dawson - 2005 - george a. bartholomew's contributions to integrative and comparative biology

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INTEGR. COMP. BIOL., 45:219230 (2005)

George A. Bartholomews Contributions to Integrative and Comparative Biology1

WILLIAM R. DAWSON2Museum of Zoology, The University of Michigan, Ann Arbor, Michigan 48109-1079

SYNOPSIS. The Bartholomew Award has now completed a decade of recognizing outstanding young inves-tigators 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 researchcontributions continue to be important in shaping these fields. Barts influence reflects a steadfast adherenceto a set of basic precepts: the inherent unity of biology; the need for an evolutionary perspective in functionalstudies; the value of modern natural history in guiding research investigations; the focus on the organismand its function in nature, even in highly reductionist studies; the importance of biological variability withinand between species; and the crucial interactions of physiology and behavior in allowing animals to dealwith environmental challenges. Were he to have done nothing else in his career, he would remain an im-portant figure in the fields with which the Society of Integrative and Comparative Biologys (SICB) Divisionof Comparative Physiology and Biochemistry is concerned. However, his influence is also felt through hisinspirational performance as an undergraduate teacher, his skill and wisdom as a graduate mentor, hismany services to the University of California, his insightful contributions to scientific committees and policyboards at the national level, and his presidency of the American Society of Zoologists (now SICB). Thissymposium 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 theGeorge A. Bartholomew Award.

INTRODUCTIONI 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 com-memorates the tenth anniversary of the George A. Bar-tholomew Award. This award, which recognizes giftedyoung investigators in integrative and comparative bi-ology, is a tangible indication of the esteem in whichBart is held by his colleagues in the Division of Com-parative Physiology and Biochemistry of The Societyof Integrative and Comparative Biology (SICB). I havebeen asked to comment on Barts contributions to in-tegrative and comparative biology. I have arbitrarilydivided his accomplishments in this regard into threecategories: definition of precepts, original research,and education and service. I shall comment on thesein order.

DEFINITION OF PRECEPTSGeorge Bartholomew in his valedictory for this

symposium (Bartholomew, 2005) discusses creativityand the precepts that have guided his scholarly activ-ities over his career. Through his adherence to theseprecepts, he has been able to exert a powerful effecton the post-World War II development of ecologicallyoriented physiology. His holistic view of biology con-tinues to inspire in this age of disciplinary fraction-ation and to convey an important message. He has rec-ognized that biology is a continuum, but that biologistsbecause of their human limitations tend to divide

1 From the Symposium Integrative Biology: A Symposium Hon-oring George A. Bartholomew presented at the Annual Meeting ofthe Society for Integrative and Comparative Biology, 59 January2004, at New Orleans, Louisiana.

2 E-mail: [email protected]

themselves into categories and then pretend that thesecategories exist in the living systems under investiga-tion (Bartholomew, 1958). Thus he has emphasizedthat animals are indivisible functionally and that hisfield of physiology is not an isolatable organismalcomponent, being inextricably linked with morpholo-gy and behavior. He pursued this view of a unifiedbiology further in an eloquent statement concerningmodern natural history (Bartholomew, 1986, p. 329)that has broad implications for integrative and com-parative biology: Because of its focus on organismsnatural history is in a unique position to supply ques-tions and integrating links among disciplines. Studiesat lower levels will delineate the machinery of struc-tural units, and the complex systems into which theseunits have been assembled through evolutionary timewill be worked out by research at the intermediate andhigher levels of biological integration. Biology is in-divisible; biologists should be undivided. Bart (1964,p. 8) had provided earlier justification for an inclusiveview of biology through recognition of this hierarchyof biological explanations: There is a familiar solu-tion to this problem [parochialism based on differencesin approach by various biologists], widely recognizedbut sometimes difficult to accept emotionally. This isthe idea that there are a number of levels of biologicalorganization and that each level offers unique prob-lems and insights, and further, that each level finds itsexplanation of mechanism in the levels below, and itssignificance in the levels above.

As is evident from his contribution to this sympo-sium (Bartholomew, 2005), George Bartholomew hasalso made it a rule to explore the evolutionary impli-cations of his research wherever feasible. One of thefoundations of this practice has been his appreciation

at Universidade Federal da Bahia on July 10, 2015

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220 WILLIAM R. DAWSON

of the evolutionary implications of biological vari-ability. Differences between individuals are the rawmaterials for evolutionary change and for the evolutionof adaptations, yet of course most physiologists treatthese differences as noise that is to be filtered out.From the standpoint of physiological ecology, the tra-ditional emphasis of physiologists on central tenden-cies rather than on variance has some unhappy con-sequences. Variation is not just noise; it is also thestuff of evolution and a central attribute of living sys-tems. . . . The physiological differences between indi-viduals in the same species or population, and also thepatterns of variation in different groups, must not beignored (Bartholomew, 1987, pp. 32-33). In this con-nection, he has emphasized (Bartholomew, 1987, p.33) the value of research efforts that can deal criticallywith intraspecific comparisons. Rather than just com-paring different species, one should adopt some of theformats developed for interspecific comparisons in anattempt to compare breeding populations within spe-cies . . . and individuals within the same breeding pop-ulation. . . . Such efforts should allow investigators toapproach more closely the dynamics of evolutionarychange, and, in appropriate situations, to integrate thefindings of physiological ecology with those of pop-ulation genetics.

