The role of terrestriality in promoting primate technology

"Complex technology" has often been considered a hallmark of human evolution. However, recent findings show that wild monkeys are also capable of habitual tool use. Here we suggest that terrestriality may have been of crucial importance for the innovation, acquisition, and maintenance of "complex" technological skills in primates. Here we define complex technological skills as tool-use variants that include at least two tool elements (for example, hammer and anvil), flexibility in manufacture or use (that is, tool properties are adjusted to the task at hand), and that skills are acquired in part by social learning. Four lines of evidence provide support for the terrestriality effect. First, the only monkey populations exhibiting habitual tool use seem to be particularly terrestrial. Second, semi-terrestrial chimpanzees have more complex tool variants in their repertoire than does their arboreal Asian relative, the orangutan. Third, tool variants of chimpanzees used in a terrestrial setting tend to be more complex than those used exclusively in arboreal contexts. Fourth, the higher frequency in tool use among captive versus wild primates of the same species may be attributed in part to a terrestriality effect. We conclude that whereas extractive foraging, intelligence, and social tolerance are necessary for the emergence of habitual tool use, terrestriality seems to be crucial for acquiring and maintaining complex tool variants, particularly expressions of cumulative technology, within a population. Hence, comparative evidence among primates supports the hypothesis that the terrestriality premium may have been a major pacemaker of hominin technological evolution.     

An Evolutionary Perspective for Bimodal Respiration: A Biological Synthesis of Fish Air Breathing

SYNOPSIS: The broad phyletic distribution of bimodal breathingamong the fishes, the diversity of this group's aerial-respiratoryspecializations, and the numerous ways that bimodality has permeatedthe natural history of many species provide a broad perspectiveon the evolution and biological significance of bimodal breathing.The long term evolutionary view of bimodal breathing emphasizesits importance in the evolutionary transition to terrestriality;a key role in this process was played by the fishes which werethe first air-breathing vertebrates. On the other hand, in mostextant fishes bimodality has not led to terrestriality. Rather,auxiliary air breathing enables a species to remain in or toexploit an aquatic habitat from which it would otherwise beexcluded.     

Terrestrial adaptations in the postcranial skeletons of guenons

Arboreal and semiterrestrial guenons show similar osteological features of the limbs across a wide range of species, environments, and geography, while the more terrestrially committed guenons exhibit greater morphological divergence. An ecomorphological comparison of two sympatric guenons living in Kibale Forest, Uganda, reveals an array of anatomical adaptations for terrestriality in the limbs of Cercopithecus lhoesti similar to those found in Erythrocebus patas. In contrast, Cercopithecus aethiops, although also frequent users of the terrestrial environment, generally exhibit fewer morphological adaptations characteristic of a terrestrial lifestyle. It appears that significant morphological modification for terrestriality has occurred twice within the diverse radiation of living guenons with C. aethiops perhaps representing a third group in the making. © 1994 Wiley-Liss, Inc.     

Of stones and monkeys: testing ecological constraints on stone handling, a behavioral tradition in Japanese macaques

Japanese macaques are known to manipulate stones by displaying various seemingly functionless behavioral patterns, including carrying a stone, rubbing two stones together, or gathering several stones into a pile. This form of solitary object play called stone handling (SH) is a behavioral tradition in Japanese macaques, showing striking intertroop differences in frequency and form. Here, we evaluated two ecologically based hypotheses invoked to account for these differences. We hypothesized that the occurrence and form of SH would be affected by stone availability and the degree of terrestriality. We used standardized sampling methods to assess differences in SH and terrestriality among four captive and six free-ranging troops of Japanese macaques, and determine site-specific stone availability. Although we demonstrated that SH is almost exclusively a terrestrial activity, our comparative analyses showed that the number of stones readily available and the relative amount of time spent on the ground by the macaques were not associated with the intertroop differences in the occurrence of SH. Failure to accept the terrestriality and stone availability hypotheses suggests that the performance of SH and the motivation to engage in this activity are both more diverse and more complex than the direct links to time spent on the ground or the number of stones locally available. Other environmental influences and sociodemographic factors should be jointly considered to identify the sources of variation in SH, as a beginning to better understand the constraints on the appearance and subsequent diffusion of stone-use traditions in nonhuman primates. Am J Phys Anthropol, 2008. (c) 2007 Wiley-Liss, Inc.     

