Geographic gradients in body size: a clarification of Bergmann's rule

1997 marked the sesquicentenary of the publication by Carl Bergmann of the observation that, in general, large-bodied animal species tend to live further north than their small-bodied relatives. This has been dubbed Bergmann's rule in his honour. However, more than 150 years on, we appear to be little closer to a general understanding of the rule, or even to any consensus as to whether it exists. This is due in large part to confusion about the taxonomic level at which the rule is considered to operate, and to the conflation of pattern and mechanism. In this paper, we attempt to resolve this confusion by highlighting its sources, and by providing a definition of Bergmann's rule that is practical and useful, yet that retains the essential features of its original formulation. We conclude by briefly reviewing the mechanisms proposed to explain Bergmann's rule as we define it.     

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.     

The interspecific range size–body size relationship in Australian frogs

Aim There is substantial residual scatter about the positive range size–body size relationship in Australian frogs. We test whether species’ life history and abundance can account for this residual scatter. Location Australia. Methods Multiple regressions were performed using both cross‐species and independent contrasts analyses to determine whether clutch size, egg size and species abundance account for variation in range size over and above the effects of body size. Results In both cross‐species and independents contrasts models with body size, clutch size and egg size as predictors, partial r² values revealed that only egg size was significantly and uniquely related to range size. Contrary to expectation, neither body size nor clutch size could account for significant variation in range size. Incorporating species abundance as a predictor in further multiple regression analysis demonstrated that while abundance accounted for a significant proportion of range size variation, the contribution of egg size was reduced but still significant. Notably, non‐significant relationships persisted between range size and both body size and clutch size. Conclusions The weak positive correlation between body size and range size in Australian frogs disappears after accounting for species abundance and egg size. Our findings demonstrate that species with both high local abundance and small eggs occupy comparatively wider geographical ranges than species with low abundance and large eggs.     

Geographic range size is predicted by plant mating system

Species' geographic ranges vary enormously, and even closest relatives may differ in range size by several orders of magnitude. With data from hundreds of species spanning 20 genera in 15 families, we show that plant species that autonomously reproduce via self‐pollination consistently have larger geographic ranges than their close relatives that generally require two parents for reproduction. Further analyses strongly implicate autonomous self‐fertilisation in causing this relationship, as it is not driven by traits such as polyploidy or annual life history whose evolution is sometimes correlated with selfing. Furthermore, we find that selfers occur at higher maximum latitudes and that disparity in range size between selfers and outcrossers increases with time since their evolutionary divergence. Together, these results show that autonomous reproduction—a critical biological trait that eliminates mate limitation and thus potentially increases the probability of establishment—increases range size.     

Body size and microclimate use in Neotropical granivorous ants

The stability of tropical microclimates has left microclimate use by tropical species little unexplored. At La Selva Costa Rica, I related foraging activity at seed baits to humidity in two forests types. I recorded 38 and 35 ant species at seed baits in closed and open canopy forest. The microclimate 5 cm above the forest floor in the younger, Open Forest was warmer, drier, more variable, and more sensitive to current weather than in the older Closed Forest. Ant species within both forests foraged at different Vapor Pressure Deficits (kPa), a measure of the drying power of the air. VPD use was not confounded with diel activity patterns. Body size explained 46% of the variance in mean VPD use among ant species. Small ant species tended to forage in moist microclimates; large species tended to be microclimate generalists. Larger species were also more active in the drier Open Forest. Foraging activity by these assemblages varies 4-fold, and peaks close to the mean VPD for each habitat. The behavior of these assemblages suggest that 1) small ant species at La Selva potentially compete with the entire range of ant body sizes, whereas large ants forage when and where small ants are inactive; and 2) seeds dispersed to the forest floor at dawn will be consumed or further dispersed by a larger suite of ants species than those falling in the heat of the tropical afternoon.     

