A fundamental goal in ecology and evolutionary biology has been to understand how microevolutionary forces affect the origin and maintenance of mutualisms over ecological and evolutionary time scales. Mutualistic partners vary in the reciprocal benefits they provide, yet the role of partner variation on microevolutionary forces that impact the maintenance of mutualisms is unclear. Using the mutualism between legumes and nitrogen fixing symbionts, my dissertation investigated the ecological and evolutionary consequences of variation in partner quality. In the first experiment, I demonstrate how insect herbivory can change the costs and benefits of associating with exploiters, and that some degree of exploitation from non-beneficial rhizobia can reduce insect herbivory, thus removing the fitness advantage of associating purely with beneficial rhizobia. In the second study, I examine how rhizobia genotype modifies competition between hosts grown in kin and non-kin groups. I show that lower fitness in plant kin groups can simply be a by-product of genetic variance in plant size and non-linear relationships between plant size and fitness. I further show that the symbiotic community can change difference in fitness between kin and non-kin groups independent of these by-product effects. In my last chapter, I provide the first empirical evidence that an important mechanism for mutualism stability-- the ability for hosts to preferentially associate with beneficial rhizobia-- is genetically variable and can evolve in response to exploitation. I also show that host preference for beneficial rhizobia can be maintained in legume populations, even in the absence of exploitation. My dissertation provides insight into the potential evolutionary dynamics of stabilizing mechanisms by suggesting that the agents of selection that affect the level of host exploitation can come from biotic factors other than the exploiters themselves. My dissertation has also shown that inclusion of other ecological interactions, such as herbivory, can provide valuable perspective on fitness effects of symbionts on their hosts, and can even change our fundamental assumptions about the effects of exploitation on host fitness, which has formed the backbone of mutualism theory.

A fundamental goal in ecology and evolutionary biology has been to understand how microevolutionary forces affect the origin and maintenance of mutualisms over ecological and evolutionary time scales. Mutualistic partners vary in the reciprocal benefits they provide, yet the role of partner variation on microevolutionary forces that impact the maintenance of mutualisms is unclear. Using the mutualism between legumes and nitrogen fixing symbionts, my dissertation investigated the ecological and evolutionary consequences of variation in partner quality. In the first experiment, I demonstrate how insect herbivory can change the costs and benefits of associating with exploiters, and that some degree of exploitation from non-beneficial rhizobia can reduce insect herbivory, thus removing the fitness advantage of associating purely with beneficial rhizobia. In the second study, I examine how rhizobia genotype modifies competition between hosts grown in kin and non-kin groups. I show that lower fitness in plant kin groups can simply be a by-product of genetic variance in plant size and non-linear relationships between plant size and fitness. I further show that the symbiotic community can change difference in fitness between kin and non-kin groups independent of these by-product effects. In my last chapter, I provide the first empirical evidence that an important mechanism for mutualism stability-- the ability for hosts to preferentially associate with beneficial rhizobia-- is genetically variable and can evolve in response to exploitation. I also show that host preference for beneficial rhizobia can be maintained in legume populations, even in the absence of exploitation. My dissertation provides insight into the potential evolutionary dynamics of stabilizing mechanisms by suggesting that the agents of selection that affect the level of host exploitation can come from biotic factors other than the exploiters themselves. My dissertation has also shown that inclusion of other ecological interactions, such as herbivory, can provide valuable perspective on fitness effects of symbionts on their hosts, and can even change our fundamental assumptions about the effects of exploitation on host fitness, which has formed the backbone of mutualism theory.

Thesis (Ph. D.)--Miami University, Dept. of Botany, 2005. / Title from second page of PDF document. Includes bibliographical references.

