Unveiling the environmental drivers of intraspecific body size variation in terrestrial vertebrates

Aim

Whether intraspecific spatial patterns in body size are generalizable across species remains contentious, as well as the mechanisms underlying these patterns. Here we test several hypotheses explaining within-species body size variation in terrestrial vertebrates including the heat balance, seasonality, resource availability and water conservation hypotheses for ectotherms, and the heat conservation, heat dissipation, starvation resistance and resource availability hypotheses for endotherms.

Location

Global.

Time period

1970–2016.

Major taxa studied

Amphibians, reptiles, birds and mammals.

Methods

We collected 235,905 body size records for 2,229 species (amphibians = 36; reptiles = 81; birds = 1,545; mammals = 567) and performed a phylogenetic meta-analysis of intraspecific correlations between body size and environmental variables. We further tested whether correlations differ between migratory and non-migratory bird and mammal species, and between thermoregulating and thermoconforming ectotherms.

Results

For bird species, smaller intraspecific body size was associated with higher mean and maximum temperatures and lower resource seasonality. Size–environment relationships followed a similar pattern in resident and migratory birds, but the effect of resource availability on body size was slightly positive only for non-migratory birds. For mammals, we found that intraspecific body size was smaller with lower resource availability and seasonality, with this pattern being more evident in sedentary than migratory species. No clear size–environment relationships were found for reptiles and amphibians.

Main conclusions

Within-species body size variation across endotherms is explained by disparate underlying mechanisms for birds and mammals. Heat conservation (Bergmann's rule) and heat dissipation are the dominant processes explaining biogeographic intraspecific body size variation in birds, whereas in mammals, body size clines are mostly explained by the starvation resistance and resource availability hypotheses. Our findings contribute to a better understanding of the mechanisms behind species adaptations to the environment across their geographic distributions.     

Laboratory infection of terrestrial isopods (Crustacea: Isopoda) with neoaplectanid and heterorhabditid nematodes (Rhabditida: Nematoda)

Under laboratory conditions, the nematodes Neoaplectana carpocapsae and Heterorhabditis heliothidis were able to infect and develop inside the hemocoel of terrestrial isopods belonging to the genus Porcellio. Armidillidium vulgare was also infected by N. carpocapsae, but this host was less susceptible than Porcellio. Results show that, under suitable ecological conditions, it would be feasible to utilize N. carpocapsae as a biological control agent of sowbugs (Porcellio spp.). This is the first report showing the ability of neoaplectanids and heterorhabditids to invade representatives of the Crustacea.     

Seasonality rather than average temperature explains body size variation in a Neotropical fruit-eating bat

We investigated variation in body size of the widely distributed Neotropical bat Chiroderma villosum across its entire range. Our objective was to verify if the size-related geographic variation in the species is related to environmental variables. We took 13 measurements of 410 specimens from 198 localities in Mesoamerica and South America, and collected information on latitude, longitude, altitude, precipitation, and temperature, totalling 22 variables. We detected clinal variation in size related to latitude and longitude, with a pattern that conforms to the Bergmann's rule. Clinal variation of size along longitude was influenced by the taxonomic component, with subspecies C. v. jesupi being smaller than C. v. villosum. In contrast the latitudinal cline was explained by temperature seasonality and precipitation, with a 14% increase in size between the north and south extremes of the range. In other words, size of individuals is larger in areas with more seasonal oscillations in temperature and with lower precipitation. Our results support the notion that low temperatures alone do not explain large size of mammals in high latitudes. One hypothesis is that large size is favoured in more seasonal climates because somatic growth is faster when resources are abundant, and also larger animals can endure food scarcity better than small ones. We also postulate that pressures related to interspecific competition and resource use may be more intense in more areas marked by seasonal climatic variations. Specifically, a larger size in seasonal areas may allow individuals to explore a wider niche. We suggest that future approaches, refining regional variation in the diet of C. villosum may serve as a further test to this hypothesis.     

