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The Society for Integrative and Comparative Biology
George A. Bartholomew's Contributions to Integrative and Comparative Biology1
1 Museum of Zoology, The University of Michigan, Ann Arbor, Michigan 48109-1079
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The Bartholomew Award has now completed a decade of recognizing outstanding young investigators in comparative physiology and biochemistry or in related fields of functional and integrative biology. It honors Professor George A. Bartholomew (Bart to his many students and other friends), whose research contributions continue to be important in shaping these fields. Bart's influence reflects a steadfast adherence to a set of basic precepts: the inherent unity of biology; the need for an evolutionary perspective in functional studies; the value of modern natural history in guiding research investigations; the focus on the organism and its function in nature, even in highly reductionist studies; the importance of biological variability within and between species; and the crucial interactions of physiology and behavior in allowing animals to deal with environmental challenges. Were he to have done nothing else in his career, he would remain an important figure in the fields with which the Society of Integrative and Comparative Biology's (SICB) Division of Comparative Physiology and Biochemistry is concerned. However, his influence is also felt through his inspirational performance as an undergraduate teacher, his skill and wisdom as a graduate mentor, his many services to the University of California, his insightful contributions to scientific committees and policy boards at the national level, and his presidency of the American Society of Zoologists (now SICB). This symposium offers the opportunity for honoring Bart for all his accomplishments and fine personal qualities, while illustrating the contributions of the impressive set of younger investigators who are recipients of the George A. Bartholomew Award.
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I want to note my pleasure at being a participant in a symposium that both honors George Bartholomew ("Bart" to his students and other friends) and commemorates the tenth anniversary of the George A. Bartholomew Award. This award, which recognizes gifted young investigators in integrative and comparative biology, is a tangible indication of the esteem in which Bart is held by his colleagues in the Division of Comparative Physiology and Biochemistry of The Society of Integrative and Comparative Biology (SICB). I have been asked to comment on Bart's contributions to integrative and comparative biology. I have arbitrarily divided his accomplishments in this regard into three categories: definition of precepts, original research, and education and service. I shall comment on these in order.
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George Bartholomew in his valedictory for this symposium (Bartholomew, 2005
) discusses creativity and the precepts that have guided his scholarly activities over his career. Through his adherence to these precepts, he has been able to exert a powerful effect on the post-World War II development of ecologically oriented physiology. His holistic view of biology continues to inspire in this age of disciplinary fractionation and to convey an important message. He has recognized that biology is a continuum, but that biologists because of their human limitations tend to divide themselves into categories and then pretend that these categories exist in the living systems under investigation (Bartholomew, 1958). Thus he has emphasized that animals are indivisible functionally and that his field of physiology is not an isolatable organismal component, being inextricably linked with morphology and behavior. He pursued this view of a unified biology further in an eloquent statement concerning modern natural history (Bartholomew, 1986, p. 329) that has broad implications for integrative and comparative biology: "Because of its focus on organisms natural history is in a unique position to supply questions and integrating links among disciplines. Studies at lower levels will delineate the machinery of structural units, and the complex systems into which these units have been assembled through evolutionary time will be worked out by research at the intermediate and higher levels of biological integration. Biology is indivisible; biologists should be undivided." Bart (1964, p. 8) had provided earlier justification for an inclusive view of biology through recognition of this hierarchy of biological explanations: "There is a familiar solution to this problem [parochialism based on differences in approach by various biologists], widely recognized but sometimes difficult to accept emotionally. This is the idea that there are a number of levels of biological organization and that each level offers unique problems and insights, and further, that each level finds its explanation of mechanism in the levels below, and its significance in the levels above."
As is evident from his contribution to this symposium (Bartholomew, 2005), George Bartholomew has also made it a rule to explore the evolutionary implications of his research wherever feasible. One of the foundations of this practice has been his appreciation of the evolutionary implications of biological variability. "Differences between individuals are the raw materials for evolutionary change and for the evolution of adaptations, yet of course most physiologists treat these differences as noise that is to be filtered out. From the standpoint of physiological ecology, the traditional emphasis of physiologists on central tendencies rather than on variance has some unhappy consequences. Variation is not just noise; it is also the stuff of evolution and a central attribute of living systems.... The physiological differences between individuals in the same species or population, and also the patterns of variation in different groups, must not be ignored" (Bartholomew, 1987, pp. 32-33). In this connection, he has emphasized (Bartholomew, 1987, p. 33) the value of research efforts that can deal critically with intraspecific comparisons. "Rather than just comparing different species, one should adopt some of the formats developed for interspecific comparisons in an attempt to compare breeding populations within species ... and individuals within the same breeding population.... Such efforts should allow investigators to approach more closely the dynamics of evolutionary change, and, in appropriate situations, to integrate the findings of physiological ecology with those of population genetics."
George Bartholomew has also consistently emphasized the important role of historical factors in shaping the functional characteristics of contemporary species ([each species] "has an evolutionary history, which means its present configuration has been shaped by natural selection" [Bartholomew, 1982a, p. 231]). He has noted further that it is important in the analysis of the adjustments of organisms to their respective environments to understand that selection results in adequacy of performance rather than perfection. He also has reflected on the fact that despite the long-term probability of extinction, every organism alive today is part of an enormously long success story in which each of its ancestors has been sufficiently well adapted to its physical and biotic environments to mature and reproduce successfully. It is the intact and functioning organism on which natural selection operates and such organisms therefore should be the primary concern of any biologist who aspires to a broad and integrated understanding of biology. Consequently, Bart regards adaptation as so central a theme as to be inseparable from life itself (Bartholomew, 1987). Undoubtedly, his views have contributed in a number of respects to the foundation of the burgeoning field of evolutionary physiology (Garland and Carter, 1994; Feder et al., 2000; Kingsolver and Huey, 2003).
Bart has also been careful to observe the principle first enunciated by Claude Bernard that an organism is inseparable from its environment (Bartholomew, 1958, 2005). Full knowledge of any species requires familiarity not just with its general surroundings but also its interaction as a self-maintaining physicochemical system with its special microenvironment (Bartholomew, 1958). Although it is convenient to maintain a verbal distinction between the two (organism and environment), he has cautioned that this should only be done if they are never treated separately.
A further precept arising from the views summarized in Bart's contribution to this symposium (Bartholomew, 2005) emphasizes interactions between functional capacities and behavior of organisms, interactions that are frequently critical for survival in difficult physical conditions (Bartholomew, 1964, 1966a). He has noted that such interactions are especially important for terrestrial animals due to the physical complexity of their environments. These animals because of their mobility and behavioral capacities can actively seek out and use those environmental situations that best allow their morphological and physiological abilities to function adequately for survival and reproduction. Most of these species are less than 1% the size of man and his domestic animals, and their environment may include shaded or sunny areas, tunnels, cracks, crevices, burrows, thick underbrush, holes in logs, and/or nests, making gross climatic indices often irrelevant (Bartholomew, 1964). These and preceding considerations have led him to expend substantial research effort in the field as well as the laboratory.
