In this thesis I investigated the importance of plant-animal mutualisms to the reproductive success of three West African mistletoe species in two genera, Globimetula braunii, Agelanthus brunneus and A. djurensis, in Ngel Nyaki Forest Reserve, Nigeria. The flowers of all three mistletoes were visited by 3 - 4 species of sunbird. Agelanthus flowers were also visited by honeybees (Apis mellifera) and a small social wasp species (Vespinae). A. mellifera appeared to be robbing nectar from the flowers of A. brunneus. To investigate the relative role of pollinators, I compared flower opening and fruit set amongst bagged, caged, natural, hand-selfed and hand-crossed treatments. The flowers of G. braunii were able to selfopen on average 66% of the time when pollinators were excluded, whereas pollinators were essential to the flower opening mechanism of both Agelanthus spp. Insects were as effective at opening the flowers of Agelanthus spp. as sunbirds. However, flower opening ability did not translate directly into pollination effectiveness, as insect access alone did not result in significantly higher fruit set than that observed under the bagged condition. There was no significant evidence for autonomous selfing within any of the three mistletoes and thus reproduction was almost entirely reliant on 3 – 4 species of sunbird. Hand-pollinations of all three species indicated a high level of self-compatibility, and in one species, G. braunii, pollen limitation was evident (PLI = 0.504). To investigate dispersal mutualisms amongst the three mistletoe species, fruit ripening and removal were monitored. The fruits of all three mistletoe species appeared to be removed rapidly from plants as they ripened, with few ripe or overripe fruits present on the branches at any time. Dispersal efficiency, or the total proportion of fruit crop removed across the fruiting season, was also very high (>90%) for the Agelanthus spp. but lower in G. braunii, for which almost a third of the total fruit crop was recorded undispersed in fruit nets beneath plants. Mistletoes are an important component of West African montane forests. Disruption to mistletoe reproductive mutualisms may affect not only mistletoes and their mutualists directly, but also an entire network of species, all linked within a web of interactions. To protect these ecosystems from further degradation, increased community involvement and greater enforcement of laws set out to manage montane forest habitat across the region is essential. Without this support, the future of these ecosystems and the web of interacting species within remains tenuous.

Seed dispersal mutualisms, including seed dispersal by ants, are critical to the assembly of communities and the function of ecosystems. However, the consequences of human-caused global change factors, such as habitat fragmentation and climate change, for the future of these mutualisms are not fully understood. My dissertation consists of five chapters that investigated the effects of habitat fragmentation and climate change on ants and their seed dispersal mutualisms. Chapter 1 is an introduction that provides background information on habitat fragmentation and anthropogenic climate change and their impacts on biodiversity. In Chapter 1, I also introduce my study system of ant-mediated seed dispersal mutualisms, myrmecochory. My next two chapters (Chapters 2 and 3) explored the effects of reconnecting fragmented habitat patches with corridors in restored longleaf pine savanna systems in South Carolina. We used a landscape scale experiment to investigate how reducing isolation affects the assembly of ant communities over time (Chapter 2) and seed dispersal of the myrmecochorous forb, Piriqueta cistoides (Chapter 3). For Chapter 2, we found evidence that both habitat connectivity and edge effects underly the effects of corridors on ant communities over time. We found that connected patches accumulated ant species faster than isolated patches over time suggesting that corridors function by facilitating colonization. We also found evidence that edge effects play a role with greater ant functional group diversity in patches with higher edge than patches with lower edge amounts. For Chapter 3, we also found evidence of corridor and edge effects with ants dispersing seeds of P. cistoides longer distances in patches connected via corridors than isolated patches, but only in the center of patches. In Chapter 4, we investigated the effects of predicted climate change scenarios for seed dispersal mutualisms in eastern deciduous forests. For this chapter, we conducted a mesocosm experiment in which we crossed temperature with altered precipitation magnitude and frequency. Our mesocosms contained a common spring ephemeral wildflower, Sanguinaria canadensis, and whole colonies of their mutualist seed disperser, Aphaenogaster rudis. This design allowed us to collect high-resolution data on how ants interacted with seeds under different climate change scenarios that incorporated warming temperatures and altered precipitation. We found that warming effects depended on the precipitation treatment with negative effects of warming on the collection of seeds by ants under historical precipitation regimes and positive effects of warming under simulated precipitation conditions altered under