Inferring coevolution in a plant–pollinator network

Mutualistic interactions are at the core of community dynamics, determining dispersal, colonization and differential survival and reproduction among individuals and species. Mutualistic interactions therefore affect the fitness of interaction partners, hence modifying their respective evolutionary trajectories reciprocally, potentially leading to coevolution. Although mathematical models predict coevolution in mutualistic interaction networks, no empirical data are available. By taking into account the patterns of interactions and reconstructing evolutionary change in plant and pollinator traits, we tested the hypothesis that coevolution occurs between plants and insects that interact more frequently, or more symmetrically. To test this hypothesis, we built an interaction network with data from five flowering seasons, measured plant and insect morphology, mapped morphology on the plant and insect phylogenies, and reconstructed ancestral character changes based on maximum parsimony. We calculated an index, called the coevolutionary ratio, which represents the amount of correlated change in traits that mediate the interaction between plants and pollinators (i.e. proboscis versus corolla length, and body width and corolla aperture). Our results suggest that high frequency of interaction, i.e. the number of times two species interact, does not lead to coevolution. Instead, symmetry of interaction strength, i.e. the reciprocal similarity in the mutual effect of interaction partners, may lead to coevolution, in spite of a pervasive lack of reciprocal specialization and high interaction frequency. Although the statistical signal is quite weak, our results hold for three statistical tests of very different nature. The most specialized species, expected to be under directional selection, do not show more evolutionary change than do generalist species, expected to be under different, perhaps opposing, selective pressures. By dissecting the complexity of an interaction network we show that coevolution may partially shape functional morphology of interaction partners, thus providing the closest evidence to date of mutualistic adaptation of organisms within a community.     

The challenge of novel abiotic conditions for species undergoing climate-induced range shifts

Coincident with recent global warming, species have shifted their geographic distributions to cooler environments, generally by moving along thermal axes to higher latitudes, higher elevations or deeper waters. While these shifts allow organisms to track their thermal niche, these three thermal axes also covary with non-climatic abiotic factors that could pose challenges to range-shifting plants and animals. Such novel abiotic conditions also present an unappreciated pitfall for researchers – from both empirical and predictive viewpoints – who study the redistribution of species under global climate change. Climate, particularly temperature, is often assumed to be the primary abiotic factor in limiting species distributions, and decades of thermal biology research have made the correlative and mechanistic understanding of temperature the most accessible and commonly used response to any abiotic factor. Receiving far less attention, however, is that global gradients in oxygen, light, pressure, pH and water availability also covary with latitude, elevation, and/or ocean depth, and species show strong physiological and behavioral adaptations to these abiotic variables within their historic ranges. Here, we discuss how non-climatic abiotic factors may disrupt climate-driven range shifts, as well as the variety of adaptations species use to overcome abiotic conditions, emphasizing which taxa may be most limited in this capacity. We highlight the need for scientists to extend their research to incorporate non-climatic, abiotic factors to create a more ecologically relevant understanding of how plants and animals interact with the environment, particularly in the face of global climate change. We demonstrate how additional abiotic gradients can be integrated into global climate change biology to better inform expectations and provide recommendations for addressing the challenge of predicting future species distributions in novel environments.     

Upward elevation and northwest range shifts for alpine Meconopsis species in the Himalaya–Hengduan Mountains region

Climate change may impact the distribution of species by shifting their ranges to higher elevations or higher latitudes. The impacts on alpine plant species may be particularly profound due to a potential lack of availability of future suitable habitat. To identify how alpine species have responded to climate change during the past century as well as to predict how they may react to possible global climate change scenarios in the future, we investigate the climatic responses of seven species of Meconopsis, a representative genus endemic in the alpine meadow and subnival region of the Himalaya–Hengduan Mountains. We analyzed past elevational shifts, as well as projected shifts in longitude, latitude, elevation, and range size using historical specimen records and species distribution modeling under optimistic (RCP 4.5) and pessimistic (RCP 8.5) scenarios across three general circulation models for 2070. Our results indicate that across all seven species, there has been an upward shift in mean elevation of 302.3 m between the pre‐1970s (1922–1969) and the post‐1970s (1970–2016). The model predictions suggest that the future suitable climate space will continue to shift upwards in elevation (as well as northwards and westwards) by 2070. While for most of the analyzed species, the area of suitable climate space is predicted to expand under the optimistic emission scenario, the area contracts, or, at best, shows little change under the pessimistic scenario. Species such as M. punicea, which already occupy high latitudes, are consistently predicted to experience a contraction of suitable climate space across all the models by 2070 and may consequently deserve particular attention by conservation strategies. Collectively, our results suggest that the alpine high‐latitude species analyzed here have already been significantly impacted by climate change and that these trends may continue over the coming decades.     

