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Egg Cannibalism in Pomacea canaliculata (Caenogastropoda: Ampullariidae) from the Southern Pampas: An Alternative Trophic Strategy?
Abstract
Pomacea canaliculata is a freshwater gastropod native to southern South America and is listed among the world's 100 worst invaders. Diverse food sources can be exploited by this apple snail, including snails with gelatinous and subaquatic egg masses. Records of ingestion of their own egg masses (egg cannibalism), which are aerial and calcareous, have only been anecdotal in P. canaliculata. Our aims were to study egg cannibalism in a natural population and also under laboratory conditions. In a stream population from the southern Pampas, we recorded P. canaliculata attacking their own fresh egg masses, which had been naturally submerged by an increase in water level. In addition, when we artificially submerged fresh and old egg masses in a field experiment, we observed several snails readily attacking both. In the laboratory, we also observed the capture by pedal surface collecting of floating remains of egg masses. In laboratory trials, juveniles fed on eggs reached larger sizes than starved snails but smaller than those fed on lettuce; adult snails also eat eggs, but their growth rates were not affected by the food regime. Pomacea canaliculata eggs present defensive and anti-nutritive compounds that apparently dissuade almost all potential predators, but this snail did not appear to be negatively affected when feeds on its own eggs. The ingestion of egg remains and submerged egg masses is probably more frequent than previously considered in P. canaliculata, which may take advantage of using these alternative food resources when others are scarce.
... In addition, P. canaliculata feeds on recently dead small fish (Alonso and Ageitos de Castellanos 1949), bryozoans (Wood et al. 2006) and on the adults, juveniles and eggs of other snails (Cazzaniga and Estebenet 1984;Kwong et al. 2009). Karraker and Dudgeon (2014) reported P. canaliculata consumption of amphibian eggs and Saveanu and Martín (2014) found it feeding cannibalistically on its own egg masses. To date, only laboratory studies have documented the consumption of animal materials, with the exception of two field studies that found scarce invertebrate remains in P. canaliculata gut contents (Kwong et al. 2010;Ocon et al. 2013). ...
... These snails (n ¼ 10 in each food regimen) were also from El Huáscar stream. Juveniles were used because of their higher growth rates relative to adults (Saveanu and Martín 2014) and the lower measurement error in their length and weight relative to hatchlings. ...
... The ontogenetic decrease found in specific rates of carrion ingestion was similar to the pattern found for lettuce (Tamburi and Martín 2009) and the snails' own eggs (Saveanu and Martín 2014), as well as the pattern of specific capture rates of neuston and surface material by pedal surface collecting (Saveanu and Martín 2013). The regression model explained a low percentage of the variation, probably because of the low absolute amount of carrion consumed by small snails, which was almost undetectable in some cases with the scale used. ...
Trophic flexibility is a relevant trait in the potential for organisms to establish widely, maintain high abundances and spread after invasion. Pomacea canaliculata is an apple snail that feeds primarily on aquatic macrophytes, although it also consumes other trophic resources that likely play an important role in its persistence and contribute to its effects in invaded wetlands. In the present study we determined the ingestion rates in P. canaliculata for carrion and subsequent effects on growth, and performed field and laboratory experiments to investigate the mechanism of carrion detection. We observed P. canaliculata snails of all sizes feeding on carrion. The specific ingestion rates of carrion decreased with snail size and were 20 times lower than when feeding on lettuce. The growth rates of snails feeding only on carrion were 15-30% higher than those of fasting snails and 30% of those snails feeding on lettuce or lettuce and carrion. We found no evidence of distant chemoreception of carrion. The importance of carrion for P. canaliculata is mostly as an alternative resource when its preferred food is absent, and not as a complementary resource that could enhance growth. Nevertheless, the ability of P. canaliculata to profit from carrion may help explain its potential to establish widely and to have effects on aquatic vegetation.
... Aerial egg laying may have evolved to avoid the predation or cannibalism that submerged egg masses suffer (Turner, 1998;Cowie, 2002;Horn et al., 2008;Saveanu & Martín, 2014), but it incurs diverse costs. There may also be a cost of producing the calcium coating of the eggs, resulting in a trade off between production of progeny and maternal defense, inasmuch as shells of female P. canaliculata tend to be thinner than those of males (see Shell Morphology). ...
... Pomacea canaliculata has also been suggested as causing the decline of Pila species, but whether this occurred through predation or competition remains unclear (Acosta & Pullin, 1991;Halwart, 1994). Apple snails will even consume conspecific eggs (Horn et al., 2008;Tiecher et al., 2014;Saveanu & Martín, 2014), hatchlings and juveniles . ...
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.
... Deposit feeders are animals that ingest sediment in marine (López and Levinton 2011) and freshwater environments (Usseglio-Polatera et al. 2000) and benefit from its organic matter, especially biofilms with high nutritional value (Lawrence et al. 2002, Krumins et al. 2013. The South American apple snail Pomacea canaliculata (Lamarck, 1822) ingests a wide variety of trophic resources including macrophytes, their preferred food item (Hayes et al. 2015), but also carrion (Saveanu et al. 2017), detritus (López van Oosterom et al. 2016), other macroinvertebrates (Maldonado et al. 2022) and freshwater snails and their eggs (Kwong et al. 2009;Saveanu and Martín 2014;Maldonado and Martín 2018). This apple snail is able to obtain trophic resources by shredding and scraping through a combination of jaw and radula movements and also by a specialized feeding behaviour in which a funnel formed by the anterior part of the foot gather materials available on the water surface (Saveanu and Martín 2013). ...
Sediment represents both a habitat and a trophic resource for many aquatic organisms, commonly known as deposit feeders. One of the most important freshwater invaders around the world is the polyphagous and opportunistic apple snail Pomacea canaliculata, in which deposit feeding has not been reported. Our aims were to study the frequency of sediment ingestion at different seasons in four watercourses within its natural range and to evaluate, under laboratory conditions, the relevance of this trophic resource for growth and survival of hatchlings and juveniles. Sediment ingestion showed very high (80-100%) and similar frequencies in snails from different waterbodies and at different seasons. This trophic behaviour was also recorded in laboratory experiments which allowed hatchlings to survive longer and to grow faster and in the case of juveniles to maintain their live weights with a high level of activity. Sediment ingestion by P. canaliculata juveniles also reduces organic matter content in the sediment. Sediment ingestion represents an alternative feeding behaviour for this apple snail whose relevance increases when other trophic resources are absent or scarce. This may help young individuals to survive and populations to persist during food shortages, increasing the chances of invasion. The reduction by P. canaliculata of the organic matter content in the sediments could alter the biogeochemical processes occurring in them and enhances the role of this apple snail as an ecosystem engineer in aquatic environments.
... Many ampullariids are omnivorous, with a diet that includes algae, plants, detritus, zooplankton, surface films, carrion and other invertebrates (Hayes et al. 2015). This trophic versatility has probably contributed to the evolutionary success of many species in their native range, as well as some species of Pomacea and Marisa to become notorious invasive pests (Qiu and Kwong 2009;Saveanu and Martín 2014). Part of the trophic versatility of ampullariids may have been facilitated by their expanded cellulase gene family (7-12 genes), which is less common in other lophotrochozoans (0-6 genes) (supplementary table S8, Supplementary Material online), and other animal groups including arthropods (Watanabe and Tokuda 2001;Gutekunst et al. 2018). ...
Data reported in this paper have been deposited in the GenBank database: genome assemblies and reads (Bioproject No: PRJNA523959 for P. canaliculata, PRJNA523958 for P. maculata, PRJNA445755 for M. cornuarietis, and PRJNA523095 for L. nyassanus); transcriptome sequences (Bioproject PRJNA473031 and PRJNA473253). Abstract The family Ampullariidae includes both aquatic and amphibious apple snails. They are an emerging model for evolutionary studies due to the high diversity, ancient history and wide geographical distribution. Insight into drivers of ampullariid evolution is hampered, however, by the lack of genomic resources. Here we report the genomes of four ampullariids spanning the Old World (Lanistes nyassanus) and New World (Pomacea canaliculata, Pomacea maculata and Marisa cornuarietis) clades. The ampullariid genomes have conserved ancient bilaterial karyotype features and a novel Hox gene cluster rearrangement, making them valuable in comparative genomic studies. They have expanded gene families related to environmental sensing and cellulose digestion, which may have facilitated some ampullarids to become notorious invasive pests. In the amphibious Pomacea, novel acquision of an egg neurotoxin and a protein for making the calcareous eggshell may have been key adaptations enabling their transition from underwater to terrestrial egg deposition.
