Abstract
BackgroundThe spread of the invasive snail Pomacea canaliculata is expanding the rat lungworm disease beyond its native range. Their toxic eggs have virtually no predators and unusual defenses including a neurotoxic lectin and a proteinase inhibitor, presumably advertised by a warning coloration. We explored the effect of egg perivitellin fluid (PVF) ingestion on the rat small intestine morphology and physiology.Methodology/Principal FindingsThrough a combination of biochemical, histochemical, histopathological, scanning electron microscopy, cell culture and feeding experiments, we analyzed intestinal morphology, growth rate, hemaglutinating activity, cytotoxicity and cell proliferation after oral administration of PVF to rats. PVF adversely affects small intestine metabolism and morphology and consequently the standard growth rate, presumably by lectin-like proteins, as suggested by PVF hemaglutinating activity and its cytotoxic effect on Caco-2 cell culture. Short-term effects of ingested PVF were studied in growing rats. PVF-supplemented diet induced the appearance of shorter and wider villi as well as fused villi. This was associated with changes in glycoconjugate expression, increased cell proliferation at crypt base, and hypertrophic mucosal growth. This resulted in a decreased absorptive surface after 3 days of treatment and a diminished rat growth rate that reverted to normal after the fourth day of treatment. Longer exposure to PVF induced a time-dependent lengthening of the small intestine while switching to a control diet restored intestine length and morphology after 4 days.Conclusions/SignificanceIngestion of PVF rapidly limits the ability of potential predators to absorb nutrients by inducing large, reversible changes in intestinal morphology and growth rate. The occurrence of toxins that affect intestinal morphology and absorption is a strategy against predation not recognized among animals before. Remarkably, this defense is rather similar to the toxic effect of plant antipredator strategies. This defense mechanism may explain the near absence of predators of apple snail eggs.
Highlights
The invasive apple snail Pomacea canaliculata (Lamarck, 1822) (Architaenioglossa, Ampullariidae) has become a serious aquatic crop pest in Asia and a vector of the rat lungworm Angiostrongylus cantonensis that causes human eosinophilic meningitis, a potentially fatal disease considered an emerging infectious disease
With the aim to further understand the role of egg defenses of a host of the lungworm disease, in the present work we studied the effect of P. canaliculata perivitellin fluid (PVF) on the small intestine of rats
Through a combination of biochemical, histopathological, cell culture and feeding experiments, we provide evidence that oral administration of apple snail PVF adversely affects rat small intestine metabolism and morphology and rat growth rate, presumably by proteins displaying lectin-like activity
Summary
The invasive apple snail Pomacea canaliculata (Lamarck, 1822) (Architaenioglossa, Ampullariidae) has become a serious aquatic crop pest in Asia and a vector of the rat lungworm Angiostrongylus cantonensis that causes human eosinophilic meningitis, a potentially fatal disease considered an emerging infectious disease. Though filled with a perivitellin fluid (PVF) containing large amounts of carbohydrates and storage proteins (called perivitellins), these toxic eggs have no predators reported in their original South American range and only one in the newly colonized habitats in SE Asia: the fire ant Solenopsis geminata (Fabricius, 1804). The presence of these egg defenses [6;8;9] would explain the behavior of the snail kite Rostrhamus sociabilis (Vieillot, 1817) and Norway rat Rattus norvegicus (Berkenhout, 1769) that invariably discard the gland that. We explored the effect of egg perivitellin fluid (PVF) ingestion on the rat small intestine morphology and physiology
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