Opportunistic attachment assembles plant–pollinator networks

Species and interactions are being lost at alarming rates and it is imperative to understand how communities assemble if we have to prevent their collapse and restore lost interactions. Using an 8‐year dataset comprising nearly 20 000 pollinator visitation records, we explore the assembly of plant–pollinator communities at native plant restoration sites in an agricultural landscape. We find that species occupy highly dynamic network positions through time, causing the assembly process to be punctuated by major network reorganisations. The most persistent pollinator species are also the most variable in their network positions, contrary to what preferential attachment – the most widely studied theory of ecological network assembly – predicts. Instead, we suggest assembly occurs via an opportunistic attachment process. Our results contribute to our understanding of how communities assembly and how species interactions change through time while helping to inform efforts to reassemble robust communities.     

Pollinators visit related plant species across 29 plant–pollinator networks

Understanding the evolution of specialization in host plant use by pollinators is often complicated by variability in the ecological context of specialization. Flowering communities offer their pollinators varying numbers and proportions of floral resources, and the uniformity observed in these floral resources is, to some degree, due to shared ancestry. Here, we find that pollinators visit related plant species more so than expected by chance throughout 29 plant–pollinator networks of varying sizes, with “clade specialization” increasing with community size. As predicted, less versatile pollinators showed more clade specialization overall. We then asked whether this clade specialization varied with the ratio of pollinator species to plant species such that pollinators were changing their behavior when there was increased competition (and presumably a forced narrowing of the realized niche) by examining pollinators that were present in at least three of the networks. Surprisingly, we found little evidence that variation in clade specialization is caused by pollinator species changing their behavior in different community contexts, suggesting that clade specialization is observed when pollinators are either restricted in their floral choices due to morphological constraints or innate preferences. The resulting pollinator sharing between closely related plant species could result in selection for greater pollinator specialization.     

Species traits and climate velocity explain geographic range shifts in an ocean‐warming hotspot

Species' ranges are shifting globally in response to climate warming, with substantial variability among taxa, even within regions. Relationships between range dynamics and intrinsic species traits may be particularly apparent in the ocean, where temperature more directly shapes species' distributions. Here, we test for a role of species traits and climate velocity in driving range extensions in the ocean‐warming hotspot of southeast Australia. Climate velocity explained some variation in range shifts, however, including species traits more than doubled the variation explained. Swimming ability, omnivory and latitudinal range size all had positive relationships with range extension rate, supporting hypotheses that increased dispersal capacity and ecological generalism promote extensions. We find independent support for the hypothesis that species with narrow latitudinal ranges are limited by factors other than climate. Our findings suggest that small‐ranging species are in double jeopardy, with limited ability to escape warming and greater intrinsic vulnerability to stochastic disturbances.     

Interaction rewiring and the rapid turnover of plant–pollinator networks

Whether species interactions are static or change over time has wide‐reaching ecological and evolutionary consequences. However, species interaction networks are typically constructed from temporally aggregated interaction data, thereby implicitly assuming that interactions are fixed. This approach has advanced our understanding of communities, but it obscures the timescale at which interactions form (or dissolve) and the drivers and consequences of such dynamics. We address this knowledge gap by quantifying the within‐season turnover of plant–pollinator interactions from weekly censuses across 3 years in a subalpine ecosystem. Week‐to‐week turnover of interactions (1) was high, (2) followed a consistent seasonal progression in all years of study and (3) was dominated by interaction rewiring (the reassembly of interactions among species). Simulation models revealed that species’ phenologies and relative abundances constrained both total interaction turnover and rewiring. Our findings reveal the diversity of species interactions that may be missed when the temporal dynamics of networks are ignored.     

