Erik E. Sotka

Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula

A long‐standing issue in marine biology is identifying spatial scales at which populations of sessile adults are connected by planktonic offspring. We examined the genetic continuity of the acorn barnacle Balanus glandula, an abundant member of rocky intertidal communities of the northeastern Pacific Ocean, and compared these genetic patterns to the nearshore oceanography described by trajectories of surface drifters. Consistent with its broad dispersal potential, barnacle populations are genetically similar at both mitochondrial (cytochrome oxidase I) and nuclear (elongation factor 1‐alpha) loci across broad swaths of the species’ range. In central California, however, there is a striking genetic cline across 475 km of coastline between northern and southern populations. These patterns indicate that gene flow within central California is far more restricted spatially than among other populations. Possible reasons for the steep cline include the slow secondary introgression of historically separated populations, a balance between diversifying selection and dispersal, or some mix of both. Geographic trajectories of oceanic drifters closely parallel geographical patterns of gene flow. Drifters placed to the north (Oregon; ∼44°N) and south (Santa Barbara, California; ∼34° N) of the cline disperse hundreds of kilometres within 40 days, yet over the long‐term their trajectories never overlapped. The lack of communication between waters originating in Oregon and southern California probably helps to maintain strong genetic differentiation between these regions. More broadly, the geographical variation in gene flow implies that focusing on species‐level averages of gene flow can mask biologically important variance within species which reflects local environmental conditions and historical events.

Global patterns in the impact of marine herbivores on benthic primary producers

Despite the importance of consumers in structuring communities, and the widespread assumption that consumption is strongest at low latitudes, empirical tests for global scale patterns in the magnitude of consumer impacts are limited. In marine systems, the long tradition of experimentally excluding herbivores in their natural environments allows consumer impacts to be quantified on global scales using consistent methodology. We present a quantitative synthesis of 613 marine herbivore exclusion experiments to test the influence of consumer traits, producer traits and the environment on the strength of herbivore impacts on benthic producers. Across the globe, marine herbivores profoundly reduced producer abundance (by 68% on average), with strongest effects in rocky intertidal habitats and the weakest effects on habitats dominated by vascular plants. Unexpectedly, we found little or no influence of latitude or mean annual water temperature. Instead, herbivore impacts differed most consistently among producer taxonomic and morphological groups. Our results show that grazing impacts on plant abundance are better predicted by producer traits than by large-scale variation in habitat or mean temperature, and that there is a previously unrecognised degree of phylogenetic conservatism in producer susceptibility to consumption.

Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing

Abstract. Tissues within individual plants can vary greatly in the strength of their constitutive (i.e., permanent) and induced resistance to herbivores. Optimal defense theory predicts that defenses should be allocated among tissues in proportion to the value of the tissues to the plant and the tissue-specific risk of attack by grazers. We examined the relationship between tissue value and defense in the highly-differentiated brown seaweed Sargassum filipendula. Tissues within S. filipendula varied widely in palatability to the herbivorous amphipod Ampithoe longimana, with younger tissues preferred over older tissues and blades preferred over stipes. Old stipes (at the base of the plant), which linked the other tissues to the seafloor and were thus the most valuable tissue to the plant, were defended constitutively and resisted amphipod grazing by virtue of their toughness rather than via deterrent chemistry. Induction of resistance as a result of amphipod grazing occurred only in the top stipes, which contain the meristematic tissue responsible for future growth. Induction in the top stipes was not due to toughness or other structural properties, as the unpalatability persisted when top stipes were dried, ground to a fine powder, and reconstituted into an agar matrix. This suggests that the induced resistance to grazing resulted from an increase in chemical defenses. The demonstration of constitutive or induced defenses in only the more valuable tissues of the seaweed is consistent with predictions of optimal defense theory. Our finding of induction due to mesograzer (amphipod) feeding is also consistent with the notion that it is these small, more sedentary, herbivores that are most likely to induce defenses in seaweeds.

