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

Rates of spread of marine pathogens

Epidemics of marine pathogens can spread at extremely rapid rates. For example, herpes virus spread through pilchard populations in Australia at a rate in excess of 10 000 km year(-1), and morbillivirus infections in seals and dolphins have spread at more than 3000 km year(-1). In terrestrial environments, only the epidemics of myxomatosis and calicivirus in Australian rabbits and West Nile Virus in birds in North America have rates of spread in excess of 1000 km year(-1). The rapid rates of spread of these epidemics has been attributed to flying insect vectors, but flying vectors have not been proposed for any marine pathogen. The most likely explanation for the relatively rapid spread of marine pathogens is the lack of barriers to dispersal in some parts of the ocean, and the potential for long-term survival of pathogens outside the host. These findings caution that pathogens may pose a particularly severe problem in the ocean. There is a need to develop epidemic models capable of generating these high rates of spread and obtain more estimates of disease spread rate.

A theory for optimal monitoring of marine reserves

Monitoring of marine reserves has traditionally focused on the task of rejecting the null hypothesis that marine reserves have no impact on the population and community structure of harvested populations. We consider the role of monitoring of marine reserves to gain information needed for management decisions. In particular we use a decision theoretic framework to answer the question: how long should we monitor the recovery of an over-fished stock to determine the fraction of that stock to reserve? This exposes a natural tension between the cost (in terms of time and money) of additional monitoring, and the benefit of more accurately parameterizing a population model for the stock, that in turn leads to a better decision about the optimal size for the reserve with respect to harvesting. We found that the optimal monitoring time frame is rarely more than 5 years. A higher economic discount rate decreased the optimal monitoring time frame, making the expected benefit of more certainty about parameters in the system negligible compared with the expected gain from earlier exploitation.

Marine actinomycetes related to the 'Salinospora' group from the Great Barrier Reef sponge Pseudoceratina clavata

Ten strains identified as marine actinomycetes related to the 'Salinospora ' group previously reported only from marine sediments were isolated from the Great Barrier Reef marine sponge Pseudoceratina clavata. The relationship of the isolates to 'Salinospora' was confirmed by phylogenetic analysis of 16S rRNA gene sequences. Colony morphology and pigmentation, occurrence and position of spores, and salinity requirements for growth were all consistent with this relationship. Genes homologous to beta-ketosynthase, an enzyme forming part of a polyketide synthesis complex, were retrieved from these isolates; these genes shared homology with other Type I ketosynthase genes, and phylogenetic comparison with amino acid sequences derived from database beta-ketosynthase genes was consistent with the close relationship of these isolates to the actinomycetes. Primers based on 16S rRNA gene sequences and designed for targeting amplification of members of the 'Salinospora' group via polymerase chain reaction have been used to demonstrate occurrence of these actinomycetes within the sponge tissue. In vitro bioassays of extracts from the isolates for antibiotic activity demonstrated that these actinomycetes have the potential to inhibit other sponge symbionts in vivo, including both Gram-negative and Gram-positive bacteria.

Accounting for uncertainty in marine reserve design

Ecosystems and the species and communities within them are highly complex systems that defy predictions with any degree of certainty. Managing and conserving these systems in the face of uncertainty remains a daunting challenge, particularly with respect to developing networks of marine reserves. Here we review several modelling frameworks that explicitly acknowledge and incorporate uncertainty, and then use these methods to evaluate reserve spacing rules given increasing levels of uncertainty about larval dispersal distances. Our approach finds similar spacing rules as have been proposed elsewhere - roughly 20-200 km - but highlights several advantages provided by uncertainty modelling over more traditional approaches to developing these estimates. In particular, we argue that uncertainty modelling can allow for (1) an evaluation of the risk associated with any decision based on the assumed uncertainty; (2) a method for quantifying the costs and benefits of reducing uncertainty; and (3) a useful tool for communicating to stakeholders the challenges in managing highly uncertain systems. We also argue that incorporating rather than avoiding uncertainty will increase the chances of successfully achieving conservation and management goals.

Adverse feedback sequences in exploited marine systems: Are deliberate interruptive actions warranted?

