James E. Byers

COMPETITION BETWEEN TWO ESTUARINE SNAILS: IMPLICATIONS FOR INVASIONS OF EXOTIC SPECIES

An introduced snail, Batillaria attramentaria, has successfully invaded sev- eral salt marshes and mud flats in northern California. In these areas populations of the native mud snail, Cerithidea californica, have declined precipitously. Since both species feed on epipelic diatoms, I hypothesized that the decline in Cerithidea was a result of exploitative competition with Batillaria. To test this hypothesis I manipulated snail densities in Bolinas Lagoon, California, to estimate their effects on, and responses to, food resources. For two size classes of each snail species I quantified (1) the effect of intraspecific density on food availability, and (2) the growth response of each size class to different food levels. These relationships were used to generate predictions of the exploitative competitive effect of each snail on the other species. These predictions were tested against direct measurements of the effect of interspecific competition on snail tissue growth using field experiments. The observed values of snail growth matched well the predicted relationships, suggesting that exploitative competition does occur. Although the two snails did not differ in their effect on resource levels at any experimental snail density, the introduced snail was always more efficient at converting limited resources to tissue growth. Similar results were obtained in three different experimental periods. Batillarias enhanced resource conversion efficiency provides a sufficient explanation for its successful invasion and subsequent exclusion of Cerithidea. Theoretically, conversion efficiency of resources should be just as important as resource suppression and uptake to exploitative competitive ability, but it is rarely examined experimentally. By separating exploitative competition into its component parts, the protocol used here allowed identification of a seldom implicated mechanism that can affect invasion success.

Cascading of habitat degradation: Oyster reefs invaded by refugee fishes escaping stress

Mobile consumers have potential to cause a cascading of habitat degradation beyond the region that is directly stressed, by concentrating in refuges where they intensify biological interactions and can deplete prey resources. We tested this hypothesis on structurally complex, species-rich biogenic reefs created by the eastern oyster, Crassostrea virginica, in the Neuse River estuary, North Carolina, USA. We (1) sampled fishes and invertebrates on natural and restored reefs and on sand bottom to compare fish utilization of these different habitats and to characterize the trophic relations among large reef-associated fishes and benthic invertebrates, and (2) tested whether bottom-water hypoxia and fishery-caused degradation of reef habitat combine to induce mass emigration of fish that then modify community composition in refuges across an estuarine seascape. Experimentally restored oyster reefs of two heights (1 m tall “degraded” or 2 m tall “natural” reefs) were constructed at 3 and 6 m depths. We sampled...

Parasites alter community structure

Parasites often play an important role in modifying the physiology and behavior of their hosts and may, consequently, mediate the influence hosts have on other components of an ecological community. Along the northern Atlantic coast of North America, the dominant herbivorous snail Littorina littorea structures rocky intertidal communities through strong grazing pressure and is frequently parasitized by the digenean trematode Cryptocotyle lingua. We hypothesized that the effects of parasitism on host physiology would induce behavioral changes in L. littorea, which in turn would modulate L. littoreas influence on intertidal community composition. Specifically, we hypothesized that C. lingua infection would alter the grazing rate of L. littorea and, consequently, macroalgal communities would develop differently in the presence of infected versus uninfected snails. Our results show that uninfected snails consumed 40% more ephemeral macroalgal biomass than infected snails in the laboratory, probably because the digestive system of infected snails is compromised by C. lingua infection. In the field, this weaker grazing by infected snails resulted in significantly greater expansion of ephemeral macroalgal cover relative to grazing by uninfected snails. By decreasing the per-capita grazing rate of the dominant herbivore, C. lingua indirectly affects the composition of the macroalgal community and may in turn affect other species that depend on macroalgae for resources or habitat structure. In light of the abundance of parasites across systems, we suggest that, through trait-mediated indirect effects, parasites may be a common determinant of structure in ecological communities.

Scale dependent effects of biotic resistance to biological invasion

As nonindigenous species continue to displace native species and disrupt ecosystems, understanding the degree to which native species richness affects the vulner- ability of communities to nonindigenous species invasions has grown in importance. Native and exotic species diversity are often positively correlated in large-scale observational studies, but negatively correlated in small-scale experimental studies. This discrepancy suggests that the scale of invasion studies may be an important influence on their outcomes. Using a competition-based model that exhibits a negative relationship on a small scale, we show that changes in the number of available resources across communities can cause invasion success to become positively correlated with native species diversity at larger scales. The strength of the positive correlation, however, depends on the relationship be- tween niche breadth and species diversity in natural communities. Adding species to a community or removing resources has a similar effect—increasing the sum of interspecific interaction strengths, which decreases invasion success.

CONTROLS OF SPATIAL VARIATION IN THE PREVALENCE OF TREMATODE PARASITES INFECTING A MARINE SNAIL

Geographic variability in abundance can be driven by multiple physical and biological factors operating at multiple scales. To understand the determinants of larval trematode prevalence within populations of the marine snail host Littorina littorea, we quantified many physical and biological variables at 28 New England intertidal sites. A hierarchical, mixed-effects model identified the abundance of gulls (the final hosts and dispersive agents of infective trematode stages) and snail size (a proxy for time of exposure) as the primary factors associated with trematode prevalence. The predominant influence of these variables coupled with routinely low infection rates (21 of the 28 populations exhibited prevalence <12%) suggest broad-scale recruitment limitation of trematodes. Although infection rates were spatially variable, formal analyses detected no regional spatial gradients in either trematode prevalence or independent environmental variables. Trematode prevalence appears to be predominantly determined by local site characteristics favoring high gull abundance.

