Chemical Defense Against Different Marine Herbivores: Are Amphipods Insect Equivalents?

Abstract

The Structurally similar diterpenoid alcohols pachydictyol-A and dictyol-E are produced by the brown seaweed Dictyota dichotoma. This seaweed and several related species that also produce these compounds are known to be relatively low preference foods for tropical fishes and urchins. We evaluated the effect of various concentrations of these compounds on feeding by the three common types of herbivores that co-occur with Dictyota in coastal North Carolina. Fish (Diplodus holbrooki), sea urchins (Arbacia punctulata), and a mixed species group of gammarid amphipods were offered pieces of the palatable seaweed Gracilaria tikvahiae coated with either (1) dictyol-E or pachydictyol-A dissolved in diethyl ether or (2) diethyl ether alone. Dictyol-E significantly reduced consumption by fish and urchins at concentrations of 0.5 and 1.0% of algal dry mass, but had no effect on amphipod grazing. Pachydictyol-A significantly reduced fish grazing at the relatively high concentrations of 1.0 and 1.3% of plant dry mass; at 0.5% it tended to decrease grazing, but the effect was not significant (P = .07). Pachydictyol-A had no effect on urchin grazing and significantly increased amphipod grazing. When Pachydictyol-A was fed to fish as 1.0% of food dry mass, their growth rate was reduced by a significant 48%. In feeding preference experiments with several seaweeds, Dictyota ranks low for fish and urchins but high for amphipods. This is consistent with the hypothesis that the secondary metabolites produced by Dictyota play a major role in determining its susceptibility to herbivores. The ability of amphipods to circumvent the chemical defenses (Dictyota, and the fact that the two species of algae most readily consumed by amphipods (Codium and Dictyota) were the two species least readily consumed by fish, suggest that predation and herbivory by fishes may be major factors selecting for amphipods that can live on, and eat, seaweeds that are unpalatable to fishes. Amphipods that fed on Dictyota did not appear to sequester the Dictyota metabolites; when exposed to fish predation, Dictyota-fed amphipods were eaten as readily as amphipods that had fed on an alga with no defensive chemistry. Tubicolous amphipods and other small marine herbivores that may spend significant portions of their lives on only a few plants my be under very different evolutionary constraints than the larger, more mobile herbivores that commonly moved between many plants. Several characteristics of these smaller, less mobile, and much less studied, marine herbivores suggest that they may be ecologically similar to terrestrial insects and may play a large, but presently unappreciated, role in structuring marine plant communities.

Polygenic control of habitat preference and its possible role in sympatric population subdivision in an estuarine crustacean

“…All these substrate situations undoubtedly elicit different chemicals that the amphipods could be responding to. Hay et al (1987) have shown that gammarid amphipods will make dramatically different food choices in response to structurally very similar algal metabolic compounds.…”

Palatability of Macroalgae that Use Different Types of Chemical Defenses

“…Alternatively, Cladophora spp. were avoided by parrotfish and some surgeonfish (Paul and Hay, 1986), yet were consumed by Z. flavescens (Wylie and Paul, 1988) and the amphipod Amphithoe longimana (Hay et al, 1987a). Ulva spp.…”

“…Ulva spp. were avoided by the sea urchins Strongylocentrotus droebachiensis (Van Alstyne and Houser, 2003), P. lividus , and L. variegatus (Lowe, 1974), the spottail pinfish Diplodus holbrooki (Hay et al, 1987a), and A. longimana (Duffy and Hay, 1994). However, Ulva spp.…”

Untitled

“…We regard cyanobacterial and microalgal secondary metabolites in the light of their defensive action, these substances stand in marked contrast to known biotoxins striking vertebrate animals during "water blooms" and "red tides" (Gol'din, 2009). The defensive activity has a disastrous influence on vital functions of competitors and/or plant-feeders, and causes stress, repellent and deterrent effects, but not obligatory death (Cembella, 2003;Amsler, 2008;Berry et al, 2008 responses are very close to inhibitory activity of terrestrial plants-producers of allelochemics for the defense from the other plants or herbivorous arthropods and microbial pathogens (Gol'din, 1995;2009;Gol'din and Gol'dina, 2002;Hay et al, 1987;Paul et al, 2007;Berge et al, 2010).…”