Inverse priority effects: A role for historical contingency during species losses.

Communities worldwide are losing multiple species at an unprecedented rate, but how communities reassemble after these losses is often an open question. It is well established that the order and timing of species arrival during community assembly shapes forthcoming community composition and function. Yet, whether the order and timing of species losses can lead to divergent community trajectories remains largely unexplored. Here, we propose a novel framework that sets testable hypotheses on the effects of the order and timing of species losses-inverse priority effects-and suggests its integration into the study of community assembly. We propose that the order and timing of species losses within a community can generate alternative reassembly trajectories, and suggest mechanisms that may underlie these inverse priority effects. To formalize these concepts quantitatively, we used a three-species Lotka-Volterra competition model, enabling to investigate conditions in which the order of species losses can lead to divergent reassembly trajectories. The inverse priority effects framework proposed here promotes the systematic study of the dynamics of species losses from ecological communities, ultimately aimed to better understand community reassembly and guide management decisions in light of rapid global change.

Invasive species modulate the structure and stability of a multilayer mutualistic network.

Species interactions are critical for maintaining community structure and dynamics, but the effects of invasive species on multitrophic networks remain poorly understood. We leveraged an ongoing invasion scenario in Patagonia, Argentina, to explore how non-native ungulates affect multitrophic networks. Ungulates disrupt a hummingbird-mistletoe-marsupial keystone interaction, which alters community composition. We sampled pollination and seed dispersal interactions in intact and invaded sites. We constructed pollination and seed dispersal networks for each site, which we connected via shared plants. We calculated pollination-seed dispersal connectivity, identified clusters of highly connected species, and quantified species' roles in connecting species clusters. To link structural variation to stability, we quantified network tolerance to single random species removal (disturbance propagation) and sequential species removal (robustness) using a stochastic coextinction model. Ungulates reduced the connectivity between pollination and seed dispersal and produced fewer clusters with a skewed size distribution. Moreover, species shifted their structural role, fragmenting the network by reducing the 'bridges' among species clusters. These structural changes altered the dynamics of cascading effects, increasing disturbance propagation and reducing network robustness. Our results highlight invasive species' role in altering community structure and subsequent stability in multitrophic communities.

A keystone mutualism promotes resistance to invasion.

It is not uncommon for one or a few species, and their interactions, to have disproportionate effects on other species in ecological communities. Such keystone interactions might affect how communities respond to the invasion of non-native species by preventing or inhibiting the establishment, spread or impact of non-native species. We explore whether a keystone mutualism among a hummingbird-mistletoe-marsupial promotes ecological resistance to an invasive pollinator, the bumblebee Bombus terrestris, by comparing data collected at sites prior to bumblebee invasion to data collected 11 years after the invasion in sites with and without the keystone mutualism. We built pollination networks and focused on network motifs, regarded as building blocks of networks, to identify the central pollinators and estimate the change in their interactions after invasion of B. terrestris. We also estimated the interaction rewiring across the season in post-invasion networks and tested it as a possible mechanism explaining how the keystone mutualism increased ecological resistance to invasion. We found two times more species in post-invasion sites with the keystone mutualism than in post-invasion sites without the keystone mutualism. Moreover, we found that invasive bumblebee reduced the strength and interaction niche of the five central pollinator species while increasing its own strength and interaction niche, suggesting a replacement of interactions. Also, we found that the keystone mutualism promoted resistance to B. terrestris invasion by reducing its negative impacts on central species. In the presence of the keystone mutualism, central species had three times more direct interactions than in sites without this keystone mutualism. The higher interaction rewiring, after invasion of B. terrestris, in sites with the keystone mutualism indicates greater chances of central pollinators to form new interactions and reduces their competence for resources with the non-native bumblebee. Our results demonstrate that a keystone mutualism can enhance community resistance against the impacts of a non-native invasive pollinator by increasing species diversity and promoting interaction rewiring in the community. This study suggests that the conservation of mutualisms, especially those considered keystone, could be essential for long-term preservation of natural communities under current and future impacts of global change.

