Body Size Responses Research Articles

Body size and the urban heat island effect modulate the temperature–size relationship in ground beetles

AbstractAimBody size is a key trait linked to other life history traits and influences several individual‐, community‐ and ecosystem‐level characteristics, processes, functions and services. Ecological and evolutionary body size responses at the intra‐ and inter‐specific level to thermal geographic gradients (e.g. latitudinal or altitudinal ones) are widely studied. Whether this temperature‐size relationship remains true for community‐wide body size is still largely unknown.LocationNorthern temperate region.TaxonGround beetles (Carabidae).MethodsWe assessed the temperature‐size relationships using data from 11 northern temperate locations, spanning 25 latitudinal degrees. Furthermore, we quantified the effects of potential competing factors, such as body size and habitat preference of carabid assemblages and sub‐assemblages along urbanisation gradients, as well as the urban heat island (UHI) effect on this relationship.ResultsWe found significant negative relationship between the community‐wide mean body size and the geographical latitude (converse Bergmann cline) for the whole ground beetle assemblage and the sub‐assemblages of large‐bodied species. This relationship was stronger in the urban localities than in rural ones. For the sub‐assemblages of small‐sized species, the relationship was not significant. We found significant negative relationship between the community‐wide mean body size and the latitude for the sub‐assemblages of both the non‐forest and the forest species, and these became stronger in the urban habitats.Main ConclusionsOur results highlight the leading role of the individual body size and the UHI effect in determining the community‐wide body size–latitude relationship in ground beetles.

Impact of warming on aquatic body sizes explained by metabolic scaling from microbes to macrofauna

Rising temperatures are associated with reduced body size in many marine species, but the biological cause and generality of the phenomenon is debated. We derive a predictive model for body size responses to temperature and oxygen (O2) changes based on thermal and geometric constraints on organismal O2 supply and demand across the size spectrum. The model reproduces three key aspects of the observed patterns of intergenerational size reductions measured in laboratory warming experiments of diverse aquatic ectotherms (i.e., the "temperature-size rule" [TSR]). First, the interspecific mean and variability of the TSR is predicted from species' temperature sensitivities of hypoxia tolerance, whose nonlinearity with temperature also explains the second TSR pattern-its amplification as temperatures rise. Third, as body size increases across the tree of life, the impact of growth on O2 demand declines while its benefit to O2 supply rises, decreasing the size dependence of hypoxia tolerance and requiring larger animals to contract by a larger fraction to compensate for a thermally driven rise in metabolism. Together our results support O2 limitation as the mechanism underlying the TSR, and they provide a physiological basis for projecting ectotherm body size responses to climate change from microbes to macrofauna. For small species unable to rapidly migrate or evolve greater hypoxia tolerance, ocean warming and O2 loss in this century are projected to induce >20% reductions in body mass. Size reductions at higher trophic levels could be even stronger and more variable, compounding the direct impact of human harvesting on size-structured ocean food webs.

Body size responses to the combined effects of climate and land use changes within an urban framework.

Alterations in body size can have profound impacts on an organism's life history and ecology with long-lasting effects that span multiple biological scales. Animal body size is influenced by environmental drivers, including climate change and land use change, the two largest current threats to biodiversity. Climate warming has led to smaller body sizes of many species due to impacts on growth (i.e., Bergmann's rule and temperature-size rule). Conversely, urbanization, which serves as a model for investigating the effects of land use changes, has largely been demonstrated to cause size increases, but few studies have examined the combined influences of climate and land use changes on organism size. We present here the background theory on how each of these factors is expected to influence body size, summarize existing evidence of how size has recently been impacted by climate and land use changes, and make several recommendations to guide future research uniting these areas of focus. Given the rapid pace of climate change and urbanization, understanding the combined effects of climate and land use changes on body size is imperative for biodiversity preservation.

Increasing Body Sizes in Anomala expansa expansa (Coleoptera: Scarabaeidae) Populations in Response to Rising Temperatures Over Time.

