Buffering and phenological mismatch: a change of perspective

The potential for climate change to disrupt phenology-mediated interactions in interaction networks has attracted considerable attention in recent decades. Frequently, studies emphasise the fragility of ephemeral seasonal interactions, and the risks posed by phenological asynchrony. Here, we argue that the fitness consequences of asynchrony in phenological interactions may often be more buffered than is typically acknowledged. We identify three main forms that buffering may take: (i) mechanisms that reduce asynchrony between consumer and resource; (ii) mechanisms that reduce the costs of being asynchronous; and (iii) mechanisms that dampen interannual variance in performance across higher organisational units. Using synchrony between the hatching of winter moth caterpillars and the leafing of their host-plants as a case study, we identify a wide variety of buffers that reduce the detrimental consequences of phenological asynchrony on caterpillar individuals, populations, and meta-populations. We follow this by drawing on examples across a breadth of taxa, and demonstrate that these buffering mechanisms may be quite general. We conclude by identifying key gaps in our knowledge of the fitness and demographic consequences of buffering, in the context of phenological mismatch. Buffering has the potential to substantially alter our understanding of the biotic impacts of future climate change—a greater recognition of the contribution of these mechanisms may reveal that many trophic interactions are surprisingly resilient, and also serve to shift research emphasis to those systems with fewer buffers and towards identifying the limits of those buffers

Buffering and trophic mismatch in spring-feeding forest caterpillars

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

The genome sequence of the vapourer moth, Orgyia antiqua (Linnaeus, 1758)

We present a genome assembly from an individual male Orgyia antiqua specimen (the Vapourer moth; Arthropoda; Insecta; Lepidoptera; Erebidae). The genome sequence is 480.1 megabases in span. Most of the assembly is scaffolded into 14 chromosomal pseudomolecules, including the Z sex chromosome. The mitochondrial genome has also been assembled and is 15.4 kilobases in length. Gene annotation of this assembly on Ensembl identified 12,475 protein coding genes

Development and validation of the Arizona Cognitive Test Battery for Down syndrome

Neurocognitive assessment in individuals with intellectual disabilities requires a well-validated test battery. To meet this need, the Arizona Cognitive Test Battery (ACTB) has been developed specifically to assess the cognitive phenotype in Down syndrome (DS). The ACTB includes neuropsychological assessments chosen to 1) assess a range of skills, 2) be non-verbal so as to not confound the neuropsychological assessment with language demands, 3) have distributional properties appropriate for research studies to identify genetic modifiers of variation, 4) show sensitivity to within and between sample differences, 5) have specific correlates with brain function, and 6) be applicable to a wide age range and across contexts. The ACTB includes tests of general cognitive ability and prefrontal, hippocampal and cerebellar function. These tasks were drawn from the Cambridge Neuropsychological Testing Automated Battery (CANTAB) and other established paradigms. Alongside the cognitive testing battery we administered benchmark and parent-report assessments of cognition and behavior. Individuals with DS (n = 74, ages 7–38 years) and mental age (MA) matched controls (n = 50, ages 3–8 years) were tested across 3 sites. A subsample of these groups were used for between-group comparisons, including 55 individuals with DS and 36 mental age matched controls. The ACTB allows for low floor performance levels and participant loss. Floor effects were greater in younger children. Individuals with DS were impaired on a number ACTB tests in comparison to a MA-matched sample, with some areas of spared ability, particularly on tests requiring extensive motor coordination. Battery measures correlated with parent report of behavior and development. The ACTB provided consistent results across contexts, including home vs. lab visits, cross-site, and among individuals with a wide range of socio-economic backgrounds and differences in ethnicity. The ACTB will be useful in a range of outcome studies, including clinical trials and the identification of important genetic components of cognitive disability

Effects of antiplatelet therapy on stroke risk by brain imaging features of intracerebral haemorrhage and cerebral small vessel diseases: subgroup analyses of the RESTART randomised, open-label trial

