Sex and life-history stage alter herbivore responses to a chemically defended red alga

Abstract

Intraspecific variation in resistance to herbivory among genders and life-history phases of primary producers can significantly alter the ecological and evolutionary consequences of plant–herbivore interactions. Seaweeds (macroalgae) with complex life histories have multiple distinct phases with associated variation in traits that can potentially lead to differences in resistance to consumers and provide a unique system in which to simultaneously test the effects of sex and life-history stage on herbivory. We tested the susceptibility to grazing of the three life-history stages and separate sexes of the chemically defended red alga Asparagopsis armata against the sea hare Aplysia parvula, and we related this to the plant quality traits of different stages and genders. Differences in nutrient content and halogenated secondary metabolites between life-history phases were highly sex dependent. Male gametophytes had a low concentration of secondary metabolites and the highest nutrient content. The highest secondary metabolite content was found within the female gametophyte, in the wall of the reproductive structures (cystocarps) that contain the microscopic carposporophyte phase. Feeding choices by A. parvula were consistent with differences in algal quality and defense and resulted in the haploid male gametophytes being the most preferred food type. The diploid carposporophyte found inside the chemically rich cystocarps was the least consumed life-history stage. Selective herbivory of male gametophytes by A. parvula is consistent with an observed shift in gametophyte sex ratio in the field from unity at the beginning of the reproductive season to female bias at the end. The variation in susceptibility to herbivory found between sex and life-history stages of A. armata represents the first example of sex-biased consumption in seaweeds and may contribute to the maintenance of complex life histories such as those found in red algae.