Ontogenetic variation in metabolic rate-temperature relationships during larval development.

Predictive models of ectotherm responses to environmental change often rely on thermal performance data from the literature. For insects, the majority of these data focus on two traits, development rate and thermal tolerance limits. Data are also often limited to the adult stage. Consequently, predictions based on these data generally ignore other measures of thermal performance and do not account for the role of ontogenetic variation in thermal physiology across the complex insect life cycle. Theoretical syntheses for predicting metabolic rate also make similar assumptions despite the strong influence of body size as well as temperature on metabolic rate. The aim of this study was to understand the influence of ontogenetic variation on ectotherm physiology and its potential impact on predictive modeling. To do this we examined metabolic rate-temperature (MR-T) relationships across the larval stage in a laboratory strain of the Spongy moth (Lymantria dispar dispar). Routine metabolic rates (RMR) of larvae were assayed at eight temperatures across the first five instars of the larval stage. After accounting for differences in body mass, larval instars showed significant variation in MR-T. Both the temperature sensitivity and allometry of RMR increased and peaked during the third instar, then declined in the fourth and fifth instar. Generally, these results show that insect thermal physiology does not remain static during larval ontogeny and suggest that ontogenetic variation should be an important consideration when modeling thermal performance.

Growth and development of an invasive forest insect under current and future projected temperature regimes.

Temperature and its impact on fitness are fundamental for understanding range shifts and population dynamics under climate change. Geographic climate heterogeneity, behavioral and physiological plasticity, and thermal adaptation to local climates make predicting the responses of species to climate change complex. Using larvae from seven geographically distinct wild populations in the eastern United States of the non-native forest pest Lymantria dispar dispar (L.), we conducted a simulated reciprocal transplant experiment in environmental chambers using six custom temperature regimes representing contemporary conditions near the southern and northern extremes of the US invasion front and projections under two climate change scenarios for the year 2050. Larval growth and development rates increased with climate warming compared with current thermal regimes and tended to be greater for individuals originally sourced from southern rather than northern populations. Although increases in growth and development rates with warming varied somewhat by region of the source population, there was not strong evidence of local adaptation, southern populations tended to outperform those from northern populations in all thermal regimes. Our study demonstrates the utility of simulating thermal regimes under climate change in environmental chambers and emphasizes how the impacts from future increases in temperature can vary based on geographic differences in climate-related performance among populations.

Ecological super-spreaders drive host-range oscillations: Omicron and risk space for emerging infectious disease.

The unusual genetic diversity of the Omicron strain has led to speculation about its origin. The mathematical modelling platform developed for the Stockholm Paradigm (SP) indicates strongly that it has retro-colonized humans from an unidentified nonhuman mammal, likely originally infected by humans. The relationship between Omicron and all other SARS-CoV-2 variants indicates oscillations among hosts, a core part of the SP. Such oscillations result from the emergence of novel variants following colonization of new hosts, replenishing and expanding the risk space for disease emergence. The SP predicts that pathogens colonize new hosts using pre-existing capacities. Those events are thus predictable to a certain extent. Novel variants emerge after a colonization and are not predictable. This makes it imperative to take proactive measures for anticipating emerging infectious diseases (EID) and mitigating their impact. The SP suggests a policy protocol, DAMA, to accomplish this goal. DAMA comprises: DOCUMENT to detect pathogens before they emerge in new places or colonize new hosts; ASSESS to determine risk; MONITOR to detect changes in pathogen populations that increase the risk of outbreaks and ACT to prevent outbreaks when possible and minimize their impact when they occur.

Phoresy in animals: review and synthesis of a common but understudied mode of dispersal.