George Bartholomew has also consistently empha-sized the important role of historical factors in shapingthe functional characteristics of contemporary species([each species] has an evolutionary history, whichmeans its present configuration has been shaped bynatural selection [Bartholomew, 1982a, p. 231]). Hehas noted further that it is important in the analysis ofthe adjustments of organisms to their respective envi-ronments to understand that selection results in ade-quacy of performance rather than perfection. He alsohas reflected on the fact that despite the long-termprobability of extinction, every organism alive todayis part of an enormously long success story in whicheach of its ancestors has been sufficiently well adaptedto its physical and biotic environments to mature andreproduce successfully. It is the intact and functioningorganism on which natural selection operates and suchorganisms therefore should be the primary concern ofany biologist who aspires to a broad and integratedunderstanding of biology. Consequently, Bart regardsadaptation as so central a theme as to be inseparablefrom life itself (Bartholomew, 1987). Undoubtedly, hisviews have contributed in a number of respects to thefoundation of the burgeoning field of evolutionaryphysiology (Garland and Carter, 1994; Feder et al.,2000; Kingsolver and Huey, 2003).

Bart has also been careful to observe the principlefirst enunciated by Claude Bernard that an organism isinseparable from its environment (Bartholomew, 1958,2005). Full knowledge of any species requires famil-iarity not just with its general surroundings but also itsinteraction as a self-maintaining physicochemical sys-tem with its special microenvironment (Bartholomew,1958). Although it is convenient to maintain a verbal

distinction between the two (organism and environ-ment), he has cautioned that this should only be doneif they are never treated separately.

A further precept arising from the views summa-rized in Barts contribution to this symposium (Bar-tholomew, 2005) emphasizes interactions betweenfunctional capacities and behavior of organisms, inter-actions that are frequently critical for survival in dif-ficult physical conditions (Bartholomew, 1964,1966a). He has noted that such interactions are espe-cially important for terrestrial animals due to the phys-ical complexity of their environments. These animalsbecause of their mobility and behavioral capacities canactively seek out and use those environmental situa-tions that best allow their morphological and physio-logical abilities to function adequately for survival andreproduction. Most of these species are less than 1%the size of man and his domestic animals, and theirenvironment may include shaded or sunny areas, tun-nels, cracks, crevices, burrows, thick underbrush, holesin logs, and/or nests, making gross climatic indicesoften irrelevant (Bartholomew, 1964). These and pre-ceding considerations have led him to expend substan-tial research effort in the field as well as the laboratory.

RESEARCHGeorge Bartholomew is a true comparative biologist

and the subjects of his studies include insects, am-phibians (Bucher et al., 1982; Ryan et al., 1983), rep-tiles, birds, and mammals, as well as the plant Philo-dendron selloum (Seymour et al., 1983, 1984). (Manyof the studies arising from his work on insects andamniotic vertebrates are cited below.) He has consis-tently operated at the interfaces of comparative phys-iology, ecology, and behavior. Pursuit of appropriateresearch animals and investigation of interesting prob-lems have led him to work in North and Central Amer-ica; Australia; Europe; Africa; Antarctica; and a num-ber of islands including the Pribiloffs, Midway, andNew Guinea. The following comments do not com-prise a comprehensive review of his total research ac-tivities (for example, in the interests of producing anessay of manageable length, I have omitted mentionof several primarily behavioral studies and have notfully indicated every publication pertaining to some ofthe topics that are considered below), but I have triedthrough the references that are included to providesome sense of the scope of his investigations, creativ-ity and, in a number of instances, truly pioneering ef-forts.

The studies by Bart and his collaborators are note-worthy for their broad perspective. His initial research,which has been cited over at least 50 years, concernedbehavior of double-crested and Brandt cormorants,Phalacrocorax auritus and P. penicillatus, on SanFrancisco Bay, CA (Bartholomew, 1942, 1943a, b).Following a three-year interruption due to World WarII, Bart resumed a publication career that would extendover the next four decades and be marked by a numberof firsts and technical innovations. His doctoral the-



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221GEORGE BARTHOLOMEWS CONTRIBUTIONS

sis established the thresholds of light intensity neces-sary for evoking photoperiodic responses in housesparrows, Passer domesticus (Bartholomew, 1949).

After joining the faculty at UCLA he was the firstphysiological ecologist to initiate an organized pro-gram of research on the physiology and behavior ofdesert birds. This resulted in a number of papers onthe thermoregulatory responses (e.g., Bartholomewand Cade, 1957a; Bartholomew and Dawson, 1958;Bartholomew et al., 1962) and on water and electrolytemetabolism (e.g., Bartholomew and MacMillen, 1960;Smyth and Bartholomew, 1966) of these animals, cul-minating in an influential review of water relations(Bartholomew and Cade, 1963) and a model that ac-counted for the ability of certain small seed eatingbirds to survive without drinking (Bartholomew,1972). Bart continued to investigate the responses ofbirds to heat challenges in several collaborations (Las-iewski and Bartholomew, 1966; Bartholomew et al.,1968; Lasiewski et al., 1970), obtaining indications incommon poor-wills (Phalaenoptilus nuttallii), double-crested cormorants, brown pelicans (Pelecanus occi-dentalis), and mourning doves (Zenaidura macroura)that gular fluttering, an activity serving to increaseevaporative water loss at high temperatures, occurredat the resonant frequency of the gular apparatus (Las-iewski and Bartholomew, 1966; Bartholomew et al.,1968). Such congruence would reduce the energy costsof this form of cooling.