Múltiplos fatores determinam as interações entre espécies em redes ecológicas, tais como as barreiras nas suas morfologias, distribuições espaços-temporais, suas abundâncias relativas e histórias evolutivas. Novos métodos estão tornando possível avaliar a importância relativa desses fatores determinantes. Todavia a capacidade de avaliar a importância das histórias evolutivas das espécies é ainda limitada pela escassez de métodos que permitam incluir informações derivadas de filogenias independentes entre os preditores das interações. Esse estudo objetiva superar essa limitação através da inclusão das histórias evolutivas das espécies entre os potenciais determinantes das interações, permitindo a análise comparativa das suas importâncias como estruturadores das redes ecológicas. Usando conceitos dos campos de redes ecológicas e da ecofilogenia foram hipotetizados possíveis cenários filogenéticos preditores das frequências de interações. Para ilustrar o uso desses cenários foi usada a base de dados de uma rede beija-flor-planta da Mata Atlântica do sudeste brasileiro, e foram avaliadas as importâncias relativas das histórias evolutivas das espécies, suas abundâncias e acoplamentos nas suas morfologias e fenologias como determinantes das suas frequências de interações. Os resultados sugerem que as histórias evolutivas de beija-flores e plantas são mais importantes do que as suas abundâncias relativas em estruturar a rede, mas são menos importantes do que barreiras morfológicas e fenológicas. Com o uso de cenários filogenéticos, é oferecida uma extensão de um arcabouço conceitual e metodológico já amplamente utilizado por representar uma forma robusta e flexível de testar a importância de múltiplos fatores e suas combinações como determinantes das interações entre espécies em comunidades. / Multiple factors determine species interactions in ecological networks, such as morphological barriers, spatio-temporal distributions, relative species abundance and their evolutionary history. Novel methods are making it possible to evaluate the relative importance of each of these determinants factors. However, the lack of methods that allow us to incorporate information from independent phylogenies among the predictors of interactions limits our capacity of evaluating the relative importance of evolutionary histories. This work aims to overcome this limitation by including the evolutionary histories of species among the potential determinants of interactions, allowing the comparative analysis of its importance in structuring ecological networks. Different possible phylogenetic scenarios were hypothesized to predict frequencies of species interactions by combining concepts from the fields of ecological networks and ecophylogenetics. The usage of these scenarios is illustrated in a hummingbird-plant interaction network database from the Atlantic Forest in southeastern Brazil, in order to evaluate the relative importance of evolutionary histories of species, species relative abundances, and morphological and phenological barriers as determinants of species interactions frequencies. The results suggests that evolutionary histories of hummingbirds and plants are more important than their relative abundances in structuring their interaction network, but less important than morphological and phenological barriers. Phylogenetic scenarios usage offers an extension to a conceptual and methodological framework widely used by representing a robust and flexible way to evaluate the relative importance of multiple factors and their combinations as determinants of species interactions in communities.

Múltiplos fatores determinam as interações entre espécies em redes ecológicas, tais como as barreiras nas suas morfologias, distribuições espaços-temporais, suas abundâncias relativas e histórias evolutivas. Novos métodos estão tornando possível avaliar a importância relativa desses fatores determinantes. Todavia a capacidade de avaliar a importância das histórias evolutivas das espécies é ainda limitada pela escassez de métodos que permitam incluir informações derivadas de filogenias independentes entre os preditores das interações. Esse estudo objetiva superar essa limitação através da inclusão das histórias evolutivas das espécies entre os potenciais determinantes das interações, permitindo a análise comparativa das suas importâncias como estruturadores das redes ecológicas. Usando conceitos dos campos de redes ecológicas e da ecofilogenia foram hipotetizados possíveis cenários filogenéticos preditores das frequências de interações. Para ilustrar o uso desses cenários foi usada a base de dados de uma rede beija-flor-planta da Mata Atlântica do sudeste brasileiro, e foram avaliadas as importâncias relativas das histórias evolutivas das espécies, suas abundâncias e acoplamentos nas suas morfologias e fenologias como determinantes das suas frequências de interações. Os resultados sugerem que as histórias evolutivas de beija-flores e plantas são mais importantes do que as suas abundâncias relativas em estruturar a rede, mas são menos importantes do que barreiras morfológicas e fenológicas. Com o uso de cenários filogenéticos, é oferecida uma extensão de um arcabouço conceitual e metodológico já amplamente utilizado por representar uma forma robusta e flexível de testar a importância de múltiplos fatores e suas combinações como determinantes das interações entre espécies em comunidades. / Multiple factors determine species interactions in ecological networks, such as morphological barriers, spatio-temporal distributions, relative species abundance and their evolutionary history. Novel methods are making it possible to evaluate the relative importance of each of these determinants factors. However, the lack of methods that allow us to incorporate information from independent phylogenies among the predictors of interactions limits our capacity of evaluating the relative importance of evolutionary histories. This work aims to overcome this limitation by including the evolutionary histories of species among the potential determinants of interactions, allowing the comparative analysis of its importance in structuring ecological networks. Different possible phylogenetic scenarios were hypothesized to predict frequencies of species interactions by combining concepts from the fields of ecological networks and ecophylogenetics. The usage of these scenarios is illustrated in a hummingbird-plant interaction network database from the Atlantic Forest in southeastern Brazil, in order to evaluate the relative importance of evolutionary histories of species, species relative abundances, and morphological and phenological barriers as determinants of species interactions frequencies. The results suggests that evolutionary histories of hummingbirds and plants are more important than their relative abundances in structuring their interaction network, but less important than morphological and phenological barriers. Phylogenetic scenarios usage offers an extension to a conceptual and methodological framework widely used by representing a robust and flexible way to evaluate the relative importance of multiple factors and their combinations as determinants of species interactions in communities.