Several mechanisms for self-enhancing feedback instabilities in marine ecosystems are identified and briefly elaborated. It appears that adverse phases of operation may be abruptly triggered by explosive breakouts in abundance of one or more previously suppressed populations. Moreover, an evident capacity of marine organisms to accomplish extensive geographic habitat expansions may expand and perpetuate a breakout event. This set of conceptual elements provides a framework for interpretation of a sequence of events that has occurred in the Northern Benguela Current Large Marine Ecosystem (off south-western Africa). This history can illustrate how multiple feedback loops might interact with one another in unanticipated and quite malignant ways, leading not only to collapse of customary resource stocks but also to degradation of the ecosystem to such an extent that disruption of customary goods and services may go beyond fisheries alone to adversely affect other major global ecosystem concerns (e.g. proliferations of jellyfish and other slimy, stingy, toxic and/or noxious organisms, perhaps even climate change itself, etc.). The wisdom of management interventions designed to interrupt an adverse mode of feedback operation is pondered. Research pathways are proposed that may lead to improved insights needed: (i) to avoid potential 'triggers' that might set adverse phases of feedback loop operation into motion; and (ii) to diagnose and properly evaluate plausible actions to reverse adverse phases of feedback operation that might already have been set in motion. These pathways include the drawing of inferences from available 'quasi-experiments' produced either by short-term climatic variation or inadvertently in the course of biased exploitation practices, and inter-regional applications of the comparative method of science.

Reliably estimating the effect of toxicants on fertilization success in marine broadcast spawners

Recently, there has been a dramatic increase in the number of ecotoxicological studies examining the effects of toxicants on fertilization success in marine broadcast spawners and it appears that this life-history stage is one of the most vulnerable to toxicants. Most of the studies examining this issue use single sperm concentrations in their assays. Here, I discuss recent advances in fertilization ecology that suggest this technique has some severe limitations resulting in unreliable estimations of the size and direction of toxicant effects. I present an alternative assay technique and two metrics (F-max and [Sperm](max)) that will reliably estimate the size of a toxicant's effect on fertilization success. This technique has the added advantage of making comparisons among species and studies easier without an impractical increase in effort. (c) 2006 Elsevier Ltd. All rights reserved.

Understanding Isolation and Change in Island Human Populations through a study of Indigenous Cultural Patterns in the Gulf of Carpentaria

This paper presents a set of hypotheses to explain the cultural differences between Aboriginal people of the North and South Wellesley Islands, Gulf of Carpentaria and to characterise the relative degree and nature of their isolation and cultural change over a 10,000-year time-scale. This opportunity to study parallelisms and divergences in the cultural and demographic histories of fisher-hunter-gatherers arises from the comparison of three distinct cultural groupings: (a) the Ganggalida of the mainland, (b) the Lardil and Yangkaal of the North Wellesley Islands, and (c) the Kaiadilt of the South Wellesley Islands. Despite occupying similar island environments and despite their languages being as closely related as for example, the West Germanic languages, there are some major differences in cultural, economic and social organization as well as striking genetic differences between the North and South Wellesley populations. This paper synthesizes data from linguistics, anthropology, archaeology, genetics and environmental science to present hypotheses of how these intriguing differences were generated, and what we might learn about early processes of marine colonization and cultural change from the Wellesley situation.

The importance of marine subsidies for terrestrial consumers in coastal Peru

The Peruvian coast is one the best examples of cross-ecosystem food web exchanges, in which resources from one of the richest marine ecosystems subsidize consumers in one of the driest deserts on Earth. Marine subsidies are resources that originate in the marine ecosystem, and that contribute to increase the density of consumers in the recipient ecosystem. I examined the effects of marine subsidies on animal populations in the Peruvian coastal desert. ^ I combined several approaches to study the linkages between marine resources and terrestrial consumers, such as surveying the spatial distribution and estimating the relative abundance of terrestrial consumers, studying the diet of geckos and lizards through stomach content analyses, and examining the desert food web with carbon and nitrogen stable isotope analyses. ^ I found that the distribution and diet of desert consumers were tightly coupled to the availability of marine subsidies. I revealed linkages along two pathways of nutrient fluxes: tidal action that washes ashore macroalgae and cadavers of marine organisms, and animal transport in places where pinnipeds and seabirds congregate for reproduction. In the first pathway, intertidal algivivores made marine resources available to terrestrial consumers by moving between the intertidal and supratidal zone. The relative contribution of terrestrial and algal carbon sources varied among terrestrial consumers, because scorpions assimilated a lower proportion of energy from macroalgae than did geckos and solifuges. In the second pathway, I found that pinniped colonies influenced the diet of desert consumers, and contributed to support large populations of lizards and geckos. By combining field observations, and stomach and stable isotope analyses, I constructed a simplified food web for a large sea lion colony, showing the number of trophic levels that originate from pinniped-derived nutrients. ^ My study demonstrates the enormous importance of marine resources for the diet of desert consumers. The near absence of rainfall along the Peruvian coast promotes an extreme dependence of terrestrial consumers on marine resources, and causes permanent food web effects that are affected by temporal variability in marine productivity, rather then temporal patterns of desert plant growth. ^

