The evolution of marine plant-herbivore interactions

Chief Investigators: Peter Steinberg, Alistair Poore
Herbivory is particularly intense in marine environments, with herbivores frequently removing almost all of the algal biomass. Such herbivory selects for the production of defensive mechanisms in plants (chemical and/or physical), which can in turn select for the feeding preferences of herbivores. While such interactions are well studied in terrestrial environments, there has been relatively little work in marine habitats with an explicitly evolutionary focus. At UNSW, we use fast growing macroalgae and their herbivores (urchins, gastropods, amphipods) to test hypotheses about the evolution of plant-herbivore interactions.

 
Selection for chemical defences in macroalgae

Theories for the evolution of chemical defences commonly assume that natural enemies act as selective agents, and that the production of these defences is costly to the plant. Research in the Centre for Marine Biofouling and Bioinnovation (CMBB) at UNSW has tested these hypotheses for the red alga Delisea pulchra (Fig.1). This alga produces variable concentrations of biologically-active halogenated furanones (Fig. 2).
 

Fig. 1. The chemically-defended red alga Delisea pulchra is common in the shallow subtidal in the Sydney region.

Fig. 2. Halogenated furanones produced by Delisea pulchra deter local herbivores, epiphytic bacteria and fouling organisms (algae and invertebrates).
We showed the potential for herbivores to select for increased concentrations of furanones by demonstrating that the concentrations of furanones are heritable, and that some of the local herbivores (gastropods, urchins) respond to quantitative variation in furanone levels (Fig. 3). Ongoing research in CMBB is examining the role of other natural enemies (fouling organisms, disease-causing bacteria) in selecting for metabolite levels.


Further reading

Wright, JT, R de Nys, AGB Poore and PD Steinberg. 2004. Chemical defense in a marine alga: heritability and potential for selection by herbivores. Ecology 85: 2946-2959.

Fig. 3. Feeding by the marine gastropod Turbo torquatus on artificial diets is reduced with increasing concentrations of a furanones in a dose-dependent manner.

 

Costs of chemical defence

From the plant’s perspective, defences are assumed to be costly if the presence of the defence results in lower individual fitness of the prey item in the absence of consumers. We have used a novel approach to measure cost by experimentally manipulating the levels of defences in Delisea pulchra. This was achieved by limiting the availability of bromine, a trace element in seawater that is required to make furanones (Fig. 2) but not otherwise needed by macroalgae. Algae grew more slowly in the presence of bromine, providing the first experimental evidence of a cost to a macroalga of acquiring defensive secondary metabolites.

Further reading

Dworjanyn, SA, JT Wright, NA Paul, R De Nys and PD Steinberg. 2006. Costs of chemical defence in the red alga Delisea pulchra. Oikos 113: 13-22.

 

Evolution of feeding specialisation

The interaction between herbivores and the plants they consume (particularly insect-plant interactions) has been an important model system for the evolution of specialisation. Most studies of marine herbivores have focussed only on the proximal determinants of feeding choices (e.g., nutritional quality, toughness, secondary metabolites). At UNSW, we have used an abundant herbivorous amphipod (Fig. 4) as a model system to examine the evolution of host use in small, marine herbivores that are closely associated with macroalgae.

Fig. 4. The herbivorous amphipod Peramphithoe parmerong consumes abundant brown algae (e.g. Sargassum spp.) in shallow subtidal habitats.
Research has measured how differences in performance on co-occurring algae select for feeding preferences and the potential for evolutionary responses to this selection via estimates of the heritability of survival and local adaptation to algae in the field. Recent work has examined variation in host use from the scales of the individual foraging in patchy environments to that of family level phylogeny (Fig. 5).

 

Further reading

Poore, AGB and PD Steinberg. 2001. Host plant adaptation in a herbivorous marine amphipod: genetic potential not realized in field populations. Evolution 55:68-80.

Poore, AGB 2004. Spatial associations among algae affect host use in a herbivorous marine amphipod. Oecologia 140:104-112.

Fig. 6. Ordination showing that the composition of host genera varies among amphipod species from different lineages (genera in the family Ampithoidae), suggesting phylogenetic constraints on host use in this abundant group of marine herbivores.