The decline in range and density of many native New Zealand birds from mammalian predation has raised concerns over the functioning of ecosystem processes such as pollination and seed dispersal. At Maungatautari, almost all mammalian pests have been eradicated from within a pest-proof fence enclosing 3400 ha of native forest. I examined whether Maungatautari is restoring pollination and seed dispersal services to native plants, compared to a nearby non-treatment site, Pirongia Mountain. Five-minute bird counts made at Maungatautari and Pirongia (in 2002 and 2005 prior to pest eradication from Maungatautari, and in 2008 and 2010 following eradication) indicated that 10 of the 12 individual bird species examined showed significant changes in abundance following pest control. Six species showed an increase in abundance, including bellbirds (Anthornis melanura), tui (Prosthemadera novaeseelandiae) and kereru (Hemiphaga novaeseelandiae). Counts of all native species combined increased at Maungatautari while counts of all exotic species showed no trend over count years. In December 2010, 140 five-minute bird counts showed tui and bellbirds, key pollinators, to be more abundant at Maungatautari than Pirongia. Higher pollen loads on the stigmas of both female and hermaphrodite Fuchsia excorticata flowers at Maungatautari, compared to Pirongia, suggest that F. excorticata at Maungatautari received better pollination service. Fuchsia excorticata pollen loads collected from 67 sites around New Zealand indicate that female plants at sites with lower abundances of mammalian predators generally received better pollination service. Hermaphrodite F. excorticata plants had similar and high pollen scores in all regions, except for in the North Island. Five-minute bird counts in December 2010 also showed that kereru and blackbirds (Turdus merula), key seed dispersers along with tui and bellbirds, were more abundant at Maungatautari than Pirongia. A second measure of bird abundance, maximum counts, showed flock sizes of tui, bellbirds and kereru were larger at Maungatautari, but only significantly so for tui and bellbirds. Fuchsia excorticata fruits were removed more rapidly from plants at Maungatautari than at Pirongia (a 6-fold difference). There was twice the density of tawa fruits (bird cleaned and fleshy) under trees at Maungatautari compared to Pirongia, perhaps from reduced mammalian fruit predation. There was no significant site effect on tawa dispersal service (percent of fruit consumed by birds), but a significant site x fruit density interaction, suggests birds at Maungatautari provided better dispersal service to large fruit crops. A similar number of miro fruit (bird cleaned and fleshy) were caught in seed traps under miro trees, but a greater percentage of fruits were consumed by birds at Maungatautari (59%) compared to Pirongia (26%). The results from this thesis indicate that increased densities of key native birds at Maungatautari are providing better pollination and dispersal services to the native plants examined. Projects which increase the density of key bird mutualists, such as tui, bellbirds and kereru, on the mainland, may have positive benefits for pollination and seed dispersal mutualisms.

