Speciation in kleptoparasites of oak gall wasps often correlates with shifts into new tree habitats, tree organs, or gall morphospace.

Host shifts to new plant species can drive speciation for plant-feeding insects, but how commonly do host shifts also drive diversification for the parasites of those same insects? Oak gall wasps induce galls on oak trees and shifts to novel tree hosts and new tree organs have been implicated as drivers of oak gall wasp speciation. Gall wasps are themselves attacked by many insect parasites, which must find their hosts on the correct tree species and organ, but also must navigate the morphologically variable galls with which they interact. Thus, we ask whether host shifts to new trees, organs, or gall morphologies correlate with gall parasite diversification. We delimit species and infer phylogenies for two genera of gall kleptoparasites, Synergus and Ceroptres, reared from a variety of North American oak galls. We find that most species were reared from galls induced by just one gall wasp species, and no parasite species was reared from galls of more than four species. Most kleptoparasite divergence events correlate with shifts to non-ancestral galls. These shifts often involved changes in tree habitat, gall location, and gall morphology. Host shifts are thus implicated in driving diversification for both oak gall wasps and their kleptoparasitic associates.

Historical forest disturbance results in variation in functional resilience of seed dispersal mutualisms.

Mutualistic interactions provide essential ecosystem functions that contribute to promoting and maintaining diversity in ecosystems. Understanding if functionally important mutualisms are "resilient" (i.e., able to resist or recover) to anthropogenic disturbance is essential for revealing the capacity for diversity to recover. Animal-mediated seed dispersal supports plant population growth and influences community structure, and disturbance affecting seed dispersal can contribute to low resiliency of plant diversity. Ant-seed dispersal mutualisms are sensitive to anthropogenic disturbance, as they rely on one to a few high-quality dispersal partners. In North American eastern deciduous forests, ants in the genus Aphaenogaster are "keystone dispersers" of understory forbs adapted to dispersal by ants (myrmecochores), which make up more than one-third of the understory herbaceous community. The majority of forests within this region have regenerated from previous disturbance in the form of clearing for agriculture. Previous studies have revealed that myrmecochore diversity is not resilient to previous clearing. Here, we ask if seed dispersal mutualisms are resilient to historical forest disturbance and if decreases in mutualistic interactions with partners, Aphaenogaster sp., or increases in antagonistic interactions cause degradation of function. In a large-scale natural experiment (20 sites), we measured seed removal, the abundance of mutualistic partners and other invertebrates interacting with seeds, myrmecochore cover, and diversity, along with ant habitat and forest structure. We found lower and more variable seed removal in secondary forests compared with remnant forests. A path analysis of all forests revealed that the abundance of mutualists was the primary determinant of the variation in seed removal, and that seed damage by antagonists (invasive slugs) negatively affected dispersal and was higher in secondary forests. In a path analysis of remnant forests, the link between mutualist abundance and seed removal was absent, but present in the secondary forest path, suggesting that seed dispersal is more variable and dependent on the mutualist abundance in secondary forests and is stable and high in remnant forests. Our results suggest that functional resilience to disturbance is variable, where seed dispersal is low in some secondary forests and not others. This work provides key insights into the effects of disturbance on mutualistic interactions and how the resilience of critical ecosystem functions impacts the capacity for diversity resiliency.

Symbiotic ant traits produce differential host-plant carbon and water dynamics in a multi-species mutualism.