Temperature's influence on the activity budget,terrestriality, and sun exposure of chimpanzees in the Budongo Forest,Uganda

Chimpanzee (Pan troglodytes schweinfurthii) activity budget, terrestriality, and sun exposure were found to be influenced by the immediate environmental temperature. Thirty adult chimpanzees in the Budongo Forest, Uganda, were observed for 247 h. Temperatures in the shade and sun, sky cover, sun exposure, activity, and terrestriality were recorded at 5‐min intervals at <15 m from the center of the party. Terrestriality frequency was 26.5% for females and 41.5% for males. Terrestriality and resting both show a significant positive correlation with temperature in the sun. Controlling for seven potential confounding factors, temperature in the sun remained the strongest predictor of terrestriality. The difference between temperatures in the sun and shade had a significant effect on chimpanzee sun exposure frequency. Time spent continuously in the sun was negatively correlated with temperature, beginning to decrease around 30°C, and markedly decreasing around 40°C. A concurrent experiment determined that dark pelage (lacking physiological coping mechanisms) exposed to the same solar regime can easily reach 60°C within minutes. This study indicates that both temperature in the sun and sun exposure play a role in influencing chimpanzee activity behavior, and specifically suggests that chimpanzees thermoregulate behaviorally both by moving to the ground and by decreasing their activity level. These results, in the context of deforestation and increasing global temperatures, have physiological and conservation implications for wild chimpanzees. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Habitat use affects morphological diversification in dragon lizards

Habitat use may lead to variation in diversity among evolutionary lineages because habitats differ in the variety of ways they allow for species to make a living. Here, we show that structural habitats contribute to differential diversification of limb and body form in dragon lizards (Agamidae). Based on phylogenetic analysis and ancestral state reconstructions for 90 species, we find that multiple lineages have independently adopted each of four habitat use types: rock‐dwelling, terrestriality, semi‐arboreality and arboreality. Given these reconstructions, we fit models of evolution to species’ morphological trait values and find that rock‐dwelling and arboreality limit diversification relative to terrestriality and semi‐arboreality. Models preferred by Akaike information criterion infer slower rates of size and shape evolution in lineages inferred to occupy rocks and trees, and model‐averaged rate estimates are slowest for these habitat types. These results suggest that ground‐dwelling facilitates ecomorphological differentiation and that use of trees or rocks impedes diversification.     

Spread of a Terrestrial Tradition in an Arboreal Primate

ABSTRACT   We present data on the spread of terrestrial activities in one group of wild northern muriqui monkeys (Brachyteles hypoxanthus). Both males and females consumed fruit, drank, rested, traveled, and socialized terrestrially, but proportionately more males spent significantly more of their time on the ground than females, and females were more likely to engage in terrestrial activities when accompanied by males than when by themselves. Terrestrial activities occurred in both open and closed habitats where arboreal substrates were available and utilized by other individuals engaged in similar activities. Ecological and demographic factors may have stimulated the muriquis' vertical niche expansion, but increases in the frequency and diversity of terrestrial activities, the high proportion of group members that engage in terrestriality, and its diffusion along male-biased social bonds are consistent with the development of a local terrestrial tradition similar to other types of traditions described in other primates. [Key words: terrestriality, ecology, predation, tradition]     

Comparison of freshwater discrimination ability in three species of sea kraits (Laticauda semifasciata, L. laticaudata and L. colubrina)