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George Bartholomew is a true comparative biologist and the subjects of his studies include insects, amphibians (Bucher et al., 1982
; Ryan et al., 1983), reptiles, birds, and mammals, as well as the plant Philodendron selloum (Seymour et al., 1983, 1984). (Many of the studies arising from his work on insects and amniotic vertebrates are cited below.) He has consistently operated at the interfaces of comparative physiology, ecology, and behavior. Pursuit of appropriate research animals and investigation of interesting problems have led him to work in North and Central America; Australia; Europe; Africa; Antarctica; and a number of islands including the Pribiloffs, Midway, and New Guinea. The following comments do not comprise a comprehensive review of his total research activities (for example, in the interests of producing an essay of manageable length, I have omitted mention of several primarily behavioral studies and have not fully indicated every publication pertaining to some of the topics that are considered below), but I have tried through the references that are included to provide some sense of the scope of his investigations, creativity and, in a number of instances, truly pioneering efforts.
The studies by Bart and his collaborators are noteworthy for their broad perspective. His initial research, which has been cited over at least 50 years, concerned behavior of double-crested and Brandt cormorants, Phalacrocorax auritus and P. penicillatus, on San Francisco Bay, CA (Bartholomew, 1942, 1943a, b). Following a three-year interruption due to World War II, Bart resumed a publication career that would extend over the next four decades and be marked by a number of "firsts" and technical innovations. His doctoral thesis established the thresholds of light intensity necessary for evoking photoperiodic responses in house sparrows, Passer domesticus (Bartholomew, 1949).
After joining the faculty at UCLA he was the first physiological ecologist to initiate an organized program of research on the physiology and behavior of desert birds. This resulted in a number of papers on the thermoregulatory responses (e.g., Bartholomew and Cade, 1957a; Bartholomew and Dawson, 1958; Bartholomew et al., 1962) and on water and electrolyte metabolism (e.g., Bartholomew and MacMillen, 1960; Smyth and Bartholomew, 1966) of these animals, culminating in an influential review of water relations (Bartholomew and Cade, 1963) and a model that accounted for the ability of certain small seed eating birds to survive without drinking (Bartholomew, 1972). Bart continued to investigate the responses of birds to heat challenges in several collaborations (Lasiewski and Bartholomew, 1966; Bartholomew et al., 1968; Lasiewski et al., 1970), obtaining indications in common poor-wills (Phalaenoptilus nuttallii), double-crested cormorants, brown pelicans (Pelecanus occidentalis), and mourning doves (Zenaidura macroura) that gular fluttering, an activity serving to increase evaporative water loss at high temperatures, occurred at the resonant frequency of the gular apparatus (Lasiewski and Bartholomew, 1966; Bartholomew et al., 1968). Such congruence would reduce the energy costs of this form of cooling.
One particularly important facet of the research on water and electrolyte balance referred to above documented variation among populations of the savannah sparrow (Passerculus sandwichensis) in patterns of use of NaCl solutions or sea water as fluid sources (Cade and Bartholomew, 1959). Members of two subspecies resident in salt marshes (P. s. beldingi and P. s. rostratus) increased their drinking with increasing concentration of the solutions provided, whereas three northern migratory subspecies of savannah sparrow (P. s. anthinus, P. s. nevadensis, and P. s. brooksi) decreased theirs, like most other birds. This indicated marked differences in electrolyte metabolism between the two groups and the salt marsh residents proved more proficient in obtaining physiologically useful water from salt and sea water solutions than the migrant subspecies. A subsequent study (Poulson and Bartholomew, 1962) revealed important physiological differences between representatives of one of the salt marsh taxa (P. s. beldingi) and those of a migrant form (P. s. brooksi). The salt marsh residents could tolerate significantly higher serum osmotic pressures and chloride concentrations and produce substantially more concentrated urine than the migrants. These studies are notable in providing an impressive early example of geographic variation at the intraspecific level in avian physiological performance.
Another of Bart's early research projects dealt with pinnipeds. This initially produced documentation of the resurgence of populations of two species of these animals on islands off Baja California and southern California (Bartholomew, 1950, 1951), but was concerned primarily with detailed investigations of population biology and reproductive behavior. Major studies were conducted on the social and reproductive behavior of the elephant seal, Mirounga angustirostris (Bartholomew, 1952); Alaska fur seal, Callorhinus ursinus (Bartholomew and Hoel, 1953); and California sea lion, Zalophus californianus (Peterson and Bartholomew, 1967). Some important thermal information was also obtained. Due to the large size and effective insulation of these animals noted above, terrestrial breeding can put them at risk of overheating, even in a cool climate (see, for example, Bartholomew and Wilkie, 1956). Bart showed how a predominantly Holarctic species, the California sea lion, could extend its range to the equatorial Galápagos Islands where warm temperatures and intense insolation prevail. Breeding male sea lions persistently maintain terrestrial territories on the coastal islands of California and Baja California, where thermal conditions are ameliorated by cool upwelling water and a persistent summer overcast. The breeding males in the Galápagos use a behavioral strategy in dealing with the heat challenge prevailing there. During the daylight hours, they protect themselves from overheating by holding aquatic territories while remaining immersed in tide pools or channels, hauling out on land only at night (Bartholomew, 1966a). This seemingly simple strategy, imposes profound effects on a breeding structure that is exclusively terrestrial in other otariids (sea lions and fur seals), but it is an excellent example of a behavioral solution to a primarily physiological problem, a theme that recurs in many of Bart's studies.
Early in his career, Bart recognized breeding colonies of seabirds as an excellent resource for thermoregulatory studies. Many of these birds nest in exposed situations and, at tropical or subtropical latitudes in particular, they and their eggs and young can be exposed to dangerously intense insolation and high air temperatures. Commencing with a relatively simple field study of western gulls, Larus occidentalis (Bartholomew and Dawson, 1952), Bart participated in several projects concerning the ontogeny of avian thermoregulatory capacity. One involved a comparison of three species of seabirds that nest concurrently on the surface of a hot desert island in the Gulf of California, Mexico, despite major differences in the thermoregulatory proficiency of their hatchlings. The results demonstrated how closely attentive behavior of parents of each species was attuned to the developmental status of their chicks (Bartholomew and Dawson, 1954). Further extensive observations of breeding seabirds on Midway Island, where intense insolation is also a problem, documented thermally significant behavior of both parents and young of various ages (Howell and Bartholomew, 1961a, b, 1962a, b). One lasting image is of older nestling albatrosses (Diomedea nigripes and D. immutabilis) with their backs to the sun resting on their heels and raising their heavily vascularized and shaded webbed feet off the ground into the cooling trade winds (Howell and Bartholomew, 1961a). Bart's discerning eye led to a particularly informative account of the behavioral repertoire (orientation away from the sun, holding its wings away from the body, elevation of the scapular feathers) used by the masked booby (Sula dactylatra) while protecting itself and shading its eggs and young chicks from the intense solar radiation and high ambient temperatures prevailing in the Galápagos during the breeding season (Bartholomew, 1966b). A later study on another island in the Gulf of California demonstrated the precise coupling of thermally protective incubation behavior by adult Heermann's gulls (Larus heermanni) to ambient conditions (Bartholomew and Dawson, 1979).
