Ecology of chemical defenses of algae against the herbivorous snail, Littorina littorea, in the New England rocky intertidal community

Abstract

In the New England rocky intertidal community, space is dominated by two perennial plant types, brown fucoid algae (Ascophyllum nodosum and several species of Fucus) in the mid zones and the red alga Chondrus crispus in the low zones. These algae are not grazed by the predominant herbivorous snail, Littorina littorea. Here I report the first direct evidence that these algae produce chemicals which inhibit feeding by the snails. Polyphenols in Fucus vesiculosus and Ascophyllum nodosum were shown to be effective chemical defenses against the snails. Feeding experiments demonstrated that the presence in the diet of as little as 1% polyphenol (dry weight), extracted from these two algal species, caused a significant reduction in feeding by L. littorea; 10% polyphenol (dry wt.) in food media inhibited snail feeding nearly 100%. The phenol and polyphenol contents in different tissues of these two algal species and in other New England rocky intertidal algal species were monitored monthly for one year. F. vesiculosus and A. nodosum showed highest polyphenol contents (1-17% dry wt.); these levels were sufficiently high in all tissues during all months to inhibit snail feeding. The mechanism of action of plant polyphenols against herbivores is through their binding to plant proteins and other nitrogenous compounds, rendering them indigestible. Polyphenol contents were therefore examined in relation to plant nitrogen contents (using polyphenol/nitrogen ratios) to estimate the unavailability of plant nitrogen to herbivores due to polyphenol binding. Annual brown algal species such as Petalonia fascia and Scytosiphon lomentaria had significantly lower levels of phenols and polyphenols than the perennial F. vesiculosus and A. nodosum. These two species are highly preferred as food by L. littorea. C. crispus and the green alga Codium fragile also had low phenol and polyphenol levels, yet they are of low food preference to the snails. Methylene chloride extracts from C. crispus and volatile halocompounds from C. fragile inhibited snail feeding, hence these species have chemical defenses quite different from those of F. vesiculosus and A. nodosum. Factors such as physical defenses, nutritional content, and temporal and spatial escapes are also important in determining algal food preference to herbivores. The release into seawater of volatile hydrocarbons and halomethanes from benthic algae and seagrass was measured to examine the possible role of these compounds as antiherbivore compounds. Bioassays indicated that CH2I2, a compound released into seawater from C. fragile, inhibited feeding of L. littorea. CHBr3, released into seawater by many algal species, appeared to have less activity against the herbivores. This study represents one of the first examinations of plant chemical defenses against herbivores in the marine environment. The findings are discussed in relation to recent theories from terrestrial studies on the commitment of plants to chemical defense.