Climate-driven variation in biotic interactions provides a narrow and variable window of opportunity for an insect herbivore at its ecological margin

Abstract

Climate-driven geographic range shifts have been associated with transitions between dietary specialism and generalism at range margins. The mechanisms underpinning these often transient niche breadth modifications are poorly known, but utilization of novel resources likely depends on phenological synchrony between the consumer and resource. We use a climate-driven range and host shift by the butterfly Aricia agestis to test how climate-driven changes in host phenology and condition affect phenological synchrony, and consider implications for host use. Our data suggest that the perennial plant that was the primary host before range expansion is a more reliable resource than the annual Geraniaceae upon which the butterfly has become specialized in newly colonized parts of its range. In particular, climate-driven phenological variation in the novel host Geranium dissectum generates a narrow and variable ‘window of opportunity' for larval productivity in summer. Therefore, although climatic change may allow species to shift hosts and colonise novel environments, specialization on phenologically limited hosts may not persist at ecological margins as climate change continues. We highlight the potential role for phenological (a)synchrony in determining lability of consumer–resource associations at range margins and the importance of considering causes of synchrony in biotic interactions when predicting range shifts. This article is part of the theme issue ‘Species’ ranges in the face of changing environments (Part II)’.

Understanding the biology of species' ranges: when and how does evolution change the rules of ecological engagement?

“…Models by Alexander et al [ 55 ] support the idea that trade-offs with biotic factors in particular decrease the evolutionary potential of populations at range limits, especially limits that are determined by climate. Also, Stewart et al [ 73 ] consider the butterfly Aricia agestis that has undergone a host shift that has reduced its host plant repertoire at its UK range margin. This host shift has allowed its spread to warming sites further north, probably through the evolution of novel genotypes at the range edge, and the loss of ancestral polyphagy.…”

Environmental variation and biotic interactions limit adaptation at ecological margins: lessons from rainforestDrosophilaand European butterflies

“…One key question in the brown argus story is: Why do southern populations retain the ability to use Geranium as well as the locally dominant host plant when maintaining both forms of preference is apparently costly (given we observe a loss of rockrose use during expansion into habitats where rockrose is rare)? One explanation is that although rockrose may provide a reliable host plant for larval growth in years when springs are wet and cold, it may limit productivity in years when climates are more clement (Stewart et al [81]). In such warmer years, eggs laid on Geranium plants found in low abundance at field margins may produce many adults, allowing local expansion of brown argus populations into neighbouring fields, followed by local contractions into rockrose habitats in cooler years.…”

Introduction to the theme issue ‘Species' ranges in the face of changing environments’

“…For example, Stewart et al . [ 25 ] investigate the role of phenological synchrony between the range-shifting butterfly Aricia agestis and its novel plant hosts at its range edge. Because climate affects the phenology of host plant and butterfly independently, and may, therefore, erode novel host suitability, host shifts may be transitory.…”

“…O'Brien et al . [ 24 ] discuss how ecological constraints imposed by antagonistic biotic interactions can reduce fitness and increase the steepness of environmental gradients, thereby sharpening limits to adaptation at range margins; alternatively, adaptation to new biotic interactions, such as host shifts [ 24 , 25 ], might facilitate rapid range expansion. Biotic interactions can also influence selection at range limits via trade-offs in responses to abiotic and biotic factors, as illustrated by a simple model developed by Alexander et al .…”

“…Here again, biotic interactions can play a key role, because selection, for example to avoid predation or match host phenology [ 26 , 27 ], can help push species towards their thermal limits. Together, studies in this theme issue emphasize that the community context is essential to understanding evolutionary constraints throughout species ranges and that alterations to biotic interactions have both ecological and evolutionary consequences for the dynamics of species' ranges as environments change [ 25 – 27 ].…”