Behavior can have a major impact on the thermal relations of terrestrial as well as aquatic birds. A particularly spectacular example of this is provided by sociable weavers (Philetairus socius). These weaver finches, which are the size of house sparrows, construct huge, communal nests in the Kalahari Desert, which they continuously occupy and maintain. Bart, F. N. White, and T. R. Howell examined the extent of thermal protection provided by these structures in summer and winter (White et al., 1975; Bartholomew et al., 1976). In the former season, outside air temperatures ranged from 16° to 33.5°C, whereas temperatures in occupied nest chambers only varied 7° or 8°C. Winter in the Kalahari often involves sustained nocturnal winds and temperatures that can drop to freezing. At this season, the insulation of the nest in combination with the heat production of roosting birds produced temperatures as high as 37°C, 23° above outside air. Only two sociable weavers occupied a nest chamber in the summer, whereas up to five did so in winter, leading Bartholomew et al. (1976) to conclude that changing this number is the principal means by which these birds maintain chamber temperatures within their zone of thermal neutrality throughout the year. This thermostability leads to energy savings of nearly 50% as compared with estimated costs were the birds to roost in the open air. This curtailment of thermoregulatory costs appears important both in allowing both higher population densities of the sociable weaver in an area of low biological productivity and in the extension of breeding into the cooler parts of the year. The latter is probably significant in helping this bird to avoid the heavy reptilian predation on parents, eggs, and young that can occur in summer. The use of burrows for nesting also can provide thermal protection, as the study by F. N. White, Bart and J. L. Kinney of a Spanish nesting colony of the European bee-eater, Merops apiaster, illustrates (White et al., 1978). However, poor nest sanitation and microbial action on the accumulated excrement can lead to buildups of NH3 and CO2, which are alleviated by the ventilation resulting from wind and the movement of adults in and out of the nest tunnel.
Bart's later research on avian development involved participation in studies of growth patterns, gas exchange, and energetics of avian embryos. One example of this involved a study of the brown pelican, a representative of the Order Pelecaniformes, a group of particular interest because it includes the largest altricial birds and the only marine birds showing this developmental pattern. Several features of the pelican's embryonic development differ from those in other altricial species (eyes open at hatching, high energy density of the egg, the large amount of yolk present in hatchlings, the relation of mass-specific oxygen consumption to embryonic age, and the high total cost of development up to hatching [121 kJ]). The brown pelican produces a relatively large chick at a relatively high cost compared to other, smaller altricial species. The divergence of its pattern of embryonic development from that in these other birds was regarded as consistent with the hypothesis that avian altriciality is polyphyletic (Bartholomew and Goldstein, 1984). Data primarily from the brown pelican and three other species from different orders were used in an analysis assessing correlates of variation among birds in growth pattern, gas exchange, and energetics of development (Bucher and Bartholomew, 1984). These three physiological variables were found to be correlated with body mass, time, energy, phylogeny, and ecological niche of the species. The study emphasized the importance of variability as a biological reality and the deficiencies of confining the analysis embryonic growth processes entirely to definitions of central tendencies. Bart also collaborated in another study of developmental variation, in this instance dealing with the Adélie (Pygoscelis adeliae) and emperor penguins (Aptenodytes forsteri), both of which lay smaller eggs than large species in other avian orders (Bucher et al., 1986). The incubation period of the former species was similar to that predicted on the basis of egg mass, but that of the emperor penguin was 50% longer. Total oxygen consumption of developing chicks of the two species over the incubation period matched values predicted for precocial birds, leading to the conclusion that these penguins were incorrectly classified as semi-altricial.
The role of heterothermy in the biology of certain birds and mammals that must deal with challenges involving heat, cold, or restriction of food or water, has long intrigued George Bartholomew. He led or participated in the first successful laboratory studies (Bartholomew et al., 1957, 1962; Howell and Bartholomew, 1959) of the common poor-will, the only bird known to hibernate. At a time when metabolic level in a given group of animals was regarded by many as solely a function of body mass, these studies documented the bird's remarkably low standard metabolic rate as well as its heterothermic capacities and extensive powers of heat defense. Information on dormancy in swifts and hummingbirds was also obtained (Bartholomew et al., 1957). Bart also collaborated in studies of dormancy in desert rodents (Bartholomew and Cade, 1957b; Bartholomew and Hudson, 1960; Bartholomew and MacMillen, 1961; Brown and Bartholomew, 1969), analyzing the capacities of pocket mice (Perognathus longimembris), Mohave ground squirrels (Spermophilus mohavensis), and kangaroo mice (Microdipodops pallidus) for entering torpor and providing the first extensive laboratory observations on the phenomenon of estivation. This form of dormancy, which was poorly understood at the time, was explored further in a review article (Hudson and Bartholomew, 1964).
Bart has extended his interest in mammalian and avian heterothermy through additional studies involving such species as speckled mouse birds, Colius striatus (Bartholomew and Trost, 1970), pygmy possums, Cercaertus nanus (Bartholomew and Hudson, 1962), and two small New Guinea flying foxes: the common tube-nosed fruit bat, Nyctimene albiventer, and the unstriped tube-nosed bat, Paranyctimene raptor (Bartholomew et al., 1970). The results for the flying foxes were noteworthy because of the two bats' tropical distribution, frugivorous diet, and the fact that a capacity for heterothermy had not been previously reported for any members of the Megachiroptera (see Bartholomew et al., 1964). Additionally, nocturnal torpor involving body temperatures as low as 26.8°C was observed in two small neotropical birds, the manakins Pipra mentalis and Manacus vitellinus (Bartholomew et al., 1983). These birds are also frugivorous. Heterothermy can reduce the energy expenditures of these small animals by more than half. Fruit is not always readily available in rain forests and Bart and his coauthors hypothesized that torpor might well occur in other small tropical songbirds dependent upon such food.
The use of torpor by the Mohave ground squirrel contrasts sharply with the behavior of the antelope ground squirrel (Ammospermophilus leucurus) in the same desert environment. The latter species neither hibernates nor estivates, though it does achieve some energetic savings by lowering its body temperature to 32°–33°C during winter nights (Chappell and Bartholomew, 1981a). Therefore, it is forced to deal with conditions on the desert surface throughout the year. Its diurnal habits expose it to severe summer heat, which it deals with by shuttling between the desert surface and its burrow. It tolerates hyperthermia when on the surface, thereby avoiding high rates of evaporative water loss. Periodic retreat to the antelope ground squirrel's burrow allows it to dump the heat it has gained, thereby surviving the stresses of the summer daytime desert through appropriately timed movements (Bartholomew and Hudson, 1961; Chappell and Bartholomew, 1981a, 1981b).