Cooperative interactions may frequently be reinforced by "partner fidelity feedback," in which high- or low-quality partners drive positive feedbacks with high or low benefits for the host, respectively. Benefits of plant-animal mutualisms for plants have been quantified almost universally in terms of growth or reproduction, but these are only two of many sinks to which a host-plant allocates its resources. By investigating how partners to host-plants impact two fundamental plant resources, carbon and water, we can better characterize plant-partner fidelity and understand how plant-partner mutualisms may be modulated by resource dynamics. In Laikipia, Kenya, four ant species compete for Acacia drepanolobium host-plants. These ants differ in multiple traits, from nectar consumption to host-plant protection. Using a 5-year ant removal experiment, we compared carbon fixation, leaf water status, and stem non-structural carbohydrate concentrations for adult ant-plants with and without ant partners. Removal treatments showed that the ants differentially mediate tree carbon and/or water resources. All three ant species known to be aggressive against herbivores were linked to benefits for host-plant resources, but only the two species that defend but do not prune the host, Crematogaster mimosae and Tetraponera penzigi, increased tree carbon fixation. Of these two species, only the nectivore C. mimosae increased tree simple sugars. Crematogaster nigriceps, which defends the tree but also castrates flowers and prunes meristems, was linked only to lower tree water stress approximated by pre-dawn leaf water potential. In contrast to those defensive ants, Crematogaster sjostedti, a poor defender that displaces other ants, was linked to lower tree carbon fixation. Comparing the effects of the four ant species across control trees suggests that differential ant occupancy drives substantial differences in carbon and water supply among host trees. Our results highlight that ant partners can positively or negatively impact carbon and/or water relations for their host-plant, and we discuss the likelihood that carbon- and water-related partner fidelity feedback loops occur across ant-plant mutualisms.

Latitudinal gradient in species diversity provides high niche opportunities for a range-expanding phytophagous insect.

When species undergo poleward range expansions in response to anthropogenic change, they likely encounter less diverse communities in new locations. If low diversity communities provide weak biotic interactions, such as reduced competition or predation, range-expanding species may experience high niche opportunities. Here, we investigated if oak gall wasp communities follow a latitudinal diversity gradient (LDG) and if lower diversity communities provide weaker interactions at the poles for a range-expanding community member, Neuroterus saltatorius. We performed systematic surveys of gall wasps on a dominant oak, Quercus garryana, throughout most of its range, from northern California to Vancouver Island, British Columbia. On 540 trees at 18 sites, we identified 23 oak gall wasp morphotypes in three guilds (leaf detachable, leaf integral, and stem galls). We performed regressions between oak gall wasp diversity, latitude, and other abiotic (e.g. temperature) and habitat (e.g. oak patch size) factors to reveal if gall wasp communities followed an LDG. To uncover patterns in local interactions, we first performed partial correlations of gall wasp morphotype occurrences on trees within regions). We then performed regressions between abundances of co-occurring gall wasps on trees to reveal if interactions are putatively competitive or antagonistic. Q. garryana-gall wasp communities followed an LDG, with lower diversity at higher latitudes, particularly with a loss of detachable leaf gall morphotypes. Detachable leaf gall wasps, including the range-expanding species, co-occurred most on trees, with weak co-occurrences on trees in the northern expanded region. Abundances of N. saltatorius and detachable and integral leaf galls co-occurring on trees were negatively related, suggesting antagonistic interactions. Overall, we found that LDGs create communities with weaker associations at the poles that might facilitate ecological release in a range-expanding community member. Given the ubiquity of LDGs in nature, poleward range-expanding species are likely moving into low diversity communities. Yet, understanding if latitudinal diversity pattern provides weak biotic interactions for range-expanding species is not well explored. Our large-scale study documenting diversity in a related community of phytophagous insects that co-occur on a host plant reveals that LDGs create high niche opportunities for a range-expanding community member. Biogeographical patterns in diversity and species interactions are likely important mechanisms contributing to altered biotic interactions under range-expansions.