Five new species of yeasts from fresh water and marine habitats in the Florida Everglades

Yeast populations in the Shark River Slough of the Florida Everglades, USA, were examined during a 3-year period (2002–2005) at six locations ranging from fresh water marshes to marine mangroves. Seventy-four described species (33 ascomycetes and 41 basidiomycetes) and an approximately equal number of undescribed species were isolated during the course of the investigation. Serious human pathogens, such as Candida tropicalis, were not observed, which indicates that their presence in coastal waters is due to sources of pollution. Some of the observed species were widespread throughout the fresh water and marine habitats, whereas others appeared to be habitat restricted. Species occurrence ranged from prevalent to rare. Five representative unknown species were selected for formal description. The five species comprise two ascomycetes: Candida sharkiensis sp. nov. (CBS 11368T) and Candida rhizophoriensis sp. nov. (CBS 11402T) (Saccharomycetales, Metschnikowiaceae), and three basidiomycetes: Rhodotorula cladiensis sp. nov. (CBS 10878T) in the Sakaguchia clade (Cystobasidiomycetes), Rhodotorula evergladiensis sp. nov. (CBS 10880T) in the Rhodosporidium toruloides clade (Microbotryomycetes, Sporidiobolales) and Cryptococcus mangaliensis sp. nov. (CBS 10870T) in the Bulleromyces clade (Agaricomycotina, Tremellales).

Herbivore and nutrient impact on primary producer assemblages in a tropical marine environment

Globally, human populations are increasing and coastal ecosystems are becoming increasingly impacted by anthropogenic stressors. As eutrophication and exploitation of coastal resources increases, primary producer response to these drivers becomes a key indicator of ecosystem stability. Despite the importance of monitoring primary producers such as seagrasses and macroalgae, detailed studies on the response of these benthic habitat components to drivers remain relatively sparse. Utilizing a multi-faceted examination of turtle-seagrass and sea urchin-macroalgae consumer and nutrient dynamics, I elucidate the impact of these drivers in Akumal, Quintana Roo, Mexico. In Yal Ku Lagoon, macroalgae bioindicators signified high nutrient availability, which is important for further studies, but did not consistently follow published trends reflecting decreased δ 15N content with distance from suspected source. In Akumal Bay, eutrophication and grazing by turtles and fishes combine to structure patches within the seagrass beds. Grazed seagrass patches had higher structural complexity and productivity than patches continually grazed by turtles and fishes. Results from this study indicate that patch abandonment may follow giving-up density theory, the first to be recorded in the marine environment. As Diadema antillarum populations recover after their massive mortality thirty years ago, the role these echinoids will have in reducing macroalgae cover and altering ecosystem state remains to be clear. Although Diadema antillarum densities within the coral reef ecosystem were comparable to other regions within the Caribbean, the echinoid population in Akumal Bay was an insufficient driver to prevent dominance of a turf-algal-sediment (TAS) state. After a four year study, declining coral cover coupled with increased algal cover suggests that the TAS-dominated state is likely to persist over time despite echinoid recovery. Studies on macroalgal diversity and nutrients within this same region of echinoids indicated diversity and nutrient content of macroalgae increased, which may further increase the persistence of the algal-dominated state. This study provides valuable insight into the variable effects of herbivores and nutrients on primary producers within a tropical coastal ecosystem. Results from this work challenge many of the currently accepted theories on primary producer response to nutrients and herbivory while providing a framework for further studies into these dynamics.

Microhabitat Selection by Marine Mesoconsumers in a Thermally Heterogeneous Habitat: Behavioral Thermoregulation or Avoiding Predation Risk?

Habitat selection decisions by consumers has the potential to shape ecosystems. Understanding the factors that influence habitat selection is therefore critical to understanding ecosystem function. This is especially true of mesoconsumers because they provide the link between upper and lower tropic levels. We examined the factors influencing microhabitat selection of marine mesoconsumers – juvenile giant shovelnose rays (Glaucostegus typus), reticulate whiprays (Himantura uarnak), and pink whiprays (H. fai) – in a coastal ecosystem with intact predator and prey populations and marked spatial and temporal thermal heterogeneity. Using a combination of belt transects and data on water temperature, tidal height, prey abundance, predator abundance and ray behavior, we found that giant shovelnose rays and reticulate whiprays were most often found resting in nearshore microhabitats, especially at low tidal heights during the warm season. Microhabitat selection did not match predictions derived from distributions of prey. Although at a course scale, ray distributions appeared to match predictions of behavioral thermoregulation theory, fine-scale examination revealed a mismatch. The selection of the shallow nearshore microhabitat at low tidal heights during periods of high predator abundance (warm season) suggests that this microhabitat may serve as a refuge, although it may come with metabolic costs due to higher temperatures. The results of this study highlight the importance of predators in the habitat selection decisions of mesoconsumers and that within thermal gradients, factors, such as predation risk, must be considered in addition to behavioral thermoregulation to explain habitat selection decisions. Furthermore, increasing water temperatures predicted by climate change may result in complex trade-offs that might have important implications for ecosystem dynamics.