Three species of amphibious sea kraits (Laticauda spp.) require drinking freshwater to regulate water balance. The extent of terrestriality is known to differ among them. Species with higher extent of terrestriality would drink freshwater accumulated on land, whereas less terrestrial species would rely totally on freshwater that runs into the sea. Consequently, we predicted that the latter species might have a better ability to follow the flow of freshwater or lower salinity water in the sea than the former. We investigated the freshwater discrimination ability of three sea krait species, using a Y-maze apparatus. We found that Laticauda semifasciata and Laticauda laticaudata, less terrestrial species, followed freshwater significantly more frequently than seawater, whereas Laticauda colubrina, more terrestrial species, unbiasedly selected freshwater and seawater. This result supports our prediction and suggests that less terrestrial sea kraits more efficiently access freshwater sources in the sea than highly terrestrial sea kraits. It is likely that behavioral rehydration systems vary among sea kraits in relation to their terrestrial tendency.     

Macroevolution of arboreality in salamanders

Evolutionary theory predicts that selection in distinct microhabitats generates correlations between morphological and ecological traits, and may increase both phenotypic and taxonomic diversity. However, some microhabitats exert unique selective pressures that act as a restraining force on macroevolutionary patterns of diversification. In this study, we use phylogenetic comparative methods to investigate the evolutionary outcomes of inhabiting the arboreal microhabitat in salamanders. We find that arboreality has independently evolved at least five times in Caudata and has arisen primarily from terrestrial ancestors. However, the rate of transition from arboreality back to terrestriality is 24 times higher than the converse. This suggests that macroevolutionary trends in microhabitat use tend toward terrestriality over arboreality, which influences the extent to which use of the arboreal microhabitat proliferates. Morphologically, we find no evidence for an arboreal phenotype in overall body proportions or in foot shape, as variation in both traits overlaps broadly with species that utilize different microhabitats. However, both body shape and foot shape display reduced rates of phenotypic evolution in arboreal taxa, and evidence of morphological convergence among arboreal lineages is observed. Taken together, these patterns suggest that arboreality has played a unique role in the evolution of this family, providing neither an evolutionary opportunity, nor an evolutionary dead end.     

Evolution of extreme body size disparity in monitor lizards (Varanus)

Many features of species' biology, including life history, physiology, morphology, and ecology are tightly linked to body size. Investigation into the causes of size divergence is therefore critical to understanding the factors shaping phenotypic diversity within clades. In this study, we examined size evolution in monitor lizards (Varanus), a clade that includes the largest extant lizard species, the Komodo dragon (V. komodoensis), as well as diminutive species that are nearly four orders of magnitude smaller in adult body mass. We demonstrate that the remarkable body size disparity of this clade is a consequence of different selective demands imposed by three major habitat use patterns-arboreality, terrestriality, and rock-dwelling. We reconstructed phylogenetic relationships and ancestral habitat use and applied model selection to determine that the best-fitting evolutionary models for species' adult size are those that infer oppositely directed adaptive evolution associated with terrestriality and rock-dwelling, with terrestrial lineages evolving extremely large size and rock-dwellers becoming very small. We also show that habitat use affects the evolution of several ecologically important morphological traits independently of body size divergence. These results suggest that habitat use exerts a strong, multidimensional influence on the evolution of morphological size and shape disparity in monitor lizards.     

Dietary copper absorption and excretion in three semi-terrestrial grapsoid crabs with different levels of terrestrial adaptation

Three species of phylogenetically related semi-terrestrial crabs (Superfamily Grapsoidea--Sesarma rectum, Goniopsis cruentata and Neohelice granulata (formerly: Chasmagnathus granulatus) with different degrees of terrestriality were studied to quantify the accumulation of copper (Cu) in hemolymph, gills, hepatopancreas and antennal gland, and its excretion through the faeces. These crabs were fed for 15 days practical diets containing 0 (A), 0.5 (B), 1.0 (C), and 1.5% (D) of added CuCl2 (corresponding to 0, 0.2, 0.5 and 0.7% of Cu2+, respectively). The amount of food ingested was directly proportional to the degree of terrestriality: S. rectum, the most terrestrial species, ate around 2-3 times more than the other crabs, whereas G. cruentata ate 1.5-2 times more than N. granulata, the least terrestrial. The amount of Cu excreted in the feces was proportional to Cu ingestion, and was 76.8% and 64.2% higher for Sesarma fed diet D compared to G. cruentata and N. granulata, respectively. Sesarma also displayed higher Cu concentration in the haemolymph, gills and antennal glands, but not in the hepatopancreas. A detoxifying mechanism followed by elimination was probably present at this last organ, preventing Cu accumulation. More terrestrial crabs, such as Sesarma, may accumulate more Cu in hemolymph and tissues, showing a correlation between metal accumulation and increased terrestriality. In this aspect, contaminated feed sources with Cu may have more impact in conservation of terrestrial crabs.     