... Many ampullariids are omnivorous, with a diet that includes algae, plants, detritus, zooplankton, surface films, carrion and other invertebrates (Hayes et al. 2015). This trophic versatility has probably contributed to the evolutionary success of many species in their native range, as well as some species of Pomacea and Marisa to become notorious invasive pests (Qiu and Kwong 2009;Saveanu and Martín 2014). Part of the trophic versatility of ampullariids may have been facilitated by their expanded cellulase gene family (7-12 genes), which is less common in other lophotrochozoans (0-6 genes) (supplementary table S8, Supplementary Material online), and other animal groups including arthropods (Watanabe and Tokuda 2001;Gutekunst et al. 2018). ...
The family Ampullariidae includes both aquatic and amphibious apple snails. They are an emerging model for evolutionary studies due to the high diversity, ancient history and wide geographical distribution. Insight into drivers of ampullariid evolution is hampered, however, by the lack of genomic resources. Here we report the genomes of four ampullariids spanning the Old World (Lanistes nyassanus) and New World (Pomacea canaliculata, Pomacea maculata and Marisa cornuarietis) clades. The ampullariid genomes have conserved ancient bilaterial karyotype features and a novel Hox gene cluster rearrangement, making them valuable in comparative genomic studies. They have expanded gene families related to environmental sensing and cellulose digestion, which may have facilitated some ampullarids to become notorious invasive pests. In the amphibious Pomacea, novel acquision of an egg neurotoxin and a protein for making the calcareous eggshell may have been key adaptations enabling their transition from underwater to terrestrial egg deposition.
... Aerial egg deposition has evolved in several groups of animals including Vertebrata [42], Arthropoda [43] and Gastropoda [6]. Hypotheses for the transition to aerial egg deposition include escaping aquatic predators or aquatic pathogens, or hypoxia in tropical waters [44,45]. Eggs laid on land, on the other hand, are exposed to terrestrial predators as well as physical stressors such as ultraviolet radiation and desiccation [42,46]. ...
Unlike most of the freshwater gastropod families, the family Ampullariidae includes members that exhibit both underwater and aerial oviposition, making it an ideal model for understanding mechanisms underlying the evolutionary transition from water to land. We applied SDS-PAGE and LC-MS/MS to analyse the proteome of the egg perivitelline fluid (PVF) of Marisa cornuarietis – an aquatic ovipositing ampullariid. Comparison with the reported PVF proteomes of two aerial ovipositing ampullariids (Pomacea canaliculata and P. maculata) showed that the three species all contain several major perivitellins that nourish the embryos. However, M. cornuarietis invests more heavily on immune-related proteins, which might be due to exposure to aquatic pathogens. Interestingly, only the PVF of out-of-water egg laying species have PV2 – a neurotoxin lethal to mice, and a calcium-binding protein which might be involved in the formation of calcareous eggshell. Integrated phylogenetic, evolutionary and gene expressional analyses detected the involvement of gene duplication, positive selection and neofunctionalisation in the formation of several major PVF proteins. Overall, our study provides multiple lines of evidence of adaptive evolution in the PVF proteins, and contributes to a better understanding of how aquatic gastropod ancestors invaded terrestrial habitats. Significance: Aerial egg deposition has evolved in several groups of animals, but except for Vertebrata little is known about the mechanisms underlying this critical evolution process. We compared aquatic and aerial egg laying apple snails to understand the molecular mechanisms enabling such a transition in egg laying habitat. We found that the composition of perivitelline fluid proteomes of underwater and aerial egg depositors was remarkably different, and then gene duplication and positive selection were responsible for the formation of such novel proteins than enabled the evolutionary transition.
... animal and vegetal parts or individuals, liquids and biofilms). These snails also feed on their own eggs when the egg masses become submerged both in the field and in the laboratory (Saveanu & Martín, 2014). ...
Pomacea canaliculata is in many respects the best known species of apple snails (family Ampullariidae), although the available information is both fragmentary and geographically biased. Most studies in its non-native range have focused on applied aspects in managed or artificial wetlands in various countries in Southeast Asia. In its natural range the emphasis has been on basic studies of its reproductive biology, ecology and behaviour in populations from small streams at the southernmost extreme of its distribution (Southern Pampas, Argentina). The extreme geographic position and the lotic nature of these populations may have biased some conclusions about the behavioural and ecological traits of P. canaliculata; contemporary evolution and genetic exchange may also have diversified these traits in the non-native range. Even though the ecological information from native populations may not be directly applicable elsewhere, it nevertheless remains as a necessary reference to understand the full potential of adaptation and spread of P. canaliculata to new environments around the world. Surprisingly enough, comparative studies of native and non-native populations of Pomacea spp. are almost lacking. This short review focuses on the distribution, thermal biology, aerial respiration, feeding, reproduction, phenotypic plasticity and shell shape of Pomacea canaliculata in its native range in Argentina.
... may not be strongly affected by short submergences, the egg masses usually detach or disintegrate if submergence occurs when they are fresh (Pizani et al. 2005;Turner 1998;Horn et al. 2008). Moreover, 13 cannibalistic behaviour occurs when egg masses become submerged and frequently results in the loss of the whole egg mass (Horn et al. 2008;Saveanu and Martín 2014). Some egg masses are probably lost every year because of natural floods but anthropogenic interference with hydrological cycles may be increasing the loss of egg masses. ...
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
Background:
Regardless of the attention the invasive gastropod Pomacea canaliculata has received in the last decades for its negative impact on crops agriculture; knowledge of their digestive physiology remains incomplete, particularly the enzymatic breakdown of macromolecules such as proteins and lipids.
Results:
Discovery proteomics revealed aspartic peptidases, cysteine peptidases, serine peptidases, metallopeptidases, and threonine peptidases, as well acid and neutral lipases and phospholipases along the digestive tract of P. canaliculata. Peptides specific to peptidases (139) and lipases (14) were quantified by targeted mass spectrometry. Digestion begins in the mouth by diverse salivary peptidases (9 serine peptidases; 7 cysteine peptidases, 1 aspartic peptidase, and 22 metallopeptidases) and then continues in the oesophagus (crop) by 3 luminal metallopeptidases (family M12) and 6 serine peptidases (family S1). Downstream, the digestive gland provides a battery of enzymes composed of aspartic peptidase (1), cysteine peptidases (9), serine peptidases (12), and metallopeptidases (24 including aminopeptidases, carboxypeptidases and dipeptidases). The coiled gut has M1 metallopeptidases that complete the digestion of small peptides. Lipid extracellular digestion is completed by triglyceride lipases.
Conclusion:
From an integrative physiological and anatomical perspective, Pomacea canaliculata shows an unexpected abundance and diversity of peptidases, which participate mainly in extracellular digestion. Moreover, the previously unknown occurrence of luminal lipases from digestive gland are reported for the first time. Salivary and digestive glands were the main tissues involved in the synthesis and secretion of these enzymes, but the few luminally exclusive peptidases are plausibly secreted by ventrolateral pouches or epithelial unicellular glands.