Thermally relevant behavior is also crucially important for other mammals. In one of the first detailed studies of thermoregulatory capacity in macropod marsupials (kangaroos, wallabies, etc.), Bart found that the quokka (Setonix brachyurus) was at least as effective in its temperature control over an ambient range of –10° to 44°C as eutherian mammals of comparable size (2.5–4.0 kg). At high ambient temperatures, this West Australian species cooled itself by the behavioral stratagem of spreading saliva over its ventral surface, limbs and tail (Bartholomew, 1956). The large Australian flying foxes Pteropus poliocephalus and P. scapulatus were found by Bartholomew et al. (1964) to maintain body temperature in the usual range for mammals at ambient temperatures from 5° to 40°C. In cooler surroundings they wrapped their wings about the body creating an "overcoat" that allowed skin temperatures to remain as much as 10°C above ambient. At high air temperatures they supplemented their panting by salivation and licking of the wings and chest. Flapping the wings also contributed to convection over the body. These behavioral actions contributed to the ability of the flying foxes roosting in exposed positions in the tops to trees to tolerate exposure the tropical or subtropical sun. Behavior also figures prominently in maintenance of thermal balance in the rock hyrax (Heterohyrax brucei), a mammal Bart studied during a sabbatical leave in Kenya. This hyrax has a behavioral repertoire that includes diurnality, basking, restricted periods of surface activity, gregarious habits within burrows, and huddling, all contributing to effective control of body temperature despite a low metabolic rate and high thermal conductance (Bartholomew and Rainy, 1971). This animal also showed an unusual physiological response at high temperatures, increasing evaporative water loss while reducing its oxygen consumption, the reduction evidently produced by lowering muscle tonus. Additionally, Bart also participated in a study (Bell et al., 1986) of the energetics of the leaf-nosed bat (Macrotus californicus), which involved important behavioral issues. The species is of special interest due to its being the northernmost representative of a primarily tropical family (Phyllostomidae) and it is does not use torpor in energy conservation. The combined field and laboratory study provided information on thermoregulatory characteristics, standard and field metabolic rates, and behavior of this animal. These data supported the conclusion that, rather than relying on special physiological adaptations for survival, the leaf-nosed bat is successful as a year-round resident in its desert environment through roosting in continuously warm (ca. 29°C) geothermal refugia such as caves and mine shafts, and through an economical method of foraging involving visual prey detection.
Bart's use of the comparative method in desert studies has extended to analysis of reproductive patterns in several rodents. G. J. Kenagy and he undertook a long-term investigation of reproductive timing in five species of rodents (two nocturnal kangaroo rats and two nocturnal pocket mice in addition to the diurnal antelope ground squirrel) coexisting in a desert community in the Owens Valley of California. They were interested in determining whether closely related species differ in reproductive timing as a result of such things as differences in body size, daily cycle, food habits, locomotor patterns, and their respective microenvironments. (Kenagy and Bartholomew, 1985). They found substantial differences among the species, all of which are long-lived and characterized by relatively stable population levels. The antelope ground squirrel is a "predictor," with a slow, lengthy reproductive period coinciding with the historical probability for rainfall and plant productivity, which can be unpredictable in a given year. The Merriam kangaroo rat (Dipodomys merriami) is a "responder," breeding in direct response to pulses in food production. Its congener, the somewhat larger Great Basin kangaroo rat (D. microps), with a dependable food supply of salt bush (Atriplex confertifolia) leaves, is an "independent," successfully ignoring rainfall and pulses of seed production. The lengthy periods of dormancy occurring in the two pocket mice (Perognathus longimembris and P. formosus) overlap the periods of winter rainfall and may extend beyond it. They are in Kenagy and Bartholomew's (1985) phrase "pulse gamblers" that produce large litters in a brief period, which survive in favorable times but may succumb in unfavorable years. This study further documents the existence of multiple pathways to survival in a particular environment, even among closely related species.
Bart in collaboration with V. A. Tucker and A. K. Lee undertook some studies on the thermal responses of lizards which had some important results. One on the agamid Amphibolurus barbatus provided the first demonstration in reptiles of a physiological capacity for modulating the rate of change of body temperature under constant conditions (Bartholomew and Tucker, 1963), capacities that were also observed in varanid lizards (Bartholomew and Tucker, 1964) and the large skink Tiliqua scincoides (Bartholomew et al., 1965). Control of heating and cooling rates was also subsequently found in the Galápagos marine iguana, Amblyrhynchus cristatus (Bartholomew and Lasiewski, 1965). In some of these lizards, though not the varanids, heart rate followed different trajectories during cooling and heating, with the lower rates associated with the former process and higher rates with the latter. This probably retarded heat loss during cooling and accelerated heat gain during warming. The role of endogenous heat production in affecting rate of change in body temperature was considered in these studies, but could not be resolved conclusively. Subsequently, it was examined directly through metabolic measurements of the marine iguana during heating and cooling (Bartholomew and Vleck, 1979). Retention of all the endogenous heat produced by a 2.5-kg individual basking at 30°C could account for only about 5% of the heat gain. On the other hand, with the metabolic rate observed when the animal was cooling through 30°C, complete retention would reduce the cooling rate by 25–30%. Marine iguanas tend to be more active during cooling than basking and thus have higher rates of heat production. Bartholomew and Vleck (1979) concluded that these rates probably result from attempts at thermoregulatory behavior rather than a specific thermogenic response to cooling. The expertise gained in his studies of lizards undoubtedly facilitated Bart's producing his extensive review of reptilian physiological control of body temperature (Bartholomew, 1982b).
The work with the Australian lizards just referred to featured the first application for reptiles of a concept developed by F. E. J. Fry (1947) concerning aerobic metabolic scope (i.e., the difference between the standard and peak rates of oxygen consumption at a particular body temperature—an index of aerobic capacity for activity) of ectotherms. In an era in which investigators were primarily concerned with standard or resting metabolic rates, Bart and his collaborators extended their studies to include measurement of the highest rates of oxygen consumption occurring spontaneously or through stimulation in their lizards (Bartholomew and Tucker, 1963, 1964; Bartholomew et al., 1965). These studies represented an important first step in the analysis of the metabolic correlates of activity and their thermal dependence in reptiles. This has provided part of the stimulus for the development of a number of studies of the energy cost of locomotion and the temperature dependence of metabolic scope in members of this group. Bart has participated in several of these pertaining to the Galápagos marine iguana (Bennett et al., 1975; Bartholomew et al., 1976; Vleck et al., 1981). The studies have examined aerobic and anaerobic metabolic scope of this species in relation to temperature. They also have quantified swimming performance. Cost of transport in marine iguanas varies inversely with body mass, and foraging patterns of various size classes appear to have been influenced by this trend. Small marine iguanas feed on algae on or near shore, whereas adults obtain this food by swimming offshore and diving (Vleck et al., 1981). It is of interest that George Bartholomew, in addition to his other laurels, is the leading contributor to knowledge of the locomotion, thermophysiology, and metabolism of the Galápagos marine iguana, through both the studies just cited and several others (Bartholomew and Lasieweski, 1965; Bartholomew, 1966c; Dawson et al., 1977; Bartholomew and Vleck, 1979).
