Testing the metabolic theory of ecology: allometric scaling exponents in mammals

Many fundamental traits of species measured at different levels of biological organization appear to scale as a power law to body mass (M) with exponents that are multiples of 1/4. Recent work has united these relationships in a "metabolic theory of ecology" (MTE) that explains the pervasiveness of quarter-power scaling by its dependence on basal metabolic rate (B), which scales as M(0.75). Central to the MTE is theory linking the observed -0.25 scaling of maximum population growth rate (rm) and body mass to the 0.75 scaling of metabolic rate and body mass via relationships with age at first reproduction (alpha) derived from a general growth model and demographic theory. We used this theory to derive two further predictions: that age at first reproduction should scale inversely to mass-corrected basal metabolic rate alpha infinity (B/M)(-l) such that rm infinity (B/M)1. We then used phylogenetic generalized least squares and model selection methods to test the predicted scaling relationships using data from 1197 mammalian species. There was a strong phylogenetic signal in these data, highlighting the need to account for phylogeny in allometric studies. The 95% confidence intervals included, or almost included, the scaling exponent predicted by MTE for B infinity M(0.75), rm infinity M(-0.25), and rm infinity alpha(-1), but not for alpha infinity M(0.25) or the two predictions that we generated. Our results highlight a mismatch between theory and observation and imply that the observed -0.25 scaling of maximum population growth rate and body mass does not arise via the mechanism proposed in the MTE.     

The ecological impact of invasive cane toads on tropical snakes: field data do not support laboratory-based predictions

Predicting which species will be affected by an invasive taxon is critical to developing conservation priorities, but this is a difficult task. A previous study on the impact of invasive cane toads (Bufo marinus) on Australian snakes attempted to predict vulnerability a priori based on the assumptions that any snake species that eats frogs, and is vulnerable to toad toxins, may be at risk from the toad invasion. We used time-series analyses to evaluate the accuracy of that prediction, based on >3600 standardized nocturnal surveys over a 138-month period on 12 species of snakes and lizards on a floodplain in the Australian wet-dry tropics, bracketing the arrival of cane toads at this site. Contrary to prediction, encounter rates with most species were unaffected by toad arrival, and some taxa predicted to be vulnerable to toads increased rather than declined (e.g., death adder Acanthophis praelongus; Children's python Antaresia childreni). Indirect positive effects of toad invasion (perhaps mediated by toad-induced mortality of predatory varanid lizards) and stochastic weather events outweighed effects of toad invasion for most snake species. Our study casts doubt on the ability of a priori desktop studies, or short-term field surveys, to predict or document the ecological impact of invasive species.     

Song repertoires do not hinder neighbor-stranger discrimination

Summary Through playback experiments and a comparative study we tested the hypothesis that song repertoires hinder individual recognition by song in birds. Our playback tests take advantage of the peculiar singing behavior of two species of parulid warblers: the American redstart (Setophaga ruticilla) and the yellow warbler (Dendroica petechia). Males of both species sing either the same song repeatedly (repeat mode) or a repertoire of songs in series (serial mode). Subjects were played the repeat song and the serial songs from a territorial neighbor and from a stranger some territories distant. Counter to the prediction of the hypothesis, they discriminated equally well between neighbors and strangers when the several serial songs were used as when the single repeat song was played. Thus, neither the small repertoires used by redstarts in serial mode (2–8 songs) nor the larger ones used by yellows (an average of over 20 songs) appear to hinder neighbor-stranger discrimination. In our comparative test, we examined the relationship between neighbor-stranger discrimination and repertoire size among 20 species for which data were available. Using two comparative methods, we did not find the predicted significant negative relationship.     

Why male orangutans do not kill infants

Infanticide is widespread among mammals, is particularly common in primates, and has been shown to be an adaptive male strategy under certain conditions. Although no infanticides in wild orangutans have been reported to date, several authors have suggested that infanticide has been an important selection pressure influencing orangutan behavior and the evolution of orangutan social systems. In this paper, we critically assess this suggestion. We begin by investigating whether wild orangutans have been studied for a sufficiently long period that we might reasonably expect to have detected infanticide if it occurs. We consider whether orangutan females exhibit counterstrategies typically employed by other mammalian females. We also assess the hypothesis that orangutan females form special bonds with particular “protector males” to guard against infanticide. Lastly, we discuss socioecological reasons why orangutan males may not benefit from infanticide. We conclude that there is limited evidence for female counterstrategies and little support for the protector male hypothesis. Aspects of orangutan paternity certainty, lactational amenorrhea, and ranging behavior may explain why infanticide is not a strategy regularly employed by orangutan males on Sumatra or Borneo.     