Exploring the molecular diversity of terrestrial nemerteans (Hoplonemertea, Monostilifera, Acteonemertidae) in a continental landmass

We report the finding of terrestrial nemerteans of the family Acteonemertidae from the northern part of Spain. The specimens were studied using molecular data from the nuclear ribosomal 18S rRNA and the mitochondrial cytochrome c oxidase subunit I genes. The 18S rRNA data strongly suggest the presence of three species of terrestrial nemerteans in the Iberian Peninsula, an old landmass where terrestrial nemerteans had not previously been reported. These specimens originate from primarily undisturbed forests across a distance of c . 1000 km. Cytochrome c oxidase subunit I data also indicate the presence of multiple lineages of Iberian terrestrial nemerteans. Nonetheless, the pattern obtained from this marker is obscured most probably by deep genetic divergences. This molecular diversity, at least in some of the clades, suggests that the Iberian species are not the result of recent introductions, as proposed for other terrestrial nemerteans found in Europe. Our data also touch upon the question of a single origin of terrestriality in nemerteans, a hypothesis rejected by both data sets. Nevertheless, terrestriality seems to have had a single origin in the family Acteonemertidae.     

The influence of ecology and genetics on behavioral variation in salamander populations across the Eastern Continental Divide

Understanding the unique contributions of ecology and history to the distribution of species within communities requires an integrative approach. The Eastern Continental Divide in southwestern Virginia separates river drainages that differ in species composition: the more aquatic, predatory Desmognathus quadramaculatus is present only in the New River drainage (which drains to the Gulf of Mexico), while Desmognathus monticola is present in both the New River drainage and the James River drainage (which drains to the Atlantic Ocean). We investigated natural distributions, behavioral variation in experimental mesocosms, population genetic, and phylogenetic implications of community structure. The presence of D. quadramaculatus increased the terrestriality of D. monticola in natural and experimental situations but to different degrees in allopatric and sympatric populations. Our ecological data suggest that the degree of terrestriality in D. monticola is a result of a balance between the optimal aquatic habitat and risks of predation. Our genetic analyses suggest that D. monticola has experienced a recent range expansion and has only a recent history of association with D. quadramaculatus in Virginia. This is surprising given the strong behavioral variation that exists in populations experiencing unique community compositions over a scale of meters. This study demonstrates the need to combine both ecology and genetics toward an understanding of the factors affecting species distributions, behavioral variation between populations, and patterns of genetic variation across a landscape.     

Oldest Pathology in a Tetrapod Bone Illuminates the Origin of Terrestrial Vertebrates

The origin of terrestrial tetrapods was a key event in vertebrate evolution, yet how and when it occurred remains obscure, due to scarce fossil evidence. Here, we show that the study of palaeopathologies, such as broken and healed bones, can help elucidate poorly understood behavioural transitions such as this. Using high-resolution finite element analysis, we demonstrate that the oldest known broken tetrapod bone, a radius of the primitive stem tetrapod Ossinodus pueri from the mid-Viséan (333 million years ago) of Australia, fractured under a high-force, impact-type loading scenario. The nature of the fracture suggests that it most plausibly occurred during a fall on land. Augmenting this are new osteological observations, including a preferred directionality to the trabecular architecture of cancellous bone. Together, these results suggest that Ossinodus, one of the first large (>2m length) tetrapods, spent a significant proportion of its life on land. Our findings have important implications for understanding the temporal, biogeographical and physiological contexts under which terrestriality in vertebrates evolved. They push the date for the origin of terrestrial tetrapods further back into the Carboniferous by at least two million years. Moreover, they raise the possibility that terrestriality in vertebrates first evolved in large tetrapods in Gondwana rather than in small European forms, warranting a re-evaluation of this important evolutionary event.     