Body size and host range co-determine the altitudinal distribution of Neotropical tephritid flies

Aim We addressed the following questions: (1) Does tephritid body size tend to increase in species found at higher elevations, as predicted by Bergmann's rule? (2) Do tephritids conform to Rapoport's rule, so that species found at higher elevations tend to have broader altitudinal ranges? (3) More generally, how do body size and host range jointly affect the patterns of altitudinal distribution among Neotropical tephritid flies? Location The Mantiqueira mountain range, south‐eastern Brazil, at sites ranging from c. 700 to 2500 m a.s.l. Methods At each site we collected flower heads of all Asteraceae species to rear out endophagous immatures (from January to June in 1998 and 1999). We used structural equation models (SEM) to evaluate jointly the relationships between body size, host range and altitudinal distribution (range and mid‐point). Results Neotropical tephritid body size showed a negative relationship with altitudinal distribution. SE modelling showed no significant direct effect of body size on altitudinal range; however, it had significant indirect negative effects through host range and altitudinal mid‐point. The SE model was a good predictor of observed correlations and accounted for 84% of the variation in tephritid altitudinal range. Main conclusions The altitudinal range of flower‐head‐feeding tephritids is related to host range and is indirectly affected by body size via host range and altitudinal mid‐point. As predicted by Rapoport's rule, tephritids that occur at higher elevations also present wider altitudinal ranges. Bergmann's rule does not apply to Neotropical tephritids along a tropical elevational gradient, but rather its converse was found. Body size may determine host range by imposing a restriction upon large individuals using small flower heads. Host species turnover along the altitudinal gradient may be the main factor explaining the strong relationship between host range and insect elevational distribution.     

Home range scaling: intraspecific and comparative trends

Summary Intraspecific and intrasexual variation in home range size, body mass and ecological productivity is examined in three selected species of Carnivora (Felis rufus: Canis latrans; Ursus americanus), reflecting different diets. We then compare the intraspecific results with prior cross-species studies. Home range size and body mass inFelis rufus are positively and significantly correlated, similar to other comparative studies. For both intraspecific and intrasexual analyses of all three species, home range size and latitude are strongly correlated. Home range size scales with latitude more steeply as the proportion of meat increases in the diet of each species. That is, the slope of home range size on latitude is greatest in the meat-eatingFelis rufus followed by a shallower slope in the omnivorousCanis latrans and the most shallow slope in the frugivorous/folivorousUrsus americanus. These differences in slope are consistent with models of trophic level biomass change with variation in productivity, and parallel the dietary differences observed in cross-species differences in home range.     

Evolutionary influences on body size in free-living and parasitic isopods

The influence of mode of life and habitat characteristics on the evolution of body size in isopods was investigated in a comparative analysis based on data from 746 free-living and parasitic species. The phylogeny of isopods allowed 24 independent comparisons to be made between higher taxa (families or superfamilies), each corresponding to a separate branching event. The evolution of parasitism was consistently associated with reductions in body size. On the contrary, invasion of freshwater habitats was consistently coupled with increases in body size. Lineages moving to higher latitudes were significantly more likely to evolve larger body sizes than those shifting toward the equator. In addition, colonizing deeper water resulted in a weak tendency to evolve larger body size. The analysis suggests that the large size of some isopod groups parasitic on fish (e.g. Cymothoidae) may have been inherited from a free-living ancestor and is not the product of directional selection toward large size and greater fecundity.     

Latitudinal and altitudinal body size variation among north-west European land snail species