Many insects have been studied over wide geographical areas to determine whether they follow Bergmann's Rule, which predicts that animal clades or populations should have smaller body sizes in warmer climates. While this ecogeographic rule is well supported in mammals and birds, insect latitudinal sizes can show Bergmann, converse Bergmann, or no size clines at all. Museum collections are typical sources of data for insect clines, and long-term collections should reflect rising global temperatures and shifting climates, possibly producing temporal size clines along with any geographical clines. We hypothesize that insects with Bergmann clines geographically will show Bergmann-like clines temporally as well, and that the converse and inverse of this rule are also true. By looking at museum samples going back a century, we tested whether Anomala expansa expansa (Bates, 1866), a species of Scarabaeidae beetle common in lowland Taiwan, was experiencing long-term changes in body size in response to rising temperatures. We found that overall, the size of these beetles increased over time. Within Taipei populations, this increase was correlated with rising average yearly temperatures. The impact of this pest species' rising size with time will need to be monitored, and temporal size clines in other pests need to be investigated.

Small workers are more persistent fighters than soldiers in the highly polymorphic Atta leaf-cutting ants

Social animals often coordinate behavioural activities for the gathering, maintenance and protection of resources. In eusocial insects, morphological and/or behavioural heterogeneity among worker caste allows division of labour and, in some instances, the specialization of individuals in specific tasks. In leaf-cutting ants (genus Atta ), the division of labour is based on body size differences (alloethism), meaning that differently sized workers will likely perform different tasks. Although alloethism is now well understood during foraging and processing of food resources in Atta , the relationship between body size and aggressive response has been poorly investigated, and, so far, it is not well understood how different morphological subcastes are integrated into the defensive strategy. Here, we quantified conspecifc and heterospecific aggression, in a within-colony social context (inside the nest), aiming to test which worker size class (subcaste) exhibits the most aggressive response against non-nestmates (NNMs). Workers were divided into three distinct subcastes, minors, majors and soldiers, and reared in subcolonies containing two individuals of each subcaste, as well as brood and the symbiotic fungus. We found a low probability of aggression towards conspecific NNMs and a high probability towards heterospecific NNMs. Quantification of aggression across subcastes showed that minors directed the most overt physical attacks towards heterospecific NNMs. We suggest that the nest, where minors perform most of their tasks, might constitute a strong social contextual stimulus for them, lowering their response threshold and increasing their aggression towards foreign ants. We also suggest that possible signals (i.e. chemical or mechanical) emitted during interactions involving minors stimulate larger workers to engage in fights, a mechanism that has been demonstrated in other ant species. The integration of size-specific behavioural traits might constitute a very efficient defensive mechanism. • Atta workers show the highest degree of morphological differentiation among ants. • However, the link between body size and aggression is little understood. • We measured aggression towards ant intruders in Atta workers of different size. • We found that the decision to attack an enemy is not related to body size. • Attack persistency, however, is far higher in small than in large workers.

Zooplankton assemblage and body size responses to severe lake eutrophication from agricultural activities near mink farms in Nova Scotia, Canada

Abstract Mink fur farming was once a widespread agricultural activity in southwestern Nova Scotia. Freshwaters near to and downstream of several mink fur farm operations have experienced severe water quality issues, including eutrophication and recurring algal blooms. Here, we use dated lake sediments to examine trends in primary producers and primary consumers from a hypereutrophic lake to assess how cladoceran assemblages have responded to extreme eutrophication. Shifts in the dominant pelagic cladoceran taxa began in the early 1900s, coinciding with an increase in sedimentary chlorophyll-a concentrations. Notably, small-bodied bosminids decreased, while taxa such as Chydorus brevilabris and Daphnia pulex spp. dominated assemblages in recent decades. Bottom-up ecological factors, such as decades of greater primary production, were the likely drivers of assemblage shifts of primary consumers. Consistent body sizes of bosminids throughout the sedimentary record suggested that pelagic cladocerans were not influenced solely by predation pressure from macroinvertebrates or fish. This study provides evidence of large-scale ecological shifts occurring at multiple trophic levels in a hypereutrophic temperate lake with mink farming operations in its catchment.