Cuando las especies se expanden hacia los polos en respuesta al cambio antropogénico, es probable que las encuentren comunidades menos diversas en sus nuevos lugares. Si las comunidades de baja diversidad proporcionan interacciones bióticas débiles, como competencia reducida o depredación, las especies que se expanden pueden tener 'oportunidades de alto nicho'. Aquí, investigamos si las comunidades de avispas de las agallas muestran un gradiente de diversidad latitudinal (LDG) y si las comunidades de menor diversidad proporcionan interacciones antagónicas más débiles en los polos para las comunidades que se expanden. Específicamente, investigamos estas relaciones en la comunidad de Neuroterus saltatorius. Realizamos estudios sistemáticos de las avispas de las agallas en un roble dominante, Quercus garryana en la mayor parte de su área de distribución, desde el norte de California hasta la isla de Vancouver, en la Columbia Británica. Sobre 540 árboles en 18 sitios y 6 regiones, nos identificamos 23 mofotipos de avispas de las agallas en tres gremios (hoja desmontable, hoja integral y agallas del tallo). Ejecutamos regresiones entre la diversidad de avispas de las agallas, la latitud, y otros factores abióticos (p. ej., temperatura) y de hábitat (p. ej., tamaño del parche de roble) para revelar si las comunidades de avispas de las agallas siguieron un LDG. Para descubrir tendencias en las interacciones locales, primero ejecutamos correlaciones parciales de ocurrencias de morfotipos de avispas de las agallas en árboles dentro de las regiones. Luego ejecutamos regresiones entre las coocurrencias de las abundancias deavispas de las agallas en los árboles para revelar si las interacciones son supuestamente competitivas o antagónicas. Las comunidades de avispas Q. garryana-gall, siguieron un LDG, con menor diversidad en latitudes más altas, particularmente con una pérdida de morfotipos de agallas de hoja desmontable. Las avispas de las agallas de las hojas desprendibles, incluidas a las especies que se expanden su hábitat, se encontraron en sobre todos los árboles, con coocurrencias débiles en los árboles de la región expandida del norte. Las coocurrencias de las las abundancias de N. saltatorius,las agallas foliares desmontables, e agallas integrales en los árboles se relacionaron negativamente, lo que sugiere interacciones antagónicas. En general, encontramos que los LDG crean comunidades con asociaciones más débiles en los polos que podrían facilitar la liberación ecológica en un miembro de la comunidad que se expanden. Debido de la ubicuidad de los LDG en la naturaleza, es probable que las especies que se expanden hacia los polos se estén trasladando a comunidades de baja diversidad. Sin embargo, no se explora bien la comprensión de si las tendenciasde diversidad latitudinal proporcionan interacciones bióticas débiles para las especies que se expanden. Nuestro estudio degran escala documenta la diversidad en una comunidad relacionada de insectos fitófagos que coexisten en una planta hospedante. Como resultado, revela que los LDG pueden crear oportunidades de grandes nichos para un miembro de la comunidad que se expande. Los patrones biogeográficos en la diversidad y las interacciones entre especies son probablemente mecanismos importantes que contribuyen a las interacciones bióticas alteradas bajo la expansión del hábitat.

Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both.

Quantifying the frequency of shifts to new host plants within diverse clades of specialist herbivorous insects is critically important to understand whether and how host shifts contribute to the origin of species. Oak gall wasps (Hymenoptera: Cynipidae: Cynipini) comprise a tribe of ∼1000 species of phytophagous insects that induce gall formation on various organs of trees in the family Fagacae-primarily the oaks (genus Quercus; ∼435 sp.). The association of oak gall wasps with oaks is ancient (∼50 my), and most oak species are galled by one or more gall wasp species. Despite the diversity of both gall wasp species and their plant associations, previous phylogenetic work has not identified the strong signal of host plant shifting among oak gall wasps that has been found in other phytophagous insect systems. However, most emphasis has been on the Western Palearctic and not the Nearctic where both oaks and oak gall wasps are considerably more species rich. We collected 86 species of Nearctic oak gall wasps from most of the major clades of Nearctic oaks and sequenced >1000 Ultraconserved Elements (UCEs) and flanking sequences to infer wasp phylogenies. We assessed the relationships of Nearctic gall wasps to one another and, by leveraging previously published UCE data, to the Palearctic fauna. We then used phylogenies to infer historical patterns of shifts among host tree species and tree organs. Our results indicate that oak gall wasps have moved between the Palearctic and Nearctic at least four times, that some Palearctic wasp clades have their proximate origin in the Nearctic, and that gall wasps have shifted within and between oak tree sections, subsections, and organs considerably more often than previous data have suggested. Given that host shifts have been demonstrated to drive reproductive isolation between host-associated populations in other phytophagous insects, our analyses of Nearctic gall wasps suggest that host shifts are key drivers of speciation in this clade, especially in hotspots of oak diversity. Although formal assessment of this hypothesis requires further study, two putatively oligophagous gall wasp species in our dataset show signals of host-associated genetic differentiation unconfounded by geographic distance, suggestive of barriers to gene flow associated with the use of alternative host plants.