The terrestrial isopods (Crustacea) of Aldabra

Among a collection of terrestrial isopods from Aldabra were 13 species, six of which are new: Littorophiloscia aldabrana, Philoscina insularis, Trichorhina triocellata, Nagurus kensleyi, Pseudodiploexochus cuspidatus and Venezillo pseudoparvus. Alloniscus pigmentatus Budde-Lund and Tura angusta Budde-Lund are re-described and figured. The taxonomy of six species of Alloniscus Dana from the Indian Ocean is discussed and Alloniscus nacreus Collinge from Madagascar is illustrated. The species Armadillo parvus Budde-Lund and Sphaerillo collaris Budde-Lund are transferred to the genus Venezillo Verhoeff. The distribution of all the species is given together with the composition of the oniscidean fauna of Aldabra.     

Recent spatial and temporal changes in body size of terrestrial vertebrates: probable causes and pitfalls

Geographical and temporal variations in body size are common phenomena among organisms and may evolve within a few years. We argue that body size acts much like a barometer, fluctuating in parallel with changes in the relevant key predictor(s), and that geographical and temporal changes in body size are actually manifestations of the same drivers. Frequently, the principal predictors of body size are food availability during the period of growth and ambient temperature, which often affects food availability. Food availability depends on net primary productivity that, in turn, is determined by climate and weather (mainly temperature and precipitation), and these depend mainly on solar radiation and other solar activities. When the above predictors are related to latitude the changes have often been interpreted as conforming to Bergmann's rule, but in many cases such interpretations should be viewed with caution due to the interrelationships among various environmental predictors. Recent temporal changes in body size have often been related to global warming. However, in many cases the above key predictors are not related to either latitude and/or year, and it is the task of the researcher to determine which particular environmental predictor is the one that determines food availability and, in turn, body size. The chance of discerning a significant change in body size depends to a large extent on sample size (specimens/year). The most recent changes in body size are probably phenotypic, but there are some cases in which they are partly genetic.     

Effects of group size on aggregation against desiccation in woodlice (Isopoda: Oniscidea)

Aggregation in terrestrial isopods, a behaviour that results in the formation of dense clusters, is readily accepted as a mechanism of resistance to desiccation. Thus, aggregation is considered to be an adaptation to terrestrial life in this fully terrestrial suborder of crustaceans. In the present study of Porcellio scaber Latreille, a cosmopolitan species, individual water loss is investigated experimentally as a function of the size of the aggregates and, for the first time, over a large range of group sizes (groups of 1, 10, 20, 40, 60, 80 and 100 individuals). From the perspective of an isolated individual, aggregation behaviour is effective in reducing the rate of water loss whatever the group size, and reduces the individual water loss rate by more than half in large groups. However, the water loss rate of an individual follows a power law according to group size. Accordingly, if the addition of individuals to small groups strongly reduces the water losses per individual, adding individuals to large groups only slightly reduces the individual water losses. Thus, the successful reduction of the water loss rate by this aggregation behaviour is confirmed, although only up to a certain limit, particularly if the number of individuals per aggregate exceeds 50–60 under the experimental conditions used in the present study. Moreover, the individual surface area exposed to the air, as a function of group size, follows a similar pattern (i.e. a similar power law). Thus, a geometrical explanation is proposed for the nonlinear water losses in woodlice aggregates. These results are discussed in relation to the group sizes observed both in the laboratory and the field.     

