Mollusca Non-Grata: The influence of top-down control and residence time on the abundance, distribution, and behavior of non-native marine snails in Washington State

Thesis (Ph.D.)--University of Washington, 2016-06

Invasive species can cause complex, unpredictable changes in ecological community dynamics because they do not share a long evolutionary history with resident species, meaning interactions could be much stronger or weaker than expected. For instance, invasive species often face a suite of both novel potential predators, and novel potential prey, but might not have the ability to recognize or respond appropriately (i.e., to increase fitness). The success or failure of recognition and response in novel predator-prey systems influences the probability of invasions success and the ecological dynamics that follow. Invasive species that fail to respond adaptively to novel, native predators, might persist in only a limited portion of their potential non-native range at low abundances. Conversely, invasive prey with effective defenses could reduce the efficacy of biotic resistance by native predators. The ability of native predators to recognize and overcome such defenses in invasive prey also influences the strength of biotic resistance. Through a combination of field and laboratory studies, I explored how native predatory crabs influence the abundance, distribution, and behavior of four species of non-native marine snail, and consider possible outcomes in conservation of native species. All four species of snail are successful invaders in Washington State nearshore systems, despite the fact that this region has a relatively high richness of large native predatory crabs that could confer biotic resistance against these species. In a field experiment, I explored the potential for an invasive snail to interact with novel native species as both predator and prey at a native oyster restoration site. In this system, invasive marine whelks, Ocenebra inornata (Japanese oyster drills) prey on native oysters (Ostrea lurida) and might be inhibiting recovery of this rare ecosystem engineer. In the laboratory, native cancrid crabs prey both on oyster drills and on oysters, but prefer to eat oysters. Thus this tri-trophic system includes intra-guild predation (IGP), and crabs might exert top-down control on oyster survival via several pathways: 1) crabs could reduce oyster survival via direct consumption; 2) crabs could increase oyster survival by reducing drill abundance through predation; and 3) crabs could increase oyster survival by reducing drill feeding rates through intimidation. I explored the separate and combined effects of crabs and drills on oyster survival using cages to control access of top predators (native cancrid crabs), and the intermediate (or intraguild) prey (oyster drills) to the resource (oysters). Though crabs were predicted to have a strong negative effect on oysters via direct predation, in fact, the presence of oyster drills had the strongest impact on oyster survival. Drills consumed up to 80% of oysters in experimental cages per month and accounted for an average of 70% of total mortality when they were present. Contrary to my prediction, crabs almost never attacked oysters directly, and consumed drills primarily during only one out of four months. Crabs also did not appear to reduce individual drill feeding rates (i.e. an intimidation effect) or initiate a strong indirect positive effect on oyster survival. This experiment demonstrated that the role of the invasive predator in IGP as well as the strength of the interaction between the native and invasive species combine to influence the dynamics of the system. In addition, these observations underscore the importance of considering non-native predators as obstacles to the recovery of threatened species, as well the value of experimentally identifying, in situ, which of the possible interactions in an invaded food web are ecologically important. This work was published in The Journal of Experimental Marine Biology and Ecology in 2016, Volume 479, pages 1-8. In a second field study, I used a combination of field surveys and laboratory experiments to assess the role of top-down control by both native and non-native species in influencing regional and local abundance and distribution of the invasive snail, Batillaria attramentaria. Two Washington populations of this species have substantially different invasion histories (~10 years versus >80 years) and exhibit markedly different densities and tidal ranges. The less-dense, vertically-restricted population was recently introduced, and thus has had less opportunity to fill the fundamental niche at that site. I investigated three possible explanations: 1) residence time, 2) infection by a co-evolved, castrating, parasite, and 3) biotic resistance by native predators. However, I only found strong support for biotic resistance from native predators; the younger population experienced much greater effects of native cancrid crabs than the older, high-density population, particularly below the minimum tidal elevation of observed snail distribution where crabs are found in the greatest densities. This is the first study documenting effects of predators on this invasive snail, which is widespread along coastlines of the northeast Pacific, whereas previous studies have suggested that the primary restriction on population growth rate was likely to be castration by the co-evolved parasite. Further, this study supports the general belief that, while novel predators can reduce the impacts or population growth rates of invasive species, such biotic resistance is not likely to preclude persistence at a given site. These observations also affirm the suggestion that residence time could be less important in predicting indicators of invasion success at the local, than at the regional or global scale. Lastly, I addressed the question of how novelty in predator-prey interactions could constrain the risk recognition ability of the prey. Though prey use a variety of information sources to assess predation risk, non-native prey might fail to recognize risk from a novel predator, with which they share only a short co-history. It has been theorized that non-native prey could compensate via generalized risk assessment, i.e., relying on general alarm signals from injured conspecific prey rather than cues from predators themselves. I tested the influence of shared predator-prey history on information use by comparing responses among three native and four non-native prey species to chemical cues from a native predator and cues from injured conspecific prey. Non-native prey demonstrated information generalism: (1) responding stronger to alarm cues released by injured conspecific prey than to the predators, and (2) responding similarly to alarm cues as to cues from predators consuming injured conspecific prey. By contrast, native prey required multiple sources of information, with increased information content, to elicit the greatest defense. The influence of other sources of chemical information on risk assessment was not predicted by co-history with the predator: only one non-native snail responded to the predator itself; digestion was only important for two native species; the identity of injured prey was generally important in risk assessments; but predator and prey cues always contributed additively to prey response. These results suggest that information generalism, though hypothesized to be costly in co-evolved interactions, might play a role in facilitating biological invasions, either as a driver of, or response to, introduction to novel habitats. The impact of generalized risk assessment, relative to other patterns of information use, on community dynamics remains an open and inviting question. Nevertheless, understanding how prey use information to assess predation risk is critical to precisely characterizing the selective forces operating on predator-prey arms races. Biological invasions afford excellent opportunities to investigate these questions because selection can be strong in novel interactions and community perturbations are often readily apparent. Together, these studies address ways in which novelty can influence predator-prey interactions with implications for predicting and managing biological invasions. Biotic resistance by novel native predators can be an important factor in reducing the impacts of invasive species, by limiting their range or abundance. However, I have also observed support for several mechanisms by explaining why biotic resistance by native predators is unlikely to completely preclude establishment and survival of invasive populations. Biotic resistance by predators varies over space and time, permitting prey to persist via spatial and temporal refuges. Moreover, even where they do co-occur, native predators might not necessarily have a novelty advantage over naïve prey; I have observed that some invasive prey are able to circumvent an inability to recognize a novel threat from a native predator via reliance on generalized alarm cues. Management strategies that take these factors into account could complement biotic resistance by targeting invasive species refuges in control and removal efforts. An improved understanding of the generalities of novel predator-prey interactions could offer novel approaches to conservation, as well as insight into the role of evolution in species interactions.