The trophic ecology of the invasive apple snail Pomacea canaliculata was intensely investigated because of the impacts of its grazing on aquatic vegetation, including crops. However, this freshwater snail also gathers food from the water surface using a pedal funnel, a distinctive trophic behavior called pedal surface collecting. We investigated the diel fluctuations of this trophic behavior through four whole-day field observations in a stream. We recorded the lowest pedal funnel frequencies during light hours and the highest after sunset, a pattern similar to that of general activity. We evaluated through laboratory experiments the influence of water temperature and velocity, photoperiod and a possible endogenous rhythm on this behavior. Pedal funnels are formed within the whole temperature range in which this snail is active. The highest pedal funnel formation rates were recorded at 30 °C, but the food captured was the same regardless of temperature. Pedal funnels were not observed at water velocities above 0.12 m• s-1 but below this limit the rate and time spent in funnels remained constant with velocity. Despite the time of day, pedal funnels were scarce under constant artificial light, ruling out an endogenous rhythm. Both in the laboratory and in the stream, the highest levels of pedal funnels were observed during dark periods, probably a strategy to avoid detection by visual predators. Pedal surface collecting on floating matter could represent an additional impact of invasive apple snails on freshwater ecosystems but it could also be used for the specific delivery of molluscicides against them.
This study investigated the predation of eggs of the apple snail Pomacea dolioides in Itacoatiara, Amazonas, Brazil. Predation was compared between rural and urban areas, period of day, shaded and unshaded clutches. In addition, we evaluated clutch height and the behaviour of predators. Between April 2017 and July 2018, 962 egg clutches were observed at different times of the day: 492 in rural areas with predation of 68 egg clutches and 470 in urban areas with predation of only 9 egg clutches. Significant differences were recorded for predation rate and differences were recorded for egg clutch height in the areas. In the rural areas, the most frequent predators during the day were ants Solenopsis invicta, Crematogaster cf. carinata and the most abundant were S. invicta, Wasmannia aff. iheringi and C. cf. carinata. During the night, S. invicta was the most frequent and abundant predator. In urban areas, the frequency of predation and abundance of S. invicta were higher during the day and night than those of other predators. Populations of P. dolioides in rural areas are more affected by egg predation, mostly by S. invicta and C. cf. carinata, and predatory behaviour depended on the species of the predator.
The conservation status in the Brazilian territory of the freshwater cosmopolitan snail "Physa marmorata Guilding, 1828" it is critically analyzed as their valid inclusion in the recent “Official List of the Brazilian
Fauna Threatened Extinction” ...
The ocurrence of freshwater and amphibian molluscs in the “Santa Catarina Island”, Florianópolis, central eastern region of Santa Catarina State/ SC is available, including a total of 24 species (6 Bivalvia and 18 Gastropoda – 1 amphibian, with 2 exotic and invasive – 1 Bivalvia and 1 Gastropoda – and 6 under immediate threat of extinction – 5 Bivalvia and 1 Gastropoda) (see pp. 29-31) ...
Apple snails are known for the strong impacts they provoke in wetlands and aquatic crops by their macrophytophagous habits. Interestingly, they are able to persist after they have eradicated most palatable aquatic macrophytes in the invaded wetlands. Pedal surface collecting is a distinctive mechanism that apple snails use to capture materials in the water surface. We were interested in knowing the relevance of neuston, the organisms associated with the air–water interface, as an alternative trophic resource. Using the invasive Pomacea canaliculata as a model, our experiments with simulated trophic resources in the laboratory showed that neuston is highly consumed even in the presence of abundant palatable macrophytes. P. canaliculata was able to grow efficiently using neuston as an alternative trophic resource both under laboratory and natural conditions. Neuston probably plays a relevant role specially when other trophic resources are inedible or absent or have been depleted by apple snails. Pedal surface collecting probably evolved in apple snails as an adaptation to cope with fluctuating trophic resources.
Copulation and spawning of male-female pairs of the South American apple-snail Pomacea canaliculata were periodically observed in aquaria. Copulation occurred under water (2.9 ± 0.3 times/ week, mean ± SEM) and was more frequently recorded in the morning (45%) and afternoon (37%) than in the evening (18%). Most copulations were recorded in one or two subsequent observations, although some were recorded in up to five subsequent observations (encompassing more than 30 h); some of these long copulations were interrupted by spawning and then resumed, which suggests that some copulation may indeed be series of several copulatory episodes. Spawning occurred above water level (1.4 ± 0.1 times/week) and mostly at night (93%). The number of eggs per spawn was 101.0 ± 6.8 eggs (mean ± SEM), its mean volume was 9.9 ± 0.2 mm3, and the percentage of fertile eggs was 42.6 ± 2.7. The number of eggs produced, the mean egg volume, and the percent of fertile eggs did not differ significantly between the first and second spawn produced directly after copulation. When several spawns (up to five) were produced in succession, without intervening copulations, the number of eggs per spawn was within the normal range, but the fertility of the eggs produced varied from normal to null values. The adaptive significance of these findings in comparison with what is known in other ampullariid gastropods is discussed.
Apple snails are freshwater gastropods with highly diverse feeding mechanisms (shredding, scraping and collecting) to exploit diverse food sources. Pomacea canaliculata is listed among the worlds 100 worst invaders, mainly due to its effects on aquatic crops and submersed macrophytes through shredding, its main feeding mechanism. In one of the alternative mechanisms, the snails obtain material from the water surface through a funnel formed by the anterior part of the foot, here termed pedal surface collecting (PSC). Our aims were to study the potential trophic spectrum of PSC and the effects of snail size and sex, density of food particles and particle size on efficiency of this feeding mechanism under laboratory conditions. We also explored occurrence and daily fluctuations in the field. Pomacea canaliculata snails were able to capture different food types irrespective of their physical nature (liquid, organic particles and biofilms) and size, although not all of them could be ingested. PSC was performed only when food was available on the surface by snails from the whole size range tested (352.8 mm shell length), although it was less frequent in snails 10 mm. The amount of food captured by unit mass decreased with animal size, but is partially compensated by a corresponding increase in frequency and duration of PSC. The specific capture rate increased, and the time spent forming pedal funnels decreased, with food density, but no effects of particle size were observed. In the field, PSC was observed only occasionally during the day, but showed a marked increase after sunset, and was observed even when submerged macrophytes and associated periphyton were abundant. The wide trophic spectrum, the high and adaptable capture rates and the wide size tolerance likely allow P. canaliculata to take advantage of highly variable and unpredictable food resources present on the water surface, thereby contributing to the invasion success of the species.
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.
The freshwater macrophyte Cabomba caroliniana induces a chemical defense when attacked by either the crayfish Procambrus clarkii or the snail Pomacea canaliculata. Induction by either consumer lowers the palatability of the plant to both consumers. When offered food ad libitum, snails feeding on non-induced C. caroliniana grew 2.6-2.7 times more than those feeding on induced C. caroliniana. Because snails fed less on induced plants, this could be a behavioral effect (reduced feeding), a physiological effect of the induced metabolites on the consumer, or both. To assess these possibilities, we made artificial diets with lipid extracts of induced versus non-induced C. caroliniana and restricted control snails to consuming only as much as treatment snails consumed. Growth measured as shell diameter was significantly lower on the diet containing extract from induced, as opposed to noninduced, plants; change in snail mass was more variable and showed a similar, but non-significant, trend. Thus, snails may reduce feeding on induced plants to avoid suppression of fitness. The induced defenses also suppressed growth of co-occurring microbes that might attack the plant through herbivore-generated feeding scars. When two bacteria and three fungi isolated from C. caroliniana surfaces were cultured with the lipid extract from induced and noninduced C. caroliniana, both extracts inhibited the microbes, but the induced extract was more potent against three of the five potential pathogens. Thus, induced plant defenses can act against both direct consumers and microbes that might invade the plant indirectly through herbivore-generated wounds.
A field survey and two experimental manipulations were made to investigate the extent of predation on eggs of the apple snail Pomacea canaliculata (Lamarck) by the fire ant Solenopsis geminata (Fabricius) in the Philippines. First, when Pomacea egg masses found along levees of paddy fields were observed, more than half of them had some damage. More fire ants were observed near egg masses with higher degrees of damage. Secondly, when egg masses were experimentally placed on levees, on average 50% of the eggs were lost (removed or damaged) within two days in March and 38% were lost within three days in August. Thirdly, egg masses were placed in cups with or without water on levees; no eggs were lost when ants were successfully excluded by water. The proportion of lost eggs was highly variable among egg masses, but there was no difference between day and night. Possible use of this ant as a biocontrol agent for the apple snail is considered.