Phoresy is a type of interaction in which one species, the phoront, uses another species, the dispersal host, for transportation to new habitats or resources. Despite being a widespread behaviour, little is known about the ecology and evolution of phoresy. Our goal is to provide a comprehensive review of phoretic dispersal in animals and to bring renewed attention to this subject. We surveyed literature published between 1900 and 2020 to understand the extent of known higher-level taxonomic diversity (phyla, classes, and orders) and functional aspects of animals that use phoretic dispersal. Species dispersing phoretically have been observed in at least 13 animal phyla, 25 classes, and 60 orders. The majority of known phoronts are arthropods (Phylum Euarthropoda) in terrestrial habitats, but phoronts also occur in freshwater and marine environments. Marine phoronts may be severely under-represented in the literature due to the relative difficulty of studying these systems. Phoronts are generally small with low mobility and use habitats or resources that are ephemeral and/or widely dispersed. Many phoronts are also parasites. In general, animals that engage in phoresy use a wide variety of morphological and behavioural traits for locating, attaching to, and detaching from dispersal hosts, but the exact mechanisms behind these activities are largely unknown. In addition to diversity, we discuss the evolution of phoresy including the long-standing idea that it can be a precursor to parasitism and other forms of symbioses. Finally, we suggest several areas of future research to improve our understanding of phoresy and its ecological and evolutionary significance.

Thermal Sensitivity of Gypsy Moth (Lepidoptera: Erebidae) During Larval and Pupal Development.

As global temperatures rise, thermal limits play an increasingly important role in determining the persistence and spread of invasive species. Gypsy moth (Lymantria dispar L. Lepidoptera: Erebidae) in North America provides an ideal system for studying the effect of high temperatures on invasive species performance. Here, we used fluctuating temperature regimes and exposed gypsy moth at specific points in development (first-fourth instar, pupa) to cycles of favorable (22-28°C) or high-temperature treatments (30-36°C, 32-38°C, 34-40°C) for either 2 or 7 d. We measured survival, growth, and prolonged effects of exposure on development time and pupal mass. Survival generally decreased as the experimental temperature treatment and duration of exposure increased for all instars and pupae, with a narrow threshold for lethal effects. In response to increasing temperature and magnified by longer exposure times, growth abruptly declined for third instars and development time increased for pupae. For those surviving the 2-d exposure treatment, development time to pupation increased for all instars, but we did not find consistent effects on final pupal mass. These negative effects of high temperature provide important data on the susceptibility of gypsy moth to heat at different points in development. This work improves our understanding of thermal limits to growth and development in gypsy moth and can aid in determining invasion potential under current and future climates.

Geographic Variation in Larval Metabolic Rate Between Northern and Southern Populations of the Invasive Gypsy Moth.

Thermal regimes can diverge considerably across the geographic range of a species, and accordingly, populations can vary in their response to changing environmental conditions. Both local adaptation and acclimatization are important mechanisms for ectotherms to maintain homeostasis as environments become thermally stressful, which organisms often experience at their geographic range limits. The spatial spread of the gypsy moth (Lymantria dispar L.) (Lepidoptera: Erebidae) after introduction to North America provides an exemplary system for studying population variation in physiological traits given the gradient of climates encompassed by its current invasive range. This study quantifies differences in resting metabolic rate (RMR) across temperature for four populations of gypsy moth, two from the northern and two from southern regions of their introduced range in North America. Gypsy moth larvae were reared at high and low thermal regimes, and then metabolic activity was monitored at four temperatures using stop-flow respirometry to test for an acclimation response. For all populations, there was a significant increase in RMR as respirometry test temperature increased. Contrary to our expectations, we did not find evidence for metabolic adaptation to colder environments based on our comparisons between northern and southern populations. We also found no evidence for an acclimation response of RMR to rearing temperature for three of the four pairwise comparisons examined. Understanding the thermal sensitivity of metabolic rate in gypsy moth, and understanding the potential for changes in physiology at range extremes, is critical for estimating continued spatial spread of this invasive species both under current and potential future climatic constraints.

Upper thermal limits differ among and within component species in a tritrophic host-parasitoid-hyperparasitoid system.

