In October 1993, growers at some commercial abalone mariculture facilities (AMFs) in Southern California brought an interesting sabellid polychaete to our attention.

The worm infested shells of cultured red abalone, Haliotis rufescens. Heavily infested abalone ceased growth. Their shells exhibited domed teratology often lacking respiratory holes. The worms appeared to bore into the shell.

We discovered that all AMFs in California were infested; several were so heavily infested that domed specimens were abundant. The objectives of our study were to describe the worm (Associate principal investigator, K. Fitzhugh, Los Angeles County Museum of Natural History), investigate transmission to abalone, its mechanism of attachment and the cause of shell damage. We also examined the host specificity among common intertidal molluscs. In the course of our research we discovered that a natural rocky intertidal site at Cayucos, California had become infested. Here we sought to investigate how the worms had escaped into the adjacent facility, determine whether the worms had become established there, quantify transmission at that site and devise and supervise an eradication plan.

As in the most complex animal societies, trematodes (parasitic flatworms) live in colonies characterized by a high degree of cooperative organization. My research started with the unexpected observation that several trematode species have a reproductive division of labor with morphologically and behaviorally distinct reproductive and non-reproductive castes. The non-reproductive individuals are smaller but have relatively large mouthparts. They are more active than their reproductive counterparts and disproportionately common in areas of the host where invasions by other trematodes occur. Finally, only non-reproductive individuals readily attack enemies with their mouths. Thus, it is clear that one major role of these individuals is to defend the colony from enemy trematode invaders; they are soldiers.

The initial discovery was followed by reports revealing the existence of soldiers in five additional trematode species and by research examining the adaptive significance of soldiers. However, descriptions of colony structure were restricted to a single trematode superfamily (Echinostomatoidea), and knowledge of colony demography and caste function was limited to snapshots of the condition of mature colonies. My doctoral dissertation has laid the foundation to explore the evolution of this remarkable social organization in trematodes, as well as the mechanisms regulating it.

Here I quantify morphology, distribution, and behavior of parasites from both establishing and fully developed colonies of sixteen species of trematodes that infect the California horn snail. While showing that eight additional species have a soldier caste, including four species from a new superfamily, I expand the phylogenetic range for which trematode sociality has been examined. I identify patterns underlying colony structure for trematode species that lack a soldier caste and establish discrete criteria to recognize colonies with and without soldiers. Finally, I develop an in vitro system for cultivation of marine trematodes that includes co-culture with Biomphalaria glabrata embryonic (Bge) cell line and media with Bge-released factors. The results presented here highlight the promise of these methods to address questions regarding trematode sociality, interspecific interactions, development and caste differentiation.

Trematode colonies are readily replicated, can be maintained in large numbers, and are amenable to in vitro studies. Hence, they provide many advantages as model systems to pursue experimental and comparative research probing general principles underlying the ecology and evolution of sociality. Furthermore, there are more than 20,000 species of trematodes worldwide. They cover a wide range of environmental and life history diversity and are both ecologically and medically important. Thus, understanding the mechanisms that shape trematode communities can have substantial public health, veterinary and wildlife disease applications.

Parasites often track food web linkages through their complex life cycles, but most food webs do not systematically include parasites. Where studied, parasites have strong effects on food web structure. Kelp forests are famous for strong trophic interactions, and their dynamic and open nature make them very different relative to the systems where parasites have been thoroughly studied (salt marsh, sand flat, and lake ecosystems). The objective of this dissertation was to build a high-resolution topological kelp-forest food web that includes parasites. I used this food web to address the research question: How do parasites affect food-web structure? Chapter 1 provides background and motivation for this work by reviewing key areas of research in kelp forest ecology and the effects of parasites in food webs. Chapter 2 describes the study system and a free-living food web with 490 species across 23 Phyla, with 546 distinct life stages and 8,759 trophic interactions. Chapter 3 describes the parasites in the food web, which adds 422 species across 10 Phyla (521 life stages) and 2,745 trophic interactions between parasites and hosts to the network for a total of 11,504 links. Adding trophic interactions between predator and parasites (concomitant predation) adds a further 9,536 links to the network. Chapter 4 examines the effects parasite addition on food-web structure. The kelp-forest food web was greatly enriched through resolution of free-living species and parasites, and parasites made up a larger proportion of the kelp-forest food web than any other published food web with parasites. Some of the effects of parasite addition were related to increasing network size and contrasted patterns in other systems (e.g. decreased connectance). On the other hand, other effects (e.g. longest chain length) were consistent with predictions based on other systems and were not due to increased network size alone. Specialist parasites and concomitant links altered the degree distribution independent of network size. Parasite life cycles are embedded throughout diverse patterns of free-living species interactions and must navigate a dense network of predators to infect appropriate hosts. The kelp forest ecosystem provides a diverse source of food and a diverse set of predators for both free-living and parasitic species, and our understanding of kelp forest ecosystems is enriched by including them.

