Buffering and trophic mismatch in spring-feeding forest caterpillars
Weir, Jamie C.
Across temperate environments, climate warming is leading to a general advancement of spring phenology in a wide range of ecologically and taxonomically diverse species. For taxa that depend on interactions with other species—predators and prey, pollinators, parasites and hosts—widespread phenological changes may cause severe problems. Divergent phenological responses to spring temperature changes among taxa could result in these crucial biotic interactions becoming mistimed. This may cause significant negative fitness effects that could ripple through a population, across trophic levels, and perhaps entire ecosystems. This concept, formalised as the match-mismatch hypothesis (MMH) has become the subject of intense speculation and debate in recent decades. Much of our understanding of the occurrence and significance of ‘phenological mismatch’ (negative fitness consequences brought about by mistiming between interacting species) due to climate change comes from the trophic interactions in the classic temperate woodland tree/caterpillar/bird food-chain. This work, however, suffers from many limitations. Spring-feeding caterpillars, forming the central link in this food-chain, are particularly important in that fluctuations in their populations can affect both higher and lower trophic levels. In the tree/caterpillar link, previous literature focuses largely on a single host and caterpillar species pairing: oak (Quercus robur) and the winter moth (Operophtera brumata). It has been argued that these caterpillars could respond more strongly than their host-plants to climate warming in terms of shifting their phenology, and that even slight mistiming between the two trophic levels has significant negative fitness effects for them. Caterpillars that hatch before bud-burst on their host tree will likely starve, and those that hatch too late are forced to feed on less palatable mature foliage. This rather narrow view, however, overlooks the fact that these caterpillars may be resilient to mistiming in many instances, and that the oak/winter moth trophic interaction may not necessarily be representative of the many other caterpillar species, or alternative host-plant species. In this thesis, I attempt to expand our knowledge and understanding of the operation of the MMH in this system by specifically addressing some of these key caveats. First, in Chapter 2, in order to address the role of different plant species in the diet of the winter moth and the relative importance of oak as a host-plant species, I consider the effects of host-plant species on survival, growth, and development of the caterpillars, across four British populations. I find that winter moth caterpillar fitness varies substantially across host-plant species, but that there are also strong population-specific responses consistent with genetic divergence. In contrast to the assumptions typically made in the literature that oak is the “primary”, “principal”, or most significant host-plant species in the field, I find that caterpillar performance on this species is consistently poor relative to other abundant and widespread host-plant species. Reconciling this apparent inconsistency represents an obvious avenue for future research. A taxonomically broad diet may serve to buffer winter moth caterpillars against the effects of mismatch on any one host-plant species—phenology varies across hosts and, averaged across a population, this might ensure there are always some food resources available for individuals to exploit. Next, in Chapters 3 and 4, to determine whether the impacts of mismatch generalise across caterpillar and host-plant species, I directly test the effects of mistiming across a range of British spring-feeding caterpillar species, including the winter moth. In Chapter 3, I consider the effects of late-hatching asynchrony on performance (and fitness in the winter moth) of up to 65 days. I find that the effects of asynchrony on performance are contingent on the particular caterpillar/host-plant species pairing in question. Depending on the host-plant species, some caterpillar species show little to no decline in performance across a period of several months (e.g. vapourer Orgyia antiqua on birch Betula pendula or sycamore Acer pseudoplatanus), while others show precipitous declines in a matter of days (e.g. fitness in winter moth on sycamore or sallow Salix caprea). This highlights the danger of extrapolating from a single caterpillar/host-plant species pairing. Indeed, in both cases, the winter moth and oak appear to be exceptional—performance of the former typically showing a steeper than average decline with increasing asynchrony, and the latter being a generally poor host for most spring-feeding caterpillar species, on which performance declines at a greater rate than other host-plants with asynchrony. Overall, I find that, in contrast to the prevailing view in the literature, synchrony is important for caterpillar fitness, but within fairly broad bounds (at a scale of weeks and months, rather