Delimiting the cryptic diversity and host preferences of Sycophila parasitoid wasps associated with oak galls using phylogenomic data.

Cryptic species diversity is a major challenge regarding the species-rich community of parasitoids attacking oak gall wasps due to a high degree of sexual dimorphism, morphological plasticity, small size and poorly known biology. As such, we know very little about the number of species present, nor the evolutionary forces responsible for generating this diversity. One hypothesis is that trait diversity in the gall wasps, including the morphology of the galls they induce, has evolved in response to selection imposed by the parasitoid community, with reciprocal selection driving diversification of the parasitoids. Using a rare, continental-scale data set of Sycophila parasitoid wasps reared from 44 species of cynipid galls from 18 species of oak across the USA, we combined mitochondrial DNA barcodes, ultraconserved elements (UCEs), morphological and natural history data to delimit putative species. Using these results, we generate the first large-scale assessment of ecological specialization and host association in this species-rich group, with implications for evolutionary ecology and biocontrol. We find most Sycophila target specific subsets of available cynipid host galls with similar morphologies, and generally attack larger galls. Our results suggest that parasitoid wasps such as Sycophila have adaptations allowing them to exploit particular host trait combinations, while hosts with contrasting traits are resistant to attack. These findings support the tritrophic niche concept for the structuring of plant-herbivore-parasitoid communities.

The Arthropod Associates of 155 North American Cynipid Oak Galls.

The identities of most arthropod associates of cynipid-induced oak galls in the western Palearctic are generally known. However, a comprehensive accounting of associates has been performed for only a small number of the galls induced by the estimated 700 species of cynipid gall wasps in the Nearctic. This gap in knowledge stymies many potential studies of diversity, coevolution, and community ecology, for which oak gall systems are otherwise ideal models. We report rearing records of insects and other arthropods from more than 527,306 individual galls representing 201 different oak gall types collected from 32 oak tree species in North America. Of the 201 gall types collected, 155 produced one or more arthropods. A total of 151,075 arthropods were found in association with these 155 gall types, and of these 61,044 (40.4%) were gall wasps while 90,031 (59.6%) were other arthropods. We identified all arthropods to superfamily, family, or, where possible, to genus. We provide raw numbers and summaries of collections, alongside notes on natural history, ecology, and previously published associations for each taxon. For eight common gall-associated genera (Synergus, Ceroptres, Euceroptres, Ormyrus, Torymus, Eurytoma, Sycophila, and Euderus), we also connect rearing records to gall wasp phylogeny, geography, and ecology -including host tree and gall location (host organ), and their co-occurrence with other insect genera. Though the diversity of gall wasps and the large size of these communities is such that many Nearctic oak gall-associated insects still remain undescribed, this large collection and identification effort should facilitate the testing of new and varied ecological and evolutionary hypotheses in Nearctic oak galls.

Interactions between seed-dispersing ant species affect plant community composition in field mesocosms.