Es común que una o unas pocas especies y sus interacciones tengan efectos desproporcionado sobre otras especies en las comunidades. Estas especies y sus interacciones claves podrían afectar el modo en que las comunidades responden a la invasión de especies no nativas al prevenir o disminuir su establecimiento, su propagación o el impacto de las mismas. En este estudio evaluamos si un mutualismo clave entre un colibrí, un muérdago y un marsupial promueve la resistencia de la comunidad frente a un polinizador invasor, el abejorro Bombus terrestris, mediante la comparación de datos colectados en sitios previos a la invasión del abejorro y datos colectados 11 años después de su invasión, en sitios con y sin el mutualismo clave. Construimos redes ecológicas planta-polinizador y nos centramos en los modos de interacción ("interaction motifs"), los cuales son usados como bloques en la construcción de las redes, para identificar los polinizadores centrales y estimar el cambio en sus interacciones después de la invasión de B. terrestris. Además, en las redes posteriores a la invasión estimamos la reconexión de interacciones a lo largo de la temporada y la evaluamos como un posible mecanismo mediante la cual el mutualismo clave aumentó la resistencia a la invasión. En sitios posteriores a la invasión con el mutualismo clave encontramos dos veces más especies que en sitios posteriores a la invasión ausentes de éste. Además, en los sitios ausentes del mutualismo clave, encontramos que el abejorro invasor redujo la fuerza y el nicho de interacción de los cinco polinizadores centrales mientras incrementó su propia fuerza y nicho de interacciones, sugiriendo un reemplazo de interacciones. Asimismo, encontramos que el mutualismo clave promovió la resistencia de la comunidad a la invasión de B. terrestris al reducir sus impactos negativos sobre las especies centrales. En presencia del mutualismo clave, las especies centrales presentaron tres veces más interacciones directas que en sitios ausentes de esta interacción. La gran reconexión de interacciones encontrada en sitios posteriores a la invasión con el mutualismo clave indica mayores probabilidades de que los polinizadores centrales formen nuevas interacciones y reduzcan la competencia por recursos con el abejorro no nativo. Nuestros resultados demuestran que un mutualismo clave puede mejorar la resistencia de la comunidad frente a los impactos de especies invasoras al incrementar la diversidad de especies y promover la reconexión de interacciones en la comunidad. Este estudio sugiere que la conservación de las interacciones mutualistas, principalmente aquellas consideradas claves, podría ser esencial para preservar las comunidades naturales frente a los impactos del cambio global.

The disruption of a keystone interaction erodes pollination and seed dispersal networks.

Understanding the impacts of global change on ecological communities is a major challenge in modern ecology. The gain or loss of particular species and the disruption of key interactions are both consequences and drivers of global change that can lead to the disassembly of ecological networks. We examined whether the disruption of a hummingbird-mistletoe-marsupial mutualism by the invasion of non-native species can have cascading effects on both pollination and seed dispersal networks in the temperate forest of Patagonia, Argentina. We focused on network motifs, subnetworks composed of a small number of species exhibiting particular patterns of interaction, to examine the structure and diversity of mutualistic networks. We found that the hummingbird-mistletoe-marsupial mutualism plays a critical role in the community by increasing the complexity of pollination and seed dispersal networks through supporting a high diversity of interactions. Moreover, we found that the disruption of this tripartite mutualism by non-native ungulates resulted in diverse indirect effects that led to less complex pollination and seed dispersal networks. Our results demonstrate that the gains and losses of particular species and the alteration of key interactions can lead to cascading effects in the community through the disassembly of mutualistic networks.

Invasive trees rely more on mycorrhizas, countering the ideal-weed hypothesis.