Aim To investigate latitudinal and altitudinal patterns in body size variation among north‐west European land snail species, as well as factors influencing such patterns. Location Latitudinal patterns were investigated in north‐west Europe from the British Isles and France in the west to Finland, Poland, Slovakia and Hungary in the east and from Norway in the north to France (with the exception of the Mediterranean part of the country), Switzerland, Austria and Hungary in the south. Altitudinal patterns were examined in the Alps in Austria and Switzerland. Methods Data on latitudinal ranges of 366 north‐west European land snail species, on altitudinal ranges of 175 species from Austria and 150 species from Switzerland, and on their body sizes were used to test for the presence of interspecific latitudinal or altitudinal body size patterns. Four methods, Stevens’ method, the midpoint method, the across‐species method, and a phylogenetically controlled analysis (CAIC) were applied. Results As a result of the predominance of some small bodied clades at higher latitudes and some large bodied clades at lower latitudes, body size of north‐west European land snails decreases significantly with increasing latitude. However, little of the body size variation across species is explained by latitude and the phylogenetically controlled analysis showed that the decrease of body size with increasing latitude is not a result of repeated and independent evolution of an association between body size and latitude in many clades. There is no significant correlation between body size of land snail species and altitude in the Alps although a negative correlation of body size and altitude is frequent within species. Main conclusion If phylogenetic effects are controlled for, neither latitudinal nor altitudinal patterns in body size could be found. Bergmann's rule, which predicts a positive correlation between body size of species and latitude, could not be confirmed for north‐west European land snails.     

Relationships between geographical range size, body size, local abundance, and habitat breadth in North American suckers and sunfishes

Aim I examine the relationship between geographical range size and three variables (body size, an index of habitat breadth, and an index of local abundance) within a phylogenetic framework in North American species of suckers and sunfishes. Location North America Methods Regressions after independent contrasts of geographical range size, body size, habitat breadth, and local abundance. Results Species with large range sizes tend to be larger-bodied, be more locally abundant, and have higher habitat breadths. Character reconstructions support the prediction that variables associated with rarity (small geographical range size, low local abundance, low niche breadth, and large body size) evolve in unison, although large body size was associated with the opposite traits in these taxa. Gaston & Blackburn (1996a) suggested using visual identification of the lower boundary of the geographical range-body size relationship to identify extinction-prone species; this resulted in thirteen species that are potentially extinction-prone. Main conclusions Similar evolutionary mechanisms appear to operate on body size and other variables related to rarity, even in distantly related taxa.     

Patterns of evolutionary transformation in the petrosal bone and some basicranial features in marsupial mammals, with special reference to didelphids

Twelve petrosal and four nonpetrosal characters were coded for representatives of all 15 extant genera of Didelphidae and for 16 additional genera of marsupials representing all extant orders. Three basal metatherians were used as outgroup comparison. Histological sections of a subset of the data were examined. An intermediate position of the hiatus Fallopii supports the monophyly of Didelphidae. Several basicranial regions support different clades within the Didelphidae that recent molecular work has identified, including a sister group relationship of Caluromys and Caluromysiops , the monophyly of large opossums, a Lestodelphys-Thylamys clade, and a Lestodelphys-Thylamys-Gracilinanus-Marmosops clade. Glironia lacks petrosal and jaw synapomorphies of Caluromys and Caluromysiops. The transverse canal, a synapomorphy of the crown-group Marsupialia, opens as a single foramen anterior to the carotid foramen in most marsupials or as numerous foramina in the pterygoid fossa in diprotodontians. It is either intramural (most marsupials) or simply endocranial (most diprotodontians excluding koalas and wombats). Loss of a deep sulcus in the anterior pole of the promontorium for the internal carotid artery and a rostral tympanic process of the petrosal also characterize the groundplan of the crown group Marsupialia. Pouch-young wombats show a groove in the anterior pole of the petrosal for the internal carotid artery. The absence of a prootic canal foramen in the tympanic side of the petrosal of adults supports the monophyly of Australidelphia. Some pouch-young marsupials possess a prootic canal that is later lost in ontogeny. A rather flat promontorium and a crest running medio-distally in the middle of the promontorium characterize Macropodidae.     

Geographic range size and evolutionary age in birds

Together with patterns of speciation and extinction, post-speciation transformations in the range sizes of individual species determine the form of contemporary species range-size distributions. However, the methodological problems associated with tracking the dynamics of a species' range size over evolutionary time have precluded direct study of such range-size transformations, although indirect evidence has led to several models being proposed describing the form that they might take. Here, we use independently derived molecular data to estimate ages of species in six monophyletic groups of birds, and examine the relationship between species age and global geographic range size. We present strong evidence that avian range sizes are not static over evolutionary time. In addition, it seems that, with the regular exception of certain taxa (for example island endemics and some threatened species), range-size transformations are non-random in birds. In general, range sizes appear to expand relatively rapidly post speciation; subsequently; and perhaps more gradually, they then decline as species age. We discuss these results with reference to the various models of range-size dynamics that have been proposed.     