In generalized mutualisms, species vary in the quality of services they provide to their partners directly via traits that affect partner fitness and indirectly via traits that influence interactions among mutualist species that play similar functional roles. Myrmecochory, or seed dispersal by ants, is a generalized mutualism with ant species varying in the quality of dispersal services they provide to their plant partners. Variation in ant species identity can directly impact seed dispersal patterns and plant community composition; however, we know less about how interactions among seed-dispersing ant species indirectly influence plant partners. The invasive ant Myrmica rubra, is a high-quality seed-disperser in its native range that interacts with myrmecochores (ant-dispersed plants) and the high-quality seed disperser Aphaenogaster sp. in its invaded range. We use this system to examine how interactions between two functionally similar mutualist ant species influence the recruitment and community composition of ant-dispersed plants. We performed a field mesocosm experiment and a laboratory behavioural experiment to compare discovery and dominance behaviours between ant species, and seed dispersal and seedling recruitment of four myrmecochore species among intraspecific interaction treatments of each ant species and an interspecific interaction treatment. We found that M. rubra was better at discovering and dispersing seeds, but Aphaenogaster sp. was dominantly aggressive over M. rubra. Interspecific interactions dampened seed dispersal relative to dispersal by the better disperser. Despite this dampening, we found no effect of interspecific interactions on seedling recruitment. However, community composition of seedlings in the interspecific interaction treatment was more similar to composition in the aggressively dominant ant (Aphaenogaster sp.) treatment than in the better discoverer ant M. rubra treatment. We show that interspecific interactions between mutualist species in the same functional guild affect the outcome of mutualistic interactions with partner species. Despite the native ant dispersing fewer seeds, its dominance over the subordinate (invasive) ant has the potential to allow for some level of biotic resistance against the effects of M. rubra on plant communities when these species coexist.

Invasive ants disperse seeds farther than native ants, affecting the spatial pattern of seedling recruitment and survival.

Mutualists can vary in the quantity and quality of service which they provide to their partners. Variation in seed disperser quality depends on seed-processing traits, dispersal distance, and deposition location, all of which ultimately affect plant fitness. Here, we compared these aspects of seed dispersal quality between a native and an invasive ant species, and examined how they affect competition and plant performance. Using experimental mesocosm communities, we examined how these two ant species affect the spatial pattern of recruitment and establishment for four myrmecochorous plant species, including one invasive species. We measured the locations of dispersed seedlings relative to ant nests, adult plants, and other dispersed seedlings, as well as measured the effects of location on plant performance. The invasive ant, Myrmica rubra, secondarily dispersed seeds farther from its nests, creating a less clumped pattern of seedling recruitment compared to the native ant, Aphaenogaster rudis. Plant species responded differently to dispersal. Invasive seedlings recruited farther from adult plants than native seedlings, and had higher survival the farther they were from conspecifics. In contrast, native plants had higher survival and grew taller when dispersed farther from invasive plants. We show that seed-dispersing ant partners differ in mutualist quality creating differences in dispersal distance and deposition location that affects a plant's competitive environment. Our results reveal the potential for long-term consequences on plant community structure with changing ant partner identity. We emphasize the need to examine dispersal quality in addition to quantity to uncover the importance of partner identity in structuring communities.

Asynchrony between ant seed dispersal activity and fruit dehiscence of myrmecochorous plants.

PREMISE OF THE STUDY: Phenological mismatch has received attention in plant-pollinator interactions, but less so in seed dispersal mutualisms. We investigated whether the seasonal availability of myrmecochorous seeds is well matched to the seasonal activity patterns of seed-dispersing ants. METHODS: We compared seasonal timing of seed removal by a keystone seed-dispersing ant, Aphaenogaster rudis, and fruit dehiscence of several species of plants whose seeds it disperses in a deciduous forest in southern Ontario, Canada. We examined the timing of elaiosome "robbing" by the nonnative slug Arion subfuscus and tested whether seed removal by ants declines in response to supplementation with additional elaiosome-bearing seeds (ant "satiation"). KEY RESULTS: Seed removal from experimental depots peaked early in the season for all plant species and correlated with temperature. In contrast, elaiosome robbing by slugs increased late in the season and thus may disproportionately affect plants with late-dehiscing fruits. Ant colonies removed seeds at similar rates regardless of seed supplementation, indicating that satiation likely does not impact seasonal patterns of seed dispersal in this system. Fruits of the five myrmecochorous plant species in our study dehisced at discrete intervals throughout the season, with minimal overlap among species. Peak dehiscence did not overlap with peak seed removal for any plant species. CONCLUSIONS: Fruit dehiscence of myrmecochorous plants and peak ant seed dispersal activity occur asynchronously. Whether future climate warming will shift ant and plant phenologies in ways that have consequences for seed dispersal remains an open question.