The California horn snail (Cerithidea californica (Haldeman, 1840) (Potamididae: Prosobranchia) dominates the heterotrophic biomass of the salt marsh estuaries of California, Baja California, and Baja California Sur. Thus, it is an ecologically important species, functioning as a significant grazer and competitor, and host to more than 19 species of trematode parasites that infect many other species of invertebrates, fish, and birds as second, intermediate, and final hosts. Any changes in the distribution and abundance of this snail would likely have strong effects throughout estuarine food webs. Here I present observational and experimental studies performed both in the laboratory and in nature that advance our knowledge about the distribution and abundance of these snails. In the first chapter, I show how snail distribution and abundance was restricted by vascular vegetation, bank orientation in channels, and water depth, due to the negative effects of shading on benthic primary production. Vascular vegetation dominates the biomass of the estuaries of California and Baja California, any changes in vegetation cover will subsequently have an effect on the abundance and distribution of snails. In chapter two, I present how crabs negatively affected snails through predation and non-lethal effects that changed the behavior and diminished the growth rates of snails. Predation pressure was especially high on eggs and the smallest size classes of snails, which had been overlooked in previous predation studies. Finally, in chapter three I present results on how low temperature seems likely to set the northern extent of the horn snail's range by reducing snail performance. Results also suggest a possible tradeoff between growth and reproduction and highlight that although temperature might be important, several other local variables such as predator abundance and parasitism also have a considerable effects on snail abundance and performance. Understanding what sets the distribution and abundance of horn snails at local and regional scales will allow us to better predict the effects of climate change and other anthropogenic effects on these estuarine ecosystems.

This dissertation describes and analyzes the Palmyra Atoll sand flat food web. This food web is unique in measuring the body sizes, densities, and feeding links for all life stages of free-living and parasitic metazoans. Chapter 1 puts the research in context by reviewing the roles of parasites in marine food webs. Chapter 2 starts by describing the physical attributes (sediment particle size, water depth, temperature) of the 35 random sampling sites. It then lists the 22 sampling methods used to estimate the body size and abundance of 670 life stages comprising 275 species. The resulting free-living community contains represents 195 free-living species across 18 phyla, and 389 separate life stages. Chapter 2 then describes how parasites were measured from >2500 hosts collected and dissected to reveal a parasite community with 80 species across 9 phyla, and 281 separate life stages. Chapter 3 then uses stomach contents, field observations, literature, and natural history to estimate 24,575 trophic interactions, ontogenetic development and parasite transmission pathways among the 670 nodes in Chapter 2. Chapter 4 compares the Palmyra sand flat food web with the only published food web described in similar detail, the west coast estuary food web. In both systems, parasites make contributions to richness, abundance, and biomass comparable to free-living consumer groups, such as birds. Further, in both systems parasites dominate network structure in ways that free-living consumers cannot. These results suggest that parasites make general and important contributions to ecosystem structure. Our understanding of food webs is incomplete without them.

The field of ecology seeks to understand and predict the patterns and processes shaping the distribution and abundance of populations, the structure and organization of communities, and the dynamics and energetics of ecosystems structure. Parasitism is understudied as an interaction driving these patterns and processes in spite of research demonstrating that parasitism is the most common type of consumer interaction and numerous case studies clearly documenting that parasitism impacts populations, communities, and has a role in ecosystem energetics.

Ecologists have used the rocky intertidal zone as a model for understanding basic ecological processes and theories; thus, elucidating the role of infectious processes in this system will provide researchers with novel insights that may translate into broad structuring principles in the field. However, there is very little research on infectious processes in the rocky intertidal zone. Thus, in spite of decades of ecological research in this system, parasitic interactions remain unexplored and research may yet reveal a strong structuring role of infections in this system.

Barnacles are infected by a protandrous, semelparous, castrator that affects only female function; this parasite is largely unexplored but potentially strongly impacts barnacle ecology. In this thesis, I addressed basic questions concerning the ecology of this host-parasite system.

First, I explored behavioral defenses of the barnacle host, Chthamalus fissus, versus its isopod parasite, Hemioniscus balani. I found when infectious stages were present, barnacles decreased filtration rate by ~ 50% when they were at high risk of infection. Barnacles not at risk did not respond to the presence of an infectious stage. The difference in response based on barnacle condition implies a high cost of reduced feeding as a parasite avoidance behavior.

Second, I explored how barnacle sex allocation varied with size, and how this differential allocation affected patterns of parasitism. The barnacle host is hermaphroditic, where gender is not fixed and individuals allocate variable energy to male or female functions. Since the parasite requires ovarian fluid, only barnacles with female reproductive function should be appropriate hosts. We documented a unimodal relationship between barnacle size and female reproductive function. This female function-size relationship was mirrored by patterns of parasitism. Further, we found within the subset of suitable hosts, parasitism increased with size.