Secondary sex ratios do not support maternal manipulation: extensive data from laboratory colonies of spiny mice (Muridae: Acomys)

Spiny mice of the genus Acomys (Muridae) represent a very suitable mammalian model for studying factors influencing the secondary sex ratio (SSR). The maternal effort in these rodents is extremely biased in favour of the prenatal period and, therefore, maternal manipulation of the SSR is potentially more advantageous. We studied the SSR in four populations/species of spiny mice kept in family groups consisting of two closely related females, one non-relative male and their descendants. The groups were established from founding animals aged about 3 months (maturing age) and were allowed to breed freely for several months. Each litter was sexed after birth, and relevant data were thoroughly recorded. Altogether, data were collected on 1684 litters: 189 of Acomys sp. from Iran, 203 of A. cilicicus, 875 of A. cahirinus, and 417 of A. dimidiatus. We recorded the sex of 4048 newborns of which 1995 were males and 2053 were females. The overall sex ratio was close to 1:1 (49.2%). Generalized linear mixed models and/or generalized linear models were constructed to evaluate the effect of four life history and eight social variables on the sex ratio. No consistent effects of these variables on the sex ratio were found and, interestingly, none of the variables associated with maternal life history had any effect on the sex ratio. Three factors associated with group composition (i.e. the number of immature males, the number of immature females and the number of breeding females) did have significant effects on the sex ratio, but these effects were not consistent across the studied species. In conclusion, our evaluation of this large dataset revealed that the sex ratio in spiny mice is surprisingly stable.     

Orchids do not pay costs at emergence for prolonged dormancy

In plants, prolonged dormancy is often considered a response to resource depletion or environmental stress that comes at a fitness cost. However, apparent costs of dormancy could reflect the state in which plants entered dormancy, rather than effects of dormancy per se. We tested this hypothesis for a terrestrial orchid, Epipactis atrorubens, by analyzing differences in vital rates of dormant and emergent plants using generalized linear mixed models, applied to eight years of demographic data. Dormant E. atrorubens plants did not form one homogeneous stage class. Instead, the vital rates of dormant plants mirrored performance of plants in their life stage before dormancy. Plants emerging from dormancy were slightly (albeit only marginally statistically significantly) larger than plants transitioning from the matching aboveground stage class, especially for smaller and younger stage classes. Because small plants were most likely to go dormant, plants emerging from dormancy were also smaller than average, if one were to compare all previously dormant plants to all previously emergent plants. Therefore, misclassifying all dormant plants into a single stage class changes whether we view dormancy as intrinsically costly, in terms of future performance upon emergence. We suggest that prolonged dormancy may be a form of phenotypic plasticity in which plants distribute their performance and reproductive effort through time, rather than a simple stress response.     

Foraging bumblebees do not rate social information above personal experience

Foraging animals can acquire new information about food sources either individually or socially, but they can also opt to rely on information that they have already acquired, termed “personal information”. Although social information can provide an adaptive shortcut to new resources, recent theory predicts that investing too much time in acquiring new information can be detrimental. Here, we investigate whether foraging bumblebees (Bombus terrestris) strategically prioritize personal information unless there is evidence of environmental change. All bees in our study had personal information that one species of artificial flower was rewarding, and bees in the scent group then experienced social information about an alternative-scented species inside the nest, while a control group did not. On their next foraging bout, bees in both groups overwhelmingly used personal information when deciding where to forage. When bees subsequently learnt that the rewards offered by their preferred species had dwindled, bees that had social information were no quicker to abandon their personal information than control bees, but once they had sampled the alternative flowers, they showed greater commitment to that species than control bees. Thus, we found no evidence that social information is particularly important when personal information fails to produce rewards (a “copy when established behaviour is unproductive” strategy). Instead, bees used social information specifically to complement personal information.     