MORE HARM THAN GOOD: WHEN INVADER VULNERABILITY TO PREDATORS ENHANCES IMPACT ON NATIVE SPECIES

Invasion biologists typically regard susceptibility of an invasive species to native predators as a fortuitous condition that increases biotic resistance to the invasion. The line of reasoning is that predation weakens the net impact of the invader and reduces its ability to displace native competitors. However, predation on invasives is a coupled interaction; every invader consumed also enhances the predator population. If these predators also consume native species, then the invaders indirect effect via predators (i.e., apparent competition) could be more harmful to natives than the effect of resource competition from the exotic. We apply general community ecology theory to determine the conditions under which the net effect of predation on the exotic species is to extirpate the native competitor. An approximation to these conditions provides a simple metric to estimate the threat of native species extinction due to apparent competition posed by an invader.

Partitioning mechanisms of Predator Interference in different Habitats

Prey are often consumed by multiple predator species. Predation rates on shared prey species measured in isolation often do not combine additively due to interference or facilitation among the predator species. Furthermore, the strength of predator interactions and resulting prey mortality may change with habitat type. We experimentally examined predation on amphipods in rock and algal habitats by two species of intertidal crabs, Hemigrapsus sanguineus (top predators) and Carcinus maenas (intermediate predators). Algae provided a safer habitat for amphipods when they were exposed to only a single predator species. When both predator species were present, mortality of amphipods was less than additive in both habitats. However, amphipod mortality was reduced more in rock than algal habitat because intermediate predators were less protected in rock habitat and were increasingly targeted by omnivorous top predators. We found that prey mortality in general was reduced by (1) altered foraging behavior of intermediate predators in the presence of top predators, (2) top predators switching to foraging on intermediate predators rather than shared prey, and (3) density reduction of intermediate predators. The relative importance of these three mechanisms was the same in both habitats; however, the magnitude of each was greater in rock habitat. Our study demonstrates that the strength of specific mechanisms of interference between top and intermediate predators can be quantified but cautions that these results may be habitat specific.

Asymmetric dispersal allows an upstream region to control population structure throughout a species’ range

In a single well-mixed population, equally abundant neutral alleles are equally likely to persist. However, in spatially complex populations structured by an asymmetric dispersal mechanism, such as a coastal population where larvae are predominantly moved downstream by currents, the eventual frequency of neutral haplotypes will depend on their initial spatial location. In our study of the progression of two spatially separate, genetically distinct introductions of the European green crab (Carcinus maenas) along the coast of eastern North America, we captured this process in action. We documented the shift of the genetic cline in this species over 8 y, and here we detail how the upstream haplotypes are beginning to dominate the system. This quantification of an evolving genetic boundary in a coastal system demonstrates that novel genetic alleles or haplotypes that arise or are introduced into upstream retention zones (regions whose export of larvae is not balanced by import from elsewhere) will increase in frequency in the entire system. This phenomenon should be widespread when there is asymmetrical dispersal, in the oceans or on land, suggesting that the upstream edge of a species’ range can influence genetic diversity throughout its distribution. Efforts to protect the upstream edge of an asymmetrically dispersing species’ range are vital to conserving genetic diversity in the species.

Differential Parasitism of Native and Introduced Snails: Replacement of a Parasite Fauna

The role of parasites in a marine invasion was assessed by first examining regional patterns of trematode parasitism in the introduced Japanese mud snail, Batillaria cumingi (= B. attramentaria), in nearly all of its introduced range along the Pacific Coast of North America. Only one parasite species, which was itself a non-native species, Cercaria batillariae was recovered. Its prevalence ranged from 3 to 86%. Trematode diversity and prevalence in B. cumingi and a native sympatric mud snail, Cerithidea californica, were also compared in Bolinas Lagoon, California. Prevalence of larval trematodes infecting snails as first intermediate hosts was not significantly different (14% in B. cumingi vs 15% in C. californica). However, while the non-native snail was parasitized only by one introduced trematode species, the native snail was parasitized by 10 native trematode species. Furthermore, only the native, C. californica, was infected as a second intermediate host, by Acanthoparyphium spinulosum(78% prevalence). Given the high host specificity of trematodes for first intermediate hosts, in marshes where B. cumingi is competitively excluding C. californica, 10 or more native trematodes will also become locally extinct.

Physical Ecosystem Engineers and the Functioning of Estuaries and Coasts

A great diversity of organisms modify the physical structure of estuarine and coastal environments. These physical ecosystem engineers – particularly, dune and marsh plants, mangroves, seagrasses, kelps, reef-forming corals and bivalves, burrowing crustaceans, and infauna – often have substantive functional impacts over large areas and across distinct geographic regions. Here, we use a general framework for physical ecosystem engineering to illustrate how these organisms can exert control on sedimentary processes, coastal protection, and habitat availability to other organisms. We then discuss the management implications of coastal and estuarine engineering, concluding with a brief prospectus on research and management challenges.