In the latter portion of George Bartholomew's professional career, he extended his research activities to involvement in a highly productive program of investigation of insect thermophysiology. He explained this extension thus (Bartholomew, 1982a, p. 233): ".... historically insect physiologists have paid relatively little attention to the behavioral and physiological control of body temperature and its energetic and ecological consequences. Whereas many students of the comparative physiology of terrestrial vertebrates have been virtually fixated on the topic. For the past ten years, several of my students and I have exploited this situation by taking the standard questions and techniques of comparative vertebrate physiology and applying them to insects (see Heinrich, 1981). It is surprising that this pattern of innovation is not more deliberately employed. It is common place to find a biologist trained in one field working in another. This represents a more demanding change than transferring questions and techniques between fields." The extension to insects is not quite as simple as this narrative suggests, for it involved some technical challenges resulting from the miniscule size of the most diminutive insects studied (see, for example, Bartholomew et al., 1988), and the transient nature of several of the responses being measured. Regarding the latter, the development of methods for calculating instantaneous oxygen consumption of animals in open circuit metabolism systems with appreciable washout times (Bartholomew et al., 1981), where dynamic situations such as changing temperatures or short-term bouts of activity are involved, has been an especially useful advance.
The work carried out on insects by Bart and his associates emphasized analysis of the endothermic capacities, thermoregulation, locomotor costs, and, in some cases, respiration of various heterothermic species. Endothermy results primarily from intense thermogenesis in the flight muscles, with the heat largely being sequestered in the thoracic region during warm-up and activity (Heinrich and Bartholomew, 1971). It was of interest not only from a comparative standpoint, but also because it allowed some species to be active with high thoracic temperatures at surprisingly low nocturnal ambient temperatures. The animals found capable of endothermy include a large array of moths (Bartholomew and Heinrich, 1973; Bartholomew and Epting, 1975a, b; Bartholomew and Casey, 1978; Bartholomew et al., 1981), with the smallest endothermic sphingids studied weighing only 1/15 as much as the smallest birds and mammals (Bartholomew and Epting, 1975a); various scarab and cerambycid beetles (Bartholomew and Casey, 1977a; Bartholomew and Heinrich, 1978; Morgan and Bartholomew, 1982); several cicadas (Bartholomew and Barnhart, 1984); a tropical cockroach, Blaberus giganteus (Bartholomew and Lighton, 1985); and the giant fly Pantophthalmus tabaninus (Bartholomew and Lighton, 1986a). The elevated temperatures produced through muscular thermogenesis are crucial for achieving flight in most of these insects. However, such temperatures also were observed during sustained terrestrial activity in a cerambycid and a scarab beetle (Bartholomew and Casey, 1977b), which attained rates of oxygen consumption matching those of active mammals of comparable size. Factorial scope (ratio between rates of oxygen consumption during rest and activity) can exceed 100 in some individuals, approximately 10x the figure characterizing homeothermic vertebrates. The discrepancy is, of course, explained by the fact that the latter during inactivity remain homeothermic through maintenance of relatively high resting metabolic rates, whereas the insects become ectothermic. The factorial scopes of endothermic insects and heterothermic birds and mammals are very similar (Bartholomew and Casey, 1978).
In a field study of dung beetles carried out in Kenya (Bartholomew and Heinrich, 1978), data were obtained on representatives of several genera (in particular Scarabaeus, Kheper, Gymnopleurus, and Heliocopris). These animals are conspicuously endothermic during flight and the production and rolling of dung balls. Take-off and flight temperatures increased with body mass up to about 2.5 g and were independent of mass beyond that. These temperatures also increased with wing loading up to about 35 N/m2, but were essentially constant at values between 35 and 65 N/m2. The nocturnal species Scarabaeus laevistriatus often maintained a thoracic temperature of 40°C or more when ambient temperature was 25°–26°C. The velocity of ball rolling by this dung beetle increased linearly with thoracic temperature from 5 cm/sec at 28°C to 18 cm/ sec at 40°C. For dung beetles a premium appears to exist on rapidity of ball production and the speed with which balls can be rolled away from areas of high beetle concentration; this probably contributes to the selective advantage of endothermy and the elevated body temperatures it produces. Additionally, Scarabaeus laevistriatus resorts to endothermy during competition for elephant dung (Heinrich and Bartholomew, 1979), the resultant high body temperatures enhancing its ability to win fights for this resource.
The range of capacities of endothermic insects is extended still further by the detection of a homeothermic response in the elephant beetle (Megasoma elephas). It responds to ambient temperature below 20°C by increasing metabolic rate, which prevents body temperature from falling below 20°–22°C. The increase is not associated with any overt activity (Morgan and Bartholomew, 1982).
Work on heterothermic moths allowed comparisons of the allometry of resting and active aerobic metabolic rates with that for reptiles, birds, and mammals (Bartholomew and Casey, 1978). A particularly interesting fact to emerge from these comparisons was that the scaling of oxygen consumption during flight in the moths is virtually identical to that for bats and birds. Detailed analyses of sphingid and saturniid moths (Bartholomew and Epting, 1975a, b) showed that this was also the case for mass-specific thermal conductance, though on this basis these animals were less well insulated than the vertebrates. However, this difference disappeared when conductance of these insects was considered on the basis of thoracic mass rather than total body mass (Bartholomew and Epting, 1975b). A more focused metabolic comparison was facilitated by the fact that the body masses of some of the larger sphingid moths overlap those of hummingbirds (Bartholomew, 1981), and this provided the opportunity for a direct comparison of energetics in analogous flight systems supporting a common mode of foraging. Both types of animals feed on nectar while hovering, yet they have very different evolutionary histories. An allometric analysis (Bartholomew, 1987) based on data for hummingbirds assembled by Bartholomew and Lighton (1986b) and on those for sphingid moths available in Bartholomew and Casey (1978) indicates that hovering costs in the two groups are very high but virtually identical. Moreover, arthropod and vertebrate structural and functional patterns support similar aerodynamic efficiencies in the size decade of 1–10 g. Bart (Bartholomew, 1987) noted further that the mass-specific rate of oxygen consumption in hummingbirds exceeds the highest metabolic rate recorded in any other vertebrate. He inferred from this that both sphingids and hummingbirds are approaching the limit of aerodynamic performance for animals in their size range.