Copulatory plugs do not assure high first male fertilisation success: sperm displacement in a lizard

Sperm competition selects for opposing male defensive and offensive reproductive traits, and its outcome may be determined by the effectiveness to which one trait has evolved to out-compete the other. We tested the effectiveness of a first male plug physical interference with a second male insemination (defence) vs the effectiveness of plug and associated sperm displacement by a second male (offence) on the outcome of sperm competition in Iberian rock lizards. We conducted a double mating experiment where we compared the proportion of eggs per clutch fertilised by the same second males (against the same first males) when they copulated with females 30 min (first male plug adhered firmly inside the female cloaca) and 4 h (first male plug loosely adhered or shed from the female cloaca) after first males. We found that second males fertilised the majority of the eggs per clutch in the 30-min treatment, whereas fertilisations were equally shared between the two males in the 4-h treatment. These results show that plugs have little defensive effectiveness, and thus, do not assure high first male fertilisation success. Instead, sperm displacement appears to be associated with plug displacement. That is, because sperm embedded in first male plugs, and displaced from competition for fertilisations by second males, is expected to increase in number with decreasing time allowed for female sperm transport, second males thus enjoy higher fertilisation success. This study shows that offensive plug displacement out-competes plug defensive role in Iberian rock lizards. Moreover, it reveals sperm displacement as a novel sperm competition mechanism in reptiles.     

Female great tits do not alter their yolk androgen deposition when infested with a low-transmittable ectoparasite

In birds as in many other taxa, parasites can have deleterious effects on offspring development. Therefore, avian mothers have evolved responses to counteract parasite virulence in offspring via transgenerational defense mechanisms that is the transfer of immune-enhancing substances such as antibodies to their eggs. Another maternal pathway is suggested by the finding that infested great tit mothers produced eggs with lower androgens, since these yolk androgens are immunosuppressive and potentially affect parasite susceptibility of the nestlings. However, whether this pathway is a specific adaptation to infestation with parasites that affect the offspring or an epiphenomenon of lower androgen production in the female due to the parasite effects on the mother itself is as yet unclear. In this study we infested female great tits (Parus major) with sheep ticks (Ixodes ricinus), which are nonnidicolous ectoparasites with low vertical transmission capability, and evaluated the effects on yolk androgen deposition. Tick-infested females did not significantly reduce their deposition of androgens (androstenedione (A₄) and testosterone) compared to tick-reduced females, which is in contrast to a previous study showing a lowered deposition of A₄ and testosterone when females were exposed to the nidicolous hen flea. Thus, females alter their hormone deposition, and thus likely offspring phenotype, when exposed to parasites that also form the parasitic environment of their offspring, but not when temporarily infested with the field-dwelling sheep ticks with low transmission capability. This suggests that selection favored the evolution of an adaptive transgenerational effect by acting mainly on the parasite-induced maternal effect.     

Consequences of paternal care on pectoral fin allometry in a desert-dwelling fish

Positive static allometry is a scaling relationship where the relative size of traits covaries with adult body size. Traditionally, positive allometry is thought to result from either altered physiological requirements at larger body size or from strongly condition-dependent allocation under sexual selection. Yet, there are no theoretical reasons why positive allometry cannot evolve in fitness-related traits that are solely under the influence of natural selection. We investigated scaling and sexual dimorphism of a naturally selected trait, pectoral fin size, in comparison to a trait important in male–male combat, head width in natural populations of a fish, the desert goby Chlamydogobius eremius. Male desert gobies provide uniparental care and use their pectoral fins to fan the brood (often under hypoxic conditions); hence, larger fins are expected to be more efficient. Male pectoral fins do not appear to fulfil a signalling function in this species. We found that, for both pectoral fin size and head width, males exhibited positive allometric slopes and greater relative trait size (allometric elevation) than females. However, for head width, females also showed positive allometry, albeit to a lesser degree than males. Because fin locomotory function typically does not result in positive allometry, our findings indicate that other naturally selected uses, such as paternal care, can exaggerate trait scaling relationships.     