Evidence at hand: Diversity, functional implications, and locomotor prediction in intrinsic hand proportions of diprotodontian marsupials

Knowledge about the diversity, locomotor adaptations, and evolution of the marsupial forelimb is limited, resulting in an underrepresentation of marsupials in comparative anatomical literature on mammalian forelimb anatomy. This study investigated hand proportions in the diverse marsupial order Diprotodontia. Fifty-two measurements of 95 specimens representing 47 species, as well as 6 non-diprotodontian specimens, were explored using principal components analysis (PCA). Bootstrapping was used to assess the reliability of the loadings. Phylogenetically independent contrasts and phylogenetic ANOVA were used to test for correlation with size and functional adaptation of forelimbs for locomotor habit, scored as arboreal vs. terrestrial. Analysis of first principal component (PC1) scores revealed significant differences between arboreal and terrestrial species, and was related to relative slenderness of their phalangeal elements. Both locomotor groups displayed allometry along PC1 scores, but with different intercepts such that PC1 discriminated between the two locomotor habits almost completely. PC2 separated some higher-level clades and burrowing species. Analysis of locomotor predictors commonly applied by palaeontologists indicates that ratios between proximal and intermediate phalanges were unsuitable as predictors of arboreality/terrestriality, but the phalangeal index was more effective. From PCA results, a phalangeal slenderness ratio was developed which proved to be a useful discriminator, suggesting that a single unallocated phalanx can be used for an impression of locomotor mode in fossils. Most Diprotodontia are laterally paraxonic or ectaxonic, with the exception of digging species whose hands are medially paraxonic. Our results complement those of studies on placental mammals, suggesting that the demands of arboreality, terrestriality, or frequent digging on intrinsic hand proportions are met with similar anatomical adaptations in marsupials.     

Terrestrial behavior and use of forest strata in a group of black-and-white snub-nosed monkeys Rhinopithecus bieti at Xiaochangdu,Tibet

Food distribution and predation pressure are considered to be the main ecological factors that influence the use of forest strata(basically arboreality vs.terrestriality)in non-human primates.Here,we investigate ground use of wild,unprovisioned black-and-white snub-nosed monkeys Rhinopithecus bieti by means of the scan sampling method.The results show that the monkeys spent 15.0% of the day time on the ground;16.6%,12.7%,and 15.6% for adult males,adult females and juveniles,respectively.Adult males and juve...     

Predator‐induced phenotypic plasticity in an arid‐adapted tropical tadpole

Adaptive phenotypic plasticity is widespread and involves diverse phenotypes. Key environmental stressors, such as predation risk, can simultaneously induce changes in multiple traits, but the magnitude of response is dependent upon the environmental conditions. Species that utilize temporary ponds are expected to exhibit stronger predator‐induced responses in the form of morphology than behaviour (i.e. reduced activity) to meet the demands of rapid development by maintaining high foraging activity while reducing predation risk via morphologically plastic traits. In a laboratory experiment, I examined the effects of predator chemical cues and conspecific alarm cues on activity, development and morphology on Leptodactylus bufonius tadpoles. This species has terrestrial oviposition and completes the early part of its development outside of ephemeral and temporary ponds in the Gran Chaco ecoregion of South America. Tadpoles in the predator treatments exhibited both behavioural and morphological predator‐induced plastic responses. Tadpoles tended to possess shorter, deeper tails when exposed to predators. The greatest reduction in activity was observed in tadpoles exposed to both predator and conspecific alarm cues, which subsequently resulted in the slowest development. Temporary and ephemeral pond adapted species with terrestrial oviposition may capitalize on a head start in development by being able to afford reduced growth rates via a reduction in activity. This may occur when the constraints imposed by pond hydroperiod (e.g. risk of pond drying) are relaxed when compared with species with aquatic oviposition, which must undergo all stages of development during the pond's hydroperiod. Thus, in addition to the predator and hydroperiod gradients, examining phenotypically plastic responses along a ‘terrestriality gradient’ in a comparative framework would provide insights as to the costs and benefits of increasing terrestriality in anuran reproductive modes to environmental stressors.     