Bart and associates also have conducted a number of studies of insects that are strictly ectothermic.. Among these, geometrid moths proved of particular interest due to the ability of some to fly at low body temperatures (Bartholomew and Heinrich, 1973). This capacity may be associated with the animals' very light wing loading and low wing beat frequency. Other research on ectothermic insects involved studies of energy metabolism and locomotor costs in three species of tropical or desert ants (Lighton et al., 1987; Bartholomew et al., 1988; Lighton and Bartholomew, 1988) and respiration and energetics of locomotion in flightless tenebrionid beetles from the Namib Desert (Bartholomew et al., 1985). In a field study of the beetles (Nicolson et al., 1984), running speed of Onymacis plana averaged a remarkable 90 cm/sec (48 body lengths/sec), an apparent championship rate for any pedestrian insect. Comparable mean running speeds for Physadesmia globosa and Epiphysa arenicola were only 23 and 3 cm/sec, respectively. The relative speeds of the three species were found to be correlated with leg length and muscle mass, as well as with prothoracic temperature during activity. This temperature was elevated to 36.7° and 30.5°C, respectively, by behavioral thermoregulation in the diurnal O. plana and P. globosa, whereas it probably approximated ambient temperaure (ca. 19°C) in the nocturnal E. arenicola.
Bart's continuing interest in energetics has provided a thread connecting many facets of his research. This interest surely results from the longstanding view stated in his chapter on general energy metabolism in Gordon et al. (1982, p. 46–93): "The rate of energy metabolism probably integrates more aspects of animal performance than any other single physiological parameter. Indeed, from a simplistic point of view, the proverbial ‘struggle for existence’ can profitably be thought of as a competition for physiologically utilizable energy." We have already seen how his interest in energetics has led, for example, to investigation of energy conservation through various forms of dormancy in birds and mammals; to determination of the thermal dependence of metabolic scope in several lizards; to assessment of the role of behavioral stratagems in shaping the energy budgets of weaver finches and leaf-nosed bats; and measurement of locomotor costs in a variety of insects, the marine iguana, and hummingbirds. However, he has also participated in other projects in this general area that merit mention. One of these concerned reproductive behavior in the neotropical frog Physalaemus pustulosus. Energy costs of calling by the male and construction by a pair of the frogs of a foam nest (including oviposition and fertilization) within a respiration chamber were determined, the two activities involving factorial aerobic metabolic scopes >2 and 5.7, respectively (Bucher et al., 1982). Females were found to expend more than 10x the energy in reproduction that males do (Ryan et al., 1983), quantifying for this frog the profound difference between the sexes in parental investment that places a premium on female selection of high quality mates.
In another energy-oriented project, Bart participated in an analysis of the adequacy of fat reserves, for supporting long-distance migration by fasting Swainson's, Buteo swainsoni, and broad-winged hawks, B. platypterus (Smith et al., 1986). Based on body masses and estimates of flight costs, basal metabolic rate, and initial fat content, it was concluded that such migration, involving fasting over distances of several thousand kilometers, was indeed feasible, provided that movement was achieved through soaring flight. The importance of a capacity for long-distance movements without feeding in these hawks is related to the low probability of successful foraging over unfamiliar territory in the company of high concentrations of conspecific individuals.
A sabbatical leave in Kenya provided Bart an opportunity to participate in a study of the energetics of the lesser flamingo (Phoeniconaias minor), which obtains nearly all of its blue-green algal food by filter feeding in the surface waters of alkaline lakes, principally in the Rift Valley. He and C. J. Pennycuick (Pennycuick and Bartholomew, 1973) combined natural history data and metabolic information from the literature to estimate the net rate at which these birds gain chemical energy as a function of algal concentration and time spent foraging. This rate under various conditions represents the difference between the rate of energy acquisition through filtration of algae from the lake water and the rate of energy expenditure due to general metabolism and the power requirement for the filtration. From the estimates made, a nonbreeding lesser flamingo should be able to achieve positive energy balance if algal concentrations exceed approximately 0.12 kg/m3 of water and the bird devotes 80% of its time to feeding. Incubation restricts foraging to less than half the time available so an estimated algal concentration of at least 0.25 kg/m3 of water is required. Bart and Pennycuick estimated from literature values for cost of avian egg production that approximately a day would be needed to produce an egg at this algal concentration. At the highest concentration they observed, substantially less than a day would be required to accumulate the energy for an egg. From these considerations these authors suggested that an opportunistic breeding strategy would be most effective: 1) where algal concentrations are high enough to allow the flamingos to accumulate fat reserves, they should use them to travel about investigating different lakes; 2) when a food concentration of 
0.25 kg per m3 of water is found adjacent to a suitable breeding site, commence breeding immediately (Pennycuick and Bartholomew, 1973).
I have described in the preceding paragraphs what I regard as the major segments of George Bartholomew's research on ecologically oriented physiology. He has explored the implications of his results with great skill and in some cases has been able to combine his conclusions with information from the literature to provide a firm evolutionary perspective for his work. I shall conclude this essay with two examples of this. The first of these dealt with the significance of bipedalism in the ecology of the protohominids. In an earlier study of kangaroo rats (Bartholomew and Caswell, 1951), it was noted that this form of locomotion is relatively uncommon in mammals, raising the question of what advantage it might afford these heteromyid rodents. They are typically associated with sparsely vegetated habitat and must forage in the open, where they are potentially vulnerable to a variety of predators. Bartholomew and Caswell (1951) concluded that the special value of bipedalism to kangaroo rats arose from the ability it imparts for rapidly changing direction in the open and thereby lowering predation risk. Bart's collaboration with the anthropologist J. B. Birdsell in an effort to reconstruct the ecology of the protohominids again raised the issue of the advantage use of this unconventional form of locomotion would provide these ancestral humans (Bartholomew and Birdsell, 1953). The two investigators concluded that bipedalism was important to protohominids in freeing the hands, thereby allowing continuous and efficient manipulation of such rudimentary tools as rocks, sticks, or bones. Bartholomew and Birdsell (1953) therefore refined the definition of man from being a tool-using animal (a host of other animals employ tools) to one of being the only mammal that is continuously dependent upon tools for survival. They concluded that movement by the protohominids into this novel dimension of behavior was importantly linked with the advent of bipedalism.
The second example of Bart's inferential abilities resulted from the work with pinnipeds cited earlier. This led him to wonder about factors leading to evolution of polygyny in this group, one of its most conspicuous features. He developed a model (Bartholomew, 1970) based on the special features of these animals, terrestrial partuition and offshore marine feeding, which have interacted with characteristics common to most mammals in such away as to produce both sexual dimorphism in size and polygynous breeding systems. Gregariousness and exclusion of most males from females in rookeries were accorded key roles. Also, large size and subcutaneous fat, characteristics serving to promote heat conservation during immersion of the animals, were recognized for their roles in permitting sustained fasting and prolonged territory occupancy by dominant males. Bart's abilities to explore the full implications of the results of his research, to maintain an evolutionary perspective, and to identify probable key steps in the evolution of particular clades represent important features of George A. Bartholomew's research legacy. They cap a remarkable record of scholarly accomplishment.