Six size classes (5-9 mm, 10-14 mm, 15-19 mm, 20-24 mm, 25-30 mm and 30-34 mm) of the ampullariid snail Pomacea bridgesi were experimentally exposed to 10-25 egg capsules of the planorbid snail Indoplanorbis exustus. With one exception, in all the trials performed with the snails of the four highest size classes, egg capsules of I. exustus were destroyed by P. bridgesi, whereas in the 5-9 mm and 10-14 mm size classes, egg capsules were destroyed in 20% and 68.96% of trials respectively. An individual of Pomacea belonging to each of the six size classes could destroy, on average, 0.28, 2.27, 2.38, 3.82, 3.75 and 3.62 egg capsules, respectively, during a period of 24 hours. Irrespective of size class, an individual could consume 0-6 (average 1.57 ± 0.08 s.e.) and damage 0-9 (average 1.14 ± 0.10 s.e.) egg capsules per 24 hours. On average there are about 20 eggs in each capsule, so an individual of P. bridgesi would be able to destroy around 60 eggs of I. exustus daily. These observations are relevant to possible biological control of Indoplanorbis. M R02002 G. Ad i ty a and S. K. Raut
Although most eggs are intensely predated, the aerial egg clutches from the aquatic snail Pomacea canaliculata have only one reported predator due to unparalleled biochemical defenses. These include two storage-proteins: ovorubin that provides a conspicuous (presumably warning) coloration and has antinutritive and antidigestive properties, and PcPV2 a neurotoxin with lethal effect on rodents. We sequenced PcPV2 and studied whether it was able to withstand the gastrointestinal environment and reach circulation of a potential predator. Capacity to resist digestion was assayed using small-angle X-ray scattering (SAXS), fluorescence spectroscopy and simulated gastrointestinal proteolysis. PcPV2 oligomer is antinutritive, withstanding proteinase digestion and displaying structural stability between pH 4.0-10.0. cDNA sequencing and protein domain search showed that its two subunits share homology with membrane attack complex/perforin (MACPF)-like toxins and tachylectin-like lectins, a previously unknown structure that resembles plant Type-2 ribosome-inactivating proteins and bacterial botulinum toxins. The protomer has therefore a novel AB toxin combination of a MACPF-like chain linked by disulfide bonds to a lectin-like chain, indicating a delivery system for the former. This was further supported by observing PcPV2 binding to glycocalix of enterocytes in vivo and in culture, and by its hemaggutinating, but not hemolytic activity, which suggested an interaction with surface oligosaccharides. PcPV2 is able to get into predator's body as evidenced in rats and mice by the presence of circulating antibodies in response to sublethal oral doses. To our knowledge, a lectin-pore-forming toxin has not been reported before, providing the first evidence of a neurotoxic lectin in animals, and a novel function for ancient and widely distributed proteins. The acquisition of this unique neurotoxic/antinutritive/storage protein may confer the eggs a survival advantage, opening new perspectives in the study of the evolution of animal defensive strategies.
Understanding factors that determine the fitness of invasive species may help us predict their spread and impact. Previous studies of the survival, growth and reproduction of Pomacea canaliculata, a freshwater apple snail native to South America now widely spread in Asia, North America and Hawaii, have emphasized the use of fresh leaves as food. We compared the consumption and growth of P. canaliculata reared on fresh and decaying leaves of three species of macrophytes with contrasting content of phenolics (general plant defence chemicals) and nutrients. We conducted 1-day consumption assays using adult snails and a 1-month survival and growth experiment using snails of various sizes. Our results showed that the consumption, survival and growth of P. canaliculata were determined by plant nutrients and phenolics, rather than plant freshness. For Murdannia nudiflora, a species with low phenolic content, fresh leaves with high nitrogen content were more palatable and valuable for growth than decaying leaves
Experimental and field studies suggest that freshwater snail species have negative effects on each other's population growth rates. Because snails share similar diets, these interactions have been interpreted as the result of exploitative competition, but they could also result from intraguild predation. Here we present three experiments aimed at testing the hypothesis that interspecific interactions among three species of freshwater gastropod (Helisoma trivolvis, Physa acuta and Stagnicola elodes) are mediated by intraguild egg predation. Foraging trials, conducted in a laboratory, showed that some snails readily prey on eggs, but the extent of egg predation depended on both the identity of the snail predator and the identity of the egg mass. Of the three species considered, Stagnicola had the largest effect on egg mortality and Physa had no effect on egg mortality. Foraging trials also showed that the eggs of Physa were the most vulnerable to predators and that the eggs of Stagnicola were largely invulnerable. A study conducted in large outdoor mesocosms assessed the occurrence of egg mortality in an environment of more extensive spatial scale and complexity. The results largely mirrored those of the laboratory study, with Stagnicola being the most voracious predator and the eggs of Physa being most vulnerable to predation. The reproductive success of Physa and Stagnicola raised in sympatry and allopatry was assessed in a mesocosm study conducted over three months. Recruitment of both species was depressed in sympatry, but patterns of growth in the survivors suggest contrasting mechanisms of suppression: Physa suppressed Stagnicola via exploitative competition, but Stagnicola suppressed Physa via egg predation. These experiments support the hypothesis that freshwater snail assemblages are structured by strong interspecific interactions and that a rich interplay of egg predation and interspecific competition underlie interactions among the members of this guild.
Laboratory feeding observations confirm that the golden apple snail (Pomacea canaliculata Lamarck, 1822) is a voracious predator of phylactolaemate bryozoans. An invasive species in Southeast Asia 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 snails (Pila spp.) do not graze on bryozoans; nor does the large indigenous Cipangopaludina chinensis.
The golden apple snail (Pomacea maculata Perry) is an invasive species that lays its eggs out of water but is otherwise aquatic. To investigate this behavior and
potential management techniques, we conducted experiments to examine the physical effects of immersion and underwater egg
predation on hatching success. Predation on submerged eggs by P. maculata adults reduced hatching success by ∼99%. In predator-free conditions, hatching success was reduced 75% by immersion in water
and was negatively correlated with time submerged. Our results suggest that both underwater egg predation and low immersion
tolerance may be exploited to limit the spread of P. maculata.
The United States hosts one native and five non-native species of aquatic apple snails (Ampullariidae). All are currently
found in or around the Everglades in Florida. Two of these introduced species have devastated wetlands in Southeast Asia,
but little is known about how they may impact the Everglades. To evaluate potential impacts of introduced apple snails relative
to the native species, we investigated plant species preference, consumption rates, growth rates, and growth efficiencies
in five introduced and the single native species across eight native macrophytes common in the Everglades. Three of the non-native
snails are invasive, one has shown no tendency to expand, and one appears to have minimal direct impact on macrophytes due
to its diet. All snails exhibited similar feeding preferences, with Utricularia sp. being the most preferred, Bacopa caroliniana, Sagittaria latifolia, and Nymphaea odorata being of intermediate preference, and Eleocharis cellulosa, Pontederia cordata, Panicum hemitomon and Typha sp. being least preferred (avoided as foods). Consumption and growth was minimal for P. diffusa on all macrophytes. On Utricularia sp. and Bacopa caroliniana, the invasive species Pomacea insularum and P. canaliculata tended to eat more, grow more, and have higher conversion efficiencies than the native P. paludosa or the non-invasive P. haustrum. These contrasts were more often significant for P. insularum than for P. canaliculata. The greater rates of expansion by the invasive species may derive from their enhanced feeding and growth rates.
