. Using snails from their native range in Argentina we investigated the changes in fecundity, egg mass traits, offspring quality, and efficiency of food conversion into eggs in response to different levels of food availability throughout different life stages. Pre-maturity mortality was not affected by chronic reductions of up to 80% in food availability. Females fed ad libitum demonstrated no significant reproductive output differences when mated with males raised at different food availability levels. For females, the number and total weight of eggs and the size of egg masses decreased at high levels of food deprivation. Their efficiency of conversion into eggs of the food ingested during the reproductive period increased with deprivation, as did the survival time of their offspring. In contrast, the egg mass laying rate and the individual egg weight did not differ under different food availability regimes. Reductions in food availability have been suggested as a control method but our results indicate that fecundity would be lessened only at deprivation levels higher than 50% and would be partially compensated by an increase in hatchling survival.

Feeding Rates and Food Conversion Efficiencies in the Apple Snail Pomacea canaliculata (Caenogastropoda: Ampullariidae)

ABSTRACT Pomacea canaliculata is the only freshwater snail listed as one of the 100 worst invaders worldwide. Recent studies have demonstrated that small Pomacea snails have higher foraging and competitive abilities than larger snails and hence that ecological and agricultural damage of this invasive snail may be size-dependent. Furthermore, females of P. canaliculata usually reach larger sizes than males, a pattern that results from higher growth rates and not from higher survivorship in females; however, the proximal causes of the sexual dimorphic growth rates are unknown. In this study, we investigate the ingestion rates and growth efficiencies of P. canaliculata in order to explain the ontogenetic and sexual differences in growth and food consumption patterns. Two experiments were performed to study specific ingestion rates and the efficiency in food conversion to body mass at different feeding conditions. Ontogenetic and sexual differences were found in the specific ingestion rates. These decreased inversely with shell length and were higher for females than for males of comparable size. Conversion efficiencies decreased with age in both sexes, in males noticeably earlier than in females. Under high food availability conditions, the decrease is sharper than under low food availability. However, the effect of food availability almost disappeared when in the effect of size was removed. The sexual dimorphism of growth efficiencies and ingestion rates explain why females tend to reach a larger adult size than males, a pattern probably explained by development of the testicle and correlated reduction of mid-gut gland size. Our results on ontogenetic patterns of ingestion rates support predictions that during the reproductive season small snails may cause a great part of the damage to aquatic crops and natural wetlands.

Influence of Temperature, Size and Sex on Aerial Respiration of Pomacea canaliculata (Gastropoda: Ampullariidae) from Southern Pampas, Argentina

Pomacea canaliculata (Lamarck 1822) is a freshwater snail belonging to the family Ampullariidae, whose natural distribution comprises most of the Plata river Basin and extends southwards to Tandilia and Ventania mountains in southern Pampas, Buenos Aires Province, Argentina (Martin et al., 2001). International concern about this voracious macrophytophagous snail rose when it, and other related species, became established as a serious pest of aquatic crops, including rice and taro, in South and East Asia (Cowie et al., 2006). In addition, the role of invading ampullariids as promoters of ecosystemic changes in invaded natural wetlands has been recently highlighted (Carlsson et al., 2004). Nowadays, P. canaliculata is listed among the top 100 worst invasive alien species of the world (Lowe et al., 2000), being the only freshwater snail included and probably the species with the greater potential for spread in North America (Rawlings et al., 2007). Ampullariids or apple snails have both a welldeveloped gill and a pulmonary sac or lung, and are commonly considered as “amphibious” snails (Andrews, 1965; Berthold, 1991). Water

Shell shape variation in the Nassariid Buccinanops globulosus in northern Patagonia

Morphological variation among natural populations is a phenomenon commonly observed in marine invertebrates and well studied, particularly, in shelled gastropods. The nassariid Buccinanops globulosus is interesting to study shell shape variation because it exhibits strong interpopulation differences in life history features, including maximum size, fecundity and growth rate. In this study, we examined the pattern of variation in size and shell shape among populations and between sexes of B. globulosus (Bahía San Antonio 40°29′S 63°01′W, Playa Villarino 40°45′S 64°40′W and Bahía Nueva 42°46′S 65°02′W). In particular, we used geometric morphometric techniques to test: (1) whether the two components of shell morphology (size and shape) are independent and (2) whether shape differences between sexes are consistently found among populations, regardless of their body sizes. Our results show shell shape variation between the populations of B. globulosus of northern Patagonia. Intra-specific shell shape variation is affected by body size, indicating allometry. Regardless of the size differences, individuals from Playa Villarino have high-spired shells, and shorter apertures and wider columellar area than individuals from the other populations. Also, sex-related shape differences were consistently found at each population, thus suggesting a common sexual dimorphism in shell morphology for this species. The functional significance of the variability found is discussed in terms of the flexibility of developmental programmes for morphology as well as the evolution of phenotypic plasticity.