Understanding how climate change affects host-parasite systems and predicting the consequences for ecosystems, economies, and human health has emerged as an important task for science and society. Some basic insight into this complex problem can be gained by comparing the thermal physiology of interacting host and parasite species. In this study, we compared upper thermal tolerance among three component species in a natural host-parasitoid-hyperparasitoid system from Virginia, USA. To assess the ecological relevance of our results, we also examined a record of maximum daily air temperatures collected near the study site in the last 124 years. We found that the caterpillar host Manduca sexta had a critical thermal maximum (CTmax) about 4°C higher than the parasitic wasp, Cotesia congregata, and the hyperparasitic wasp, Conura sp., had a CTmax about 6°C higher than its host, C. congregata. We also found significant differences in CTmax among instars and between parasitized and non-parasitized M. sexta. The highest maximum daily air temperature recorded near the study in the last 124 years was 42°C, which equals the average CTmax of one species (C. congregata) but is several degrees lower than the average CTmax of the other two species (M. sexta, Conura sp.) in this study. Our results combined with other studies suggest that significant differences in thermal performance within and among interacting host and parasite species are common in nature and that climate change may be largely disruptive to these systems with responses that are highly variable and complex.

Acorn size and tolerance to seed predators: the multiple roles of acorns as food for seed predators, fruit for dispersal and fuel for growth.

Fitness of parents and offspring is affected by offspring size. In oaks (Quercus spp.), acorns vary considerably in size across, and within, species. Seed size influences dispersal and establishment of oaks, but it is not known whether size imparts tolerance to seed predators. Here, we examine the relative extent to which cotyledon size serves as both a means for sustaining partial consumption and energy reserves for developing seedlings during early stages of establishment. Acorns of 6 oak species were damaged to simulate acorn predation by vertebrate and invertebrate seed predators. Seedling germination/emergence and growth rates were used to assess seedling performance. We predicted that if cotyledons are important for dispersal, acorns should show tolerance to partial seed consumption. Alternatively, if the cotyledon functions primarily as an energy reserve, damage should significantly influence seedling performance. Acorns of each species germinated and produced seedlings even after removing >50% of the cotyledon. Seed mass explained only some of the variation in performance. Within species, larger acorns performed better than smaller acorns when damaged. Undamaged acorns performed as well or better than damaged acorns. There was no pattern among individual species with increasing amounts of damage. In some species, simulated invertebrate damage resulted in the poorest performance, suggesting alternative strategies of oaks to sustain damage. Large cotyledons in acorns may be important for attracting seed dispersers and sustaining partial damage, while also providing energy to young seedlings. Success of oak establishment may follow from the resilience of acorns to sustain damage at an early stage.

Reduced Mitochondrial Efficiency Explains Mismatched Growth and Metabolic Rate at Supraoptimal Temperatures.

The relationship between whole-organism growth and metabolism is generally assumed to be positive and causative; higher metabolic rates support higher growth rates. In Manduca sexta, existing data demonstrate a deviation from this simple prediction: at supraoptimal temperatures for larval growth, metabolic rate keeps increasing while growth rate is decreasing. This mismatch presumably reflects the rising "cost of maintenance" with temperature. Precisely what constitutes this cost is not clear, but we suspect the efficiency with which mitochondria harness oxygen and organic substrates into cellular energy (ATP) is key. We tested this by integrating existing data on M. sexta growth and metabolism with new data on mitochondrial bioenergetics across the temperature range 14°-42°C. Across this range, our measure of mitochondrial efficiency closely paralleled larval growth rates. At supraoptimal temperatures for growth, mitochondrial efficiency was reduced, which could explain the mismatch between growth and metabolism observed at the whole-organism level.

Organismal responses to habitat change: herbivore performance, climate and leaf traits in regenerating tropical dry forests.