KeywordsAquatic–Consumption rates–Exotic species–Macrophyte–Food choice
While many invertebrates sequester toxic compounds to endow eggs with chemical defences, here we show, for the first time to our knowledge, the identification of a neurotoxin of proteinaceous nature localized inside an egg. Egg extracts from the freshwater apple snail Pomacea canaliculata displayed a neurotoxic effect in mice upon intraperitoneal injection (i.p.) (LD50, 96h 2.3mg/kg). Egg protein and total lipids were analysed separately and the only fraction displaying a highly toxic effect (LD50, 96h 0.25mg/kg, i.p.) was further purified to homogeneity as an oligomeric glyco-lipoprotein of 400kDa and two subunits biochemically and immunologically indistinguishable from the previously described perivitellin PV2. The neurotoxin was heat sensitive and there was evidence of circulating antibody response to sublethal i.p. doses on mice. Clinical signs, histopathological and immunocytochemical studies revealed damage mostly in mice spinal cord. Experiments showed chromatolysis and a decreased response to calbindin D-28K associated with a significant increase of TUNEL-positive cells in the dorsal horn neurons. These results suggest that calcium buffering and apoptosis may play a role in the neurological disorders induced by the toxin in mammalian central nervous system. This is the first report of a mollusc neurotoxin genetically encoded outside the cone-snail species.
Fieldwork has thoroughly established that most eggs are intensely predated. Among the few exceptions are the aerial egg clutches from the aquatic snail Pomacea canaliculata which have virtually no predators. Its defenses are advertised by the pigmented ovorubin perivitellin providing a conspicuous reddish coloration. The nature of the defense however, was not clear, except for a screening for defenses that identified a neurotoxic perivitellin with lethal effect on rodents. Ovorubin is a proteinase inhibitor (PI) whose role to protect against pathogens was taken for granted, according to the prevailing assumption. Through biochemical, biophysical and feeding experiments we studied the proteinase inhibitor function of ovorubin in egg defenses.
Mass spectrometry sequencing indicated ovorubin belongs to the Kunitz-type serine proteinase inhibitor family. It specifically binds trypsin as determined by small angle X-ray scattering (SAXS) and cross-linking studies but, in contrast to the classical assumption, it does not prevent bacterial growth. Ovorubin was found extremely resistant to in vitro gastrointestinal proteolysis. Moreover feeding studies showed that ovorubin ingestion diminishes growth rate in rats indicating that this highly stable PI is capable of surviving passage through the gastrointestinal tract in a biologically active form.
To our knowledge, this is the first direct evidence of the interaction of an egg PI with a digestive protease of potential predators, limiting predator's ability to digest egg nutrients. This role has not been reported in the animal kingdom but it is similar to plant defenses against herbivory. Further, this would be the only defense model with no trade-offs between conspicuousness and noxiousness by encoding into the same molecule both the aposematic warning signal and an antinutritive/antidigestive defense. These defenses, combined with a neurotoxin and probably unpalatable factors would explain the near absence of predators, opening new perspectives in the study of the evolution and ecology of egg defensive strategies.
The freshwater macrophyte Cabomba caroliniana induces a chemical defense when attacked by either the crayfish Procambrus clarkii or the snail Pomacea canaliculata. Induction by either consumer lowers the palatability of the plant to both consumers. When offered food ad libitum, snails feeding on non-induced C. caroliniana grew 2.6-2.7 times more than those feeding on induced C. caroliniana. Because snails fed less on induced plants, this could be a behavioral effect (reduced feeding), a physiological effect of the induced metabolites on the consumer, or both. To assess these possibilities, we made artificial diets with lipid extracts of induced versus non-induced C. caroliniana and restricted control snails to consuming only as much as treatment snails consumed. Growth measured as shell diameter was significantly lower on the diet containing extract from induced, as opposed to non-induced, plants; change in snail mass was more variable and showed a similar, but non-significant, trend. Thus, snails may reduce feeding on induced plants to avoid suppression of fitness. The induced defenses also suppressed growth of co-occurring microbes that might attack the plant through herbivore-generated feeding scars. When two bacteria and three fungi isolated from C. caroliniana surfaces were cultured with the lipid extract from induced and non-induced C. caroliniana, both extracts inhibited the microbes, but the induced extract was more potent against three of the five potential pathogens. Thus, induced plant defenses can act against both direct consumers and microbes that might invade the plant indirectly through herbivore-generated wounds.
Several species of Ampullariidae have been suggested as agents for the the control of planorbid snails. Their destructive effect on schistosome-bearing gastropods has been attributed to competition for food, devouring egg clutches, and direct predation on young snails (Ferguson, 1978; Pointier et al., 1988). Demain and Lutfy (1965a,b) experimentally investigated the predatory activity of Marisa cornuarietis on Bulinus truncatus and Biomphalaria alexandrina. They stated that, while the wide aperture of the Bulinus shell enables Marisa to introduce its proboscis and consume the prey's soft parts, adult Biomphalaria escape from the attacks by withdrawing deeply into their shells, so becoming inaccessible because of the narrowness of the shell's opening. Some preliminary observations on breeding aquaria showed us that the Argentine applesnail, Pomacea canaliculata, is able not only to swallow the eggs and young of Biomphalaria peregrina but also to destroy adults, suggesting that the 'withdrawing-into-shell strategy' is, to some extent, ineffective against the attack of this ampullariid. The aim of this note is to describe the damage to the Biomphalaria shells; and some preliminary experiments on the predation of the apple-snail on adult planorbids are described. The P. canaliculata used were 38.4-55.4 mm long. The planorbid snails were 9.0-13.0 mm at their greatest diameter; that is, they were full-sized snails (Paraense, 1966). The observations were made on 30 1 breeding aquaria with mixed populations, with some preliminary observations on 3 1 aquaria containing one Pomacea and five Biomphalaria each. Crushed Biomphalaria were also dropped into every aquarium to test the reaction of the predators to easily-attainable planorbid flesh. Control aquaria, with only Biomphalaria, were also maintained.
Since the mid 1990s populations of non-native apple snails (Ampullariidae) have been discovered with increasing frequency in the continental United States. Given the dramatic effects that introduced apple snails have had on both natural habitats and agricultural areas in Southeast Asia, their introduction to the mainland U.S. is cause for concern. We combine phylogenetic analyses of mtDNA sequences with examination of introduced populations and museum collections to clarify the identities, introduced distributions, geographical origins, and introduction histories of apple snails.
Based on sampling to date, we conclude there are five species of non-native apple snails in the continental U.S. Most significantly, we recognize three species within what has been called the channeled apple snail: Pomacea canaliculata (California and Arizona), Pomacea insularum, (Florida, Texas, and Georgia) and Pomacea haustrum (Florida). The first established populations of P. haustrum were discovered in the late 1970s in Palm Beach County Florida, and have not spread appreciably in 30 years. In contrast, populations of P. insularum were established in Texas by 1989, in Florida by the mid to late 1990s, and in Georgia by 2005, and this species continues to spread rapidly. Most introduced P. insularum haplotypes are a close match to haplotypes from the Río Uruguay near Buenos Aires, indicating cold tolerance, with the potential to spread from Florida, Georgia, and Texas through Louisiana, Alabama, Mississippi, and South Carolina. Pomacea canaliculata populations were first discovered in California in 1997. Haplotypes of introduced P. canaliculata match native-range haplotypes from near Buenos Aires, Argentina, also indicating cold tolerance and the potential to establish farther north.
The term "channeled apple snail" is descriptive of a morphology found in many apple snail species. It does not identify a single species or a monophyletic group. Clarifying species identifications permits a more accurate assessment of introduction histories and distributions, and provides a very different picture of the tempo and pattern of invasions than was inferred when the three species with channeled sutures were considered one. Matching introduced and native-range haplotypes suggests the potential for range expansion, with implications for native aquatic ecosystems and species, agriculture, and human health.
This 19-chapter book discusses the biology (including reproduction, life history, feeding preferences and sexual behaviour) of molluscs as pests of horticultural, field and fodder crops, and outlines the development of appropriate mechanisms for the control of these pests (mainly biological, cultural and chemical). Two chapters review progress towards the development of chemical control strategies, one addressing the toxicology of chemicals, the other the deployment of molluscicides in baits. These chapters also highlight the statistical and biological procedures for screening and evaluating molluscicides which are not a component of the standard procedure of mollusc control. A series of chapters focus on specific crop situations, providing a synopsis of the current pest status of gastropod species or species groups.