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In a professorial career spanning 1947–1987, George Bartholomew distinguished himself in biological instruction and is regarded at the University of California at Los Angeles as one of the top 20 professors in the history of the institution (Anonymous, 2000
). I had the privilege of being an undergraduate student in two of his courses during his early years. His lectures were models of clarity and he showed a knack for linking individual facts to larger issues in biology. The lectures dealing with what I have referred to as ‘experimental natural history" (Dawson, 1988) were instrumental in my decision to pursue a postgraduate career in environmentally oriented physiology. For this I shall be forever grateful. Bart has also been a spectacularly successful mentor of graduate students and postdoctoral scholars and has directed the theses of 42 of the former and guided 15 of the latter. A. F. Bennett and C. Lowe (2005) have constructed an academic geneology that includes not only these individuals, but their students as well:
(http://128.200.122.57/login.html).
This reveals that more than 900 persons can trace their intellectual lineage directly to George A. Bartholomew (A. F. Bennett, personal communication), a significant fraction of the physiological ecologists active today. Bart has always been a very approachable, supportive, and patient mentor, stimulating graduate students and postdoctoral scholars to do their best through personal interaction and his seminar courses. As is evident from the REFERENCES section of this essay, he made a point of involving many of these individuals in his research program, imparting to us a concern for defining meaningful questions for investigation and for rigorously interpreting our research results. Individuals working with him were exposed to his graceful writing style and rigorous editorial standards—excellent preparation for completing theses. The writing of papers resulting from research collaborations additionally schooled us in the publication process.
In addition to his direct interactions with students, George Bartholomew has contributed to the educational process by producing some valuable instructional materials. These include chapters in two textbooks, one for introductory students in biology (Gordon et al., 1976) and the other for seniors and even graduate students in this field (Gordon et al., 1982). The chapters in the latter book, which is especially relevant to the interests of integrative and comparative biologists, deal, respectively, with the general features of energy metabolism and with body temperature and energy metabolism and are notable among textbook chapters in providing valuable reference information for researchers in physiological ecology, as well as students. Thirty-two educational films provide a further important part of the Bartholomew educational legacy. These analyze significant behaviors and processes of animals and illustrate a number of biological principles. The extensive film series on the Galápagos Islands as an evolutionary laboratory are especially noteworthy.
Bart's fairness and calm good judgment have also allowed him to contribute important service to a number of groups. He was been Chair of the Department of Zoology at UCLA and also participated in several boards or committees at the national level. These include advisory panels for the National Science Foundation, the Board of Trustees of the California Academy of Sciences, and the Council of the Smithsonian Institution. Additionally, he served as a Scientific Advisor to U.S. Marine Mammal Commission. He organized and served as Chief Scientist of R/V Alpha Helix expeditions to New Guinea and the Galápagos Islands, facilitating the research of groups of colleagues and graduate students while conducting his own research. His service to scientific societies includes terms as Vice President of the American Ornithologists' Union and President of the predecessor of the Society of Integrative and Comparative Biology, the American Society of Zoologists.
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Professor George A. Bartholomew has played a major role in shaping ecologically oriented physiological studies of animals in the period from just after World War II until the present. His importance to physiological ecology and to the Society of Integrative and Comparative Biology results from contributions at several levels.. An inspiring teacher, effective graduate mentor, and innovative and productive researcher, George A. Bartholomew has maintained a clear vision of what can be accomplished by realizing that biology is a continuum and has strived to work at interfaces between disciplines. His holistic view of biology and his recognition of the ultimate connection of organismal studies with enquiries conducted at other levels of biological integration have made him a voice of reason in elucidating the drawbacks for creative scholarship of excessive disciplinary fractionation. Perhaps we can give him no higher accolade than recognizing him as a truly broad scholar who has had a major impact on his many students and postdoctoral scholars as well as on their students, on ecologically oriented physiology, and on comparative and integrative biology generally. The George A. Bartholomew Award provides a tangible indication of the esteem in which Bart is held by colleagues in the Division of Comparative Biochemistry and Physiology and throughout the SICB.
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1 From the Symposium Integrative Biology: A Symposium Honoring George A. Bartholomew presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5–9 January 2004, at New Orleans, Louisiana.
2 E-mail: wrdawson{at}umich.edu
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Anonymous., 2000. The Bruin century. UCLA Today 20(9).
Bartholomew, G. A., Jr. 1942. The fishing activities of double-crested cormorants on San Francisco Bay. Condor, 44:13-21.
Bartholomew, G. A., Jr. 1943a. The daily movements of cormorants on San Francisco Bay. Condor, 45:3-18.
Bartholomew, G. A., Jr. 1943b. Contests of double-crested cormorants for perching sites. Condor, 45:186-195.
Bartholomew, G. A., Jr. 1949. The effect of light intensity and day length on reproduction in the English sparrow. Bull. Mus. Comp. Zool, 101:433-476.
Bartholomew, G. A., Jr. 1950. Reoccupation by the elephant seal of Los Coronados Islands, Baja California, Mexico. J. Mamm, 31:98.
Bartholomew, G. A., Jr. 1951. Spring, summer, and fall censuses of the pinnipeds on San Nicolas Island, California. J. Mamm, 32:15-21.[Medline]
Bartholomew, G. A., Jr. 1952. Reproductive and social behavior of the northern elephant seal. U. Calif. Publ. Zoöl, 47:369-472.
Bartholomew, G. A. 1956. Temperature regulation in the macropod marsupial, Setonix brachyurus. Physiol. Zool, 29:26-40.
Bartholomew, G. A. 1958. The role of physiology in the distribution of terrestrial vertebrates. In Zoogeography, pp. 81–95. AAAS, Washington, D.C.
Bartholomew, G. A. 1964. The roles of physiology and behaviour in the maintenance of homeostasis in the desert environment. In G. M. Hughes (ed.), Homeostasis and feedback mechanisms, Symp. Soc. Exp. Biol 18:7–29. Cambridge University Press, Cambridge, U. K.
Bartholomew, G. A. 1966a. Interaction of physiology and behavior under natural conditions. In R. I. Bowman (ed.), The Galápagos, pp. 39–45. University of California Press, Berkeley and Los Angeles.
Bartholomew, G. A. 1966b. The role of behavior in the temperature regulation of the masked booby. Condor, 68:523-535.[CrossRef][Web of Science]
Bartholomew, G. A. 1966c. A field study of temperature relations in the Galápagos marine iguana. Copeia 1966:241–250.
Bartholomew, G. A. 1970. A model for the evolution of pinniped polygyny. Evolution, 24:546-559.[CrossRef][Web of Science]
Bartholomew, G. A. 1972. The water economy of seed-eating birds that survive without drinking. In Proc. XVth Internat. Ornithol. Congr., pp. 237–254. E. J. Brill, Leiden.
Bartholomew, G. A. 1981. A matter of size: An examination of endothermy in insects and terrestrial vertebrates. In B. Heinrich (ed.), Insect thermoregulation, pp. 45–78. John Wiley & Sons, New York.
Bartholomew, G. A. 1982a. Scientific innovation and creativity: A zoologist's point of view. Amer. Zool, 22:227-235.
Bartholomew, G. A. 1982b. Physiological control of body temperature. In C. Gans and F. H. Pough (eds.), Biology of the Reptilia, Vol. 12, pp. 167–211. Academic Press, London and New York.