One particularly important facet of the research onwater and electrolyte balance referred to above docu-mented variation among populations of the savannahsparrow (Passerculus sandwichensis) in patterns of useof NaCl solutions or sea water as fluid sources (Cadeand Bartholomew, 1959). Members of two subspeciesresident in salt marshes (P. s. beldingi and P. s. ros-tratus) increased their drinking with increasing con-centration of the solutions provided, whereas threenorthern migratory subspecies of savannah sparrow(P. s. anthinus, P. s. nevadensis, and P. s. brooksi)decreased theirs, like most other birds. This indicatedmarked differences in electrolyte metabolism betweenthe two groups and the salt marsh residents provedmore proficient in obtaining physiologically useful wa-ter from salt and sea water solutions than the migrantsubspecies. A subsequent study (Poulson and Barthol-omew, 1962) revealed important physiological differ-ences between representatives of one of the salt marshtaxa (P. s. beldingi) and those of a migrant form (P.s. brooksi). The salt marsh residents could tolerate sig-nificantly higher serum osmotic pressures and chlorideconcentrations and produce substantially more concen-trated urine than the migrants. These studies are no-table in providing an impressive early example of geo-graphic variation at the intraspecific level in avianphysiological performance.

Another of Barts early research projects dealt withpinnipeds. This initially produced documentation ofthe resurgence of populations of two species of theseanimals on islands off Baja California and southern

California (Bartholomew, 1950, 1951), but was con-cerned primarily with detailed investigations of pop-ulation biology and reproductive behavior. Major stud-ies were conducted on the social and reproductive be-havior of the elephant seal, Mirounga angustirostris(Bartholomew, 1952); Alaska fur seal, Callorhinus ur-sinus (Bartholomew and Hoel, 1953); and Californiasea lion, Zalophus californianus (Peterson and Bar-tholomew, 1967). Some important thermal informationwas also obtained. Due to the large size and effectiveinsulation of these animals noted above, terrestrialbreeding can put them at risk of overheating, even ina cool climate (see, for example, Bartholomew andWilkie, 1956). Bart showed how a predominantly Hol-arctic species, the California sea lion, could extend itsrange to the equatorial Galapagos Islands where warmtemperatures and intense insolation prevail. Breedingmale sea lions persistently maintain terrestrial territo-ries on the coastal islands of California and Baja Cal-ifornia, where thermal conditions are ameliorated bycool upwelling water and a persistent summer over-cast. The breeding males in the Galapagos use a be-havioral strategy in dealing with the heat challengeprevailing there. During the daylight hours, they pro-tect themselves from overheating by holding aquaticterritories while remaining immersed in tide pools orchannels, hauling out on land only at night (Barthol-omew, 1966a). This seemingly simple strategy, im-poses profound effects on a breeding structure that isexclusively terrestrial in other otariids (sea lions andfur seals), but it is an excellent example of a behavioralsolution to a primarily physiological problem, a themethat recurs in many of Barts studies.

Early in his career, Bart recognized breeding colo-nies of seabirds as an excellent resource for thermo-regulatory studies. Many of these birds nest in exposedsituations and, at tropical or subtropical latitudes inparticular, they and their eggs and young can be ex-posed to dangerously intense insolation and high airtemperatures. Commencing with a relatively simplefield study of western gulls, Larus occidentalis (Bar-tholomew and Dawson, 1952), Bart participated inseveral projects concerning the ontogeny of avian ther-moregulatory capacity. One involved a comparison ofthree species of seabirds that nest concurrently on thesurface of a hot desert island in the Gulf of California,Mexico, despite major differences in the thermoregu-latory proficiency of their hatchlings. The results dem-onstrated how closely attentive behavior of parents ofeach species was attuned to the developmental statusof their chicks (Bartholomew and Dawson, 1954). Fur-ther extensive observations of breeding seabirds onMidway Island, where intense insolation is also aproblem, documented thermally significant behavior ofboth parents and young of various ages (Howell andBartholomew, 1961a, b, 1962a, b). One lasting imageis of older nestling albatrosses (Diomedea nigripes andD. immutabilis) with their backs to the sun resting ontheir heels and raising their heavily vascularized andshaded webbed feet off the ground into the cooling



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trade winds (Howell and Bartholomew, 1961a). Bartsdiscerning eye led to a particularly informative ac-count of the behavioral repertoire (orientation awayfrom the sun, holding its wings away from the body,elevation of the scapular feathers) used by the maskedbooby (Sula dactylatra) while protecting itself andshading its eggs and young chicks from the intensesolar radiation and high ambient temperatures prevail-ing in the Galapagos during the breeding season (Bar-tholomew, 1966b). A later study on another island inthe Gulf of California demonstrated the precise cou-pling of thermally protective incubation behavior byadult Heermanns gulls (Larus heermanni) to ambientconditions (Bartholomew and Dawson, 1979).