Energy partitioning within the developing eggs and early juveniles of the gastropod Pomacea canaliculata was investigated from the time of fertilization to newly hatched snails. The forms and locations of the energy stored as well as their changes while development proceeded were studied in six stages (from morula to 3-day hatchlings). The rates of utilization of different lipid classes, protein classes, and total carbohydrates were measured for the first time in embryos and perivitelline fluid. Perivitelline fluid is the primary energy store. Its biochemical composition at stage I is represented by carbohydrates, proteins, and lipids with 34.8%, 13.0%, and 1.5% dry weight, respectively. Dry weight of eggs showed no significant increase during development, indicating there was no important mass exchange with the medium. Carbohydrates and proteins were identified as the major energy-providing components, and lipids as the minor one, contributing 142, 56, and 12 cal/100 mg egg, dry weight, respectively. The overall conversion efficiency (CE) was 32.8% (calculated as percentage of perivitellus energy transformed into embryonic tissues). Carbohydrates were the most important energy reserve supplying virtually all the catabolic demand (CE 14.6%). Protein electrophoretic profiles during embryogenesis showed three distinct phases: An accumulation period (up to stage IV); a more active accumulation and selective utilization phase (stage V), and a selective consumption and protein synthesis period (hatchlings). Structural lipids from perivitellus (phospholipids and free sterols) were selectively conserved in embryos and juveniles, whereas triacylglycerols, hydrocarbons, and esterified sterols were preferentially depleted by hatchlings. Therefore, protein and lipid reserves in P. canaliculata perivitellus provide structural precursors during embryogenesis, while they partially contribute to the energy supplied by carbohydrates. (C) 1998 Wiley-Liss, Inc.
The Argentinean apple snail Pomacea canaliculata is a recent invader in paddy fields in most Southeast Asian countries, where it has dispersed explosively since about 1980. Determinants of the natural range of P. canaliculata in its original area are poorly understood. In this study, factors affecting its distribution in the southern limit of its native area in Buenos Aires Province were investigated. Salty, alkaline, poorly vegetated aquatic environments with high desiccation risk in the western part of the study area probably act as a natural barrier for its dispersal toward the south and west. Sites inhabited by P. canaliculata are generally shallow, quiet, turbid, with low Na +/(K + + Mg ++) ratios compared to the uninhabited sites. Contrary to previous statements, P. canaliculata is frequently found in streams, where it reaches the highest densities. Most of the inhabited environments are located on the northern slope of the Tandilia and Ventania mountains, this physical barrier, and not temperature, being probably the main factor impeding the species' spread southwards in Buenos Aires Province. Pomacea canaliculata also inhabits isolated sites on the southern slopes of these mountains, where it appears to have been introduced. Its spread is slow within and among water bodies in this area. Repeated introductions, tropical climate, and integrated and flood-prone drainage systems probably account for the faster expansion of this species in southeastern Asia.
Pomacea canaliculata is a neotropical freshwater snail that has invaded many countries around the world, becoming a serious pest of rice and a menace to native snails. In southern Pampas (Argentina) from late spring to early fall females deposit aerial clutches composed of hundreds of calcareous eggs on emergent substrates. Local bodies of water frequently undergo fluctuations in water level, resulting in extensive submersion of clutches or dropping of hatchlings out of water. The effects of aerial exposure on hatchlings and of submersion on development were analyzed experimentally. The submersion of the egg masses of P. canaliculata increased the duration of development up to approximately 50% and caused a decrease of up to 32% in hatching rate. The calcareous capsule, large size, and dense packaging of eggs probably impede an adequate oxygen supply to embryos when submersed or may interfere with the hatching mechanism. The embryos were unable to develop completely and to hatch under water. Submersion frequently caused the disintegration of newly laid clutches and the premature hatching of eggs in late stages of development, resulting in hatchlings with underdeveloped bodies. Aerial exposure of hatchlings, under conditions similar to those occurring in the field in midsummer, killed 99% after only four days, irrespective of the presence or absence of moist soil. During droughts of several consecutive years recruitment could be seriously affected.
Patterns of density dependence in growth, reproduction and survival are important for predicting the population dynamics of a species. The patterns may change with environmental factors, such as the harshness of winter, but very little is known about such patterns and their mechanisms in unmanipulated natural populations of invasive animal species.
We studied the extent of density dependence in the growth, reproduction and survival of an invasive freshwater snail, P omacea canaliculata , in rice fields in Nara (cold district) and Kumamoto (warm district), Japan, over 2‐ and 1‐year periods, respectively.
In both areas, growth was negatively density dependent within the same generation, and the density of snails in the parental generation negatively affected the growth of offspring. The number of eggs per unit area was independent of adult density, suggesting eggs per adult female were few at high densities. Survival over the cold winter of 2005–2006 was independent of density in Nara. However, survival over the warm winter of 2006–2007 in both Nara and Kumamoto was negatively density dependent.
Irrespective of the various negative density‐dependent patterns, population density tended to show positive correlations with the density of the previous generation. This appears to reflect the substantial capacity of this snail to resist extremely low densities due to the various negative density‐dependent patterns rather than indicating susceptibility to extinction at low densities.
Pomacea canaliculata (Lamarck) is an invasive snail species that has become a serious pest of rice and other hydrophytes. Usually it is aquatic but likes to lay its eggs higher than the waterline. In order to seek a feasible and efficient way to control the egg hatchling of this pest, here we systematically studied the effects of water spraying and submersion on its egg hatchling rates and durations. Our results demonstrated that water spraying and submersion could dramatically decrease the hatchling rates to maximal 5.8% and increase the hatchling duration up to 26.4 days on P. canaliculata. Not only the beginning time of water treatment, but also the frequencies of the water spraying is critical to control the hatchling rate and duration of P. canaliculata. Water submersion that began in 12 h after the eggs laid and lasted at least 48 h will significantly decrease the snails’ hatchling rates and extend the hatchling time. In addition, compared to spraying, the water submersion could achieve more remarkable effects. The capsule of the snail’s egg is able to withstand the water treatment. Based on our water spraying and submersion results, it can be inferred that 0–6 h after egg being laid, egg capsule precipitates are beginning to form, and this process will complete after 12–24 h. This special breeding characteristic of P. canaliculata makes the physical control by water treatment become feasible.
Pomacea canaliculata deposit egg masses above the waterline, and the embryos fully develop inside the cleidoic eggs (Pizani et al., 2005). During development, the embryos are submersed in a perivitelline fluid providing them with structural precursors and energy supplies (Heras et al., 1998) until eggs hatch by mechanical fracture of the calcareous egg shell. It seems highly improbable that the embryos can fill the lungs except at the final stages of development when the perivitelline fluid has been totally incorporated. However, it is unknown whether lung ventilation begins just before falling from the egg mass or, alternatively, how long after the snails have fallen into the water.
Aerial respiration allows Pomacea spp. to thrive in freshwater habitats with poorly oxygenated waters and to endure dry-down conditions (Andrews, 1965; Cowie, 2002; Yusa et al., 2006). However, a number of drawbacks to the use of atmospheric oxygen has been suggested, such as limitations in distribution due to dependence on air access (Darby et al., 2002) and a higher vulnerability to specialized visual predators such as the snail kite Rostrhamus sociabilis (Vieillot, 1817) (Bennetts et al., 1994; Stevens et al., 2002). To better understand the role of aerial respiration on the ecology and behaviour of P. canaliculata, we analyzed the effect of temperature, size and sex on lung ventilation frequency and duration and number of pumping movements in this species.