predicted climate change. Finally, Chapter 5 describes my general conclusions from this body of work. Taken together, the research making up my dissertation provides valuable insights into how changing environmental conditions under habitat fragmentation and climate change may alter ant seed dispersal mutualisms. Importantly, we often found that the impacts of global change were context dependent and that our experiments were important tools in disentangling that context dependency. Further, this work demonstrates the value of understanding the basic ecology of the interactions among organisms. Understanding the natural history of organisms across changing environmental conditions will benefit the ways in which we conserve and restore ecosystems in a fragmented and warmer world. / Doctor of Philosophy / Most plants and animals engage in mutualisms, which are interactions between species in which both benefit from interacting with each other. The focus of this dissertation are the impacts of human-caused environmental change on the mutualism between ants and plants in which ants move a plant's seeds. The dispersal of ant-dispersed plants is considered a mutualism because the ants receive a food reward in the form of a fat- and protein-rich appendage that grows on the seed while the seeds of the plant get moved to a better location for germination. The mutualisms between ants and the plants they disperse are critical to how plants are distributed in many ecosystems, yet the consequences of human-caused environmental change, such as habitat loss and climate change, for these mutualisms are not fully understood. My dissertation consists of five chapters that investigated the effects of habitat fragmentation (the breaking apart of larger habitats into smaller, more isolated patches as a result of habitat loss) and climate change on ants and their seed dispersal mutualisms. My first chapter introduces background on the consequences of habitat fragmentation and climate change on organisms, ant seed dispersal mutualisms, and the potential effects of altered environmental conditions on seed dispersal by ants. My second two chapters (Chapters 2 and 3) explored the effects of reconnecting isolated habitat patches with habitat corridors (strips of habitat restored between the isolated habitat patches). In restored longleaf pine savanna systems in South Carolina, we used a long-term, landscape scale experiment to study how increasing connectivity and changing the shape of habitats via corridors affects ant community diversity over time (Chapter 2) and seed dispersal of the ant-dispersed plant, pitted stripeseed (Piriqueta cistoides) (Chapter 3). For Chapter 2, we found both habitat connectivity and patch shape effects underly the effects of corridors on ant community over time. We found that connected patches accumulated ant species faster than isolated patch types which suggests that corridors may function by facilitating colonization into the patches they connect. We also found evidence that patch shape plays a role in supporting greater ant functional group diversity in patches with greater perimeter (more edge habitat) than patches with less perimeter (less edge habitat). We found that ants in patches with more edge habitat represented a greater number of functional groups, which are categories that describe the roles ants play in ecosystems. For Chapter 3, we also found evidence of corridor and patch shape effects with ants dispersing seeds of pitted stripeseed longer distances in patches connected via corridors than isolated patches, but only in the center of patches. In Chapter 4, we investigated the effects of predicted climate change scenarios on seed dispersal mutualisms in eastern deciduous forests. For this chapter, we conducted an experiment in which we crossed temperature with altered precipitation in mesocosms, which are small, simulated ecosystems that allowed us to investigate the effects of warming and altered precipitation in a controlled setting. Our mesocosms contained a common spring ephemeral wildflower, bloodroot (Sanguinaria canadensis), and whole colonies of their mutualist seed disperser, winnow ants (Aphaenogaster rudis). We found that the effects of warming temperatures depended on the precipitation treatment. Warming had a negative effect on the number of seeds collected by ants under historical precipitation regimes, but a positive effect under simulated precipitation conditions under predicted climate change (higher in magnitude and lower in frequency). Finally, Chapter 5 describes my general conclusions from this body of work. Taken together, the research making up my dissertation provides valuable insights into how changing environmental conditions under habitat fragmentation and climate change may alter ant seed dispersal mutualisms. Importantly, we often found that the impacts of global change were context dependent. Our experiments were important tools in disentangling that context dependency. Further, this work demonstrates the value of understanding the basic ecology of the interactions among organisms. Understanding the natural history of organisms, especially their responses to changing environmental conditions, will ultimately benefit the ways in which we conserve and restore ecosystems in a fragmented and warmer world.