Economy of scale: third partner strengthens a keystone ant-plant mutualism.

While foundation species can stabilize ecosystems at landscape scales, their ability to persist is often underlain by keystone interactions occurring at smaller scales. Acacia drepanolobium is a foundation tree, comprising >95% of woody cover in East African black-cotton savanna ecosystems. Its dominance is underlain by a keystone mutualistic interaction with several symbiotic ant species in which it provides housing (swollen thorns) and carbohydrate-rich nectar from extra-floral nectaries (EFN). In return, it gains protection from catastrophic damage from mega-herbivores. Crematogaster mimosae is the ecologically dominant symbiotic ant in this system, also providing the highest protection services. In addition to tending EFN, C. mimosae tend scale insects for carbohydrate-rich honeydew. We investigated the role of scale insects in this specialized ant-plant interaction. Specifically, does this putatively redundant third partner strengthen the ant-plant mutualism by making the ant a better protector of the tree? Or does it weaken the mutualism by being costly to the tree while providing no additional benefit to the ant-plant mutualism? We coupled observational surveys with two scale-manipulation experiments and found evidence that this third partner strengthens the ant-plant mutualism. Trees with scale insects experimentally removed experienced a 2.5X increase in elephant damage compared to trees with scale insects present over 10 months. Reduced protection was driven by scale removal causing a decrease in ant colony size and per capita baseline activity and defensive behavior. We also found that ants increased scale-tending and the density of scale insects on trees when EFN were experimentally reduced. Thus, in this system, scale insects and EFN are likely complementary, rather than redundant, resources with scale insects benefitting ants when EFN production is low (such as during annual dry periods in this semi-arid ecosystem). This study reveals that a third-partner strengthens an ant-plant mutualism that serves to stabilize a whole ecosystem.

Large herbivores promote habitat specialization and beta diversity of African savanna trees.

Edaphic variation in plant community composition is widespread, yet its underlying mechanisms are rarely understood and often assumed to be physiological. In East African savannas, Acacia tree species segregate sharply across soils of differing parent material: the ant-defended whistling thorn, A. drepanolobium (ACDR), is monodominant on cracking clay vertisols that are nutrient rich but physically stressful, whereas poorly defended species such as A. brevispica (ACBR) dominate on nutrient-poor but otherwise less-stressful sandy loams. Using a series of field experiments, we show that large-mammal herbivory interacts with soil properties to maintain this pattern. In the absence of large herbivores, transplanted saplings of both species established on both soil types. Browsers strongly suppressed survival and growth of ACDR saplings on sandy soil, where resource limitation constrained defensive investment. On clay soil, ACBR saplings established regardless of herbivory regime, but elephants prevented recruitment to maturity, apparently because trees could not tolerate the combination of biotic and abiotic stressors. Hence, each tree species was filtered out of one habitat by browsing in conjunction with different edaphic factors and at different ontogenetic stages. Browser abundance was greater on sandy soil, where trees were less defended, consistent with predicted feedbacks between plant community assembly and herbivore distributions. By exploring two inversely related axes of soil "quality" (abiotic stress and nutrient content), our study extends the range of mechanisms by which herbivores are known to promote edaphic specialization, illustrates how the high cost of a protection mutualism can constrain the realized niche of host trees, and shows that large-scale properties of savanna ecosystems are shaped by species interactions in cryptic ways that mimic simple abiotic determinism. These results suggest that ongoing declines in large-herbivore populations may relax spatial heterogeneity in plant assemblages and reduce the beta diversity of communities.