Background Findings from the RESTART trial suggest that starting antiplatelet therapy might reduce the risk of recurrent symptomatic intracerebral haemorrhage compared with avoiding antiplatelet therapy. Brain imaging features of intracerebral haemorrhage and cerebral small vessel diseases (such as cerebral microbleeds) are associated with greater risks of recurrent intracerebral haemorrhage. We did subgroup analyses of the RESTART trial to explore whether these brain imaging features modify the effects of antiplatelet therapy

Interleukin 12B (IL12B) Genetic Variation and Pulmonary Tuberculosis: A Study of Cohorts from The Gambia, Guinea-Bissau, United States and Argentina

We examined whether polymorphisms in interleukin-12B (IL12B) associate with susceptibility to pulmonary tuberculosis (PTB) in two West African populations (from The Gambia and Guinea-Bissau) and in two independent populations from North and South America. Nine polymorphisms (seven SNPs, one insertion/deletion, one microsatellite) were analyzed in 321 PTB cases and 346 controls from Guinea-Bissau and 280 PTB cases and 286 controls from The Gambia. For replication we studied 281 case and 179 control African-American samples and 221 cases and 144 controls of European ancestry from the US and Argentina. First-stage single locus analyses revealed signals of association at IL12B 3′ UTR SNP rs3212227 (unadjusted allelic p = 0.04; additive genotypic p = 0.05, OR = 0.78, 95% CI [0.61–0.99]) in Guinea-Bissau and rs11574790 (unadjusted allelic p = 0.05; additive genotypic p = 0.05, OR = 0.76, 95% CI [0.58–1.00]) in The Gambia. Association of rs3212227 was then replicated in African-Americans (rs3212227 allelic p = 0.002; additive genotypic p = 0.05, OR = 0.78, 95% CI [0.61–1.00]); most importantly, in the African-American cohort, multiple significant signals of association (seven of the nine polymorphisms tested) were detected throughout the gene. These data suggest that genetic variation in IL12B, a highly relevant candidate gene, is a risk factor for PTB in populations of African ancestry, although further studies will be required to confirm this association and identify the precise mechanism underlying it

Grand challenges in entomology: priorities for action in the coming decades

Entomology is key to understanding terrestrial and freshwater ecosystems at a time of unprecedented anthropogenic environmental change and offers substantial untapped potential to benefit humanity in a variety of ways, from improving agricultural practices to managing vector-borne diseases and inspiring technological advances. We identified high priority challenges for entomology using an inclusive, open, and democratic four-stage prioritisation approach, conducted among the membership and affiliates (hereafter ‘members’) of the UK-based Royal Entomological Society (RES). A list of 710 challenges was gathered from 189 RES members. Thematic analysis was used to group suggestions, followed by an online vote to determine initial priorities, which were subsequently ranked during an online workshop involving 37 participants. The outcome was a set of 61 priority challenges within four groupings of related themes: (i) ‘Fundamental Research’ (themes: Taxonomy, ‘Blue Skies’ [defined as research ideas without immediate practical application], Methods and Techniques); (ii) ‘Anthropogenic Impacts and Conservation’ (themes: Anthropogenic Impacts, Conservation Options); (iii) ‘Uses, Ecosystem Services and Disservices’ (themes: Ecosystem Benefits, Technology and Resources [use of insects as a resource, or as inspiration], Pests); (iv) ‘Collaboration, Engagement and Training’ (themes: Knowledge Access, Training and Collaboration, Societal Engagement). Priority challenges encompass research questions, funding objectives, new technologies, and priorities for outreach and engagement. Examples include training taxonomists, establishing a global network of insect monitoring sites, understanding the extent of insect declines, exploring roles of cultivated insects in food supply chains, and connecting professional with amateur entomologists. Responses to different challenges could be led by amateur and professional entomologists, at all career stages. Overall, the challenges provide a diverse array of options to inspire and initiate entomological activities and reveal the potential of entomology to contribute to addressing global challenges related to human health and well-being, and environmental change