Body size variability across habitats in the Brachionus plicatilis cryptic species complex

The body size response to temperature is one of the most recognizable but still poorly understood ecological phenomena. Other covarying environmental factors are frequently invoked as either affecting the strength of that response or even driving this pattern. We tested the body size response in five species representing the Brachionus plicatilis cryptic species complex, inhabiting 10 brackish ponds with different environmental characteristics. Principal Component Analysis selected salinity and oxygen concentration as the most important factors, while temperature and pH were less influential in explaining variation of limnological parameters. Path analysis showed a positive interclonal effect of pH on body size. At the interspecific level, the size response was species- and factor-dependent. Under the lack of a natural thermo-oxygenic relationship, the negative response of size to temperature, expected according to ‘size-to-temperature response’ rules, disappeared, but a positive response of size to oxygen, expected according to predictions selecting oxygen as a factor actually driving these rules, remained. Our results confirm the crucial role of oxygen in determining the size-to-temperature patterns observed in the field.

Distinct body-size responses to warming climate in three rodent species.

In mammals, body-size responses to warming climates are diverse, and the mechanisms underlying these different responses have been little investigated. Using temporal and spatial datasets of three rodent species distributed across different climatic zones in China, we investigated temporal and spatial trends of body size (length and mass), identified the critical drivers of these trends, and inferred the potential causes underlying the distinct body-size responses to the critical drivers. We found that body mass of all species remained stable over time and across space. Body length, however, increased in one species over time and in two species across space. Generally, body-length variation was predicted best by minimum ambient temperature. Moreover, in two species, body length changed linearly with temperature differences between ancestral and colonization areas. These distinct temperature-length patterns may jointly be caused by species-specific temperature sensitivities and experienced magnitudes of warming. We hypothesize that species or populations distributed across distinct temperature gradients evolved different intrinsic temperature sensitivities, which affect how their body sizes respond to warming climates. Our results suggest that size trends associated with climate change should be explored at higher temporal and spatial resolutions, and include clades of species with similar distributions.

The steroid hormone ecdysone regulates growth rate in response to oxygen availability

In almost all animals, physiologically low oxygen (hypoxia) during development slows growth and reduces adult body size. The developmental mechanisms that determine growth under hypoxic conditions are, however, poorly understood. Here we show that the growth and body size response to moderate hypoxia (10% O2) in Drosophila melanogaster is systemically regulated via the steroid hormone ecdysone. Hypoxia increases level of circulating ecdysone and inhibition of ecdysone synthesis ameliorates the negative effect of low oxygen on growth. We also show that the effect of ecdysone on growth under hypoxia is through suppression of the insulin/IGF-signaling pathway, via increased expression of the insulin-binding protein Imp-L2. These data indicate that growth suppression in hypoxic Drosophila larvae is accomplished by a systemic endocrine mechanism that overlaps with the mechanism that slows growth at low nutrition. This suggests the existence of growth-regulatory mechanisms that respond to general environmental perturbation rather than individual environmental factors.

A low-sugar diet enhances Drosophila body size in males and females via sex-specific mechanisms.

In Drosophila, changes to dietary protein elicit different body size responses between the sexes. Whether these differential body size effects extend to other macronutrients remains unclear. Here, we show that lowering dietary sugar (0S diet) enhanced body size in male and female larvae. Despite an equivalent phenotypic effect between the sexes, we detected sex-specific changes to signalling pathways, transcription and whole-body glycogen and protein. In males, the low-sugar diet augmented insulin/insulin-like growth factor signalling pathway (IIS) activity by increasing insulin sensitivity, where increased IIS was required for male metabolic and body size responses in 0S. In females reared on low sugar, IIS activity and insulin sensitivity were unaffected, and IIS function did not fully account for metabolic and body size responses. Instead, we identified a female-biased requirement for the Target of rapamycin pathway in regulating metabolic and body size responses. Together, our data suggest the mechanisms underlying the low-sugar-induced increase in body size are not fully shared between the sexes, highlighting the importance of including males and females in larval studies even when similar phenotypic outcomes are observed.