Third, I explored spatial patterns of parasitism in the field as mediated by parasite predators. I investigated whether a sea anemone, protects an associated barnacles from parasitism. Barnacles associated with anemones had reduced parasitism and higher reproductive productivity than did barnacles remote from sea anemones. In the laboratory, anemones readily consumed the transmission stage cryptoniscus larvae of the parasite. Hence, anemone consumption of parasite transmission stages may provide a mechanism by which community context regulates, and in this case reduces, parasitism at a local scale.

The brown box crab, Lopholithodes foraminatus, is a deepwater crab that is found along the eastern Pacific Coast. Historically, landings in California have been low for this species, but an increase in fishing pressure prompted the state to designate it as an emerging fishery and implement an experimental fishery program for it. With no known biological studies on brown box crab in California, gathering essential fisheries information to evaluate the feasibility of a targeted fishery is necessary. We investigated the reproductive capacity of the brown box crab in southern California. From 2018 – 2021 brown box crabs were collected monthly from fishermen. Size at sexual maturity was determined by presence/absence of mature gonads (physiological), relative growth of the chela for males and abdomen width for females (morphometric), and presence/absence of eggs on females (functional). We found that females reach physiological maturity at a carapace width between 50.8 mm and 71.7 mm, and males between 43.3 mm and 66.3 mm. Morphometric maturity analysis showed a clear inflection point of abdomen width between immature and mature females. Females were 50% functionally mature at 75 mm carapace width. Morphometric and functional maturity was not detected for males, albeit samples of small male crabs were extremely limited thus warranting further study. Females followed a biennial reproduction pattern, mating in the fall followed by an 18-month brooding period with hatching the following spring. Fecundity was positively related to size and ranged from 8,352 and 62,181 eggs per female for crabs measuring 67.8 to 130.5 mm carapace width, respectively. These findings provide biological information that can inform the evaluation of a fishery for the brown box crab, including potential management strategies and models for assessing stock condition.  

Emerging infections in both humans and wildlife can often be traced back to human mediated changes in host densities, host communities, and the environment. In Chapter 1, I reviewed how humans affect wildlife nematodes. Nematode responses to human actions vary, thus knowing host and parasite natural history, and the mechanisms underlying disease dynamics are critical for predicting parasite responses and managing disease.

Among wildlife nematodes, raccoon roundworm (Baylisascaris procyonis) is infamous for its ability to cause fatal disease in both humans and wildlife. This parasite infects millions of raccoons in North America. Although adult worms cause little pathology in raccoons, larval worms undergo extensive tissue migrations in other hosts, often causing neurological damage. Disease risk is driven by environmental egg contamination, which increases with raccoon density, worm intensity, and worm prevalence. In Chapter 2, I examined 189 raccoons from southern California to investigate how host age and season affect parasite abundance, demography, and fecundity. Roundworm infected 90% of Santa Barbara County raccoons, juveniles hosted more worms than adults, and more heavily infected raccoons released more eggs.

In Chapter 3, I investigated whether animals can avoid raccoon roundworm contaminated sites, and if such avoidance balances disease costs and foraging preferences. Using wildlife cameras, I monitored animal behavior at raccoon latrines — sites that concentrate both seeds and pathogenic parasite eggs, and found that latrine contact rates reflected background activity, diet preferences and disease risk. Disease-tolerant raccoons and rats displayed significant site attraction, while susceptible birds and small mammals avoided these high-risk sites.

The introduced black rat, Rattus rattus, occurs throughout the native range of the raccoon roundworm, Baylisascaris procyonis, and frequently forages in latrines. In Chapter 4, I examined the role of these rats and other California rodents in B. procyonis transmission. I surveyed wild rodents for B. procyonis and found that B. procyonis infected R. rattus at intensities more than 100 times greater than loads in co-occurring native Reithrodotomys megalotis and Peromyscus maniculatus. I also conducted scavenger trials using motion activated cameras and found that rodent carcasses were scavenged by opossums, skunks and raccoons, suggesting that these infected rodents, particularly R. rattus, contribute to B. procyonis transmission in this coastal California ecosystem.

Raccoon roundworm infects both rodents and raccoons in southern California, but we know little about infection risk for other species. In Chapter 5, I used information on animal time allocation and behavior to build a model for predicting community-wide exposure risk for raccoon roundworm. This model suggests that larval worms are likely widespread in the animal community and provides a novel non-invasive method for identifying “at-risk” species.

Raccoon roundworm infection can cause devastating pathology in humans, but there is growing evidence that subclinical cases also occur. As there is limited information on the frequency of these subclinical human infections, in Chapter 6 I surveyed 150 adults from California for B. procyonis antibodies. Eleven participants were seropositive suggesting that subclinical infection does occur and that previously undetectable infections warrant further study.