Behavior can have a major impact on the thermalrelations of terrestrial as well as aquatic birds. A par-ticularly spectacular example of this is provided bysociable weavers (Philetairus socius). These weaverfinches, which are the size of house sparrows, con-struct huge, communal nests in the Kalahari Desert,which they continuously occupy and maintain. Bart, F.N. White, and T. R. Howell examined the extent ofthermal protection provided by these structures insummer and winter (White et al., 1975; Bartholomewet al., 1976). In the former season, outside air tem-peratures ranged from 168 to 33.58C, whereas temper-atures in occupied nest chambers only varied 78 or 88C.Winter in the Kalahari often involves sustained noc-turnal winds and temperatures that can drop to freez-ing. At this season, the insulation of the nest in com-bination with the heat production of roosting birds pro-duced temperatures as high as 378C, 238 above outsideair. Only two sociable weavers occupied a nest cham-ber in the summer, whereas up to five did so in winter,leading Bartholomew et al. (1976) to conclude thatchanging this number is the principal means by whichthese birds maintain chamber temperatures within theirzone of thermal neutrality throughout the year. Thisthermostability leads to energy savings of nearly 50%as compared with estimated costs were the birds toroost in the open air. This curtailment of thermoregu-latory costs appears important both in allowing bothhigher population densities of the sociable weaver inan area of low biological productivity and in the ex-tension of breeding into the cooler parts of the year.The latter is probably significant in helping this birdto avoid the heavy reptilian predation on parents, eggs,and young that can occur in summer. The use of bur-rows for nesting also can provide thermal protection,as the study by F. N. White, Bart and J. L. Kinney ofa Spanish nesting colony of the European bee-eater,Merops apiaster, illustrates (White et al., 1978). How-ever, poor nest sanitation and microbial action on theaccumulated excrement can lead to buildups of NH3and CO2, which are alleviated by the ventilation re-sulting from wind and the movement of adults in andout of the nest tunnel.

Barts later research on avian development involvedparticipation in studies of growth patterns, gas ex-change, and energetics of avian embryos. One example

of this involved a study of the brown pelican, a rep-resentative of the Order Pelecaniformes, a group ofparticular interest because it includes the largest altri-cial birds and the only marine birds showing this de-velopmental pattern. Several features of the pelicansembryonic development differ from those in other al-tricial species (eyes open at hatching, high energy den-sity of the egg, the large amount of yolk present inhatchlings, the relation of mass-specific oxygen con-sumption to embryonic age, and the high total cost ofdevelopment up to hatching [121 kJ]). The brown pel-ican produces a relatively large chick at a relativelyhigh cost compared to other, smaller altricial species.The divergence of its pattern of embryonic develop-ment from that in these other birds was regarded asconsistent with the hypothesis that avian altriciality ispolyphyletic (Bartholomew and Goldstein, 1984). Dataprimarily from the brown pelican and three other spe-cies from different orders were used in an analysisassessing correlates of variation among birds in growthpattern, gas exchange, and energetics of development(Bucher and Bartholomew, 1984). These three physi-ological variables were found to be correlated withbody mass, time, energy, phylogeny, and ecologicalniche of the species. The study emphasized the im-portance of variability as a biological reality and thedeficiencies of confining the analysis embryonicgrowth processes entirely to definitions of central ten-dencies. Bart also collaborated in another study of de-velopmental variation, in this instance dealing with theAdelie (Pygoscelis adeliae) and emperor penguins(Aptenodytes forsteri), both of which lay smaller eggsthan large species in other avian orders (Bucher et al.,1986). The incubation period of the former specieswas similar to that predicted on the basis of egg mass,but that of the emperor penguin was 50% longer. Totaloxygen consumption of developing chicks of the twospecies over the incubation period matched values pre-dicted for precocial birds, leading to the conclusionthat these penguins were incorrectly classified as semi-altricial.

The role of heterothermy in the biology of certainbirds and mammals that must deal with challenges in-volving heat, cold, or restriction of food or water, haslong intrigued George Bartholomew. He led or partic-ipated in the first successful laboratory studies (Bar-tholomew et al., 1957, 1962; Howell and Bartholo-mew, 1959) of the common poor-will, the only birdknown to hibernate. At a time when metabolic levelin a given group of animals was regarded by many assolely a function of body mass, these studies docu-mented the birds remarkably low standard metabolicrate as well as its heterothermic capacities and exten-sive powers of heat defense. Information on dormancyin swifts and hummingbirds was also obtained (Bar-tholomew et al., 1957). Bart also collaborated in stud-ies of dormancy in desert rodents (Bartholomew andCade, 1957b; Bartholomew and Hudson, 1960; Bar-tholomew and MacMillen, 1961; Brown and Barthol-omew, 1969), analyzing the capacities of pocket mice



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(Perognathus longimembris), Mohave ground squirrels(Spermophilus mohavensis), and kangaroo mice (Mi-crodipodops pallidus) for entering torpor and provid-ing the first extensive laboratory observations on thephenomenon of estivation. This form of dormancy,which was poorly understood at the time, was exploredfurther in a review article (Hudson and Bartholomew,1964).