Ecological interactions such as predation, competition, and mutualism are important forces that influence species evolution. Coevolution is defined as reciprocal evolutionary change in interacting species. The Geographic Mosaic Theory of Coevolution (GMTC) provides a theoretical framework to explain how collections of populations should coevolve across space. Two fundamental aspects of the GMTC are gene flow among populations and the presence of selection mosaics, which are collections of localities with particular selection regimes. Several studies have explored how phenotypic trait matching between species evolves in pairs or small groups of species. However, ecological interactions frequently form large networks that connect dozens of species present in a given community. In networks of mutualisms, for instance, the organization of interactions may affect ecological and evolutionary processes. A next step in understanding the coevolutionary process is to investigate how aspects of the GMTC affect the evolution of species embedded in interaction networks. In this dissertation, we tried to fill this gap using a mathematical model of coevolution, complex networks tools, and information on empirical mutualistic networks. Our numerical simulations of the coevolutionary model allow us to draw three main conclusions. First, gene flow affects trait patterns generated by coevolution and may favor the emergence of trait matching depending on the selection mosaic. Second, the organization of mutualistic networks influences coevolution, but this effect may vanish when gene flow favors trait matching. Intimate mutualisms, such as protection of host plants by ants, form small and compartmentalized networks that generate higher trait matching than large and nested networks typical of mutualisms among free-living species, such as pollination. Third, habitat fragmentation resulting in the disruption of gene flow should reduce the reciprocal adaptations between interacting species and at the same time promote adaptations to the local abiotic environment. In conclusion, we show that a complex interplay between gene flow, the geographic structure of selection, and the organization of ecological networks shapes the evolution of large groups of species. Our results therefore allow predictions of how environmental impacts such as habitat fragmentation will modify the evolution of species interactions / Interações ecológicas como predação, competição e mutualismo são importantes forças que influenciam a evolução de espécies. Chamamos de coevolução a mudança evolutiva recíproca em espécies que interagem. A Teoria do Mosaico Geográfico da Coevolução (TMGC) fornece um arcabouço teórico para entender como conjuntos de populações coevoluem ao longo do espaço. Dois aspectos fundamentais da TMGC são o fluxo gênico entre populações e a presença de mosaicos de seleção, isto é, conjuntos de locais com regimes de seleção particulares. Diversos estudos exploraram como o acoplamento entre fenótipos de diferentes espécies evolui em pares ou pequenos grupos de espécies. Entretanto, interações ecológicas frequentemente formam grandes redes que conectam dezenas de espécies presentes em uma comunidade. Em redes de mutualismos, por exemplo, a organização das interações pode influenciar processos ecológicos e evolutivos. Um próximo passo para a compreensão do processo coevolutivo consiste em investigar como aspectos da TMGC influenciam a evolução de espécies em redes de interações. Nesta dissertação, tentamos preencher esta lacuna usando um modelo matemático de coevolução, ferramentas de redes complexas e informação sobre redes mutualistas empíricas. Nossas simulações numéricas do modelo coevolutivo apontam para três principais conclusões. Primeiro, o fluxo gênico influencia os padrões fenotípicos gerados por coevolução e pode favorecer a emergência de acoplamento fenotípico entre espécies dependendo do mosaico de seleção. Segundo, a organização de redes mutualistas influencia a coevolução, mas este efeito pode desaparecer quando o fluxo gênico favorece acoplamento fenotípico. Mutualismos íntimos, como proteção de plantas hospedeiras por formigas, formam redes pequenas e compartimentalizadas que geram um maior acoplamento fenotípico do que as redes grandes e aninhadas típicas de mutualismos entre espécies de vida livre, como polinização. Por fim, a fragmentação de habitat, ao extinguir o fluxo gênico, pode reduzir as adaptações recíprocas entre espécies e ao mesmo tempo tornar cada espécie mais adaptada ao seu ambiente abiótico local. Em suma, mostramos que interações complexas entre fluxo gênico, estrutura geográfica da seleção e organização de redes ecológicas moldam a evolução de grandes grupos de espécies. Dessa forma, podemos traçar previsões sobre como impactos ambientais como a fragmentação de habitat irão alterar a evolução de interações ecológicas

Several aspects of plant-pollinator interactions are presented in the thesis. It contains a review on the open questions of plant-pollinator interactions from single species to complex networks. The following sections document novel results. Firstly, the conservation of complex pollination networks is addressed through the hierarchy of species' importance. In addition, the habitat requirements and interactions of a threatened rare pollinator species are explored. In the following chapters, the results from manipulative approaches applied in the field to plant-pollinator interactions are presented. The effect of pollinator's population decline on pollinators' foraging for pollen is investigated. Moreover, the way plant species loss impact several aspects of pollinator visitation is presented. Lastly, the impact of species removal on plant-pollinator network topology and on species ability of establishing new interactions is investigated.