An invasive slug exploits an ant-seed dispersal mutualism.

Plant-animal mutualisms, such as seed dispersal, are often vulnerable to disruption by invasive species. Here, we show for the first time how a non-ant invasive species negatively affects seed dispersal by ants. We examined the effects of several animal species that co-occur in a temperate deciduous forest-including native and invasive seed-dispersing ants (Aphaenogaster rudis and Myrmica rubra, respectively), an invasive slug (Arion subfuscus), and native rodents-on a native myrmecochorous plant, Asarum canadense. We experimentally manipulated ant, slug, and rodent access to seed depots and measured seed removal. We also video-recorded depots to determine which other taxa interact with seeds. We found that A. rudis was the main disperser of seeds and that A. subfuscus consumed elaiosomes without dispersing seeds. Rodent visitation was rare, and rodent exclusion had no significant effect on seed or elaiosome removal. We then used data obtained from laboratory and field mesocosm experiments to determine how elaiosome robbing by A. subfuscus affects seed dispersal by A. rudis and M. rubra. We found that elaiosome robbing by slugs reduced seed dispersal by ants, especially in mesocosms with A. rudis, which picks up seeds more slowly than M. rubra. Taken together, our results show that elaiosome robbing by an invasive slug reduces seed dispersal by ants, suggesting that invasive slugs can have profound negative effects on seed dispersal mutualisms.

Mutualism between co-introduced species facilitates invasion and alters plant community structure.

Generalized mutualisms are often predicted to be resilient to changes in partner identity. Variation in mutualism-related traits between native and invasive species however, can exacerbate the spread of invasive species ('invasional meltdown') if invasive partners strongly interact. Here we show how invasion by a seed-dispersing ant (Myrmica rubra) promotes recruitment of a co-introduced invasive over native ant-dispersed (myrmecochorous) plants. We created experimental communities of invasive (M. rubra) or native ants (Aphaenogaster rudis) and invasive and native plants and measured seed dispersal and plant recruitment. In our mesocosms, and in laboratory and field trials, M. rubra acted as a superior seed disperser relative to the native ant. By contrast, previous studies have found that invasive ants are often poor seed dispersers compared with native ants. Despite belonging to the same behavioural guild, seed-dispersing ants were not functionally redundant. Instead, native and invasive ants had strongly divergent effects on plant communities: the invasive plant dominated in the presence of the invasive ant and the native plants dominated in the presence of the native ant. Community changes were not due to preferences for coevolved partners: variation in functional traits of linked partners drove differences. Here, we show that strongly interacting introduced mutualists can be major drivers of ecological change.

The influence of species interactions on geographic range change under climate change.

The fossil record tells us that many species shifted their geographic distributions during historic climate changes, but this record does not portray the complete picture of future range change in response to climate change. In particular, it does not provide information on how species interactions will affect range shifts. Therefore, we also need modern research to generate understanding of range change. This paper focuses on the role that species interactions play in promoting or preventing geographic ranges shifts under current and future climate change, and we illustrate key points using empirical case studies from an integrated study system. Case studies can have limited generalizability, but they are critical to defining possible outcomes under climate change. Our case studies emphasize host limitation that could reduce range shifts and enemy release that could facilitate range expansion. We also need improvements in modeling that explicitly consider species interactions, and this modeling can be informed by empirical research. Finally, we discuss how species interactions have implications for range management by people.

Impact of an invasive oak gall wasp on a native butterfly: a test of plant-mediated competition.