Fungal fruit body assemblages are tougher in harsh microclimates

Forest species are affected by macroclimate, however, the microclimatic variability can be more extreme and change through climate change. Fungal fruiting community composition was affected by microclimatic differences. Here we ask whether differences in the fruiting community can be explained by morphological traits of the fruit body, which may help endure harsh conditions. We used a dead wood experiment and macrofungal fruit body size, color, and toughness. We exposed logs of two host tree species under closed and experimentally opened forest canopies in a random-block design for four years and identified all visible fruit bodies of two fungal lineages (Basidio- and Ascomycota). We found a consistently higher proportion of tough-fleshed species in harsher microclimates under open canopies. Although significant, responses of community fruit body size and color lightness were inconsistent across lineages. We suggest the toughness-protection hypothesis, stating that tough-fleshed fruit bodies protect from microclimatic extremes by reducing dehydration. Our study suggests that the predicted increase of microclimatic harshness with climate change will likely decrease the presence of soft-fleshed fruit bodies. Whether harsh microclimates also affect the mycelium of macrofungi with different fruit body morphology would complement our findings and increase predictability under climate change.

The trace fossil Gyrolithes lorcaensis from the Lower Cretaceous of the Kopet-Dagh Basin, NE Iran

The helical, vertical trace fossil Gyrolithes lorcaensis is described from marine to marginal-marine deposits of the Lower Cretaceous of the Sarcheshmeh Formation near the city Kalat-e-Naderi in the Kopet-Dagh Basin. This is the first report of Gyrolithes from Iran and thus expands the geographic range of this trace fossil. G. lorcaensis is characterized by its unique morphometric parameters, a small burrow size and whorl radius, which distinguishes it as the smallest Gyrolithes ichnospecies. The most likely producers of the Iranian Gyrolithes were crustacean decapods, which is supported by the paleoenvironment (shallow and warm water ramp) in which it is found. The function of the spiral structure in the described Gyrolithes of the Sarcheshmeh Formation can be explained as a permanent dwelling structure with the main purpose of farming bacteria via increasing the surface area of the burrow margin that allows more microbial activities. The small burrow dimensions may reflect reduced burrower body size in response to the dysoxic to anoxic conditions suggested by sedimentological evidence.

Rapid phenotypic change in a polymorphic salamander over 43\xa0years

Color polymorphic animals offer a unique system for studying intraspecific phenotypic responses to climate change. Discrete color morphs are easy to identify, and correlated trait responses of morphs can indicate how climate warming may facilitate long-term maintenance of polymorphisms. We use a historical dataset spanning 43 years to examine temporal shifts in color morph frequency and body size in response to climate in the Eastern Red-backed Salamander, Plethodon cinereus, which contains a widespread striped/unstriped color polymorphism. We created a pipeline to extract high-throughput trait data from fluid-preserved museum specimens where we batch-photographed salamanders, de-aggregated individual specimens from photographs, and solicited help of community scientists to score color morphs. We used a linear modeling framework that includes information about spatial population structure to demonstrate that color morph frequency and body size vary in response to climate, elevation, and over time, with an overall trend of higher frequency and decreased body size of the striped morph, but increased size of the unstriped morph. These surprising results suggest that morphs may be responding to multiple climate and geographic drivers through co-adapted morphological changes. This work highlights new practices of extracting trait data from museum specimens to demonstrate species phenotypes response to climate change.

Towards a modular theory of trophic interactions

Abstract Species traits and environmental conditions determine the occurrence and strength of trophic interactions. If we understand the relationship between these factors and trophic interactions, we can make more accurate predictions and build better trophic‐interaction models. We can compare traits and conditions by considering their effect on different parts (steps) of a trophic interaction, such as the steps search and pursuit. By linking traits to relevant steps, we can use these relationships to build trophic‐interaction models. Currently, this is done ad hoc, defining steps based on the species and traits of interest. This makes it difficult to compare across traits and species and gain an overarching understanding of how traits and the environment drive trophic interactions. We present a comprehensive approach for the explicit choice of interaction steps and species traits or environmental conditions, which is readily integrated into existing models. The core of this framework is that it is modular; we present eight steps that occur in all trophic interactions and use them to build a modular, general dynamic model. When applying the framework, one explicitly selects only the most relevant steps and uses those to build a specific model. To build our modular framework, we revisit and expand the functional and numerical response functions, dividing the trophic interaction into eight steps: (1) search, (2) prey detection, (3) attack decision, (4) pursuit, (5) subjugation, (6) ingestion, (7) digestion and (8) nutrient allocation. Together these steps form a general dynamical model where trophic interactions can be explicitly parameterized for multiple traits and environmental factors. We then concretize this approach by outlining how a specific community can be modelled by selecting key modules (steps) and parameterizing them for relevant factors. This we exemplify for a community of terrestrial arthropods using empirical data on body size and temperature responses. With species interactions at the core of community dynamics, our modular approach allows for quantification and comparisons of the importance of different steps, traits, and abiotic factors across ecosystems and trophic‐interaction types, and provides a powerful tool for trait‐based prediction of food‐web structure and dynamics. A free Plain Language Summary can be found within the Supporting Information of this article.