GEOGRAPHIC VARIATION AMONG HERBIVORE POPULATIONS IN TOLERANCE FOR A CHEMICALLY RICH SEAWEED

Previous investigations have shown that the sedentary amphipod Ampithoe longimana escapes consumers by selectively living on and eating chemically defended seaweeds in the genus Dictyota. However, A. longimana and Dictyota overlap only in the southern portion of the amphipods range; Dictyota is not available to amphipods from more northerly regions. We used this disjunction in distribution to test the hypothesis that A. longimana populations co-occurring with Dictyota would have greater tolerance for the seaweeds chemical defenses and would display higher feeding preference for, and fitness on, the seaweed than would more northerly populations. We also evaluated the genetic vs. phenotypic basis of these patterns and attempted to detect trade-offs between tolerance for Dictyota and ability to use other plants as foods. Such geographic studies of herbivory have been conducted using terrestrial insects, but few studies have focused on other her- bivores, and this is especially true for marine systems. In multiple-choice feeding assays with both field-collected and laboratory-reared adults, a North Carolina population of A. longimana sympatric with Dictyota more readily fed on Dictyota and was more resistant to Dictyotas deterrent chemistry than was a Connecticut population from outside of Dic- tyotas geographic range. When raised on Dictyota menstrualis and D. ciliolata, A. lon- gimana juveniles from North Carolina grew faster, matured faster, and produced more reproductive females than did Connecticut juveniles. The differential tolerance for Dictyota has a genetic basis, as it was maintained through two generations grown to maturity in a common environment. When several northern and southern populations were assayed, they displayed similar regional differences in feeding preferences. Though southern juveniles had higher fitness onDictyota than northern juveniles, south- ern juveniles performed as well as northern juveniles when raised on seven other seaweeds, including seaweeds (e.g., Fucus vesiculosus and Sargassum filipendula ) that produce sec- ondary metabolites in a different class from those found in Dictyota. Thus, tolerating Dictyota did not incur detectable performance trade-offs when juveniles were confined to feeding on alternative seaweeds. Our results suggest that the evolution of host preferences may depend more on the host value as a refuge from enemies than on minimizing the costs of tolerating plant secondary metabolites.

Biodiversity mediates top–down control in eelgrass ecosystems: a global comparative‐experimental approach

Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom-up and top-down forcing remain unresolved. We factorially added nutrients and reduced grazing at 15 sites across the range of the marine foundation species eelgrass (Zostera marina) to quantify how top-down and bottom-up control interact with natural gradients in biodiversity and environmental forcing. Experiments confirmed modest top-down control of algae, whereas fertilisation had no general effect. Unexpectedly, grazer and algal biomass were better predicted by cross-site variation in grazer and eelgrass diversity than by global environmental gradients. Moreover, these large-scale patterns corresponded strikingly with prior small-scale experiments. Our results link global and local evidence that biodiversity and top-down control strongly influence functioning of threatened seagrass ecosystems, and suggest that biodiversity is comparably important to global change stressors.

THE USE OF GENETIC CLINES TO ESTIMATE DISPERSAL DISTANCES OF MARINE LARVAE

Many unresolved issues in the ecology and evolution of marine populations center on how far planktonic larvae disperse away from their parents. Genetic tools provide a promising way to define the spatial spread of larvae, yet their accurate interpretation depends on the extent to which genetic loci are under selection. Genetic clines, geographic zones in which genetically differentiated populations interbreed, provide opportunities to explicitly and simultaneously quantify the relative roles of selection and dispersal. Here, we review the theory and analysis of genetic clines and apply these techniques to published studies of multilocus clines in the sea. The geographic width of a stable genetic cline is determined by a balance between the homogenizing effects of dispersal and the diversifying effects of selection. For marine researchers, the power of genetic clines is that, if selection and clinal width are quantified, then the average geographic distances that larvae move can be inferred. Measuring selection or dispersal through laboratory or field-based experimentation is possible, though logistically difficult, for pelagically dispersed organisms. Instead, dispersal may be more robustly quantified from the degree of linkage disequilibrium between two or more loci, because linkage disequilibrium integrates selection across multiple life stages and generations. It is also relatively insensitive to whether exogenous or endogenous selection operates. Even without quantifying linkage disequilibrium, the theory of genetic clines indicates that the average dispersal distance of larvae is a fraction (i.e., generally <35%) of the clinal width. Because cline theory is based on several underlying assumptions, including near-equilibrium between selection and migration, the dispersal distances inferred from empirical data should be of the correct order but may not be precise. Even so, such estimates of larval dispersal are valuable, as they can be utilized to design appropriate scales for future investigations and provide some guidance to conservation efforts.