Bart has extended his interest in mammalian andavian heterothermy through additional studies involv-ing such species as speckled mouse birds, Colius stria-tus (Bartholomew and Trost, 1970), pygmy possums,Cercaertus nanus (Bartholomew and Hudson, 1962),and two small New Guinea flying foxes: the commontube-nosed fruit bat, Nyctimene albiventer, and the un-striped tube-nosed bat, Paranyctimene raptor (Bar-tholomew et al., 1970). The results for the flying foxeswere noteworthy because of the two bats tropical dis-tribution, frugivorous diet, and the fact that a capacityfor heterothermy had not been previously reported forany members of the Megachiroptera (see Bartholomewet al., 1964). Additionally, nocturnal torpor involvingbody temperatures as low as 26.88C was observed intwo small neotropical birds, the manakins Pipra men-talis and Manacus vitellinus (Bartholomew et al.,1983). These birds are also frugivorous. Heterothermycan reduce the energy expenditures of these small an-imals by more than half. Fruit is not always readilyavailable in rain forests and Bart and his coauthorshypothesized that torpor might well occur in othersmall tropical songbirds dependent upon such food.

The use of torpor by the Mohave ground squirrelcontrasts sharply with the behavior of the antelopeground squirrel (Ammospermophilus leucurus) in thesame desert environment. The latter species neither hi-bernates nor estivates, though it does achieve someenergetic savings by lowering its body temperature to328338C during winter nights (Chappell and Barthol-omew, 1981a). Therefore, it is forced to deal with con-ditions on the desert surface throughout the year. Itsdiurnal habits expose it to severe summer heat, whichit deals with by shuttling between the desert surfaceand its burrow. It tolerates hyperthermia when on thesurface, thereby avoiding high rates of evaporative wa-ter loss. Periodic retreat to the antelope ground squir-rels burrow allows it to dump the heat it has gained,thereby surviving the stresses of the summer daytimedesert through appropriately timed movements (Bar-tholomew and Hudson, 1961; Chappell and Bartholo-mew, 1981a, 1981b).

Thermally relevant behavior is also crucially im-portant for other mammals. In one of the first detailedstudies of thermoregulatory capacity in macropod mar-supials (kangaroos, wallabies, etc.), Bart found that thequokka (Setonix brachyurus) was at least as effectivein its temperature control over an ambient range of2108 to 448C as eutherian mammals of comparablesize (2.54.0 kg). At high ambient temperatures, thisWest Australian species cooled itself by the behavioralstratagem of spreading saliva over its ventral surface,

limbs and tail (Bartholomew, 1956). The large Austra-lian flying foxes Pteropus poliocephalus and P. sca-pulatus were found by Bartholomew et al. (1964) tomaintain body temperature in the usual range for mam-mals at ambient temperatures from 58 to 408C. In cool-er surroundings they wrapped their wings about thebody creating an overcoat that allowed skin tem-peratures to remain as much as 108C above ambient.At high air temperatures they supplemented their pant-ing by salivation and licking of the wings and chest.Flapping the wings also contributed to convection overthe body. These behavioral actions contributed to theability of the flying foxes roosting in exposed positionsin the tops to trees to tolerate exposure the tropical orsubtropical sun. Behavior also figures prominently inmaintenance of thermal balance in the rock hyrax(Heterohyrax brucei), a mammal Bart studied duringa sabbatical leave in Kenya. This hyrax has a behav-ioral repertoire that includes diurnality, basking, re-stricted periods of surface activity, gregarious habitswithin burrows, and huddling, all contributing to ef-fective control of body temperature despite a low met-abolic rate and high thermal conductance (Bartholo-mew and Rainy, 1971). This animal also showed anunusual physiological response at high temperatures,increasing evaporative water loss while reducing itsoxygen consumption, the reduction evidently producedby lowering muscle tonus. Additionally, Bart also par-ticipated in a study (Bell et al., 1986) of the energeticsof the leaf-nosed bat (Macrotus californicus), whichinvolved important behavioral issues. The species is ofspecial interest due to its being the northernmost rep-resentative of a primarily tropical family (Phyllostom-idae) and it is does not use torpor in energy conser-vation. The combined field and laboratory study pro-vided information on thermoregulatory characteristics,standard and field metabolic rates, and behavior of thisanimal. These data supported the conclusion that, rath-er than relying on special physiological adaptations forsurvival, the leaf-nosed bat is successful as a year-round resident in its desert environment through roost-ing in continuously warm (ca. 298C) geothermal re-fugia such as caves and mine shafts, and through aneconomical method of foraging involving visual preydetection.

Barts use of the comparative method in desert stud-ies has extended to analysis of reproductive patternsin several rodents. G. J. Kenagy and he undertook along-term investigation of reproductive timing in fivespecies of rodents (two nocturnal kangaroo rats andtwo nocturnal pocket mice in addition to the diurnalantelope ground squirrel) coexisting in a desert com-munity in the Owens Valley of California. They wereinterested in determining whether closely related spe-cies differ in reproductive timing as a result of suchthings as differences in body size, daily cycle, foodhabits, locomotor patterns, and their respective micro-environments. (Kenagy and Bartholomew, 1985).They found substantial differences among the species,all of which are long-lived and characterized by rela-



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tively stable population levels. The antelope groundsquirrel is a predictor, with a slow, lengthy repro-ductive period coinciding with the historical probabil-ity for rainfall and plant productivity, which can beunpredictable in a given year. The Merriam kangaroorat (Dipodomys merriami) is a responder, breedingin direct response to pulses in food production. Its con-gener, the somewhat larger Great Basin kangaroo rat(D. microps), with a dependable food supply of saltbush (Atriplex confertifolia) leaves, is an indepen-dent, successfully ignoring rainfall and pulses of seedproduction. The lengthy periods of dormancy occur-ring in the two pocket mice (Perognathus longimem-bris and P. formosus) overlap the periods of winterrainfall and may extend beyond it. They are in Kenagyand Bartholomews (1985) phrase pulse gamblersthat produce large litters in a brief period, which sur-vive in favorable times but may succumb in unfavor-able years. This study further documents the existenceof multiple pathways to survival in a particular envi-ronment, even among closely related species.

