Induced chemical defenses in a freshwater macrophyte suppress herbivore fitness and the growth of associated microbes

Abstract

The freshwater macrophyte Cabomba caroliniana induces a chemical defense when attacked by either the crayWsh Procambrus clarkii or the snail Pomacea canaliculata. Induction by either consumer lowers the palatability of the plant to both consumers. When oVered 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 eVect (reduced feeding), a physiological eVect of the induced metabolites on the consumer, or both. To assess these possibilities, we made artiWcial 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 signiWcantly 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-signiWcant, trend. Thus, snails may reduce feeding on induced plants to avoid suppression of Wtness. 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 Wve potential pathogens. Thus, induced plant defenses can act against both direct consumers and microbes that might invade the plant indirectly through herbivore-generated wounds.

Are lower‐latitude plants better defended? Palatability of freshwater macrophytes

“…5 Pomacea paludosa is restricted to southern Florida (Morrison and Hay 2011). Herbivores included the omnivorous crayfishes Procambarus spiculifer, Procambarus clarkii, and Orconectes rusticus and the herbivorous apple snail Pomacea paludosa.…”

“…Just 20 years ago, it was common for researchers to assume that freshwater herbivores had no impact on freshwater plants (see discussion in Lodge 1991). As one example of the state of our understanding, there are hundreds of terrestrial and marine plants documented to produce chemical defenses against herbivores, but only 22 freshwater macrophytes are known to chemically deter herbivores (Morrison and Hay 2011). As one example of the state of our understanding, there are hundreds of terrestrial and marine plants documented to produce chemical defenses against herbivores, but only 22 freshwater macrophytes are known to chemically deter herbivores (Morrison and Hay 2011).…”

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

“…Pomacea canaliculata will use both fresh and decaying macrophyte leaves as long as they contain adequate levels of nutrients and low levels of phenolics (Qiu et al, 2011). Ampullariid grazing can also induce the production of unidentified defense chemicals (Morrison & Hay, 2011b).…”

Induced responses to grazing by an insect herbivore (Acentria ephemerella) in an immature macrophyte (Myriophyllum spicatum): an isotopic study

“…), detailed comparisons between induced resistance mechanisms described in freshwater plants are limited. This is because generalizations about herbivory in aquatic systems have to be based on relatively few data (e.g., Morrison and Hay ; Fornoff and Gross). Thus, far, induced defense has been reported in two recent studies of marine angiosperms (Steele and Valentine ; Darnell and Heck ) and in a limited number of earlier studies of freshwater angiosperms (Jeffries ; Bolser et al.…”

“…Finally, while patterns of constitutive chemical resistance in aquatic ecosystems have been well studied (e.g., Prusak et al 2005;Agrawal and Fishbein 2006;Erhard et al 2007), detailed comparisons between induced resistance mechanisms described in freshwater plants are limited. This is because generalizations about herbivory in aquatic systems have to be based on relatively few data (e.g., Morrison and Hay 2011;Fornoff and Gross2014). Thus, far, induced defense has been reported in two recent studies of marine angiosperms (Steele and Valentine 2012;Darnell and Heck 2013) and in a limited number of earlier studies of freshwater angiosperms (Jeffries 1990;Bolser et al 1998;Lemoine et al 2009;Morrison and Hay 2011;Fornoff and Gross 2014).…”