Contradictory results in sex ratio studies: populations do not necessarily differ

In avian sex ratio studies, results often differ between species and between populations within species. Some researchers argued that positive results were simply statistical artefacts and that sex ratio adjustment did not exist. However, many of the proposed mechanisms of sex ratio adjustment result in costly laying gaps. In these cases, females laying large clutches may restrict the sex manipulation to the first egg of the clutch. Consequently, detectability of sex ratio adjustment on the level of the clutch can be low. Though obvious, this fact is often neglected in the literature. Using simulations, I show that the proportion of undetected sex manipulation can be surprisingly high when the manipulation is restricted to the first egg. If the sample size is 50 broods, there is 47% and 71% chance in 6- and 12-egg clutches, respectively, that sex manipulation is undetected. Even with large samples (n = 100), the figures are 15% and 46%. These data suggest that nonsignificant results for clutch sex ratios do not necessarily mean that sex is not manipulated in a portion of the brood, e.g. in first-laid eggs. Hence, whenever possible, data on laying order-specific sex manipulation should also be collected. Without such data, contradictory results on brood sex ratios should be interpreted cautiously.     

Microbes do not follow the elevational diversity patterns of plants and animals

The elevational gradient in plant and animal diversity is one of the most widely documented patterns in ecology and, although no consensus explanation exists, many hypotheses have been proposed over the past century to explain these patterns. Historically, research on elevational diversity gradients has focused almost exclusively on plant and animal taxa. As a result, we do not know whether microbes exhibit elevational gradients in diversity that parallel those observed for macroscopic taxa. This represents a key knowledge gap in ecology, especially given the ubiquity, abundance, and functional importance of microbes. Here we show that, across a montane elevational gradient in eastern Peru, bacteria living in three distinct habitats (organic soil, mineral soil, and leaf surfaces) exhibit no significant elevational gradient in diversity (r2<0.17, P>0.1 in all cases), in direct contrast to the significant diversity changes observed for plant and animal taxa across the same montane gradient (r2>0.75, P<0.001 in all cases). This finding suggests that the biogeographical patterns exhibited by bacteria are fundamentally different from those of plants and animals, highlighting the need for the development of more inclusive concepts and theories in biogeography to explain these disparities.     

Song rates of dark-eyed juncos do not increase when females are fertile

Frequency of singing by birds may vary with reproductive stage in ways that reflect variation in the functions of song in intersexual and intrasexual communication. In dark-eyed juncos (Junco hyemalis) high-amplitude song is produced only by males. To investigate the function of this song, we tested whether fertility of females affected singing by their mates or by neighboring males. Using focal observations, song censuses, and radiotracking data, we determined whether song production varied between and among periods when females were fertile and non-fertile. Our findings show that males do not increase song production when their mates are fertile, nor do they increase song production when neighboring females are fertile. These results suggest that male juncos do not signal their intent to defend territories (or mates) more when females are fertile and that they do not use song to advertise to specific potential participants in extra-pair fertilizations. Received: 13 February 1997 / Accepted after revison: 2 May 1997     

Current analyses do not resolve whether extra-pair paternity is male or female driven

Recent studies question the importance of indirect genetic effects in explaining female benefits of extra-pair matings in socially monogamous species. Compiling data on 14 wild bird species, Arnqvist and Kirkpatrick (Am Nat 165:S26–S37, 2005) estimated the average direct cost in terms or reduced parental care to be an order of magnitude larger than the potential effect of genetic benefits. This study has sparked a debate regarding potential confounding factors but no consensus appears to have been reached. Here we focus on the implicit assumption that all individuals face the same selective pressures and argue that this assumption is probably too strong in most cases. Using a theoretical model we show that when the amount of resources that a male provides depends on territory quality, his physical condition or prospects for alternative breeding opportunities, a female may respond to such differences by altering her mating behaviour. Such confounding factors may lead to direct fitness effects that result in negative correlations between paternal care and paternity even if females that produce extra-pair young experience a net benefit. Negative correlations can also result when males forcefully seek copulations and females resist them. We discuss the studies included in the analysis in this light, and conclude that current analyses on the net selective pressures remain uninformative. In addition to considering average effects across individuals and species we suggest giving attention to individual differences and the influence of ecological factors such as territory quality and predation pressures on female mating behaviour.     

Allometric scaling predicts preferences for burned patches in a guild of East African grazers

The high herbivore diversity in savanna systems has been attributed to the inherent spatial and temporal heterogeneity related to the quantity and quality of food resources. Allometric scaling predicts that smaller-bodied grazers rely on higher quality forage than larger-bodied grazers. We replicated burns at varying scales in an East African savanna and measured visitation by an entire guild of larger grazers ranging in size from hare to elephant. We found a strong negative relationship between burn preference and body mass with foregut fermenters preferring burns to a greater degree than hindgut fermenters. Burns with higher quality forage were preferred more than burns with lower quality forage by small-bodied grazers, while the opposite was true for large-bodied grazers. Our results represent some of the first experimental evidence demonstrating the importance of body size in predicting how large herbivores respond to fire-induced changes in plant quality and quantity.     