Ants are ubiquitous in most communities and many form opportunistic mutualisms with honeydew-producing hemipterans (e.g. treehoppers). Hemipterans excrete honeydew, a carbohydrate rich substance, that ants harvest and, in return, ants protect their honeydew-producing partners from parasitoids, predators, and competitors. Given the efficacy of tending ants in removing hemipteran antagonists, and the strong roles that ants play within their communities as predators, competitors, and seed dispersers, surprisingly little is known of the effects of ant-hemipteran mutualisms (AHM) on the invertebrate communities in which they are embedded or on the plants that host AHM. Using observational and manipulative field experiments, I examined the long-term effect of AHM on their host plant’s, honey mesquite (Prosopis glandulosa), reproductive potential and quality. In addition, I measured how the presence of AHM affects the abundance, richness, diversity, and composition of the invertebrate communities living on honey mesquite. Plants hosting AHM may indirectly benefit (through the removal of herbivore arthropods) or suffer (through the loss pollinators) due to the defensive behavior of tending ants. To determine the effects of AHM on their host plant, I established a four-year press experiment in which I removed AHM from 50 randomly trees, while leaving 50 as controls. In addition, I marked and followed 30 trees from which AHM were naturally absent. To assess if mesquite quality differed between trees hosting AHM and trees in which AHM were naturally absent, in 2012 I assayed foliar condensed tannin concentrations, a secondary defense compound, and, in 2015, I measured foliar nitrogen, phosphorous, potassium, magnesium, and iron as they are essential for growth and reproduction. I compared the reproductive potential between AHM present and removed trees by counting flowers and fruits across all 4 years of the study. Mesquite that hosted AHM contained significantly less condensed tannins and significantly higher concentrations of N%, Mg, and Fe. Furthermore, over the duration of the study mesquite hosting AHM contained significantly more flowers than those from which AHM were removed or naturally absent. My results indicate that AHM select trees of high quality and their continued presence is associated with high levels of reproductive potential. Most studies that have evaluated community-level effects of AHM compare total abundance and species richness in communities (or host plants) with and without AHMs. However, both measures are dependent on sampling effort, complicating comparisons across different studies. To examine the effects of AMH on the arthropod community in mesquite, I first compared family richness and alpha diversity using standardized rarefaction and extrapolation curves. I then measured beta diversity and turnover in community composition from one year to the next. The removal of AHM increased invertebrate diversity and significantly altered community composition. Although treatments did not statistically differ in turnover rates, replacements occurred among treatments at the family level which may be biologically meaningful. Furthermore, herbivore and predator populations increased, and pollinator populations decreased following the removal of AHM. These results suggest that the presence of AHM can alter the composition of arthropod communities and food-web dynamics. However, these effects were significant in some years and not others, suggesting the importance of temporal variation in drivers of communities. Overall, my work demonstrates that AHM can be drivers of community composition and illustrate the importance of examining their effects across multiple seasons.