Phylogenetic relationships, diversification and biogeography in Neotropical Brotogeris parakeets

Aim We present a molecular phylogenetic analysis of Brotogeris (Psittacidae) using several distinct and complementary approaches: we test the monophyly of the genus, delineate the basal taxa within it, uncover their phylogenetic relationships, and finally, based on these results, we perform temporal and spatial comparative analyses to help elucidate the historical biogeography of the Neotropical region. Location Neotropical lowlands, including dry and humid forests. Methods Phylogenetic relationships within Brotogeris were investigated using the complete sequences of the mitochondrial genes cyt b and ND2, and partial sequences of the nuclear intron 7 of the gene for Beta Fibrinogen for all eight species and 12 of the 17 taxa recognized within the genus (total of 63 individuals). In order to delinetae the basal taxa within the genus we used both molecular and plumage variation, the latter being based on the examination of 597 skin specimens. Dates of divergence and confidence intervals were estimated using penalized likelihood. Spatial and temporal comparative analyses were performed including several closely related parrot genera. Results Brotogeris was found to be a monophyletic genus, sister to Myiopsitta. The phylogenetic analyses recovered eight well‐supported clades representing the recognized biological species. Although some described subspecies are diagnosably distinct based on morphology, there was generally little intraspecific mtDNA variation. The Amazonian species had different phylogenetic affinities and did not group in a monophyletic clade. Brotogeris diversification took place during the last 6 Myr, the same time‐frame as previously found for Pionus and Pyrilia. Main conclusions The biogeographical history of Brotogeris implies a dynamic history for South American biomes since the Pliocene. It corroborates the idea that the geological evolution of Amazonia has been important in shaping its biodiversity, argues against the idea that the region has been environmentally stable during the Quaternary, and suggests dynamic interactions between wet and dry forest habitats in South America, with representatives of the Amazonian biota having several independent close relationships with taxa endemic to other biomes.     

Diet of Neotropical parrots is independent of phylogeny but correlates with body size and geographical range

Body mass and geographical range are two main drivers of diet in animals, yet how these factors influence diet in the morphologically and ecologically diverse avian group of Psittaciformes is little known. We reviewed current knowledge of the diet of Neotropical parrots and assessed the relation between diet (breadth and composition), phylogeny, body mass and geographical range. Diet has been documented for 98 of 165 species, but information is available only for 34 of 59 threatened species, and countries with high species diversity (> 20 species) had few studies (one to seven). Neotropical parrot species consumed 1293 plant species of 125 families. When assessing the relative frequency of different food items in the diet (seed, fruits, flowers, leaves, nectar, bark and stems), we found that parrots mostly exploited seeds (41.9%) and fruits (38.3%) of native species. Diet overlap was very low among genera (0.006–0.321). At the species level, geographical range and body size explained the variation in diet composition. In particular, small parrots of restricted distribution had a distinct diet composition relative to either large or widely distributed species. Although body size and geographical range showed phylogenetic inertia, diet was independent of phylogenetic history. Our review not only reveals ecological factors explaining diet in a generalist group but also exposes information gaps across the Neotropical region.     

Area-relationships in the Neotropical lowlands: an hypothesis based on raw distributions of Passerine birds

Abstract. Using raw geographic distributions for Neotropical species and subspecies of the perching birds (Order Passeriformes), we present an hypothesis of area-relationships for twelve avian areas of endemism in the lowland Neotropics. With 1717 characters (distributions of species and subspecies) we find a single most parsimonious tree of area-relationships. This topology does not match area-relationships determined from phylogenetic studies of morphologic characters in some Neotropical birds. Analyses of data partitions representing major taxonomic subdivisions within Passerine birds provide many different hypotheses of area-relationships. These results suggest that a single set of Neotropical area-relationships is not likely. In the future, we suggest greater emphasis be placed on research to document patterns in the Neotropics, particularly phylogenetic patterns, than on speculation about what processes have been important for diversification.     