Blue eggs do not reduce nest predation in the song thrush,Turdus philomelos

Summary Many passerine birds with open cup-shaped nests lay blue or blue-green eggs. In thrushes, blue eggs may be cryptic and provide camouflage by imitating spots of light on green leaves. Alternatively, egg coloration may be selectively neutral because nest predators detect nests and not eggs, or it may be maladaptive because organisms are not always well adapted to their present environment. I evaluated these hypotheses by studying predation on artificial song thrush (Turdus philomelos) nests with quail eggs, painted either white, blue, or spotted (cryptic to a human eye). Corvids were the major nest predators. For concealed as well as exposed nests, I found no differences in the predation rates of nests with white, blue, or spotted eggs. Predators apparently detected the nests, and not the eggs, first. In a second experiment, I placed egg groups without nests in trees to study the effect of color per se. The predation rate of the spotted egg groups was significantly lower than that of the white and blue egg groups, for concealed as well as exposed egg groups. These results suggest that blue eggs in the song thrush are not cryptic but may be selectively neutral or even maladaptive with regard to nest predation.     

Experimentally elevated plasma levels of testosterone do not increase male reproductive success in blue tits

In temperate passerines, increased testosterone (T) levels during breeding mediate male aggressive and mating behaviour. If individual variability in T levels is reflected in behavioural differences during mating, males with higher T might gain higher reproductive success. This can be tested experimentally by elevating T levels. However, high exogenous T levels are known to have negative effects on male sperm production. This may reduce male fitness, particularly if sperm competition is intense. We experimentally elevated T levels in breeding blue tit males to investigate how T levels above the natural mean influence male reproductive success. Contrary to most—if not all—previous experimental manipulations of T levels in birds, we restricted the treatment with exogenous T to the time when females were fertile and T levels were naturally high in males. In blue tits, extra-pair paternity is an important component of male reproductive success, and its frequency is likely influenced by androgen-mediated behaviours such as mate attraction and aggression towards other males. Here we show that T-males were equally likely to become cuckolded and did not gain more extra-pair paternity than control males. Cuckolded T-males, however, lost more paternity than control males. We discuss the possibility that this is caused by negative effects of T treatment on sperm production.Communicated by M. Webster     

Bottom-up and top-down effects on insect herbivores do not vary among sites of different salinity

It has been suggested, but rarely tested, that the relative strength of top-down and bottom-up factors in communities varies along an environmental stress gradient. We compared the strength of bottom-up and top-down effects on the densities of insect herbivores along a range of sites of different salinities in west-central Florida. We used a 2 x 2 factorial design with plots divided into four treatments: (1) bottom-up manipulation, where fertilizer was applied to increase plant quality; (2) top-down manipulation, where sticky traps were used to reduce the effects of natural enemies (parasitoids); (3) bottom-up and top-down manipulation, where fertilizer was applied and sticky traps were used; and (4) control plots. These plots were established along a range of salinities among seven different sites containing the salt marsh plant Borrichia frutescens. In each plot, we determined the parasitism levels and abundances of the sap sucker Pissonotus quadripustulatus, the gall maker Asphondylia borrichiae, and the lepidopteran stem borer Argyresthia spp. Gall density, Pissonotus density, and stem borer density were significantly higher in lower salinity sites, suggesting a strong effect of environmental stress. There was a significant increase of galls and Pissonotus and a marginally significant increase of bored stems on fertilized plots but not on trapped plots. There was a significant interaction of site and fertilizer on gall parasitism. There were no interactions of either treatment with salinity on herbivore densities. The general lack of interaction between salinity level and other treatments on herbivore densities contrasts with our previous result where treatment effects did vary with salinity level on a large experimentally generated salinity gradient at one site. Thus, the results of the present paper suggest that, while environmental stress can modify top-down and bottom-up effects on herbivores at single sites, variation in site-to-site factors, possibly including clonal identity of plant, affects herbivore densities so much as to swamp out any observable interaction between environmental stress and top-down or bottom-up factors.