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.

THRESHOLD TEMPERATURES AND DEGREE-DAY ESTIMATES FOR EMBRYONIC DEVELOPMENT OF THE INVASIVE APPLE SNAIL POMACEA CANALICULATA (CAENOGASTROPODA: AMPULLARIIDAE)

ABSTRACT Pomacea canaliculate is a freshwater snail native to subtropical-temperate South America that has invaded several countries around the world. Temperature is probably one of the main limitations to the expansion of this and other apple snails to higher latitudes in invaded regions. Egg masses are aerial, and the duration of embryonic development varies greatly with air temperature. We compared different methods for determining the lower temperature thresholds and the cumulative degree-days (DD) required for the completion of the embryonic development of P. canaliculate. The lower temperature threshold was estimated with four methods: the least standard deviation from the mean of degree-days, the least standard deviation from the mean of days, the coefficient of variation in days and the linear regression coefficient method. The cumulative degree-days were estimated using hourly records and daily averages (calculated according to the single triangle and the single sine methods) of air temperature. The lower temperature thresholds ranged between 15.8°C and 18.3°C and the cumulative DD between 88.8°C.d and 133.8°C.d. The estimations obtained with the single triangle and the single sine methods were exactly the same. The values obtained with the method of the least standard deviation in degree-days and the corresponding cumulative DD were the poorest estimations. The estimates obtained with daily mean temperatures were close to those obtained with hourly records, indicating that recording only maximum and minimum temperatures should be sufficient. The use of degree-day models for egg development in Pomacea will serve to increase the effectiveness and efficacy of control measures targeted to egg masses through a better timing in their application, especially in localities with highly variable temperatures.

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

Mating behavior, egg laying, and embryonic development in the South American apple snail Asolene pulchella (Ampullariidae, Caenogastropoda)

Asolene pulchella is a dioecious freshwater snail from the La Plata basin, belonging to the Ampullariidae family. Our aim was to study the reproductive biology, including mating behavior, egg laying, and embryonic development under laboratory conditions. Copulations occurred underwater and lasted 2.66 h on average. The males produce fusiform paraspermatic cells (with seven to nine flagella) in addition to euspermatic cells with a corkscrew head, straight middle piece and long flagellum. Females stored sperm for up to 169 days. The egg masses (containing 98.1 eggs on average) are deposited underwater and are composed of many gelatinous packs of 1–4 eggs; the jelly matrix presented numerous calcite microcrystals. The spheroidal egg capsules measured 2.25 mm and contained a yellowish perivitellus of rubbery consistence. The embryonic development extends for 10.8 days on average. Hatchlings measured 1.4 mm and remained on the egg mass, feeding on the jelly. They resemble miniature adults but only began to feed on senescent plant material in their third week of age and begin aerial lung respiration after 8–10 weeks. The details of the structure of the egg masses and development constitute a rich source of traits for comparative and taxonomic studies in the Ampullariidae.

Age, growth and mortality in Buccinanops globulosus (Gastropoda: Nassariidae) from Golfo Nuevo (Argentina)

Abstract Buccinanops globulosus is a commercially exploited gastropod common in coastal waters of the Southwestern Atlantic Ocean. We determined the age and estimated growth and mortality rates of B. globulosus in a population from Golfo Nuevo (Patagonia, Argentina). Age was determined by counting opercular rings and growth was described by the von Bertalanffy function fitted to data of length-at-age. Mortality rate (Z) was estimated by the linearized catch curve method. The maximum age was determined at 8 years. Growth parameters estimated for the whole population were TSL ∞ =37.87 mm, k=0.33 year−1 and t 0=−0.65 year. Likelihood ratio tests indicated significant differences in asymptotic length and fitted growth models between sexes. Annual mortality rate (the first reported for the species) was estimated to be 0.34 year−1 (0.49–0.20). Information on growth parameters of B. globulosus showed that TSL ∞ and the index of overall growth performance of the population studied here were intermediate compared to previously studied populations, thus indicating site-specific growth differences. Taking into account that the most common management strategy in gastropod fisheries is the use of a minimum size limit (MSL), we suggest that fishery measurements such as MSL for this species should be established only for small geographical scales.