The ideal-weed hypothesis predicts that invasive plants should be less dependent on mutualisms. However, evidence in favor of or against this hypothesis comes mainly from observational studies. Here, we experimentally tested this hypothesis using a two-factor greenhouse experiment, comparing the seedling growth response of different Pinus species (varying in invasiveness) to ectomycorrhizal fungal inoculation. Most species showed no response until they were 6 mo old, at which point inoculation increased growth between 10 and 260% among the different species. This growth response was higher for species with lower seed mass, higher dispersal ability, higher Z score (a proxy for invasiveness) and higher number of naturalized regions, all of which correspond to higher invasiveness. Our results show that timing is a crucial factor when comparing mycorrhizal dependency of different species. Dependence on mutualistic microorganisms could be part of a strategy in which invasive species produce smaller seeds, in greater number, which can disperse further, but where seedlings are more reliant on mycorrhizas to improve access to water, nutrients, and protection from pathogens. Our results suggest that reliance on mutualisms may enhance, rather than limit, nonnative species in their ability to spread, establish, and colonize.

Highly invasive tree species are more dependent on mutualisms.

Why some species become invasive while others do not remains an elusive question. It has been proposed that invasive species should depend less on mutualisms, because their spread would then be less constrained by the availability of mutualistic partners. We tested this idea with the genus Pinus, whose degree of invasiveness is known at the species level (being highly and negatively correlated with seed size), and which forms obligate mutualistic associations with ectomycorrhizal fungi (EMF). Mycorrhizal dependence is defined as the degree to which a plant needs the mycorrhizal fungi to show the maximum growth. In this regard, we use plant growth response to mycorrhizal fungi as a proxy for mycorrhizal dependence. We assessed the responsiveness of Pinus species to EMF using 1,206 contrasts published on 34 species, and matched these data with data on Pinus species invasiveness. Surprisingly, we found that species that are more invasive depend more on mutualisms (EMF). Seedling growth of species with smaller seeds benefited more from mutualisms, indicating a higher dependence. A higher reliance on EMF could be part of a strategy in which small-seeded species produce more seeds that can disperse further, and these species are likely to establish only if facilitated by mycorrhizal fungi. On the contrary, big-seeded species showed a lower dependence on EMF, which may be explained by their tolerance to stressful conditions during establishment. However, the limited dispersal of larger seeds may limit the spread of these species. We present strong evidence against a venerable belief in ecology that species that rely more on mutualisms are less prone to invade, and suggest that in certain circumstances greater reliance on mutualists can increase spread capacity.

Seed predation does not explain pine invasion success.

Why some non-native plant species invade, and others fail remains an elusive question. Plant invasion success has been associated with specific species traits. Yet, we have limited knowledge of the mechanisms relating these traits to invasion potential. General patterns of biotic resistance by seed predation may provide a mechanism that helps separate invasive from non-invasive plants. Seed predation is an important barrier against plant establishment for many plant species. It may, therefore, create a selective filter against non-native plant establishment based on plant traits related to seed predation rate. In two cafeteria-style seed predation experiments in a steppe ecosystem in Patagonia (Argentina) we provided seeds of 16 non-native Pinaceae covering a 300-fold variation in seed mass, a 200-fold variation in seed volume and 75-fold variation in seed toughness. Seed removal decreased with seed mass and seed volume. Seed toughness was not a significant predictor while seed volume was the best predictor of predators' preference. However, for species of this family small seed size is the most important predictor of species invasiveness. Our results show that seed predation does not explain Pinaceae invasive success. In our system, species that have smaller seeds (i.e., more invasive) are preferentially consumed by seed predators. Seed mass was not the best predictor of granivory rates, despite being the seed trait on which most studies have been focused. Our ability to predict future invasion and understand invasion success could benefit from other studies that focus on the mechanisms behind invasive traits.

Genetic variation in resistance to leaf fungus indirectly affects spider density.

Many host-plants exhibit genetic variation in resistance to pathogens; however, little is known about the extent to which genetic variation in pathogen resistance influences other members of the host-plant community, especially arthropods at higher trophic levels. We addressed this knowledge gap by using a common garden experiment to examine whether genotypes of Populus trichocarpa varied in resistance to a leaf-blistering pathogen, Taphrina sp., and in the density of web-building spiders, the dominant group of predatory arthropods. In addition, we examined whether variation in spider density was explained by variation in the density and size of leaf blisters caused by Taphrina. We found that P. trichocarpa genotypes exhibited strong differences in their resistance to Taphrina and that P. trichocarpa genotypes that were more susceptible to Taphrina supported more web-building spiders, the dominant group of predatory arthropods. We suspect that this result is caused by blisters increasing the availability of suitable habitat for predators, and not due to variation in herbivores because including herbivore density as a covariate did not affect our models. Our study highlights a novel pathway by which genetic variation in pathogen resistance may affect higher trophic levels in arthropod communities.