The origin of terrestrial isopods (Crustacea: Isopoda: Oniscidea)

Living isopods of the suborder Oniscidea (commonly called woodlice) are the only group of Crustacea almost entirely composed of terrestrial forms. Furthermore, woodlice are completely independent from the aquatic environment from which they originally arose. From marine ancestors, woodlice are a key taxon to study the conquest of the land among arthropods because of their interesting gradation of morphological, physiological and behavioral adaptations for terrestriality. However, the origin and evolution of this model group are still poorly known. Herein, we provide a synthesis of the oniscidean fossil record to replace this group in a deep-time context. Because members of the Oniscidea are difficult to fossilize, their fossil record alone is undoubtedly fragmentary and not representative of their complete evolutionary history, but it maintains an important relevance by providing reference points. To date, the first attested occurrences of Oniscidea are recorded from the Early Cretaceous. At this time, woodlice were already widely distributed (from Western Europe to Eastern Asia) with several species. By evaluating phylogenetic studies, palaeobiogeographic context of fossil specimens and current biological considerations, we discuss and support a pre-Pangaean origin of the Oniscidea, in the Late Paleozoic—most likely during the Carboniferous.     

Life on the edge: carnivore body size variation is all over the place

Evolutionary biologists have long been fascinated by both the ways in which species respond to ecological conditions at the edges of their geographic ranges and the way that species'' body sizes evolve across their ranges. Surprisingly, though, the relationship between these two phenomena is rarely studied. Here, we examine whether carnivore body size changes from the interior of their geographic range towards the range edges. We find that within species, body size often varies strongly with distance from the range edge. However, there is no general tendency across species for size to be either larger or smaller towards the edge. There is some evidence that the smallest guild members increase in size towards their range edges, but results for the largest guild members are equivocal. Whether individuals vary in relation to the distance from the range edges often depends on the way edge and interior are defined. Neither geographic range size nor absolute body size influences the tendency of size to vary with distance from the range edge. Therefore, we suggest that the frequent significant association between body size and the position of individuals along the edge-core continuum reflects the prevalence of geographic size variation and that the distance to range edge per se does not influence size evolution in a consistent way.     

Selection does not favor larger body size at lower temperature in a seed-feeding beetle

Body size of many animals increases with increasing latitude, a phenomenon known as Bergmann's rule (Bergmann clines). Latitudinal gradients in mean temperature are frequently assumed to be the underlying cause of this pattern because temperature covaries systematically with latitude, but whether and how temperature mediates selection on body size is unclear. To test the hypothesis that the "relative" advantage of being larger is greatest at cooler temperatures we compare the fitness of replicate lines of the seed beetle, Stator limbatus, for which body size was manipulated via artificial selection ("Large,"Control," and "Small" lines), when raised at low (22 degrees C) and high (34 degrees C) temperatures. Large-bodied beetles (Large lines) took the longest to develop but had the highest lifetime fecundity, and highest fitness (r(C)), at both low and high temperatures. However, the relative difference between the Large and Small lines did not change with temperature (replicate 2) or was greatest at high temperature (replicate 1), contrary to the prediction that the fitness advantage of being large relative to being small will decline with increasing temperature. Our results are consistent with two previous studies of this seed beetle, but inconsistent with prior studies that suggest that temperature-mediated selection on body size is a major contributor to the production of Bergmann clines. We conclude that other environmental and ecological variables that covary with latitude are more likely to produce the gradient in natural selection responsible for generating Bergmann clines.     

Body size evolution in South American Liolaemus lizards of the boulengeri clade: a contrasting reassessment

Bergmann's rule predicts larger body sizes in species living in higher latitudes and altitudes. This rule appears to be valid for endotherms, but its relevance to ectotherm vertebrates has largely been debated. In squamate reptiles (lizards and snakes), only one study, based on Liolaemus species of the boulengeri clade, has provided phylogenetic evidence in favour of Bergmann's clines. We reassessed this model in the same lizard clade, using a more representative measure of species body size and including a larger number of taxa in the sample. We found no evidence to support Bergmann's rule in this lineage. However, these non-significant results appear to be explained only by the inclusion of further species rather than by a different estimation of body size. Analyses conducted on the 16 species included in the previous study always revealed significant relationships between body size and latitude-altitude, whereas, the enlarged sample always rejected the pattern predicted by Bergmann's rule.     