Bart in collaboration with V. A. Tucker and A. K.Lee undertook some studies on the thermal responsesof lizards which had some important results. One onthe agamid Amphibolurus barbatus provided the firstdemonstration in reptiles of a physiological capacityfor modulating the rate of change of body temperatureunder constant conditions (Bartholomew and Tucker,1963), capacities that were also observed in varanidlizards (Bartholomew and Tucker, 1964) and the largeskink Tiliqua scincoides (Bartholomew et al., 1965).Control of heating and cooling rates was also subse-quently found in the Galapagos marine iguana, Am-blyrhynchus cristatus (Bartholomew and Lasiewski,1965). In some of these lizards, though not the var-anids, heart rate followed different trajectories duringcooling and heating, with the lower rates associatedwith the former process and higher rates with the latter.This probably retarded heat loss during cooling andaccelerated heat gain during warming. The role of en-dogenous heat production in affecting rate of changein body temperature was considered in these studies,but could not be resolved conclusively. Subsequently,it was examined directly through metabolic measure-ments of the marine iguana during heating and cooling(Bartholomew and Vleck, 1979). Retention of all theendogenous heat produced by a 2.5-kg individualbasking at 308C could account for only about 5% ofthe heat gain. On the other hand, with the metabolicrate observed when the animal was cooling through308C, complete retention would reduce the cooling rateby 2530%. Marine iguanas tend to be more activeduring cooling than basking and thus have higher ratesof heat production. Bartholomew and Vleck (1979)concluded that these rates probably result from at-tempts at thermoregulatory behavior rather than a spe-cific thermogenic response to cooling. The expertisegained in his studies of lizards undoubtedly facilitatedBarts producing his extensive review of reptilian

physiological control of body temperature (Bartholo-mew, 1982b).

The work with the Australian lizards just referred tofeatured the first application for reptiles of a conceptdeveloped by F. E. J. Fry (1947) concerning aerobicmetabolic scope (i.e., the difference between the stan-dard and peak rates of oxygen consumption at a par-ticular body temperaturean index of aerobic capacityfor activity) of ectotherms. In an era in which inves-tigators were primarily concerned with standard orresting metabolic rates, Bart and his collaborators ex-tended their studies to include measurement of thehighest rates of oxygen consumption occurring spon-taneously or through stimulation in their lizards (Bar-tholomew and Tucker, 1963, 1964; Bartholomew et al.,1965). These studies represented an important first stepin the analysis of the metabolic correlates of activityand their thermal dependence in reptiles. This has pro-vided part of the stimulus for the development of anumber of studies of the energy cost of locomotionand the temperature dependence of metabolic scope inmembers of this group. Bart has participated in severalof these pertaining to the Galapagos marine iguana(Bennett et al., 1975; Bartholomew et al., 1976; Vlecket al., 1981). The studies have examined aerobic andanaerobic metabolic scope of this species in relationto temperature. They also have quantified swimmingperformance. Cost of transport in marine iguanasvaries inversely with body mass, and foraging patternsof various size classes appear to have been influencedby this trend. Small marine iguanas feed on algae onor near shore, whereas adults obtain this food byswimming offshore and diving (Vleck et al., 1981). Itis of interest that George Bartholomew, in addition tohis other laurels, is the leading contributor to knowl-edge of the locomotion, thermophysiology, and metab-olism of the Galapagos marine iguana, through boththe studies just cited and several others (Bartholomewand Lasieweski, 1965; Bartholomew, 1966c; Dawsonet al., 1977; Bartholomew and Vleck, 1979).

In the latter portion of George Bartholomews pro-fessional career, he extended his research activities toinvolvement in a highly productive program of inves-tigation of insect thermophysiology. He explained thisextension thus (Bartholomew, 1982a, p. 233): . . . .historically insect physiologists have paid relativelylittle attention to the behavioral and physiological con-trol of body temperature and its energetic and ecolog-ical consequences. Whereas many students of the com-parative physiology of terrestrial vertebrates have beenvirtually fixated on the topic. For the past ten years,several of my students and I have exploited this situ-ation by taking the standard questions and techniquesof comparative vertebrate physiology and applyingthem to insects (see Heinrich, 1981). It is surprisingthat this pattern of innovation is not more deliberatelyemployed. It is common place to find a biologisttrained in one field working in another. This representsa more demanding change than transferring questionsand techniques between fields. The extension to in-



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sects is not quite as simple as this narrative suggests,for it involved some technical challenges resultingfrom the miniscule size of the most diminutive insectsstudied (see, for example, Bartholomew et al., 1988),and the transient nature of several of the responsesbeing measured. Regarding the latter, the developmentof methods for calculating instantaneous oxygen con-sumption of animals in open circuit metabolism sys-tems with appreciable washout times (Bartholomew etal., 1981), where dynamic situations such as changingtemperatures or short-term bouts of activity are in-volved, has been an especially useful advance.