Grand challenges in entomology: Priorities for action in the coming decades

Entomology is key to understanding terrestrial and freshwater ecosystems at a time of unprecedented anthropogenic environmental change and offers substantial untapped potential to benefit humanity in a variety of ways, from improving agricultural practices to managing vector-borne diseases and inspiring technological advances. We identified high priority challenges for entomology using an inclusive, open, and democratic four-stage prioritisation approach, conducted among the membership and affiliates (hereafter ‘members’) of the UK-based Royal Entomological Society (RES). A list of 710 challenges was gathered from 189 RES members. Thematic analysis was used to group suggestions, followed by an online vote to determine initial priorities, which were subsequently ranked during an online workshop involving 37 participants. The outcome was a set of 61 priority challenges within four groupings of related themes: (i) ‘Fundamental Research’ (themes: Taxonomy, ‘Blue Skies’ [defined as research ideas without immediate practical application], Methods and Techniques); (ii) ‘Anthropogenic Impacts and Conservation’ (themes: Anthropogenic Impacts, Conservation Options); (iii) ‘Uses, Ecosystem Services and Disservices’ (themes: Ecosystem Benefits, Technology and Resources [use of insects as a resource, or as inspiration], Pests); (iv) ‘Collaboration, Engagement and Training’ (themes: Knowledge Access, Training and Collaboration, Societal Engagement). Priority challenges encompass research questions, funding objectives, new technologies, and priorities for outreach and engagement. Examples include training taxonomists, establishing a global network of insect monitoring sites, understanding the extent of insect declines, exploring roles of cultivated insects in food supply chains, and connecting professional with amateur entomologists. Responses to different challenges could be led by amateur and professional entomologists, at all career stages. Overall, the challenges provide a diverse array of options to inspire and initiate entomological activities and reveal the potential of entomology to contribute to addressing global challenges related to human health and well-being, and environmental change

Grand challenges in entomology: priorities for action in the coming decades

1. Entomology is key to understanding terrestrial and freshwater ecosystems at a time of unprecedented anthropogenic environmental change and offers substantial untapped potential to benefit humanity in a variety of ways, from improving agricultural practices to managing vector-borne diseases and inspiring technological advances. 2. We identified high priority challenges for entomology using an inclusive, open, and democratic four-stage prioritisation approach, conducted among the membership and affiliates (hereafter ‘members’) of the UK-based Royal Entomological Society (RES). 3. A list of 710 challenges was gathered from 189 RES members. Thematic analysis was used to group suggestions, followed by an online vote to determine initial priorities, which were subsequently ranked during an online workshop involving 37 participants. 4. The outcome was a set of 61 priority challenges within four groupings of related themes: (i) ‘Fundamental Research’ (themes: Taxonomy, ‘Blue Skies’ [defined as research ideas without immediate practical application], Methods and Techniques); (ii) ‘Anthropogenic Impacts and Conservation’ (themes: Anthropogenic Impacts, Conservation Options); (iii) ‘Uses, Ecosystem Services and Disservices’ (themes: Ecosystem Benefits, Technology and Resources [use of insects as a resource, or as inspiration], Pests); (iv) ‘Collaboration, Engagement and Training’ (themes: Knowledge Access, Training and Collaboration, Societal Engagement). 5. Priority challenges encompass research questions, funding objectives, new technologies, and priorities for outreach and engagement. Examples include training taxonomists, establishing a global network of insect monitoring sites, understanding the extent of insect declines, exploring roles of cultivated insects in food supply chains, and connecting professional with amateur entomologists. Responses to different challenges could be led by amateur and professional entomologists, at all career stages. 6. Overall, the challenges provide a diverse array of options to inspire and initiate entomological activities and reveal the potential of entomology to contribute to addressing global challenges related to human health and well-being, and environmental change