Global patterns of body size evolution are driven by precipitation in legless amphibians

Body size shapes ecological interactions across and within species, ultimately influencing the evolution of large‐scale biodiversity patterns. Therefore, macroecological studies of body size provide a link between spatial variation in selection regimes and the evolution of animal assemblages through space. Multiple hypotheses have been formulated to explain the evolution of spatial gradients of animal body size, predominantly driven by thermal (Bergmann's rule), humidity (‘water conservation hypothesis’) and resource constraints (‘resource rule’, ‘seasonality rule’) on physiological homeostasis. However, while integrative tests of all four hypotheses combined are needed, the focus of such empirical efforts needs to move beyond the traditional endotherm–ectotherm dichotomy, to instead interrogate the role that variation in lifestyles within major lineages (e.g. classes) play in creating neglected scenarios of selection via analyses of largely overlooked environment–body size interactions. Here, we test all four rules above using a global database spanning 99% of modern species of an entire Order of legless, predominantly underground‐dwelling amphibians (Gymnophiona, or caecilians). We found a consistent effect of increasing precipitation (and resource abundance) on body size reductions (supporting the water conservation hypothesis), while Bergmann's, the seasonality and resource rules are rejected. We argue that subterranean lifestyles minimize the effects of aboveground selection agents, making humidity a dominant selection pressure – aridity promotes larger body sizes that reduce risk of evaporative dehydration, while smaller sizes occur in wetter environments where dehydration constraints are relaxed. We discuss the links between these principles with the physiological constraints that may have influenced the tropically‐restricted global radiation of caecilians.     

Ecological drivers of body size evolution and sexual size dimorphism in short‐horned grasshoppers (Orthoptera: Acrididae)

Sexual size dimorphism (SSD) is widespread and variable in nature. Although female‐biased SSD predominates among insects, the proximate ecological and evolutionary factors promoting this phenomenon remain largely unstudied. Here, we employ modern phylogenetic comparative methods on eight subfamilies of Iberian grasshoppers (85 species) to examine the validity of different models of evolution of body size and SSD and explore how they are shaped by a suite of ecological variables (habitat specialization, substrate use, altitude) and/or constrained by different evolutionary pressures (female fecundity, strength of sexual selection, length of the breeding season). Body size disparity primarily accumulated late in the history of the group and did not follow a Brownian motion pattern, indicating the existence of directional evolution for this trait. We found support for the converse of Rensch's rule (i.e. females are proportionally bigger than males in large species) across all taxa but not within the two most speciose subfamilies (Gomphocerinae and Oedipodinae), which showed an isometric pattern. Our results do not provide support for the fecundity or sexual selection hypotheses, and we did not find evidence for significant effects of habitat use. Contrary to that expected, we found that species with narrower reproductive window are less dimorphic in size than those that exhibit a longer breeding cycle, suggesting that male protandry cannot solely account for the evolution of female‐biased SSD in Orthoptera. Our study highlights the need to consider alternatives to the classical evolutionary hypotheses when trying to explain why in certain insect groups males remain small.     

Description of the postmarsupial manca stages of Armadillidium granulatum (Crustacea,Isopoda, Oniscidea)

The development of the postmarsupial manca stages of Armadillidium granulatum Brandt, 1833 was studied in detail by morphological analysis. Ovigerous females were reared separately under controlled conditions, allowing us to follow the stages of development from release from the marsupium until the appearance of the first juvenile stage, identified by the full development of the seventh pair of pereopods. Each newborn was followed to record the subsequent moults that identify the three postmarsupial manca stages. Manca stage M I had a mean duration of 6 h, manca stage M II 15 days, and manca stage M III 32 days. The cephalothorax width was measured to provide a growth measure for each stage. The mean values of the cephalothorax width were: 0.512 mm (± 0.083 SD) for M I, 0.677 mm (± 0.058 SD) for M II and 1.194 mm (± 0.079 SD) for M III. The morphological modifications in the three postmarsupial manca stages were described, the body parts illustrated, and SEM images taken. The distinguishing characteristics among mancas were discussed, and comparisons made with manca stages of other terrestrial isopod species.     