Comparative genomics suggests local adaptations in the invasive small hive beetle.

Invasive species are a major driver of ecological and environmental changes that affect human health, food security, and natural biodiversity. The success and impact of biological invasions depend on adaptations to novel abiotic and biotic selective pressures. However, the molecular mechanisms underlying adaptations in invasive parasitic species are inadequately understood. Small hive beetles, Aethina tumida, are parasites of bee nests. Originally endemic to sub‐Saharan Africa, they are now found nearly globally. Here, we investigated the molecular bases of the adaptations to novel environments underlying their invasion routes. Genomes of historic and recent adults A. tumida from both the endemic and introduced ranges were compared. Analysis of gene–environment association identified 3049 candidate loci located in 874 genes. Functional annotation showed a significant bias toward genes linked to growth and reproduction. One of the genes from the apoptosis pathway encodes an “ecdysone‐related protein,” which is a crucial regulator in controlling body size in response to environmental cues for holometabolous insects during cell death and renewal. Genes whose proteins regulate organ size, ovary activation, and oviposition were also detected. Functions of these enriched pathways parallel behavioral differences between introduced and native A. tumida populations, which may reflect patterns of local adaptation. The results considerably improve our understanding of the underlying mechanisms and ecological factors driving adaptations of invasive species. Deep functional investigation of these identified loci will help clarify the mechanisms of local adaptation in A. tumida.

The proximate sources of genetic variation in body size plasticity: The relative contributions of feeding behaviour and development in Drosophila melanogaster

Body size is a key life-history trait that influences many aspects of an animal’s biology and is shaped by a variety of factors, both genetic and environmental. While we know that locally-adapted populations differ in the extent to which body size responds plastically to environmental conditions like diet, we have a limited understanding of what causes these differences. We hypothesized that populations could differ in the way body size responds to nutrition either by modulating growth rate, development time, feeding rate, or a combination of the above. Using three locally-adapted populations of Drosophila melanogaster from along the east coast of Australia, we investigated body size plasticity across five different diets. We then assessed how these populations differed in feeding behaviour and developmental timing on each of the diets. We observed population-specific plastic responses to nutrition for body size and feeding rate, but not development time. However, differences in feeding rate did not fully explain the differences in the way body size responded to diet. Thus, we conclude that body size variation in locally-adapted populations is shaped by a combination of growth rate and feeding behaviour. This paves the way for further studies that explore how differences in the regulation of the genetic pathways that control feeding behaviour and growth rate contribute to population-specific responses of body size to diet.

Ectoparasitic fungi Rickia wasmannii infection is associated with smaller body size in Myrmica ants

Parasitism-generated negative effects on ant societies are multifaceted, implying individual and colony-level responses. Though laboratory based evidence shows that the sublethal fungus Rickia wasmannii is responsible for physiological and behavioral responses that may negatively affect individual workers’ resilience and life expectancy in Myrmica ant workers, colony-level stress response to this parasite is largely unknown. Here, we focus on understanding of a long-term, colony-level effect of Rickia infection on Myrmica scabrinodis ant populations by tracking trait size-based changes. We collected worker specimens from infected and uninfected colonies from the same population in order to: (1) compare body size in response to parasitism, (2) assess the extent to which possible changes in size are associated with the severity of infection, and (3) investigate shifts in body size in response to infection over time by testing correlation of workers’ ages and sizes. We found that workers from infected colonies were significantly smaller than their healthy congeners, but neither infection level nor the age of the workers showed significant correlation with the size in infected colonies. Decreasing body sizes in infected colonies can be ascribed to workers’ mediated effect toward developing larvae, which are unable to attain the average body size before they pupate.

