Host-plant specialization by a non-herbivorous amphipod: advantages for the amphipod and costs for the seaweed

Studies of factors affecting host plant specialization by herbivores commonly highlight the value of the plant as both food and habitat, but often cannot distinguish the relative importance of these plant traits. A different approach is to study non-herbivorous animals that specialize on particular plants but do not feed on tissue from these plants. Such animals will not be affected directly by the nutritional, chemical, or morphological traits that determine the value of the plant as a food. This study reports on a filter-feeding amphipod, Ericthoniusbrasiliensis, that lives in domiciles it constructs by curling terminal segments of the green, calcified, and chemically defended seaweed Halimedatuna. We examined the temporal (1850s–1990s) and spatial (Caribbean, Mediterranean, and Pacific regions) scale of the association, the factors that may select for specialization on H. tuna, and the effect of the amphipod on growth of its host. Sampling along 125 km of coral reefs in the Florida Keys (USA) indicated that almost all populations of H. tuna had been colonized by this amphipod. Infested plants occurred on nine of ten reefs that supported H. tuna populations, with between 8 and 75% of the plants on those reefs colonized by the amphipod. For infested plants, 2–23% of all segments on each plant had been curled by the amphipod. Common co-occurring congeners of H. tuna (H. opuntia and H. goreaui) were never used for domicile construction. A survey of 1498 Halimeda specimens collected during the last 140 years and archived in the U.S. National Museum of Natural History (Smithsonian Institution, Washington, D.C.) indicated that the association has existed for >100 years and occurs throughout the Caribbean region, never in the Indo-Pacific or Mediterranean, and only on H. tuna. Predation by fishes could select for amphipod specialization on H. tuna. Laboratory experiments demonstrated that amphipods inhabiting curled segments of H. tuna were relatively immune from fish predation while those on the exterior surface of the plant or in open water were rapidly eaten. Segments of H. tuna are large enough to provide full protection from predators, while those of the co-occurring congeners H. goreaui and H. opuntia are of a size that may provide only partial protection. Experimental addition of E. brasiliensis to H. tuna plants in the field significantly decreased segment accumulation on infested relative to uninfested control plants. Whether this negative effect was a direct or indirect consequence of amphipod occupancy is unclear. Rolling plant portions into domiciles could directly decrease host growth by increasing shading and decreasing exposure of plant surface area to water column nutrient flux. Amphipod occupancy could indirectly slow net host growth if fishes selectively feed on plant sections occupied by amphipods. Underwater video showed that herbivorous fishes did not graze infested plants more than uninfested plants, but small predatory fishes did prefer feeding from infested plants. These non-herbivorous fishes may slow host growth by damaging the terminal meristematic tissues of plants during attacks on amphipods. This study demonstrates that habitat specialists can negatively impact hosts without consuming them and that specialization on a plant can occur due to its habitat value alone (as opposed to its value as a food).