Widespread anthropogenic invasions have prompted concerns that naturalized organisms could threaten biodiversity. In particular, invasive weeds can negatively affect native biota through a variety of means, including disrupting mutualisms. This thesis was designed to observe and test dispersal mutualisms in a native forest during autumn when the majority of plant species are fruiting. In this thesis I examined whether the invasive plant barberry (Berberis glaucocarpa) was influencing the behaviour of a native frugivore bellbird (Anthornis melanura) and a range of dispersal related services in a native forest, Kowhai Bush near Kaikoura. To test these 18 banded bellbirds were followed through autumn 2011. These observe bellbirds were split between control and test bird. Barberry fruit was removed from the test bird territories. I recorded whether bellbirds changed their territory sizes, foraging and daily behaviours. During 52 hours of observations, bellbirds were never observed feeding on barberry fruit. No significant changes to bellbird behaviour or territories were observed after the removal of barberry fruit. Bellbird diet overall was dominated by invertebrates (83% of foraging observations), with smaller contributions from fruit (16%, nearly all on Coprosma robusta), nectar and honeydew. Since bellbirds did not eat barberry fruit, removal of this weed is unlikely to negatively affect bellbirds during autumn. Which other bird species were dispersing barberry was recorded. I recorded 242 hours of videotape footage on 24 fruiting plants. A total of 101 foraging events were recorded of 4 different bird species: silvereyes (Zosterops lateralis) 42 visits, blackbirds (Turdus merula) 27 visits, song thrush (Turdus philomelos) 29, and starlings (Sturnus vulgaris) 3 visits. The species differed in the mean length of time they spent in plants, so the overall contribution to barberry fruit removal was 32.6% silvereyes, 24.3% blackbirds, 42.9% song thrush and 0.1% starlings. To find out the relative contribution of exotic and native birds to dispersal of fruits in Kowhai Bush, I mist-netted 221 birds of 10 species and identified any seeds in the 183 faeces they deposited. A total of 21 plant species were observed fruiting in Kowhai Bush during this time. A total of 11 different plant species were identified from 1092 seeds. Birds were further observed feeding on 3 other plant species which were not observed in faecal samples. This left 7 plants with unobserved dispersal vectors. There were likely four main dispersers, bellbirds, silvereyes, song thrush and blackbirds and five minor, brown creeper (Mohoua novaeseelandiae), tui (Prosthemadera novaeseelandiae), fantails (Rhipidura fuliginosa), dunnock (Prunella modularis) and starlings. However there was considerable variability between these bird species dispersal abilities. Introduced birds’ song thrush and blackbirds were observed dispersing naturalized plant seeds at higher than expected rates in comparison to native frugivores bellbirds and silvereyes. I also measured the gape sizes on mist netted birds and on samples of fruit from Kowhai Bush. Both silvereyes and bellbirds were found to be eating fruit larger than their gape, but despite this two native (Hedycarya arborea and Ripogonum scandens) and three exotic plants (Vitis vinifera, Taxus baccata and Crataegus monogyna) had large fruit that were probably mainly dispersed by song thrush and blackbirds. Hence, introduced birds were important seed dispersers for large fleshy fruited seeds in Kowhai Bush. Demonstrating that interactions among native and exotic flesh fruited plants and frugivores is important within forest communities.