1. Pomacea paludosa exhibits a variety of defenses against predation, including aposematic eggs and dropoff-burial responses to odors of turtles, odors of crushed conspecific snails, and mechanical disturbance. 2. The conspicuous pinkish-white eggs are laid out of the water and hatch after several weeks incubation. Distastefulness is strong at first but disappears by hatching time. After hatching, snails are apparently tasty food items for a great variety of predators. The brightly colored eggs of other species of Pomacea may also be aposematic, though we have direct evidence for unpalatability in only one other species, Pomacea dolioides. 3. The self-burial alarm responses to turtle odors and intraspecific juices appear identical in form but are not identical in ontogeny. Response to intraspecific juice is not present on hatching, develops gradually over the first few weeks of free existence, and continues throughout the life of the snail. Burial responses to turtle odors are present in snails prior to the normal hatching date and continue for varying lengths of time after hatching. Response to Sternotherus minor odor continues until snails are about 3 grams in weight; response to Chelydra serpentina odor continues until snails are at least 20 grams in weight. Ontogeny of response to other turtle odors has not yet been investigated, though young Pomacea paludosa have been reactive to odors of all turtles tested to date. 4. The ontogenies of response to Sternotherus minor and Chelydra serpentina odors correlate closely with the abilities of adults of these turtles to eat snails. Adult Sternotherus minor in the laboratory have been unable to eat snails much larger than about 3 grams in weight, while an adult Chelydra serpentina has eaten snails over 20 grams in weight. Snails apparently discriminate between the odors of these two turtles on the basis of qualitative rather than quantitative differences in odor, and preliminary evidence suggests that snails do not discriminate between different-sized turtles within a species. 5. Intraspecific juice is potent in producing alarm in total darkness just as in the light. Response to turtle odors is almost completely inhibited by darkness, red light, or dim incandescent light. 6. Odors of most predators other than turtles produced no response in young Pomacea paludosa. Weak, inconsistent responses were seen to alligator and crocodile odors. 7. Both intraspecific juice and odor of Sternotherus minor are stable to 5 minutes boiling, but both lose potency after varying lengths of time in water solution. 8. Threshold to intraspecific juice is about .000,000,2 grams crude snail juice per liter. Threshold to Sternotherus minor odor can best be expressed as the amount of water a turtle can make alarming in a given length of time. For a 54 gram Sternotherus minor this figure was about 1500 liters in 10 minutes. 9. Attempts to detect active release of alarm substance in snails stimulated with alarm substance failed. 10. Other species of Pomacea also have analogous (homologous?) alarm reactions. Pomacea dolioides has a response to intraspecific juice similar in its ontogeny to the response of Pomacea paludosa to intraspecific juice, but Pomacea dolioides lacks a response to odor of Sternotherus minor. Pomacea glauca has no response to intraspecific juice but responds strongly to odor of Sternotherus minor during a short period of youth. Both Pomacea glauca and Pomacea dolioides also have alarm responses to mechanical disturbance.
Under natural conditions hatchlings of the land snail Arianta arbustorum cannibalize unhatched sibling eggs. Newly hatched A. arbustorum from different populations (from a lowland forest, a subalpine forest and an alpine pasture in Switzerland) differed significantly in the frequency of cannibalistic attacks on conspecific eggs. The percentage of cannibalistic hatchlings ranged from 50·0% in a subalpine forest to 87·8% in a lowland forest. Two populations were consistent in the proportion of cannibalistic hatchlings over 3 years, while in a third population the proportion of cannibalistic hatchlings varied between years. Hatchlings from populations with a high frequency of cannibals also began to eat eggs at an earlier age. In two populations, the proportion of cannibalistic hatchlings per batch increased over the course of the season, while in a third population the proportion of cannibals per batch was constantly high. Propensity for egg cannibalism was not correlated with absolute egg size, suggesting that the amount of energy and nutrients received during embryonic development did not affect cannibalistic behaviour during the hatchling stage. Differences in the investment in single eggs could explain the inter-population variation in propensity for egg cannibalism in A. arbustorum.
Ampullariidae comprises two lineages of freshwater gastropods: one Old World and one New World. Recent molecular work confirmed the monophyly of the family and began to clarify generic relationships, but current systematics remains unsatisfactory. With more than 300 available species group names for New World taxa alone, taxonomic confusion is rampant, as illustrated by two species that have been introduced widely and are difficult to differentiate conchologically, Pomacea maculata Perry, 1810 and Pomacea canaliculata (Lamarck, 1822). Misidentification hampers efforts to manage their spread and impacts as invasives, and prevents meaningful comparative analyses of their biology. Here we clarify the taxonomy, describe the morphological and genetic distinctiveness of the two species, and re-evaluate their biogeographic ranges. They differ most clearly genetically, with no shared haplotypes and a mean genetic distance of 0.135 at cytochrome c oxidase subunit I (COI). Differences in shell morphology are most obvious in recently hatched juveniles; the number of eggs per clutch is higher in P. maculata, and the individual eggs are smaller, so P. canaliculata hatchlings are nearly twice as large as those of P. maculata. Adult shells differ primarily in the angulation of the whorl shoulder and pigmentation of the inner pallial lip, with the latter a distinctive feature of P. maculata. They also differ in reproductive anatomy, most notably in P. canaliculata having two distinctive glandular tissues in the apical penial sheath gland, and P. maculata lacking a medial sheath gland but possessing a basal sheath gland. Pomacea canaliculata is restricted to a narrower southern range, whereas P. maculata ranges extensively throughout much of South America. Ampullaria gigas Spix, 1827 and Ampullaria insularum d'Orbigny, 1835 are herein synonymized with P. maculata. Neotypes are designated for P. maculata and A. gigas, and a lectotype is designated for A. insularum. A neotype is designated for P. canaliculata.
© 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 166, 723–753.
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.
The invasive apple snail Pomacea canaliculata is known as an omnivorous species, but there are only few reports of its predation. This study examined the potential of this snail as a predator of common freshwater snails in southern China. Laboratory experiments were conducted to quantify the damage of the apple snail to both early stages (eggs and/or neonates) and adults of five species of freshwater snails (Austropeplea ollula, Biomphalaria straminea, Melanoides tuberculata, Physa acuta, Sinotaia quadrata). The apple snail caused significant mortality to all of the early stages of the five snails, as well as adults of the pulmonates A. ollula, B. straminea and P. acuta, but did not consume adults of the prosobranchs M. tuberculata and S. quadrata. Such differential survival of the prey might be explained by differences in shell hardness and structure, as the adult prosobranchs were well protected by a hard shell and an operculum, whereas the pulmonates had a relatively fragile shell and lacked an operculum. The apple snail was unable to detect its prey from a distance, but it crawled quickly, which could create opportunities for direct contact with potential prey. Apple snails may therefore influence invaded ecosystems through predation on other freshwater snails.
1. By selective grazing, invasive grazers can alter macrophyte-herbivore relationships in shallow freshwater bodies. Evaluating the palatability of macrophytes and understanding the determinants of plant palatability can help predict grazing impact. In no-choice feeding assays, we tested the palatability of 21 species of freshwater macrophytes to the invasive freshwater apple snail Pomacea canaliculata.
2. Daily feeding rate varied greatly with plant species, ranging from 1.1 to 22% of snail body mass. We assessed six plant properties and examined their correlation with feeding rate. Total nitrogen content was positively related, and C:N ratio and dry matter content (DMC) negatively related, to snail feeding rate. There was no significant correlation between snail feeding rate and plant phenolic content, but the feeding rate on Myriophyllum aquaticum (the plant with the highest phenolic content) was very low.
3. We repeated the feeding assays for 15 species that were not palatable as fresh leaves with reconstituted plant tissues formed by mixing ground up dried leaves with agar. The feeding rate still differed greatly among macrophyte species. Phragmites australis and Vallisneria natans (two species with the highest DMC) were eaten much more as reconstituted plant than as fresh leaves, indicating that structure (i.e. DMC) may be important in their defence against snail herbivory. For two plants (M. aquaticum and Alternanthera philoxeroides) that had moderate amounts of nitrogen/phosphorus but were consumed very little as fresh and reconstituted tissues, we incorporated their extracts into a palatable agar-based food. The extracts from both species greatly reduced snail feeding rate, indicating the presence of chemical defences in these two species.
4. These results indicated that feeding was affected by several plant traits. The snail favoured plants with a high nitrogen content and avoided plants with a high DMC. Only a few plants possessed chemical feeding deterrents that were effective against this snail. Given the invasive spread of P. canaliculata in Asia, ecologists and managers should consider plant palatability when selecting plants for use in wetland restoration and when predicting the impact of further invasion by this species.