Adaptive genetic variation mediates bottom-up and top-down control in an aquatic ecosystem.

Research in eco-evolutionary dynamics and community genetics has demonstrated that variation within a species can have strong impacts on associated communities and ecosystem processes. Yet, these studies have centred around individual focal species and at single trophic levels, ignoring the role of phenotypic variation in multiple taxa within an ecosystem. Given the ubiquitous nature of local adaptation, and thus intraspecific variation, we sought to understand how combinations of intraspecific variation in multiple species within an ecosystem impacts its ecology. Using two species that co-occur and demonstrate adaptation to their natal environments, black cottonwood (Populus trichocarpa) and three-spined stickleback (Gasterosteus aculeatus), we investigated the effects of intraspecific phenotypic variation on both top-down and bottom-up forces using a large-scale aquatic mesocosm experiment. Black cottonwood genotypes exhibit genetic variation in their productivity and consequently their leaf litter subsidies to the aquatic system, which mediates the strength of top-down effects from stickleback on prey abundances. Abundances of four common invertebrate prey species and available phosphorous, the most critically limiting nutrient in freshwater systems, are dictated by the interaction between genetic variation in cottonwood productivity and stickleback morphology. These interactive effects fit with ecological theory on the relationship between productivity and top-down control and are comparable in strength to the effects of predator addition. Our results illustrate that intraspecific variation, which can evolve rapidly, is an under-appreciated driver of community structure and ecosystem function, demonstrating that a multi-trophic perspective is essential to understanding the role of evolution in structuring ecological patterns.

Testing a 'genes-to-ecosystems' approach to understanding aquatic-terrestrial linkages.

A 'genes-to-ecosystems' approach has been proposed as a novel avenue for integrating the consequences of intraspecific genetic variation with the underlying genetic architecture of a species to shed light on the relationships among hierarchies of ecological organization (genes → individuals → communities → ecosystems). However, attempts to identify genes with major effect on the structure of communities and/or ecosystem processes have been limited and a comprehensive test of this approach has yet to emerge. Here, we present an interdisciplinary field study that integrated a common garden containing different genotypes of a dominant, riparian tree, Populus trichocarpa, and aquatic mesocosms to determine how intraspecific variation in leaf litter alters both terrestrial and aquatic communities and ecosystem functioning. Moreover, we incorporate data from extensive trait screening and genome-wide association studies estimating the heritability and genes associated with litter characteristics. We found that tree genotypes varied considerably in the quality and production of leaf litter, which contributed to variation in phytoplankton abundances, as well as nutrient dynamics and light availability in aquatic mesocosms. These 'after-life' effects of litter from different genotypes were comparable to the responses of terrestrial communities associated with the living foliage. We found that multiple litter traits corresponding with aquatic community and ecosystem responses differed in their heritability. Moreover, the underlying genetic architecture of these traits was complex, and many genes contributed only a small proportion to phenotypic variation. Our results provide further evidence that genetic variation is a key component of aquatic-terrestrial linkages, but challenge the ability to predict community or ecosystem responses based on the actions of one or a few genes.

Ant-mediated seed dispersal in a warmed world.