The ecological effects of large-scale climate change have received much attention, but the effects of the more acute form of climate change that results from local habitat alteration have been less explored. When forest is fragmented, cut, thinned, cleared or otherwise altered in structure, local climates and microclimates change. Such changes can affect herbivores both directly (e.g. through changes in body temperature) and indirectly (e.g. through changes in host plant traits). We advance an eco-physiological framework to understand the effects of changing forests on herbivorous insects. We hypothesize that if tropical forest caterpillars are climate and resource specialists, then they should have reduced performance outside of mature forest conditions. We tested this hypothesis with a field experiment contrasting the performance of Rothschildia lebeau (Saturniidae) caterpillars feeding on the host plant Casearia nitida (Salicaceae) in two different aged and structured tropical dry forests in Area de Conservación Guanacaste, Costa Rica. Compared to more mature closed-canopy forest, in younger secondary forest we found that: (1) ambient conditions were hotter, drier and more variable; (2) caterpillar growth and development were reduced; and (3) leaves were tougher, thicker and drier. Furthermore, caterpillar growth and survival were negatively correlated with these leaf traits, suggesting indirect host-mediated effects of climate on herbivores. Based on the available evidence, and relative to mature forest, we conclude that reduced herbivore performance in young secondary forest could have been driven by changes in climate, leaf traits (which were likely climate induced) or both. However, additional studies will be needed to provide more direct evidence of cause-and-effect and to disentangle the relative influence of these factors on herbivore performance in this system.

Predator diversity reduces habitat colonization by mosquitoes and midges.

Changes in predator diversity via extinction and invasion are increasingly widespread and can have important ecological and socio-economic consequences. Anticipating and managing these consequences requires understanding how predators shape ecological communities. Previous predator biodiversity research has focused on post-colonization processes. However, predators can also shape communities by altering patterns of prey habitat selection during colonization. The sensitivity of this non-consumptive top down mechanism to changes in predator diversity is largely unexamined. To address this gap, we examined patterns of dipteran oviposition habitat selection in experimental aquatic habitats in response to varied predator species richness while holding predator abundance constant. Caged predators were used in order to disentangle behavioural oviposition responses to predator cues from potential post-oviposition consumption of eggs and larvae. We hypothesized that because increases in predator richness often result in greater prey mortality than would be predicted from independent effects of predators, prey should avoid predator-rich habitats during colonization. Consistent with this hypothesis, predator-rich habitats received 48% fewer dipteran eggs than predicted, including 60% fewer mosquito eggs and 38% fewer midge eggs. Our findings highlight the potentially important links between predator biodiversity, prey habitat selection and the ecosystem service of pest regulation.

Budget-limited thermal biology: Design, construction and performance of a large, walk-in style temperature-controlled chamber.

We describe a partial redesign of the conventional air-conditioning system and apply it to the construction of a relatively large (1.87m(3) air mass), walk-in style temperature-controlled chamber (TCC) using parts easily obtained in most countries. We conducted several tests to demonstrate the performance of the TCC. Across the physiologically relevant range of 5-37°C, the TCC took 26.5-50.0min to reach the desired set point temperature. Once at set point, temperature inside the chamber was controlled with an accuracy of ±1.0°C. User-entry effects on deviations from and return times to set point temperature were minimal. Overall, performance of the TCC was sufficient to make precise physiological measurements of insect metabolic rate while controlling assay temperature. Major advantages of the TCC include its simplicity, flexibility, and low cost.

Understanding Host-Switching by Ecological Fitting.

Despite the fact that parasites are highly specialized with respect to their hosts, empirical evidence demonstrates that host switching rather than co-speciation is the dominant factor influencing the diversification of host-parasite associations. Ecological fitting in sloppy fitness space has been proposed as a mechanism allowing ecological specialists to host-switch readily. That proposal is tested herein using an individual-based model of host switching. The model considers a parasite species exposed to multiple host resources. Through time host range expansion can occur readily without the prior evolution of novel genetic capacities. It also produces non-linear variation in the size of the fitness space. The capacity for host colonization is strongly influenced by propagule pressure early in the process and by the size of the fitness space later. The simulations suggest that co-adaptation may be initiated by the temporary loss of less fit phenotypes. Further, parasites can persist for extended periods in sub-optimal hosts, and thus may colonize distantly related hosts by a "stepping-stone" process.

Performance of Wild and Laboratory-Reared Gypsy Moth (Lepidoptera: Erebidae): A Comparison between Foliage and Artificial Diet.