Geographic variation of body size in New World anurans: energy and water in a balance

The validity of Bergmann's rule, perhaps the best known ecogeographical rule, has been questioned for ectothermic species. Here, we explore the interspecific version of the rule documenting body size gradients for anurans across the whole New World and evaluating which environmental variables best explain the observed patterns. We assembled a dataset of body sizes for 2761 anuran species of the Western Hemisphere and conducted assemblage‐based and cross‐species analyses that consider the spatial and phylogenetic structure in the data. In accordance with heat and water‐related explanations for body size clines, we found a consistent association of median body size and potential evapotranspiration across the New World. A relevant role of water availability also emerges, suggesting the joint importance of body size for thermoregulation and hydroregulation in anurans. Anurans do not follow a simple Bergmannian pattern of increasing size towards high latitudes. Consistent with previous regional findings, our Hemisphere‐wide analyses detect that the geographic variation in anuran body sizes is highly dependent on a trade‐off between heat and water balance. The observed size‐climate relationships possibly emerge from the interplay between thermoregulatory abilities and the benefits inherent to reduced surface‐to‐volume ratios in larger species, which decrease the rates of evaporative water loss and favour heat retention. Our results also show how temperature becomes important for species that are directly in contact with the substrate and water, like burrowing and terrestrial anurans, while arboreal species exhibit a body size cline linked with potential evapotranspiration.     

Environmental correlates of body size influence range size and extinction risk: A global study in rodents

Aim

Species-level traits, such as body and range sizes, are important correlates of extinction risk. However, both are often related and are driven by environmental factors. Here, we elucidated links between environmental factors, body size, range size and susceptibility to extinction, across the whole order of rodents.

Location

Global.

Time period

Current.

Major taxa studied

Rodents (order Rodentia).

Methods

We compiled an unprecedentedly large database of rodent morphology, phylogeny, range size, conservation status, global climate and normalized difference vegetation index (NDVI), comprising >86% of all described species. Using phylogenetic regressions, we initially explored the environmental factors driving body size. Next, we modelled the relationship between body size and range size. From this relationship, we computed and mapped (at the assemblage level) an index of relative range size, corresponding to the deviation from the expected range size of each species, given its body size. Finally, we tested whether relative range was correlated with the risk of extinction of the species derived from an assessment by the International Union for Conservation of Nature.

Results

We found that, contrary to the expectations of Bergmann's rule, the body size of rodents was mostly influenced by variation in NDVI (rather than latitude/temperature). Body size, in turn, imposed a constraint on species range size, as evidenced by a triangular relationship that was segmented at the lower bound. The relative species range size derived from this relationship highlighted four geographical regions where rodents with small relative range were concentrated globally. We demonstrated that lower relative range size was associated with increased risk of extinction.

Main conclusions

Species that, given their body size, are distributed across ranges that are smaller than expected have elevated extinction risk. Therefore, investigating the relationships between environmental drivers, body size and range size might help to detect species that could become threatened in the near future.     

Variation in body size and sexual size dimorphism in the most widely ranging lizard: testing the effects of reproductive mode and climate