Climate change affects communities both directly and indirectly via changes in interspecific interactions. One such interaction that may be altered under climate change is the ant-plant seed dispersal mutualism common in deciduous forests of eastern North America. As climatic warming alters the abundance and activity levels of ants, the potential exists for shifts in rates of ant-mediated seed dispersal. We used an experimental temperature manipulation at two sites in the eastern US (Harvard Forest in Massachusetts and Duke Forest in North Carolina) to examine the potential impacts of climatic warming on overall rates of seed dispersal (using Asarum canadense seeds) as well as species-specific rates of seed dispersal at the Duke Forest site. We also examined the relationship between ant critical thermal maxima (CTmax) and the mean seed removal temperature for each ant species. We found that seed removal rates did not change as a result of experimental warming at either study site, nor were there any changes in species-specific rates of seed dispersal. There was, however, a positive relationship between CTmax and mean seed removal temperature, whereby species with higher CTmax removed more seeds at hotter temperatures. The temperature at which seeds were removed was influenced by experimental warming as well as diurnal and day-to-day fluctuations in temperature. Taken together, our results suggest that while temperature may play a role in regulating seed removal by ants, ant plant seed-dispersal mutualisms may be more robust to climate change than currently assumed.

Genetic variation within a dominant shrub structures green and brown community assemblages.

Two rising challenges in ecology are understanding the linkages between above- and belowground components of terrestrial ecosystems and connecting genes to their ecological consequences. Here, we blend these emerging perspectives using a long-term common-garden experiment in a coastal dune ecosystem, whose dominant shrub species, Baccharis pilularis, exists as erect or prostrate architectural morphotypes. We explored variation in green (foliage-based) and brown (detritus-based) community assemblages, local ecosystem processes, and understory microclimate between the two morphs. Prostrate morphs supported more individuals, species, and different compositions of foliage arthropods, litter microarthropods, and soil bacteria than erect morphs. The magnitude of community compositional differences was maintained from crown to litter to soil. Despite showing strikingly similar responses, green and brown assemblages were associated with different underlying mechanisms. Differences in estimated shrub biomass best explained variation in the green assemblage, while understory abiotic conditions accounted for variation in the brown assemblage. Prostrate morphs produced more biomass and litter, which corresponded with their strong lateral growth in a windy environment. Compared to erect morphs, the denser canopy and thicker litter layer of prostrate morphs helped create more humid understory conditions. As a result, decomposition rates were higher under prostrate shrubs, despite prostrate litter being of poorer quality. Together, our results support the hypothesis that intraspecific genetic variation in primary producers is a key mediator of above- and belowground linkages, and that integrating the two perspectives can lead to new insights into how terrestrial communities are linked with ecosystem pools and processes.

Node-by-node disassembly of a mutualistic interaction web driven by species introductions.

Interaction webs summarize the diverse interactions among species in communities. The addition or loss of particular species and the alteration of key interactions can lead to the disassembly of the entire interaction web, although the nontrophic effects of species loss on interaction webs are poorly understood. We took advantage of ongoing invasions by a suite of exotic species to examine their impact in terms of the disassembly of an interaction web in Patagonia, Argentina. We found that the reduction of one species (a host of a keystone mistletoe species) resulted in diverse indirect effects that led to the disassembly of an interaction web through the loss of the mistletoe, two key seed-dispersers (a marsupial and a bird), and a pollinator (hummingbird). Our results demonstrate that the gains and losses of species are both consequences and drivers of global change that can lead to underappreciated cascading coextinctions through the disruption of mutualisms.

Tradeoffs, competition, and coexistence in eastern deciduous forest ant communities.

Ecologists have long sought to explain the coexistence of multiple potentially competing species in local assemblages. This is especially challenging in species-rich assemblages in which interspecific competition is intense, as it often is in ant assemblages. As a result, a suite of mechanisms has been proposed to explain coexistence among potentially competing ant species: the dominance-discovery tradeoff, the dominance-thermal tolerance tradeoff, spatial segregation, temperature-based niche partitioning, and temporal niche partitioning. Through a series of observations and experiments, we examined a deciduous forest ant assemblage in eastern North America for the signature of each of these coexistence mechanisms. We failed to detect evidence for any of the commonly suggested mechanisms of coexistence, with one notable exception: ant species appear to temporally partition foraging times such that behaviourally dominant species foraged more intensely at night, while foraging by subdominant species peaked during the day. Our work, though focused on a single assemblage, indicates that many of the commonly cited mechanisms of coexistence may not be general to all ant assemblages. However, temporal segregation may play a role in promoting coexistence among ant species in at least some ecosystems, as it does in many other organisms.