The effects of long-term mass rearing of laboratory insects on ecologically relevant traits is an important consideration when applying research conclusions to wild populations or developing management strategies. Laboratory strains of the gypsy moth, Lymantria dispar (L.), an invasive forest pest in North America, have been continuously reared since 1967. Selection on these strains has enhanced a variety of traits, resulting in faster development, shorter diapause, and greater fecundity. As in many mass-reared insects, laboratory strains of the gypsy moth are also reared exclusively on artificial diets that lack much of the phytochemical and nutritional complexity associated with natural foliage. We tested for differences in growth and development of wild gypsy moth populations from across the invasive range in comparison to laboratory strains when reared on artificial diet and a preferred foliage host species, northern red oak (Quercus rubra L.). Overall, caterpillars reared on foliage had higher survival and faster development rates, with smaller differences among populations. When reared on artificial diet, laboratory strains had the highest performance as expected. The response from the wild populations was mixed, with two populations performing poorly on artificial diet and another performing nearly as well as the laboratory strains. Performance on diet was enhanced when larvae received cubed portions changed regularly, as opposed to filled cups. Understanding these relationships between food source and population performance is important for informing studies that examine population comparisons using wild and laboratory-reared strains.

Multi level ecological fitting: indirect life cycles are not a barrier to host switching and invasion.

Many invasive species are able to escape from coevolved enemies and thus enjoy a competitive advantage over native species. However, during the invasion phase, non-native species must overcome many ecological and/or physiological hurdles before they become established and spread in their new habitats. This may explain why most introduced species either fail to establish or remain as rare interstitials in their new ranges. Studies focusing on invasive species have been based on plants or animals where establishment requires the possession of preadapted traits from their native ranges that enables them to establish and spread in their new habitats. The possession of preadapted traits that facilitate the exploitation of novel resources or to colonize novel habitats is known as 'ecological fitting'. Some species have evolved traits and life histories that reflect highly intimate associations with very specific types of habitats or niches. For these species, their phenological windows are narrow, and thus the ability to colonize non-native habitats requires that a number of conditions need to be met in accordance with their more specialized life histories. Some of the strongest examples of more complex ecological fitting involve invasive parasites that require different animal hosts to complete their life cycles. For instance, the giant liver fluke, Fascioloides magna, is a major parasite of several species of ungulates in North America. The species exhibits a life cycle whereby newly hatched larvae must find suitable intermediate hosts (freshwater snails) and mature larvae, definitive hosts (ungulates). Intermediate and definitive host ranges of F. magna in its native range are low in number, yet this parasite has been successfully introduced into Europe where it has become a parasite of native European snails and deer. We discuss how the ability of these parasites to overcome multiple ecophysiological barriers represents an excellent example of 'multiple-level ecological fitting'.

An integrated parasitology: revealing the elephant through tradition and invention.

The field of parasitology contributes to the elucidation of patterns and processes in evolution, ecology, and biogeography that are of fundamental importance across the biosphere, leading to a thorough understanding of biodiversity and varied responses to global change. Foundations from taxonomic and systematic information drive biodiversity discovery and foster considerable infrastructure and integration of research programs. Morphological, physiological, behavioral, life-history, and molecular data can be synthesized to discover and describe global parasite diversity, in a timely manner. In fully incorporating parasitology in policies for adaptation to global change, parasites and their hosts should be archived and studied within a newly emergent conceptual universe (the 'Stockholm Paradigm'), embracing the inherent complexity of host-parasite systems and improved explanatory power to understand biodiversity past, present, and future.

A macrophysiological analysis of energetic constraints on geographic range size in mammals.