Reproductive mode, ancestry, and climate are hypothesized to determine body size variation in reptiles but their effects have rarely been estimated simultaneously, especially at the intraspecific level. The common lizard (Zootoca vivipara) occupies almost the entire Northern Eurasia and includes viviparous and oviparous lineages, thus representing an excellent model for such studies. Using body length data for >10,000 individuals from 72 geographically distinct populations over the species' range, we analyzed how sex‐specific adult body size and sexual size dimorphism (SSD) is associated with reproductive mode, lineage identity, and several climatic variables. Variation in male size was low and poorly explained by our predictors. In contrast, female size and SSD varied considerably, demonstrating significant effects of reproductive mode and particularly seasonality. Populations of the western oviparous lineage (northern Spain, south‐western France) exhibited a smaller female size and less female‐biased SSD than those of the western viviparous (France to Eastern Europe) and the eastern viviparous (Eastern Europe to Far East) lineages; this pattern persisted even after controlling for climatic effects. The phenotypic response to seasonality was complex: across the lineages, as well as within the eastern viviparous lineage, female size and SSD increase with increasing seasonality, whereas the western viviparous lineage followed the opposing trends. Altogether, viviparous populations seem to follow a saw‐tooth geographic cline, which might reflect the nonmonotonic relationship of body size at maturity in females with the length of activity season. This relationship is predicted to arise in perennial ectotherms as a response to environmental constraints caused by seasonality of growth and reproduction. The SSD allometry followed the converse of Rensch's rule, a rare pattern for amniotes. Our results provide the first evidence of opposing body size—climate relationships in intraspecific units.     

Developmental variation in ecogeographic body proportions

While ecogeographic variation in adult human body proportions has been extensively explored, relatively less attention has been paid to the effect of Bergmann's and Allen's rules on human body shape during growth. The relationship between climate and immature body form is particularly important, as immature mortality is high, mechanisms of thermoregulation differ between young and mature humans, and immature body proportions fluctuate due to basic parameters of growth. This study explores changes in immature ecogeographic body proportions via analyses of anthropometric data from children included in Eveleth and Tanner's (1976) Worldwide Variation in Human Growth, as well as limb proportion measurements in eight different skeletal samples. Moderate to strong correlations exist between climatic data and immature stature, weight, BMI, and bi-iliac breadth; these relationships are as strong, if not stronger, in immature individuals as they are in adults. Correlations between climate and trunk height relative to stature are weak or nonexistent. Altitude also has significant effects on immature body form, with children from higher altitudes displaying smaller statures and lower body weights. Brachial and crural indices remain constant over the course of growth and display consistent, moderate correlations with latitude across ontogeny that are just as high as those detected in adults. The results of this study suggest that while some features of immature body form, such as bi-iliac breadth and intralimb indices, are strongly dictated by ecogeographic principles, other characteristics of immature body proportions are influenced by intrinsic and extrinsic factors such as nutrition and basic constraints of growth.     

Moth body size increases with elevation along a complete tropical elevational gradient for two hyperdiverse clades

The body size of an animal is probably its most important functional trait. For arthropods, environmental drivers of body size variation are still poorly documented and understood, especially in tropical regions. We use a unique dataset for two species‐rich, phylogenetically independent moth taxa (Lepidoptera: Geometridae; Arctiinae), collected along an extensive tropical elevational gradient in Costa Rica, to investigate the correlates and possible causes of body‐size variation. We studied 15 047 specimens (794 species) of Geometridae and 4167 specimens (308 species) of Arctiinae to test the following hypotheses: 1) body size increases with decreasing ambient temperature, as predicted by the temperature–size rule; 2) body size increases with increasing rainfall and primary productivity, as predicted from considerations of starvation resistance; and 3) body size scales allometrically with wing area, as elevation increases, such that wing loading (the ratio of body size to wing area) decreases with increasing elevation to compensate for lower air density. To test these hypotheses, we examined forewing length as a proxy for body size in relation to ambient temperature, rainfall, vegetation index and elevation as explanatory variables in linear and polynomial spatial regression models. We analysed our data separately for males and females using two principal approaches: mean forewing length of species at each site, and mean forewing length of complete local assemblages, weighted by abundance. Body size consistently increased with elevation in both taxa, both approaches, both sexes, and also within species. Temperature was the best predictor for this pattern (–0.98 < r < –0.74), whereas body size was uncorrelated or weakly correlated with rainfall and enhanced vegetation index. Wing loading increased with elevation. Our results support the temperature–size rule as an important mechanism for body size variation in arthropods along tropical elevational gradients, whereas starvation resistance and optimization of flight mechanics seem to be of minor importance.