Terrestriality and tree stratum use in a group of Sichuan snub-nosed monkeys

Morphological characters allow the Sichuan snub-nosed monkey (Rhinopithecus roxellana) to use multiple tree levels, but very few studies have quantified the terrestriality and tree stratum use of the species. I investigated the terrestriality and tree stratum use in a group of the monkeys from July 2003 to September 2004 (except February) in the Qianjiaping area of Shennongjia Nature Reserve, China. I collected data on the vertical position of individual monkeys in forest in relation to behavior types, diet, age/sex classes, vegetation types, tree height, and distribution of predators. The monkeys were much more arboreal than they were thought to be. They spent 97.1% of their time in trees (n=21,234 records) and 2.9% on the ground, and mainly used the middle (74.4%) and upper strata (17.4%). The monkeys displayed all behavioral types except searching in the middle and upper strata. The percentage of use of a stratum (except the low stratum) varied among months, and there was a difference in the percentage of use of a stratum among age/sex classes and between vegetation types. Approximately 94.2% of trees used by the monkeys were >6 m tall. They mainly fed on lichens, young leaves, mature leaves, flowers, fruits or seeds, and buds in the middle and upper strata, bark in the low and middle strata and herbs on the ground. Wolf (Canis lupus), leopard (Panthera pardus), and golden eagle (Aquila chrysaetos) are predators threatening the survival of individual monkeys in the study site. The results suggested that the seasonal vertical distribution of food items eaten in forest, predators, and vegetation types had important effects on the terrestriality and tree stratum use of the monkeys.     

Evaporative water loss, corporal temperature and the distribution of sympatric fiddler crabs (Uca) from south Texas

Desiccation and thermal stress are among the primary factors limiting terrestriality in crustaceans. Water loss was estimated as weight change in five sympatric species of Uca from south Texas for periods up to 7 hr in dry air. Simultaneously, corporal temperature was measured with a thermocouple placed under the carapace. To estimate integumental permeability to water, 115 mm2 portions of dorsal carapace were glued to U-shaped tubes containing a crab Ringer's solution. These were exposed to dry air and water permeability was estimated from weight change. In whole-animal studies, most rapid weight loss occurred in the first 5 min of exposure to dry air as the body temperature fell below ambient (25 degrees C) in all species. The three most terrestrial species exhibited significant survival over more aquatic congeners after prolonged desiccation. The greatest rate of water loss was observed in Uca subcylindrica which lost 22.9+/-3.0% body weight. Uca panacea and Uca spinicarpa lost 14.1+/-1.6% and 18.5+/-1.8%, respectively. Based on blood osmolarity changes, Uca longisignalis and Uca rapax were more resistant to water loss than Uca subcylindrica under these conditions. Water loss from sections of the dorsal carapace were highest in Uca spinicarpa (10.4 mg/hr/cm2) and Uca longisignalis (8.9 mg/ hr/cm2). Uca subcylindrica and Uca panacea were intermediate (4.5 and 4.2 mg/hr/cm2) while Uca rapax expressed the lowest value (2.9 mg/hr/cm2). These observations support the notion that water loss can effectively lower body temperature in fiddler crabs. However, an inverse relationship between terrestriality and integumental permeability was not evident in these sympatric congeners. Ultimately a balance between physiological and behavioral mechanisms must be achieved for adaptation to the semi-arid habitats in south Texas.