than days), though this varies across hosts and species. In Chapter 4, I consider asynchrony in the opposite direction, and investigate the ability of spring-feeding caterpillars to cope with hatching too early, before bud-burst on their natal tree. Early hatching caterpillars can simply tolerate a lack of food and wait until it becomes available, or they may be able to exploit the unopened buds of their host-plants as a food source in the intervening period. I found that across five spring-feeding caterpillar species, there is often a considerable ability to tolerate starvation, ranging from several days in the winter moth and mottled umber Erannis defoliaria, to over thirty in the black arches Lymantria monacha. Increased temperatures, however, significantly reduced the time which caterpillars could survive without food, often by a substantial margin (e.g. by twenty days in the black arches moth at temperatures of 21°C versus 5°C). In the winter moth, I show experimentally for the first time that caterpillars are indeed able to feed on the unopened and opening buds of a range of their host-plant species. However, the likelihood of establishment on buds is initially low and increases steeply as buds mature and softer tissue becomes more exposed. Nonetheless, this clearly demonstrates that many spring-feeding caterpillar species have at least some ability to tolerate early hatching on their host tree. In Chapter 5, I consider in more detail the widely-held assumption that foliage becomes unsuitable for caterpillar consumption very soon after bud-burst. In contrast to Chapter 3, I reared caterpillars on frozen foliage collected from a sample of trees across a two week period after bud-burst, to determine the effects of any changes in their structure and secondary chemistry across this period on palatability. Specifically, I focussed here on the effects of caterpillar asynchrony on growth rate and rate of survival across time, both of which have distinct fitness implications versus overall mass attained or survival probability (cf. Chapter 3). I find no consistent effects of leaf age on rates of mortality across time, suggesting that leaf maturation occurring within the first two weeks after bud-burst generally has little effect on caterpillar performance. There are, however, significant effects of host-plant species and age on growth rates—on older oak foliage, growth rates are higher, the implications of which are unclear. Additionally, I find that there is substantial variation in caterpillar performance between individual trees and broods. Taken together, these findings may indicate that phenological variation between individual trees could serve to ameliorate mismatch, buffering against it at the population level. Finally, in Chapter 6, I discuss the concept of ‘buffering’ in detail—a phrase widely used but little considered. I argue that buffering is related to concepts of stability in living systems, and that it represents the means by which stability is maintained, via a range of ‘buffering mechanisms’. I define buffering as “the amelioration of any fitness effects resulting from an environmental change”. I explore the concept specifically within the spring-feeding caterpillar system, and argue that the very unpredictability and uncertainty that is an inherent part of their niche has driven the evolution of many of the buffering mechanisms by which that variation can be tolerated. By extension, I propose that a predisposition to tolerating environmental uncertainty may mean these species will be buffered against at least some of the negative effects of future climate change, such as an increased incidence of asynchrony. Taken together, my analyses suggest that the overwhelming focus placed on the winter moth/oak interaction in literature on the MMH is likely to be misleading—these taxa are not necessarily representative of other species at these trophic levels in the woodland food web, and the effects of asynchrony on caterpillar performance and fitness is highly contingent on both taxa involved. It is therefore difficult and perhaps unwise to make excessively broad generalisations about the effects of climate change on the broader spring-feeding caterpillar guild, and any cascading effects to other species with which they interact. Contrary to the widespread view in the literature, the caterpillars of a range of moth species seem able to cope with at least some degree of both early- and late-hatching asynchrony: by feeding on a range of host-plant species; by tolerating more mature foliage; by tolerating starvation when food is unavailable; and, by utilising the young, unopened buds of their host-plants as food. These traits may equally well buffer caterpillars against potential mismatch resulting from divergent phenological responses to future climatic change relative to their host-plants. More broadly, this particular instance highlights the potential general importance of buffering as a phenomenon in other groups of organisms, where it could play a key role in ameliorating some of the negative effects of climate change.