Cooperation is pervasive in nature but paradoxically also provides opportunity to cheaters. My dissertation involves the study of both cooperation and conflict in two species of Megalopta bees. Megalopta is a Neotropical genus of halictid bees whose biology is characterized by complex life cycles that can range from solitary to eusocial. These bees nest in dead wood and forage under dim light conditions. Megalopta’s nests are inhabited by an extensive array of organisms and each nest therefore constitutes a miniature ecosystem providing opportunities for cooperation and conflict, both within and between species. I first delineate the social structure of M. genalis and M. ecuadoria nests in several Panamanian populations and integrate the factors that play a role in the behavioral decisions of females when joining a social group or not. Within a kin-selection framework, I discuss how genetic relatedness plays a role in the formation of social nests. Second, I investigate the conflict between host bees and a congener social parasite, and I elucidate reproductive structures that are relevant for understanding the evolution of parasitism. Finally, I describe a cleaning mutualism between Megalopta bees and their mite associates. Bee-mite associations encompass a broad spectrum of interspecific interactions. Some bee-mites are thought to perform cleaning services for their hosts in exchange for suitable environments for reproduction and dispersal. Field observations and experimental manipulation reveal a significant correlation between the presence of mites and the absence of fungi inside the brood cells, as well as between the absence of mites and increased bee mortality. This study therefore provides evidence of the sanitary effect of mites in nests of Megalopta bees. This bee-mite association constitutes one of the few examples of terrestrial cleaning mutualisms. / text

abstract: For interspecific mutualisms, the behavior of one partner can influence the fitness of the other, especially in the case of symbiotic mutualisms where partners live in close physical association for much of their lives. Behavioral effects on fitness may be particularly important if either species in these long-term relationships displays personality. Animal personality is defined as repeatable individual differences in behavior, and how correlations among these consistent traits are structured is termed behavioral syndromes. Animal personality has been broadly documented across the animal kingdom but is poorly understood in the context of mutualisms. My dissertation focuses on the structure, causes, and consequences of collective personality in Azteca constructor colonies that live in Cecropia trees, one of the most successful and prominent mutualisms of the neotropics. These pioneer plants provide hollow internodes for nesting and nutrient-rich food bodies; in return, the ants provide protection from herbivores and encroaching vines. I first explored the structure of the behavioral syndrome by testing the consistency and correlation of colony-level behavioral traits under natural conditions in the field. Traits were both consistent within colonies and correlated among colonies revealing a behavioral syndrome along a docile-aggressive axis. Host plants of more active, aggressive colonies had less leaf damage, suggesting a link between a colony personality and host plant health. I then studied how aspects of colony sociometry are intertwined with their host plants by assessing the relationship among plant growth, colony growth, colony structure, ant morphology, and colony personality. Colony personality was independent of host plant measures like tree size, age, volume. Finally, I tested how colony personality influenced by soil nutrients by assessing personality in the field and transferring colonies to plants the greenhouse under different soil nutrient treatments. Personality was correlated with soil nutrients in the field but was not influenced by soil nutrient treatment in the greenhouse. This suggests that soil nutrients interact with other factors in the environment to structure personality. This dissertation demonstrates that colony personality is an ecologically relevant phenomenon and an important consideration for mutualism dynamics. / Dissertation/Thesis / Doctoral Dissertation Biology 2018

Ecological interactions such as predation, competition, and mutualism are important forces that influence species evolution. Coevolution is defined as reciprocal evolutionary change in interacting species. The Geographic Mosaic Theory of Coevolution (GMTC) provides a theoretical framework to explain how collections of populations should coevolve across space. Two fundamental aspects of the GMTC are gene flow among populations and the presence of selection mosaics, which are collections of localities with particular selection regimes. Several studies have explored how phenotypic trait matching between species evolves in pairs or small groups of species. However, ecological interactions frequently form large networks that connect dozens of species present in a given community. In networks of mutualisms, for instance, the organization of interactions may affect ecological and evolutionary processes. A next step in understanding the coevolutionary process is to investigate how aspects of the GMTC affect the evolution of species embedded in interaction networks. In this dissertation, we tried to fill this gap using a mathematical model of coevolution, complex networks tools, and information on empirical mutualistic networks. Our numerical simulations of the coevolutionary model allow us to draw three main conclusions. First, gene flow affects trait patterns generated