Obligate nursery pollination mutualisms such as the fig–fig wasp system, with their central plant–pollinator mutualism associated with non-pollinating satellite wasp species, can function as closed system microcosms representative of tritrophic communities. In this system, enclosed inflorescences (syconia) function as sites of seed production, as well as brood-sites for the progeny of herbivorous mutualistic pollinators, non-pollinating gallers and parasitoids of the two. Plant reproductive traits such as inflorescence size (syconium volume) and within-plant phenology (within-tree asynchrony) as can affect inter-species relationships among the three trophic levels in such plant–herbivore–parasitoid systems. Induced or natural variations in such plant traits could influence various direct and indirect effects among the organisms in the community and could even lead to the formation of feedback cycles. Furthermore, changes in the abiotic environment could have major impacts on the biotic associations in the system either by affecting the community members directly, or through their effects on plant reproductive traits. Ficus racemosa with its fig wasp community comprised of a single herbivorous pollinator mutualist, three non-pollinating parasitic gallers and three non-pollinating parasitoids was used as a model to investigate: (1) the role of mutualistic and parasitic fig wasps in affecting within-tree phenology; (2) direct and indirect biotic associations between various groups of fig wasps (pollinators, gallers and parasitoids) and the influence of inflorescence size and within-tree phenology on them; and (3) variations in the reproduction of and the biotic associations between the organisms of the community under variable abiotic climatic conditions. Patterns of plant reproductive phenology are usually considered evolved responses directed at optimizing resource use, pollen receipt/donation schedules and seed dispersal for plant individuals. Within-plant reproductive synchrony or asynchrony can arise due to variation in floral initiation patterns, as well as from localised proximate mechanistic responses to interactants such as pollinators, parasites and herbivores which could affect floral longevity or fruit development time. The investigation was begun by exploring the role of a mutualistic pollinator, and for the first time in a brood-site mutualism, that of parasitic herbivores (gallers) and parasitoids in influencing within-plant reproductive phenology. Since a syconium functions as an inflorescence which develops into a fruit after pollination, investigations were carried out on the impact on syconium synchrony of fig wasps that began their development within the brood site syconium at pre-pollination, pollination, and post-pollination stages via their effects on the development time of individual syconia in Ficus racemosa. We found that syconium initiation patterns were not the only proximate mechanism for within-tree reproductive asynchrony, and that individual syconia (even within a tree) had highly plastic development times dependent on their sizes, pollination time and the species of wasp progeny developing within them. Syconium volume, pollination early in the pollen-receptive phase and presence of early-ovipositing galler progeny reduced syconium development time, whereas the presence of late-ovipositing parasitoid progeny or pollination late in the pollen-receptive phase increased syconium development time. These results suggest an ongoing tug-of-war between syconium inhabitants to modify syconium development times. Parasitic fig wasps pull in different directions to suit their own needs, such that final syconium development times are likely to be a compromise between conflicting demands from developing seeds and from different wasp species. Inter-species relationships among the three trophic levels in plant–herbivore–parasitoid systems can potentially include various direct and indirect effects possibly mediated by induced or natural variations in plant traits. Analysing the seed and fig wasp compositions of microcosm replicates, i.e. individual syconia, shows that besides direct competition for resources and predator–prey interactions, the F. racemosa community also displays exploitative or apparent competition and trait-mediated indirect interactions. Syconium volume and within-tree asynchrony were reproductive plant traits that not only affected plant–herbivore and plant–parasitoid associations, but also possibly modified herbivore–herbivore and herbivore–parasitoid interactions. Our results also indicated that the reciprocal effects of higher trophic level fauna on plant traits (and vice versa) within this system drive a positive feedback cycle between syconium inhabitants and within-tree reproductive asynchrony. In the F. racemosa system, abiotic environmental factors could affect the reproduction of mutualistic pollinators, non-mutualistic parasites and seed production via seasonal changes in plant reproductive traits such as syconium volume within-tree asynchrony. Temperature, relative humidity and rainfall defined four seasons: winter; hot days, cold nights; summer and wet seasons. Syconium volumes were highest in winter and lowest in summer, and affected syconium contents positively across all seasons. Greater transpiration from the nurseries was possibly responsible for smaller syconia in summer. The 3–5°C increase in mean temperatures between the cooler seasons and summer reduced fig wasp reproduction and increased seed production nearly two-fold. Yet, seed and pollinator progeny production were never negatively related in any season confirming the mutualistic fig–pollinator association across seasons. Parasites affected seed production negatively in some seasons, but had a surprisingly positive relationship with pollinators in most seasons. While within-tree reproductive phenology did not vary across seasons, its effect on syconium inhabitants varied with season. In all seasons, within-tree reproductive asynchrony affected parasite reproduction negatively, whereas it had a positive effect on pollinator reproduction in winter and a negative effect in summer. Seasonally variable syconium volumes probably caused the differential effect of within-tree reproductive phenology on pollinator reproduction. Within-tree reproductive asynchrony itself was positively affected by intra-tree variation in syconium contents and volume, creating a unique feedback loop which varied across seasons. Therefore, nursery size affected fig wasp reproduction, seed production and within-tree reproductive phenology via the feedback cycle in this system. Climatic factors affecting plant reproductive traits can cause biotic relationships between plants, mutualists and parasites to vary seasonally and must be accorded greater attention, especially in the context of climate change.