Physiological processes are essential for understanding the distribution and abundance of organisms, and recently, with widespread attention to climate change, physiology has been ushered back to the forefront of ecological thinking. We present a macrophysiological analysis of the energetics of geographic range size using combined data on body size, basal metabolic rate (BMR), phylogeny and range properties for 574 species of mammals. We propose three mechanisms by which interspecific variation in BMR should relate positively to geographic range size: (i) Thermal Plasticity Hypothesis, (ii) Activity Levels/Dispersal Hypothesis, and (iii) Energy Constraint Hypothesis. Although each mechanism predicts a positive correlation between BMR and range size, they can be further distinguished based on the shape of the relationship they predict. We found evidence for the predicted positive relationship in two dimensions of energetics: (i) the absolute, mass-dependent dimension (BMR) and (ii) the relative, mass-independent dimension (MIBMR). The shapes of both relationships were similar and most consistent with that expected from the Energy Constraint Hypothesis, which was proposed previously to explain the classic macroecological relationship between range size and body size in mammals and birds. The fact that this pattern holds in the MIBMR dimension indicates that species with supra-allometric metabolic rates require among the largest ranges, above and beyond the increasing energy demands that accrue as an allometric consequence of large body size. The relationship is most evident at high latitudes north of the Tropics, where large ranges and elevated MIBMR are most common. Our results suggest that species that are most vulnerable to extinction from range size reductions are both large-bodied and have elevated MIBMR, but also, that smaller species with elevated MIBMR are at heightened risk. We also provide insights into the global latitudinal trends in range size and MIBMR and more general issues of phylogenetic and geographic scale.

New macroecological insights into functional constraints on mammalian geographical range size.

Understanding the determinants of variation in the extent of species distributions is a fundamental goal of ecology. The diversity of geographical range sizes (GRSs) in mammals spans 12 orders of magnitude. A long-standing macroecological model of this diversity holds that as body size increases, species are increasingly restricted to occupying larger GRS. Here, we show that the body size-GRS relationship is more complex than previously recognized. Our study reveals that the positive relationship between body size and GRS does not hold across the entire size range of mammals. Instead, there is a break point in the relationship around the modal mammal body size. For species smaller than the mode, GRS actually decreases with body size. We discuss mechanisms to account for these observations in the context of the energetics of body size. We also examine the possibility that the patterns are the result of a statistical artefact from combining two random, uni-modal, skewed distributions, but conclude that the patterns we describe are not artefactual. Our results redefine our view of the functional relationship between body size, energetics and GRS in mammals with implications for assessing vulnerability to extinction resulting from range size reductions driven by large-scale environmental change.

Ability of chestnut oak to tolerate acorn pruning by rodents: The role of the cotyledonary petiole.

Acorns of many white oak species germinate soon after autumn seed fall, a characteristic widely interpreted as a general adaptation to escape predation by small rodents. However, the mechanism by which early, rapid germination allows escape and/or tolerance of seed damage remains unclear. Here we reported how specific germination traits of chestnut oak (Quercus montana) acorns, and those of other white oak species, allow successful escape from acorn pruning by rodents. During germination, chestnut oak acorns develop elongated cotyledonary petioles, which extend beyond the distal end of the acorn (1-2 cm) to the point at which the epicotyl and radicle diverge. However, granivorous rodents often prune the taproots above or below the plumule when eating or caching these germinated acorns in autumn. Hence, we hypothesized elongation of cotyledonary petioles allows chestnut oaks to escape acorn pruning by rodents. We simulated pruning by rodents by cutting the taproot at different stages of germination (radicle length) to evaluate the regeneration capacity of four resulting seedling remnants following taproot pruning: acorns with the plumule (remnant I), acorns without the plumule (remnant II), and pruned taproots with (remnant III) or without the plumule (remnant IV). Our results showed that remnant I germinated into seedlings regardless of the length of the taproot previously pruned and removed. Remnant III successfully germinated and survived provided that taproots were ≥6 cm in length, whereas remnant IV was unable to produce seedlings. Remnant II only developed adventitious roots near the severed ends of the cotyledonary petioles. Field experiments also showed that pruned taproots with the plumule successfully regenerated into seedlings. We suggest that the elongated cotyledonary petioles, typical of most white oak species in North America, represent a key adaptation that allows frequent escape from rodent damage and predation. The ability of pruned taproots to produce seedlings suggests a far greater resilience of white oaks to seed predation than previously anticipated.