PHYLOGENETIC AND GEOGRAPHIC VARIATION IN HOST BREADTH AND COMPOSITION BY HERBIVOROUS AMPHIPODS IN THE FAMILY AMPITHOIDAE

Abstract Predicting the host range for herbivores has been a major aim of research into plant–herbivore interactions and an important model system for understanding the evolution of feeding specialization. Among many terrestrial insects, host range is strongly affected by herbivore phylogeny and long historical associations between particular herbivore and plant taxa. For small herbivores in marine environments, it is known that the evolution of host use is sculpted by several ecological factors (e.g., food quality, value as a refuge from predators, and abiotic forces), but the potential for phylogenetic constraints on host use remains largely unexplored. Here, we analyze reports of host use of herbivorous amphipods from the family Ampithoidae (102 amphipod species from 12 genera) to test the hypotheses that host breadth and composition vary among herbivore lineages, and to quantify the extent to which nonpolar secondary metabolites mediate these patterns. The family as a whole, and most individual species, are found on a wide variety of macroalgae and seagrasses. Despite this polyphagous host use, amphipod genera consistently differed in host range and composition. As an example, the genus Peramphithoe rarely use available macrophytes in the order Dictyotales (e.g., Dictyota) and as a consequence, display a more restricted host range than do other genera (e.g., Ampithoe, Cymadusa, or Exampithoe). The strong phylogenetic effect on host use was independent of the uneven distribution of host taxa among geographic regions. Algae that produced nonpolar secondary metabolites were colonized by higher numbers of amphipod species relative to chemically poor genera, consistent with the notion that secondary metabolites do not provide algae an escape from amphipod herbivory. In contrast to patterns described for some groups of phytophagous insects, marine amphipods that use chemically rich algae tended to have broader, not narrower, host ranges. This result suggests that an evolutionary advantage to metabolite tolerance in marine amphipods may be that it increases the availability of appropriate algal hosts (i.e., enlarges the resource base).

GEOGRAPHIC AND GENETIC VARIATION IN FEEDING PREFERENCE FOR CHEMICALLY DEFENDED SEAWEEDS

Abstract Genetic variation in tolerance for seaweed chemical defenses among populations of marine herbivores is poorly described, either because few marine studies have addressed the issue or because the feeding preferences of populations of marine herbivores rarely differentiate. We address this using the polyphagous amphipod Ampithoe longimana (Crustacea), which commonly consumes, and lives on, terpene‐rich brown seaweeds in the tropical genus Dictyota. Previous work demonstrated that in areas where the amphipod and seaweeds overlap geographically, these chemically deterrent seaweeds provide the amphipod with spatial refuges from predation by omnivorous fishes that avoid consuming Dictyota. However, the amphipods distribution extends northward of the seaweeds distribution, making this benefit of association unavailable to more northerly populations of amphipods. On average, populations sympatric with Dictyota have stronger feeding preference for Dictyota species and greater fitness when raised on Dictyota than do populations that are outside Dictyotas geographic endpoint. These results are consistent with the hypothesis that in areas where the amphipods co‐exist with Dictyota, selection favors amphipods that tolerate Dictyotas chemical defenses and thereby access its enemy‐free space. Amphipods allopatric with Dictyota are unable to tolerate Dictyotas chemical defenses, either because of selection, drift, or some mix of both forces. A trade‐off between preference for Dictyota and for the chemically distinct seaweed Hypnea musciformis is suggested by the finding that populations with high preference for Dictyota tended to have lower preference for Hypnea. However, this population‐level pattern appears to be the result of independent evolution and not a genetic trade‐off: an analysis of full‐sib families within a single population detected heritable variation in preferences for Dictyota and suggested this for Hypnea (although the latter was not statistically significant), yet no family‐level covariation was detected. Phylogeo‐graphic analysis of mitocondrial DNA and nuclear sequences indicates a strong historical break between populations sympatric with Dictyota and populations more than 500 km beyond Dictyotas geographic endpoint. The historical separation of these most northerly populations could have allowed a random accumulation of alleles to effectively degrade tolerance for Dictyota, although selection may also be responsible for the degradation.

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

Abstract 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).

Tissue-specific induction of resistance to herbivores in a brown seaweed: the importance of direct grazing versus waterborne signals from grazed neighbors

In theory, plants could induce resistance to herbivores after being directly grazed or after sensing cues from the grazing of neighboring plants (i.e., the “talking trees” effect). Despite an extensive literature on induced defenses in plants, the relative importance of direct attack versus cues from neighbors in mediating induction is not well understood; this is especially true for seaweeds, where few investigations of induction due to attacks on neighbors have been conducted. We measured changes in resistance to grazing for stipes and blades of the brown seaweed Sargassum filipendula (Phaeophyta; Fucales) when it was directly grazed by amphipods or when it received potential waterborne cues from the grazing of neighboring plants, relative to plants that experienced neither direct grazing nor cues from grazed neighbors. After 25 days of these treatments in outdoor tanks, the amphipod Ampithoe longimana consumed top stipes from control plants 2.8 times more rapidly than top stipes from directly grazed plants, but did not differentiate between top blades in the same comparison. The amphipod did not discriminate between plants with grazed neighbors and plants with control neighbors when feeding on either stipes or blades. Thus, induction of resistance in S. filipendula was tissue-specific and occurred as a result of direct grazing, but not due to the grazing of neighboring plants.