Contrasting patterns of individual specialization and trophic coupling in two marine apex predators

1. Apex predators are often assumed to be dietary generalists and, by feeding on prey from multiple basal nutrient sources, serve to couple discrete food webs. But there is increasing evidence that individual level dietary specialization may be common in many species, and this has not been investigated for many marine apex predators. 2. Because of their position at or near the top of many marine food webs, and the possibility that they can affect populations of their prey and induce trophic cascades, it is important to understand patterns of dietary specialization in shark populations. 3. Stable isotope values from body tissues with different turnover rates were used to quantify patterns of individual specialization in two species of ‘generalist’ sharks (bull sharks, Carcharhinus leucas, and tiger sharks, Galeocerdo cuvier). 4. Despite wide population-level isotopic niche breadths in both species, isotopic values of individual tiger sharks varied across tissues with different turnover rates. The population niche breadth was explained mostly by variation within individuals suggesting tiger sharks are true generalists. In contrast, isotope values of individual bull sharks were stable through time and their wide population level niche breadth was explained by variation among specialist individuals. 5. Relative resource abundance and spatial variation in food-predation risk tradeoffs may explain the differences in patterns of specialization between shark species. 6. The differences in individual dietary specialization between tiger sharks and bull sharks results in different functional roles in coupling or compartmentalizing distinct food webs. 7. Individual specialization may be an important feature of trophic dynamics of highly mobile marine top predators and should be explicitly considered in studies of marine food webs and the ecological role of top predators.

Non-consumptive effects of predators in coral reef communities and the indirect consequences of marine protected areas

Predators exert strong direct and indirect effects on ecological communities by intimidating their prey. Non-consumptive effects (NCEs) of predators are important features of many ecosystems and have changed the way we understand predator-prey interactions, but are not well understood in some systems. For my dissertation research I combined a variety of approaches to examine the effect of predation risk on herbivore foraging and reproductive behaviors in a coral reef ecosystem. In the first part of my dissertation, I investigated how diet and territoriality of herbivorous fish varied across multiple reefs with different levels of predator biomass in the Florida Keys National Marine Sanctuary. I show that both predator and damselfish abundance impacted diet diversity within populations for two herbivores in different ways. Additionally, reef protection and the associated recovery of large predators appeared to shape the trade-off reef herbivores made between territory size and quality. In the second part of my dissertation, I investigated context-dependent causal linkages between predation risk, herbivore foraging behavior and resource consumption in multiple field experiments. I found that reef complexity, predator hunting mode, light availability and prey hunger influenced prey perception of threat and their willingness to feed. This research argues for more emphasis on the role of predation risk in affecting individual herbivore foraging behavior in order to understand the implications of human-mediated predator removal and recovery in coral reef ecosystems.^

Environmental stability affects phenotypic evolution in a globally distributed marine picoplankton

Marine phytoplankton can evolve rapidly when confronted with aspects of climate change because of their large population sizes and fast generation times. Despite this, the importance of environment fluctuations, a key feature of climate change, has received little attention-selection experiments with marine phytoplankton are usually carried out in stable environments and use single or few representatives of a species, genus or functional group. Here we investigate whether and by how much environmental fluctuations contribute to changes in ecologically important phytoplankton traits such as C:N ratios and cell size, and test the variability of changes in these traits within the globally distributed species Ostreococcus. We have evolved 16 physiologically distinct lineages of Ostreococcus at stable high CO2 (1031±87?µatm CO2, SH) and fluctuating high CO2 (1012±244?µatm CO2, FH) for 400 generations. We find that although both fluctuation and high CO2 drive evolution, FH-evolved lineages are smaller, have reduced C:N ratios and respond more strongly to further increases in CO2 than do SH-evolved lineages. This indicates that environmental fluctuations are an important factor to consider when predicting how the characteristics of future phytoplankton populations will have an impact on biogeochemical cycles and higher trophic levels in marine food webs.