Protected areas not likely to serve as steppingstones for species undergoing climate-induced range shifts

Species across the planet are shifting their ranges to track suitable climate conditions in response to climate change. Given that protected areas have higher quality habitat and often harbor higher levels of biodiversity compared to unprotected lands, it is often assumed that protected areas can serve as steppingstones for species undergoing climate-induced range shifts. However, there are several factors that may impede successful range shifts among protected areas, including the distance that must be traveled, unfavorable human land uses and climate conditions along potential movement routes, and lack of analogous climates. Through a species-agnostic lens, we evaluate these factors across the global terrestrial protected area network as measures of climate connectivity, which is defined as the ability of a landscape to facilitate or impede climate-induced movement. We found that over half of protected land area and two-thirds of the number of protected units across the globe are at risk of climate connectivity failure, casting doubt on whether many species can successfully undergo climate-induced range shifts among protected areas. Consequently, protected areas are unlikely to serve as steppingstones for a large number of species under a warming climate. As species disappear from protected areas without commensurate immigration of species suited to the emerging climate (due to climate connectivity failure), many protected areas may be left with a depauperate suite of species under climate change. Our findings are highly relevant given recent pledges to conserve 30% of the planet by 2030 (30 × 30), underscore the need for innovative land management strategies that allow for species range shifts, and suggest that assisted colonization may be necessary to promote species that are adapted to the emerging climate.     

Thermoregulatory traits combine with range shifts to alter the future of montane ant assemblages

Predicting and understanding the biological response to future climate change is a pressing challenge for humanity. In the 21st century, many species will move into higher latitudes and higher elevations as the climate warms. In addition, the relative abundances of species within local assemblages are likely to change. Both effects have implications for how ecosystems function. Few biodiversity forecasts, however, take account of both shifting ranges and changing abundances. We provide a novel analysis predicting the potential changes to assemblage‐level relative abundances in the 21st century. We use an established relationship linking ant abundance and their colour and size traits to temperature and UV‐B to predict future abundance changes. We also predict future temperature driven range shifts and use these to alter the available species pool for our trait‐mediated abundance predictions. We do this across three continents under a low greenhouse gas emissions scenario (RCP2.6) and a business‐as‐usual scenario (RCP8.5). Under RCP2.6, predicted changes to ant assemblages by 2100 are moderate. On average, species richness will increase by 26%, while species composition and relative abundance structure will be 26% and 30% different, respectively, compared with modern assemblages. Under RCP8.5, however, highland assemblages face almost a tripling of species richness and compositional and relative abundance changes of 66% and 77%. Critically, we predict that future assemblages could be reorganized in terms of which species are common and which are rare: future highland assemblages will not simply comprise upslope shifts of modern lowland assemblages. These forecasts reveal the potential for radical change to montane ant assemblages by the end of the 21st century if temperature increases continue. Our results highlight the importance of incorporating trait–environment relationships into future biodiversity predictions. Looking forward, the major challenge is to understand how ecosystem processes will respond to compositional and relative abundance changes.     