Ecological consistency across space: a synthesis of the ecological aspects of Dromiciops gliroides in Argentina and Chile.

Dromiciops gliroides is an arboreal marsupial found in the temperate forests of South America (36-43 °S). This species is the sole extant representative of the order Microbiotheria, and is a key seed disperser of many native plant species, including the keystone mistletoe Tristerix corymbosus. Here, we synthesized the current knowledge on the ecological aspects of this species, and compared the available information from Argentina and Chile. Population density (23 ± 2 (mean ± SE) individual/ha) and home range (1.6 ± 0.6 ha) appear to be relatively similar across a marked ecological gradient in the mainland, but lower densities (7 ± 2 individual/ha) and smaller home ranges (0.26 ± 0.04 ha) were detected at island sites. We detected regional variation in body condition in Chile, but there were no significant differences across a wider E-W gradient. Movement patterns fit a random walk model; such behavior might have important consequences in shaping plant's spatial patterns. Although our data suggest that D. gliroides is more tolerant to habitat disturbance than previously thought, its incapability to disperse across non-forested areas suggests that the rapid rate of habitat loss and fragmentation that characterizes southern temperate forests likely poses a serious threat to this species. These ecological similarities are surprising given that forests studied receive dramatically different rainfall and correspond to distinct forest types. The evidence synthetized here dispels some of the myths about this species but also stresses the need for more comprehensive ecological studies across its distribution range.

Benefits for plants in ant-plant protective mutualisms: a meta-analysis.

Costs and benefits for partners in mutualistic interactions can vary greatly, but surprisingly little is known about the factors that drive this variation across systems. We conducted a meta-analysis of ant-plant protective mutualisms to quantify the effects of ant defenders on plant reproductive output, to evaluate if reproductive effects were predicted from reductions in herbivory and to identify characteristics of the plants, ants and environment that explained variation in ant protection. We also compared our approach with two other recent meta-analyses on ant-plant mutualisms, emphasizing differences in our methodology (using a weighted linear mixed effects model) and our focus on plant reproduction rather than herbivore damage. Based on 59 ant and plant species pairs, ant presence increased plant reproductive output by 49% and reduced herbivory by 62%. The effects on herbivory and reproduction within systems were positively correlated, but the slope of this relationship (0.75) indicated that tolerance to foliar herbivory may be a common plant response to absence of ant guards. Furthermore, the relationship between foliar damage and reproduction varied substantially among systems, suggesting that herbivore damage is not a reliable surrogate for fitness consequences of ant protection. Studies that experimentally excluded ants reported a smaller effect of ant protection on plant reproduction than studies that relied upon natural variation in ant presence, suggesting that study methods can affect results in these systems. Of the ecological variables included in our analysis, only plant life history (i.e., annual or perennial) explained variation in the protective benefit of mutualistic ants: presence of ants benefitted reproduction of perennials significantly more than that of annuals. These results contrast with other quantitative reviews of these relationships that did not include plant life history as an explanatory factor and raise several questions to guide future research on ant-plant protection mutualisms.

Quantitative analysis of the effects of the exotic Argentine ant on seed-dispersal mutualisms.

Although it is increasingly clear that exotic invasive species affect seed-dispersal mutualisms, a synthetic examination of the effect of exotic invasive species on seed-dispersal mutualisms is lacking. Here, we review the impacts of the invasive Argentine ant (Linepithema humile) on seed dispersal. We found that sites with L. humile had 92 per cent fewer native ant seed dispersers than did sites where L. humile was absent. In addition, L. humile did not replace native seed dispersers, as rates of seed removal and seedling establishment were all lower in the presence of L. humile than in its absence. We conclude that potential shifts in plant diversity and concomitant changes in ecosystem function may be a consequence of Argentine ant invasions, as well as invasions by other ant species. Because very few studies have examined the effects of non-ant invasive species on seed-dispersal mutualisms, the prevalence of disruption of seed-dispersal mutualisms by invasive species is unclear.