The work carried out on insects by Bart and hisassociates emphasized analysis of the endothermic ca-pacities, thermoregulation, locomotor costs, and, insome cases, respiration of various heterothermic spe-cies. Endothermy results primarily from intense ther-mogenesis in the flight muscles, with the heat largelybeing sequestered in the thoracic region during warm-up and activity (Heinrich and Bartholomew, 1971). Itwas of interest not only from a comparative stand-point, but also because it allowed some species to beactive with high thoracic temperatures at surprisinglylow nocturnal ambient temperatures. The animalsfound capable of endothermy include a large array ofmoths (Bartholomew and Heinrich, 1973; Bartholo-mew and Epting, 1975a, b; Bartholomew and Casey,1978; Bartholomew et al., 1981), with the smallest en-dothermic sphingids studied weighing only 1/15 asmuch as the smallest birds and mammals (Bartholo-mew and Epting, 1975a); various scarab and ceram-bycid beetles (Bartholomew and Casey, 1977a; Bar-tholomew and Heinrich, 1978; Morgan and Bartholo-mew, 1982); several cicadas (Bartholomew and Barn-hart, 1984); a tropical cockroach, Blaberus giganteus(Bartholomew and Lighton, 1985); and the giant flyPantophthalmus tabaninus (Bartholomew and Ligh-ton, 1986a). The elevated temperatures producedthrough muscular thermogenesis are crucial for achiev-ing flight in most of these insects. However, such tem-peratures also were observed during sustained terres-trial activity in a cerambycid and a scarab beetle (Bar-tholomew and Casey, 1977b), which attained rates ofoxygen consumption matching those of active mam-mals of comparable size. Factorial scope (ratio be-tween rates of oxygen consumption during rest andactivity) can exceed 100 in some individuals, approx-imately 103 the figure characterizing homeothermicvertebrates. The discrepancy is, of course, explainedby the fact that the latter during inactivity remain ho-meothermic through maintenance of relatively highresting metabolic rates, whereas the insects become ec-tothermic. The factorial scopes of endothermic insectsand 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 obtainedon representatives of several genera (in particularScarabaeus, 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 bodymass up to about 2.5 g and were independent of massbeyond that. These temperatures also increased withwing loading up to about 35 N/m2, but were essentiallyconstant at values between 35 and 65 N/m2. The noc-turnal species Scarabaeus laevistriatus often main-tained a thoracic temperature of 408C or more whenambient temperature was 258268C. The velocity ofball rolling by this dung beetle increased linearly withthoracic temperature from 5 cm/sec at 288C to 18 cm/sec at 408C. For dung beetles a premium appears toexist on rapidity of ball production and the speed withwhich balls can be rolled away from areas of highbeetle concentration; this probably contributes to theselective advantage of endothermy and the elevatedbody temperatures it produces. Additionally, Scara-baeus laevistriatus resorts to endothermy during com-petition for elephant dung (Heinrich and Bartholomew,1979), the resultant high body temperatures enhancingits ability to win fights for this resource.

The range of capacities of endothermic insects isextended still further by the detection of a homeother-mic response in the elephant beetle (Megasoma ele-phas). It responds to ambient temperature below 208Cby increasing metabolic rate, which prevents bodytemperature from falling below 208228C. The in-crease is not associated with any overt activity (Mor-gan and Bartholomew, 1982).

Work on heterothermic moths allowed comparisonsof the allometry of resting and active aerobic meta-bolic rates with that for reptiles, birds, and mammals(Bartholomew and Casey, 1978). A particularly inter-esting fact to emerge from these comparisons was thatthe scaling of oxygen consumption during flight in themoths is virtually identical to that for bats and birds.Detailed analyses of sphingid and saturniid moths(Bartholomew and Epting, 1975a, b) showed that thiswas also the case for mass-specific thermal conduc-tance, though on this basis these animals were lesswell insulated than the vertebrates. However, this dif-ference disappeared when conductance of these insectswas considered on the basis of thoracic mass ratherthan total body mass (Bartholomew and Epting,1975b). A more focused metabolic comparison wasfacilitated by the fact that the body masses of some ofthe larger sphingid moths overlap those of humming-birds (Bartholomew, 1981), and this provided the op-portunity for a direct comparison of energetics in anal-ogous flight systems supporting a common mode offoraging. Both types of animals feed on nectar whilehovering, yet they have very different evolutionaryhistories. An allometric analysis (Bartholomew, 1987)based on data for hummingbirds assembled by Bar-tholomew and Lighton (1986b) and on those for sphin-gid moths available in Bartholomew and Casey (1978)indicates that hovering costs in the two groups are veryhigh but virtually identical. Moreover, arthropod andvertebrate structural and functional patterns supportsimilar aerodynamic efficiencies in the size decade of



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110 g. Bart (Bartholomew, 1987) noted further thatthe mass-specific rate of oxygen consumption in hum-mingbirds exceeds the highest metabolic rate recordedin any other vertebrate. He inferred from this that bothsphingids and hummingbirds are approaching the limitof aerodynamic performance for animals in their sizerange.