Phytophagous insects commonly interact through shared host plants. These interactions, however, do not occur in accordance with traditional paradigms of competition, and competition in phytophagous insects is still being defined. It remains unclear, for example, if particular guilds of insects are superior competitors or important players in structuring insect communities. Gall-forming insects are likely candidates for such superior competitors because of their ability to manipulate host plants, but their role as competitors is understudied. We investigate the effect of invasive populations of an oak gall wasp, Neuroterus saltatorius, on a native specialist butterfly, Erynnis propertius, as mediated by their shared host plant, Quercus garryana. This gall wasp occurs at high densities in its introduced range, where we stocked enclosures with caterpillars on trees that varied in gall wasp density. Biomass production of butterflies was lower in enclosures on high-density than on low-density trees because overwintering caterpillars were smaller, and fewer of them eclosed into adults the following spring. To see if the gall wasp induced changes in foliar quality, we measured host plant quality before and after gall induction on 30 trees each at two sites. We found a positive relationship between gall wasp density and the percentage change in foliar C:N, a negative relationship between gall wasp density and the percentage change in foliar water at one site, and no relationship between the percentage change in protein-binding capacity (i.e., phenolics) and gall-wasp density. Additionally, there was a negative relationship between foliar quality and butterfly performance. Our results provide evidence for a plant-mediated impact of an invasive oak gall wasp on a native butterfly and suggest that gall wasps could act as superior competitors, especially when they occur at high densities.

Translocation experiments with butterflies reveal limits to enhancement of poleward populations under climate change.

There is a pressing need to predict how species will change their geographic ranges under climate change. Projections typically assume that temperature is a primary fitness determinant and that populations near the poleward (and upward) range boundary are preadapted to warming. Thus, poleward, peripheral populations will increase with warming, and these increases facilitate poleward range expansions. We tested the assumption that poleward, peripheral populations are enhanced by warming using 2 butterflies (Erynnis propertius and Papilio zelicaon) that co-occur and have contrasting degrees of host specialization and interpopulation genetic differentiation. We performed a reciprocal translocation experiment between central and poleward, peripheral populations in the field and simulated a translocation experiment that included alternate host plants. We found that the performance of both central and peripheral populations of E. propertius were enhanced during the summer months by temperatures characteristic of the range center but that local adaptation of peripheral populations to winter conditions near the range edge could counteract that enhancement. Further, poleward range expansion in this species is prevented by a lack of host plants. In P. zelicaon, the fitness of central and peripheral populations decreased under extreme summer temperatures that occurred in the field at the range center. Performance in this species also was affected by an interaction of temperature and host plant such that host species strongly mediated the fitness of peripheral individuals under differing simulated temperatures. Altogether we have evidence that facilitation of poleward range shifts through enhancement of peripheral populations is unlikely in either study species.

The response of two butterfly species to climatic variation at the edge of their range and the implications for poleward range shifts.

To predict changes in species' distributions due to climate change we must understand populations at the poleward edge of species' ranges. Ecologists generally expect range shifts under climate change caused by the expansion of edge populations as peripheral conditions increasingly resemble the range core. We tested whether peripheral populations of two contrasting butterflies, a small-bodied specialist (Erynnis propertius) and a large-bodied generalist (Papilio zelicaon), respond favorably to warmer conditions. Performance of populations related to climate was evaluated in seven peripheral populations spanning 1.2 degrees latitude (160 km) using: (1) population density surveys, an indirect measure of site suitability; and (2) organismal fitness in translocation experiments. There was evidence that population density increased with temperature for P. zelicaon whose population density declined with latitude in 1 of 3 sample years. On the other hand, E. propertius showed a positive relationship of population density with latitude, apparently unrelated to climate or measured habitat variables. Translocation experiments showed increased larval production at increased temperatures for both species, and in P. zelicaon, larval production also increased under drier conditions. These findings suggest that both species may increase at their range edge with warming but the preference for core-like conditions may be stronger in P. zelicaon. Further, populations of E. propertius at the range boundary may be large enough to act as sources of colonists for range expansions, but range expansion in this species may be prevented by a lack of available host plants further north. In total, the species appear to respond differently to climate and other factors that vary latitudinally, factors that will likely affect poleward expansion.