by coevolution and may favor the emergence of trait matching depending on the selection mosaic. Second, the organization of mutualistic networks influences coevolution, but this effect may vanish when gene flow favors trait matching. Intimate mutualisms, such as protection of host plants by ants, form small and compartmentalized networks that generate higher trait matching than large and nested networks typical of mutualisms among free-living species, such as pollination. Third, habitat fragmentation resulting in the disruption of gene flow should reduce the reciprocal adaptations between interacting species and at the same time promote adaptations to the local abiotic environment. In conclusion, we show that a complex interplay between gene flow, the geographic structure of selection, and the organization of ecological networks shapes the evolution of large groups of species. Our results therefore allow predictions of how environmental impacts such as habitat fragmentation will modify the evolution of species interactions / Interações ecológicas como predação, competição e mutualismo são importantes forças que influenciam a evolução de espécies. Chamamos de coevolução a mudança evolutiva recíproca em espécies que interagem. A Teoria do Mosaico Geográfico da Coevolução (TMGC) fornece um arcabouço teórico para entender como conjuntos de populações coevoluem ao longo do espaço. Dois aspectos fundamentais da TMGC são o fluxo gênico entre populações e a presença de mosaicos de seleção, isto é, conjuntos de locais com regimes de seleção particulares. Diversos estudos exploraram como o acoplamento entre fenótipos de diferentes espécies evolui em pares ou pequenos grupos de espécies. Entretanto, interações ecológicas frequentemente formam grandes redes que conectam dezenas de espécies presentes em uma comunidade. Em redes de mutualismos, por exemplo, a organização das interações pode influenciar processos ecológicos e evolutivos. Um próximo passo para a compreensão do processo coevolutivo consiste em investigar como aspectos da TMGC influenciam a evolução de espécies em redes de interações. Nesta dissertação, tentamos preencher esta lacuna usando um modelo matemático de coevolução, ferramentas de redes complexas e informação sobre redes mutualistas empíricas. Nossas simulações numéricas do modelo coevolutivo apontam para três principais conclusões. Primeiro, o fluxo gênico influencia os padrões fenotípicos gerados por coevolução e pode favorecer a emergência de acoplamento fenotípico entre espécies dependendo do mosaico de seleção. Segundo, a organização de redes mutualistas influencia a coevolução, mas este efeito pode desaparecer quando o fluxo gênico favorece acoplamento fenotípico. Mutualismos íntimos, como proteção de plantas hospedeiras por formigas, formam redes pequenas e compartimentalizadas que geram um maior acoplamento fenotípico do que as redes grandes e aninhadas típicas de mutualismos entre espécies de vida livre, como polinização. Por fim, a fragmentação de habitat, ao extinguir o fluxo gênico, pode reduzir as adaptações recíprocas entre espécies e ao mesmo tempo tornar cada espécie mais adaptada ao seu ambiente abiótico local. Em suma, mostramos que interações complexas entre fluxo gênico, estrutura geográfica da seleção e organização de redes ecológicas moldam a evolução de grandes grupos de espécies. Dessa forma, podemos traçar previsões sobre como impactos ambientais como a fragmentação de habitat irão alterar a evolução de interações ecológicas

Human domination of global nutrient cycles is profoundly altering our planet. Yet on coral reefs, the effects of changing nutrient regimes have likely been over-simplified. This dissertation investigates the complexity of animal-nutrient interactions at the organismal level and explores how the outcomes of these interactions cascade through levels of biological organization. To do so, I examined the effects of nitrogen (N) and phosphorus (P) on corals and macroalgae, and how these effects in turn influenced reef communities and entire ecosystems. I show that P consistently increases coral growth rates while N has variable, often negative, effects on coral growth. The majority of this variability was explained by the contrasting responses of corals to ammonium, which had negligible effects on coral growth, versus nitrate, which consistently had negative effects on corals. Experimental manipulations of nutrient regimes revealed that these effects could be attributed, in part, to increased damage to the photosynthetic components of the corals’ endosymbionts. Nitrogen and P-enrichment also impacted macroalgae, increasing the nutrient content of algal tissue and in turn, consumption patterns of herbivorous fishes. Initial phase parrotfishes and juvenile surgeonfishes increased their feeding rates on algae rich in N and P respectively. However, adults from both species were irresponsive to algal nutrient content. At the community level, the effects of N and P on corals, algae and herbivory were linked to the development of distinct benthic communities. Algae cover was lower and coral growth rates higher around reef structures that were consistently enriched with N and P excreted by sheltering fishes. At the ecosystem level, I found that the responses of corals to N and P enrichment were similar to those of other nutrient-sharing mutualists. Across terrestrial and marine environments, I show that N and P enrichment consistently decouples mutualism performance, benefiting one partner at the expense of the other. Thus, collectively this dissertation demonstrates that the impacts of global nutrient loading resonate from single organisms through whole ecosystems.

No description available.