Energy partitioning within the developing eggs and early juveniles of the gastropod Pomacea canaliculata was investigated from the time of fertilization to newly hatched snails. The forms and locations of the energy stored as well as their changes while development proceeded were studied in six stages (from morula to 3-day hatchlings). The rates of utilization of different lipid classes, protein classes, and total carbohydrates were measured for the first time in embryos and perivitelline fluid. Perivitelline fluid is the primary energy store. Its biochemical composition at stage I is represented by carbohydrates, proteins, and lipids with 34.8%, 13.0%, and 1.5% dry weight, respectively. Dry weight of eggs showed no significant increase during development, indicating there was no important mass exchange with the medium. Carbohydrates and proteins were identified as the major energy-providing components, and lipids as the minor one, contributing 142, 56, and 12 cal/100 mg egg, dry weight, respectively. The overall conversion efficiency (CE) was 32.8% (calculated as percentage of perivitellus energy transformed into embryonic tissues). Carbohydrates were the most important energy reserve supplying virtually all the catabolic demand (CE 14.6%). Protein electrophoretic profiles during embryogenesis showed three distinct phases: An accumulation period (up to stage IV); a more active accumulation and selective utilization phase (stage V), and a selective consumption and protein synthesis period (hatchlings). Structural lipids from perivitellus (phospholipids and free sterols) were selectively conserved in embryos and juveniles, whereas triacylglycerols, hydrocarbons, and esterified sterols were preferentially depleted by hatchlings. Therefore, protein and lipid reserves in P. canaliculata perivitellus provide structural precursors during embryogenesis, while they partially contribute to the energy supplied by carbohydrates.
1. Biological invasions have become a serious threat to ecosystems worldwide. Various factors can contribute to the success of biological invasion. We examined how different macrophyte food affected feeding and life-history traits of the invasive herbivorous snail Pomacea canaliculata, and whether differences in snail life-history traits could explain its successful infestation of agricultural and non-agricultural wetlands in Asia.
2. We tested five cultivated and five wild semi-aquatic macrophytes. Snail daily feeding rate varied substantially with plant species, ranging from 1.3% to 22% of its body mass. Snails fed with four (Amaranthus gangeticus, Apium graveolens dulce, Ipomoea aquatica and Nasturtium officinale) of the five cultivated macrophyte species exhibited high survivorship, fast growth and high fecundity. Snails fed with Colocasia esculenta, however, grew poorly, did not reproduce and eventually died.
3. Of the five wild species (Eichhornia crassipes, Ludwigia adscendens, Murdannia nudiflora, Myriophyllum aquaticum and Polygonum hydropiper), M. nudiflora supported a high snail survival, but snails had slower growth and lower fecundity than those reared on the four palatable cultivated species. Snails fed with L. adscendens grew substantially slower than those fed with M. nudiflora, and produced only a small clutch of eggs. Snails fed with E. crassipes, M. aquaticum and P. hydropiper had very low survivorship, grew very little and did not reproduce.
4. We determined six plant properties and their correlation with the feeding, growth and reproduction of the apple snails. Cultivated macrophytes in general had a higher nutritional value and lower physical and chemical defences. Phenolic content was negatively correlated with snail feeding rate, while plant nitrogen and phosphorus contents were positively correlated with snail egg production and growth, respectively.
5. These results indicate that, due to their higher nutritional value and lower chemical and physical defences, cultivated macrophytes are in general desirable for the apple snail which may partly explain its successful invasion into wet agricultural areas in Asia. This snail may also selectively graze poorly defended wild macrophytes in non-agricultural wetlands, leading to changes in floral diversity and wetland functioning. Management of this and other apple snails with similar life-history traits should thus focus on the prevention of their further spread.
The relationships between local population density and adult size, clutch size and spatial distribution of egg batches were investigated in 11 natural populations of the land snail Arianta arbustorum in a forest near Uppsala, Sweden. Shell size of adults decreased with increasing population density as did clutch size. Within populations, clutch size scaled allometrically with shell size indicating size-specific fecundity. It is hypothesized that food unpalatability caused by mucus deposition slows down juvenile growth rate in high density populations, resulting in small adults and thus reducing their fecundity in subsequent years. The influence of the distance between batches on the incidence of egg cannibalism by hatchlings was examined in a laboratory experiment. In this experiment the number of eggs cannibalized increased with decreasing distance to the batch of hatching snails. Thus, in the field, eggs of highly aggregated batches suffer a high risk of cannibalism. In the 3 populations with the highest snail density, 21–39% of all batches were deposited close to each other (nearest neighbour distance 5 cm, i.e. less than hatchlings more within 1 day). These findings indicate that egg cannibalism can act as a population regulating factor.
The invasive Neotropical snail Pomacea canaliculata is usually regarded as amphibious, although the relative significance of aerial and aquatic respiration is unknown. To investigate
the degree of dependence on aerial respiration and its influences on microdistribution, experiments were performed in the
laboratory and under seminatural and natural conditions. Restriction of aerial respiration negatively affected survivorship,
activity and feeding, its effects worsening with temperature and water fouling; females were more seriously affected than
males although the effect depended on reproductive effort. Snails were unevenly distributed relative to the access to air,
both in a stream and in an outdoor tank, being concentrated less than 2–4m from the nearest emergent substratum. Accessibility
to air would be an important trait of waterbodies prone to invasions of P. canaliculata, especially in tropical areas. The effectiveness of some control measures could be increased by focusing on areas where snails
are concentrated due to their dependence on air.
KeywordsApple snail-Water fouling-Temperature-Surfacing-Survivorship-Activity
To examine density dependence in the survival, growth, and reproduction of Pomacea canaliculata, we conducted an experiment in which snail densities were manipulated in a paddy field. We released paint-marked snails of
15–20 mm shell height into 12 enclosures (pens) of 16 m2 at one of five densities – 8, 16, 32, 64, or 128 snails per pen. The survival rate of released snails was 95% and was independent
of snail density. The snail density had a significant effect on the growth and egg production of individual snails. This density
dependence may have been caused by reduced food availability. The females at high density deposited fewer and smaller egg
masses than those at low density, and consequently produced fewer eggs. The females at densities 8 and 16 deposited more than
3000 eggs per female, while the females at density 128 oviposited only 414 eggs. The total egg production per pen was, however,
higher at higher snail density. The survival rates of juvenile snails were 21%–37% and were independent of adult density.
The juvenile density was positively correlated with the total egg production per pen and hence was higher at higher adult
density. However, the density of juveniles larger than 5 mm in shell height, i.e., juveniles that can survive an overwintering
period, was not significantly different among density treatments. These results suggest that snail density after the overwintering
period is independent of the density in the previous year. Thus, density dependence in growth and reproduction might regulate
the population of P. canaliculata in paddies.
There is little information on the egg proteins of gastropod mollusks. Here we focus on PV2, a novel neurotoxin from snail eggs, studying its size, shape, structure, and stability, using small angle X-ray scattering (SAXS), absorption and fluorescence spectroscopy, circular dichroism, electron microscopy and partial proteolysis. Results indicate that PV2 is a compact and well folded oligomer of 130x44 A. It is an octamer of four 98 kDa heterodimers composed of 67 and 31 kDa subunits. Subunits are held together by disulfide bonds. Dimers are assembled into native PV2 by non-covalent forces. The larger subunit is more susceptible to proteolysis, indicating it is less compactly folded and/or more exposed. Quenching of tryptophan fluorescence showed a single class of tryptophyl side chains occluded in hydrophobic regions. Native structure shows loss of secondary structure (alpha+beta) at 6 M urea or 60-70 degrees C; the effects on the quaternary structure suggest an unfolding without disassembling of the protein. The 3D model of PV2 presented here is the first for an egg proteinaceous neurotoxin in animals.
Algunos datos sobre alimentación de las ampularias
- A S Z J Alonso
- De Castella-Nos
ALONSO, A. S. & Z. J. AGEITOS DE CASTELLA-NOS, 1949, Algunos datos sobre alimentación
de las ampularias. Notas del Museo de La Plata,
14(Zoología, 115): 31-34, 4 láminas.
On the reproductive processes and development of Pila globosa (Swainson)
- K N Bahl
BAHL, K. N., 1928, On the reproductive processes
and development of Pila globosa (Swainson).