Illuminating geographical patterns in species' range shifts

Species' range shifts in response to ongoing climate change have been widely documented, but although complex spatial patterns in species' responses are expected to be common, comprehensive comparisons of species' ranges over time have undergone little investigation. Here, we outline a modeling framework based on historical and current species distribution records for disentangling different drivers (i.e. climatic vs. nonclimatic) and assessing distinct facets (i.e. colonization, extirpation, persistence, and lags) of species' range shifts. We used extensive monitoring data for stream fish assemblages throughout France to assess range shifts for 32 fish species between an initial period (1980–1992) and a contemporary one (2003–2009). Our results provide strong evidence that the responses of individual species varied considerably and exhibited complex mosaics of spatial rearrangements. By dissociating range shifts in climatically suitable and unsuitable habitats, we demonstrated that patterns in climate‐driven colonization and extirpation were less marked than those attributed to nonclimatic drivers, although this situation could rapidly shift in the near future. We also found evidence that range shifts could be related to some species' traits and that the traits involved varied depending on the facet of range shift considered. The persistence of populations in climatically unsuitable areas was greater for short‐lived species, whereas the extent of the lag behind climate change was greater for long‐lived, restricted‐range, and low‐elevation species. We further demonstrated that nonclimatic extirpations were primarily related to the size of the species' range, whereas climate‐driven extirpations were better explained by thermal tolerance. Thus, the proposed framework demonstrated its potential for markedly improving our understanding of the key processes involved in range shifting and also offers a template for informing management decisions. Conservation strategies would greatly benefit from identifying both the geographical patterns and the species' traits associated with complex modifications of species' distributions in response to global changes.     

Lags in the response of mountain plant communities to climate change

Rapid climatic changes and increasing human influence at high elevations around the world will have profound impacts on mountain biodiversity. However, forecasts from statistical models (e.g. species distribution models) rarely consider that plant community changes could substantially lag behind climatic changes, hindering our ability to make temporally realistic projections for the coming century. Indeed, the magnitudes of lags, and the relative importance of the different factors giving rise to them, remain poorly understood. We review evidence for three types of lag: “dispersal lags” affecting plant species’ spread along elevational gradients, “establishment lags” following their arrival in recipient communities, and “extinction lags” of resident species. Variation in lags is explained by variation among species in physiological and demographic responses, by effects of altered biotic interactions, and by aspects of the physical environment. Of these, altered biotic interactions could contribute substantially to establishment and extinction lags, yet impacts of biotic interactions on range dynamics are poorly understood. We develop a mechanistic community model to illustrate how species turnover in future communities might lag behind simple expectations based on species’ range shifts with unlimited dispersal. The model shows a combined contribution of altered biotic interactions and dispersal lags to plant community turnover along an elevational gradient following climate warming. Our review and simulation support the view that accounting for disequilibrium range dynamics will be essential for realistic forecasts of patterns of biodiversity under climate change, with implications for the conservation of mountain species and the ecosystem functions they provide.     

Projecting marine species range shifts from only temperature can mask climate vulnerability

Climate change is causing range shifts in many marine species, with implications for biodiversity and fisheries. Previous research has mainly focused on how species' ranges will respond to changing ocean temperatures, without accounting for other environmental covariates that could affect future distribution patterns. Here, we integrate habitat suitability modeling approaches, a high‐resolution global climate model projection, and detailed fishery‐independent and ‐dependent faunal datasets from one of the most extensively monitored marine ecosystems—the U.S. Northeast Shelf. We project the responses of 125 species in this region to climate‐driven changes in multiple oceanographic factors (e.g., ocean temperature, salinity, sea surface height) and seabed characteristics (i.e., rugosity and depth). Comparing model outputs based on ocean temperature and seabed characteristics to those that also incorporated salinity and sea surface height (proxies for primary productivity and ocean circulation features), we explored how an emphasis on ocean temperature in projecting species' range shifts can impact assessments of species' climate vulnerability. We found that multifactor habitat suitability models performed better in explaining and predicting species historical distribution patterns than temperature‐based models. We also found that multifactor models provided more concerning assessments of species' future distribution patterns than temperature‐based models, projecting that species' ranges will largely shift northward and become more contracted and fragmented over time. Our results suggest that using ocean temperature as a primary determinant of range shifts can significantly alter projections, masking species' climate vulnerability, and potentially forestalling proactive management.     