Bartholomew, G. A. 1986. The role of natural history in contemporary biology. BioScience, 36:324-329.[CrossRef]
Bartholomew, G. A. 1987. Interspecific comparison as a tool for ecological physiologists. In M. E. Feder, A. F. Bennett, W. W. Burggren, and R. B. Huey (eds.), New directions in ecological physiology, pp. 11–37. Cambridge University Press, Cambridge, U.K.
Bartholomew, G. A. 2005. Integrative biology: An organismic biologist's point of view. Integr. Comp. Biol, 45:330-332.
Bartholomew, G. A., and M. C. Barnhart. 1984. Tracheal gases, respiratory gas exchange, body temperature and flight in some tropical cicadas. J. Exp. Biol, 111:131-144.
Bartholomew, G. A., A. F. Bennett, and W. R. Dawson. 1976. Swimming, diving, and lactate production of the marine iguana, Amblyrhynchus cristatus. Copeia 1976:709–720.
Bartholomew, G. A., Jr., and J. B. Birdsell. 1953. Ecology and the protohominids. Am. Anthropologist, 55:481-498.[CrossRef]
Bartholomew, G. A., and T. J. Cade. 1957a. The body temperature of the American kestrel, Falco sparverius. Wilson Bull, 69:149-154.
Bartholomew, G. A., and T. J. Cade. 1957b. Temperature regulation, hibernation, and aestivation in the little pocket mouse, Perognathus longimembris. J. Mamm, 38:60-71.[CrossRef]
Bartholomew, G. A., and T. J. Cade. 1963. The water economy of land birds. Auk, 80:504-539.
Bartholomew, G. A., and T. M. Casey. 1977a. Body temperature and oxygen consumption during rest and activity in relation to body size in some tropical beetles. J. Therm. Biol, 2:173-176.[Medline]
Bartholomew, G. A., and T. M. Casey. 1977b. Endothermy during terrestrial activity in large beetles. Science:, 195:882-883.
Bartholomew, G. A., and T. M. Casey. 1978. Oxygen consumption of moths during rest, pre-flight warm-up, and flight in relation to body size and wing morphology. J. Exp. Biol, 76:11-25.
Bartholomew, G. A., and H. H. Caswell Jr. 1951. Locomotion in kangaroo rats and its adaptive significance. J. Mamm, 32:155-169.[CrossRef]
Bartholomew, G. A., and W. R. Dawson. 1952. Body temperatures in nestling western gulls. Condor, 54:58-60.
Bartholomew, G. A., and W. R. Dawson. 1954. Temperature regulation in young pelicans, herons, and gulls. Ecology, 35:466-472.[CrossRef]
Bartholomew, G. A., and W. R. Dawson. 1958. Body temperatures in California and Gambel's quail. Auk, 75:150-156.
Bartholomew, G. A., and W. R. Dawson. 1979. Thermoregulatory behavior during incubation in Heermann's gulls. Physiol. Zool, 52:422-437.
Bartholomew, G. A., W. R. Dawson, and R. C. Lasiewski. 1970. Thermoregulation and heterothermy in some of the smaller flying foxes (Megachiroptera) of New Guinea. Z. vergl. Physiol, 70:196-209.[CrossRef]
Bartholomew, G. A., and R. J. Epting. 1975a. Rates of post-flight cooling in sphinx moths. In D. M. Gates and R. B. Schmerl (eds.), Perspectives in biophysical ecology, pp. 405–415. Springer-Verlag, New York.
Bartholomew, G. A., and R. J. Epting. 1975b. Allometry of post-flight cooling rates in moths: a comparison with vertebrate homeotherms. J. Exp. Biol, 63:603-613.
Bartholomew, G. A., and D. L. Goldstein. 1984. The energetics of development in a very large altricial bird, the brown pelican. In R. S. Seymour (ed.), Respiration and metabolism of embryonic vertebrates. Perspectives in vertebrate science, Vol. 3, pp. 347– 357. Dr. W. Junk, Dordrecht, Boston, Lancaster.
Bartholomew, G. A., and B. Heinrich. 1973. A field study of flight temperatures in moths in relation to body weight and wing loading. J. Exp. Biol, 58:123-135.
Bartholomew, G. A., and B. Heinrich. 1978. Endothermy in African dung beetles during flight, ball making, and ball rolling. J. Exp. Biol, 73:65-83.
Bartholomew, G. A., Jr., and P. G. Hoel. 1953. Reproductive behavior of the Alaska fur seal, Callorhinus ursinus. J. Mamm, 34:417-436.[CrossRef]
Bartholomew, G. A., T. R. Howell, and T. J. Cade. 1957. Torpidity in the white-throated swift, Anna hummingbird, and poor-will. Condor, 59:145-155.[CrossRef]
Bartholomew, G. A., and J. W. Hudson. 1960. Aestivation in the Mohave ground squirrel Citellus mohavensis. In C. P. Lyman and A. R. Dawe (eds.), Mammalian hibernation, Bull. Mus. Comp. Zool. 124:193–208.
Bartholomew, G. A., and J. W. Hudson. 1961. Desert ground squirrels. Sci. Amer, 205:107-116.
Bartholomew, G. A., and J. W. Hudson. 1962. Hibernation, estivation, temperature regulation, evaporative water loss, and heart rate of the pygmy possum, Cercaertus nanus. Physiol. Zool, 35:94-107.
Bartholomew, G. A., J. W. Hudson, and T. R. Howell. 1962. Body temperature, oxygen consumption, evaporative water loss, and heart rate in the poor-will. Condor, 64:117-125.
Bartholomew, G. A., and R. C. Lasiewski. 1965. Heating and cooling rates, heart rate and simulated diving in the Galapagos marine iguana. Comp. Biochem. Physiol, 16:573-582.[Medline]
Bartholomew, G. A., R. C. Lasiewski, and E. C. Crawford Jr. 1968. Patterns of gular flutter in cormorants, pelicans, owls, and doves. Condor, 70:31-34.
Bartholomew, G. A., P. Leitner, and J. E. Nelson. 1964. Body temperature, oxygen consumption, and heart rate in three species of Australian flying foxes. Physiol. Zool, 37:179-198.
Bartholomew, G. A., and J. R. B. Lighton. 1985. Ventilation and oxygen consumption during rest and locomotion in a tropical cockroach, Blaberus giganteus. J. Exp. Biol, 118:449-454.
Bartholomew, G. A., and J. R. B. Lighton. 1986a. Endothermy and energy metabolism of a giant tropical fly Pantophthalmus tabaninus. J. Comp. Physiol. B, 156:461-468.
Bartholomew, G. A., and J. R. B. Lighton. 1986b. Oxygen consumption during hover-feeding in free-ranging Anna hummingbirds Calypte anna. J. Exp. Biol, 123:191-200.
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Bartholomew, G. A., J. R. B. Lighton, and G. N. Louw. 1985. Energetics of locomotion and patterns of respiration in tenebrionid beetles from the Namib Desert. J. Comp. Physiol. B, 155:155-162.
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