Changes in the body size of black-veined white, Aporia crataegi (Lepidoptera: Pieridae), recorded in a natural population in response to different spring weather conditions and at different phases of an outbreak

Changes in body size in response to environmental factors (especially temperature) is one of the crucial traits studied in connection with insect adaptation to climate change. However, current data on the strength and direction of temperature-size responses in Lepidoptera are inconsistent and the reasons for this are unclear. This study investigates the relationship between the adult size of Aporia crataegi L. (Lepidoptera: Pieridae) and spring weather conditions (temperature and rainfall) at different phases in its outbreak cycle (low population density or high abundance). The forewing area of A. crataegi, a univoltine and irruptive Lepidopteran species, was used as a proxy for overall body size. It was found that temperature in the last month before imago emergence (May) and temperature in the larval growth period following overwintering (April) had differing effects on imago size. The fact that the wing size of both male and female A. crataegi increased following higher temperatures in May corresponds with the converse temperature-size rule and is consistent with the predictions of life history theory for univoltine species. Conversely, while imago size decreased following higher temperatures in April, increased rainfall had a slightly positive effect on imago size. The wings of A. crataegi at the peak of abundance were larger than when sampled during periods of low population density, contradicting available data on changes in the body weight of A. crataegi recorded during outbreaks.

Long-term study shows that increasing body size in response to warmer summers is associated with a higher mortality risk in a long-lived bat species.

Change in body size is one of the universal responses to global warming, with most species becoming smaller. While small size in most species corresponds to low individual fitness, small species typically show high population growth rates in cross-species comparisons. It is unclear, therefore, how climate-induced changes in body size ultimately affect population persistence. Unravelling the relationship between body size, ambient temperature and individual survival is especially important for the conservation of endangered long-lived mammals such as bats. Using an individual-based 24-year dataset from four free-ranging Bechstein's bat colonies (Myotis bechsteinii), we show for the first time a link between warmer summer temperatures, larger body sizes and increased mortality risk. Our data reveal a crucial time window in June-July, when juveniles grow to larger body sizes in warmer conditions. Body size is also affected by colony size, with larger colonies raising larger offspring. At the same time, larger bats have higher mortality risks throughout their lives. Our results highlight the importance of understanding the link between warmer weather and body size as a fitness-relevant trait for predicting species-specific extinction risks as consequences of global warming.

Body size and shape responses to warming and resource competition

Abstract Body size is a fundamental trait that impacts many aspects of species biology and ecology. It is, in turn, influenced by a suite of environmental factors, and often decreases with warming. Although environmental conditions can also impact body shape, which is another functional trait that influences locomotion, resource acquisition and potentially physiological processes, such responses are poorly understood and rarely quantified. We experimentally tested the independent and combined effects of environmental temperature, resource level and interspecific competition on the body shape and size responses of two model protist species. We also tested the degree to which these individual‐level phenotypic responses are associated with population densities and species coexistence. Body shape was strongly influenced by resource competition, whereas body size changes were mainly driven by environmental temperature. In both species, lower resource levels resulted in body shape elongation, suggesting that relatively more elongate individuals with potentially higher swimming speed were advantaged in the resource scarce environment. However, competition had contrasting influence on the body shape of the two species. Competition decreased the population densities of Blepharisma japonicum, which exhibited relative body shape elongation, similar to the response at low resource levels. In contrast, competition increased the population densities of Paramecium aurelia, which exhibited reduced elongation similar to body shape response at high resource levels. Hence, body shape responses could be indicative of changes in resource availability, aiding our understanding of competitive hierarchies and species interactions. Coexistence was observed in all treatment combinations, likely because body size of both species decreased similarly under warming, potentially maintaining constant per capita competitive intensity. These findings, along with recent research on phytoplankton, diverse pelagic invertebrates, and birds highlight the importance of body shape and morphology across different taxonomic groups. Hence, we call for body size and shape to be considered in concert when investigating ecological consequences of climate warming. A free Plain Language Summary can be found within the Supporting Information of this article.