Combined effects of climate and biotic interactions on the elevational range of a phytophagous insect

1. The ranges of many species have expanded in cool regions but contracted at warm margins in response to recent climate warming, but the mechanisms behind such changes remain unclear. Particular debate concerns the roles of direct climatic limitation vs. the effects of interacting species in explaining the location of low latitude or low elevation range margins. 2. The mountains of the Sierra de Guadarrama (central Spain) include both cool and warm range margins for the black-veined white butterfly, Aporia crataegi, which has disappeared from low elevations since the 1970s without colonizing the highest elevations. 3. We found that the current upper elevation limit to A. crataegi's distribution coincided closely with that of its host plants, but that the species was absent from elevations below 900 m, even where host plants were present. The density of A. crataegi per host plant increased with elevation, but overall abundance of the species declined at high elevations where host plants were rare. 4. The flight period of A. crataegi was later at higher elevations, meaning that butterflies in higher populations flew at hotter times of year; nevertheless, daytime temperatures for the month of peak flight decreased by 6.2 degrees C per 1 km increase in elevation. 5. At higher elevations A. crataegi eggs were laid on the south side of host plants (expected to correspond to hotter microclimates), whereas at lower sites the (cooler) north side of plants was selected. Field transplant experiments showed that egg survival increased with elevation. 6. Climatic limitation is the most likely explanation for the low elevation range margin of A. crataegi, whereas the absence of host plants from high elevations sets the upper limit. This contrasts with the frequent assumption that biotic interactions typically determine warm range margins, and thermal limitation cool margins. 7. Studies that have modelled distribution changes in response to climate change may have underestimated declines for many specialist species, because range contractions will be exacerbated by mismatch between the future distribution of suitable climate space and the availability of resources such as host plants.     

Ecological correlates of range shifts of Late Pleistocene mammals

Understanding and predicting how species' distributions will shift as climate changes are central questions in ecology today. The late Quaternary of North America represents a natural experiment in which we can evaluate how species responded during the expansion and contraction of the glaciers. Here, we ask whether species' range shifts differ because of taxonomic affinity, life-history traits, body size or topographic heterogeneity and whether the species survived the megafaunal extinction. There was no difference in range shifts between victims and survivors of the megafaunal extinction. In general, the change in the size of a species' range is not well correlated with any of the ecological or life-history traits evaluated. However, there are significant relationships between some variables and the movements of the centroids of ranges. Differences in the distances shifted exist among orders, although this is probably a result of body size differences as larger bodied species show larger shifts. Although there are a few exceptions, the distance that species shifted their range was weakly correlated with life-history traits. Finally, species in more topographically heterogeneous areas show smaller shifts than species in less-diverse areas. Overall, these results indicate that when trying to predict species range shifts in the future, body size, lifespan and the topographic relief of the landscape should be taken into account.     

Intraspecific variation in herbivore‐induced plant volatiles influences the spatial range of plant–parasitoid interactions

Chemical information influences the behaviour of many animals, thus affecting species interactions. Many animals forage for resources that are heterogeneously distributed in space and time, and have evolved foraging behaviour that utilizes information related to these resources. Herbivore‐induced plant volatiles (HIPVs), emitted by plants upon herbivore attack, provide information on herbivory to various animal species, including parasitoids. Little is known about the spatial scale at which plants attract parasitoids via HIPVs under field conditions and how intraspecific variation in HIPV emission affects this spatial scale. Here, we investigated the spatial scale of parasitoid attraction to two cabbage accessions that differ in relative preference of the parasitoid Cotesia glomerata when plants were damaged by Pieris brassicae caterpillars. Parasitoids were released in a field experiment with plants at distances of up to 60 m from the release site using intervals between plants of 10 or 20 m to assess parasitism rates over time and distance. Additionally, we observed host‐location behaviour of parasitoids in detail in a semi‐field tent experiment with plant spacing up to 8 m. Plant accession strongly affected successful host location in field set‐ups with 10 or 20 m intervals between plants. In the semi‐field set‐up, plant finding success by parasitoids decreased with increasing plant spacing, differed between plant accessions, and was higher for host‐infested plants than for uninfested plants. We demonstrate that parasitoids can be attracted to herbivore‐infested plants over large distances (10 m or 20 m) in the field, and that stronger plant attractiveness via HIPVs increases this distance (up to at least 20 m). Our study indicates that variation in plant traits can affect attraction distance, movement patterns of parasitoids, and ultimately spatial patterns of plant–insect interactions. It is therefore important to consider plant‐trait variation in HIPVs when studying animal foraging behaviour and multi‐trophic interactions in a spatial context.