Neotropical frogs and mating songs: The evolution of advertisement calls in glassfrogs

Anurans emit advertisement calls with the purpose of attracting mates and repelling conspecific competitors. The evolution of call traits is expected to be associated with the evolution of anatomical and behavioural traits due to the physics of call emission and transmission. The evolution of vocalizations might imply trade‐offs with other energetically costly behaviours, such as parental care. Here, we investigated the association between body size, calling site, parental care and call properties (call duration, number of notes, peak frequency, frequency bandwidth and call structure) of the advertisement calls of glassfrogs (Centrolenidae)—a family of Neotropical, leaf‐dwelling anurans—using phylogenetic comparative methods. We also explored the tempo and mode of evolution of these traits and compared them with those of three morphological traits associated with body size, locomotion and feeding. We generated and compiled acoustic data for 72 glassfrog species (46% of total species richness), including representatives of all genera. We found that almost all acoustic traits have significant, but generally modest, phylogenetic signal. Peak frequency of calls is significantly associated with body size, whereas call structure is significantly associated with calling site and paternal care. Thus, the evolution of body size, calling site and paternal care could constrain call evolution. The estimated disparity of acoustic traits was larger than that of morphological traits and the peak in disparity of acoustic traits generally occurred later in the evolution of glassfrogs, indicating a historically recent outset of the acoustic divergence in this clade.     

Interspecific geographic range size–body size relationship and the diversification dynamics of Neotropical furnariid birds

Among the earliest macroecological patterns documented, is the range and body size relationship, characterized by a minimum geographic range size imposed by the species’ body size. This boundary for the geographic range size increases linearly with body size and has been proposed to have implications in lineages evolution and conservation. Nevertheless, the macroevolutionary processes involved in the origin of this boundary and its consequences on lineage diversification have been poorly explored. We evaluate the macroevolutionary consequences of the difference (hereafter the distance) between the observed and the minimum range sizes required by the species’ body size, to untangle its role on the diversification of a Neotropical species‐rich bird clade using trait‐dependent diversification models. We show that speciation rate is a positive hump‐shaped function of the distance to the lower boundary. The species with highest and lowest distances to minimum range size had lower speciation rates, while species close to medium distances values had the highest speciation rates. Further, our results suggest that the distance to the minimum range size is a macroevolutionary constraint that affects the diversification process responsible for the origin of this macroecological pattern in a more complex way than previously envisioned.     

Geographic patterns of genetic variation in four Neotropical rodents: conservation implications for small game mammals in French Guiana

The Neotropics contributes significantly to global biodiversity yet little is known about its mammalian fauna. Given our limited knowledge, concerns are that extinctions at the local level may cause a decline in genetic diversity through the loss of unique alleles. Here we report the geographical population structure of four rodent species from French Guiana: Dasyprocta leporina , Agouti paca , Proechimys cayennensis and P. cuvieri . Two of them ( Dasyprocta and Agouti ) are commonly harvested throughout the country for subsistence and/or game hunting. Cytochrome b and control region sequences revealed the presence of a number of maternal lineages occurring in sympatry throughout French Guiana. We applied two cytochrome b rodent clock calibrations (7.5% and 12% per million years) to our data, and placed the divergence of the maternal lineages to between 160 000 and 260 000 years ago for the more diverse D. leporina and P. cuvieri , and between 66 000 and 46 000 years ago for the more recent A. paca and P. cayennensis . The clades appear to be widespread throughout South America as indicated by specimens sampled in Brazil, Peru, and Venezuela. At the population level, AMOVA revealed little or no geographical structure within French Guiana. However, this conclusion is based on a single genetic marker and relatively few specimens.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 203–218.