Bart and associates also have conducted a numberof studies of insects that are strictly ectothermic..Among these, geometrid moths proved of particularinterest due to the ability of some to fly at low bodytemperatures (Bartholomew and Heinrich, 1973). Thiscapacity may be associated with the animals verylight wing loading and low wing beat frequency. Otherresearch on ectothermic insects involved studies of en-ergy metabolism and locomotor costs in three speciesof tropical or desert ants (Lighton et al., 1987; Bar-tholomew et al., 1988; Lighton and Bartholomew,1988) and respiration and energetics of locomotion inflightless tenebrionid beetles from the Namib Desert(Bartholomew et al., 1985). In a field study of thebeetles (Nicolson et al., 1984), running speed of On-ymacis plana averaged a remarkable 90 cm/sec (48body lengths/sec), an apparent championship rate forany pedestrian insect. Comparable mean runningspeeds for Physadesmia globosa and Epiphysa areni-cola were only 23 and 3 cm/sec, respectively. The rel-ative speeds of the three species were found to be cor-related with leg length and muscle mass, as well aswith prothoracic temperature during activity. This tem-perature was elevated to 36.78 and 30.58C, respective-ly, by behavioral thermoregulation in the diurnal O.plana and P. globosa, whereas it probably approxi-mated ambient temperaure (ca. 198C) in the nocturnalE. arenicola.

Barts continuing interest in energetics has provideda thread connecting many facets of his research. Thisinterest surely results from the longstanding view stat-ed in his chapter on general energy metabolism in Gor-don et al. (1982, p. 4693): The rate of energy me-tabolism probably integrates more aspects of animalperformance than any other single physiological pa-rameter. Indeed, from a simplistic point of view, theproverbial struggle for existence can profitably bethought of as a competition for physiologically utiliz-able energy. We have already seen how his interestin energetics has led, for example, to investigation ofenergy conservation through various forms of dorman-cy in birds and mammals; to determination of the ther-mal dependence of metabolic scope in several lizards;to assessment of the role of behavioral stratagems inshaping the energy budgets of weaver finches and leaf-nosed bats; and measurement of locomotor costs in avariety of insects, the marine iguana, and humming-birds. However, he has also participated in other pro-jects in this general area that merit mention. One ofthese concerned reproductive behavior in the neotrop-ical frog Physalaemus pustulosus. Energy costs of call-ing by the male and construction by a pair of the frogsof a foam nest (including oviposition and fertilization)

within a respiration chamber were determined, the twoactivities involving factorial aerobic metabolic scopes.2 and 5.7, respectively (Bucher et al., 1982). Fe-males were found to expend more than 103 the energyin reproduction that males do (Ryan et al., 1983),quantifying for this frog the profound difference be-tween the sexes in parental investment that places apremium on female selection of high quality mates.

In another energy-oriented project, Bart participatedin an analysis of the adequacy of fat reserves, for sup-porting long-distance migration by fasting Swainsons,Buteo swainsoni, and broad-winged hawks, B. platyp-terus (Smith et al., 1986). Based on body masses andestimates of flight costs, basal metabolic rate, and ini-tial fat content, it was concluded that such migration,involving fasting over distances of several thousandkilometers, was indeed feasible, provided that move-ment was achieved through soaring flight. The impor-tance of a capacity for long-distance movements with-out feeding in these hawks is related to the low prob-ability of successful foraging over unfamiliar territoryin the company of high concentrations of conspecificindividuals.

A sabbatical leave in Kenya provided Bart an op-portunity to participate in a study of the energetics ofthe lesser flamingo (Phoeniconaias minor), which ob-tains nearly all of its blue-green algal food by filterfeeding in the surface waters of alkaline lakes, prin-cipally in the Rift Valley. He and C. J. Pennycuick(Pennycuick and Bartholomew, 1973) combined nat-ural history data and metabolic information from theliterature to estimate the net rate at which these birdsgain chemical energy as a function of algal concentra-tion and time spent foraging. This rate under variousconditions represents the difference between the rateof energy acquisition through filtration of algae fromthe lake water and the rate of energy expenditure dueto general metabolism and the power requirement forthe filtration. From the estimates made, a nonbreedinglesser flamingo should be able to achieve positive en-ergy balance if algal concentrations exceed approxi-mately 0.12 kg/m3 of water and the bird devotes 80%of its time to feeding. Incubation restricts foraging toless than half the time available so an estimated algalconcentration of at least 0.25 kg/m3 of water is re-quired. Bart and Pennycuick estimated from literaturevalues for cost of avian egg production that approxi-mately a day would be needed to produce an egg atthis algal concentration. At the highest concentrationthey observed, substantially less than a day would berequired to accumulate the energy for an egg. Fromthese considerations these authors suggested that anopportunistic breeding strategy would be most effec-tive: 1) where algal concentrations are high enough toallow the flamingos to accumulate fat reserves, theyshould use them to travel about investigating differentlakes; 2) when a food concentration of $0.25 kg perm3 of water is found adjacent to a suitable breedingsite, commence breeding immediately (Pennycuickand Bartholomew, 1973).



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I have described in the preceding paragraphs whatI regard as the major segments of George Bartholo-mews research on ecologically oriented physiology.He has explored the implications of his results withgreat skill and in some cases has been able to combinehis conclusions with information from the literature toprovide 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 biped-alism in the ecology of the protohominids. In an earlierstudy of kangaroo rats (Bartholomew and Caswell,1951), it was noted that this form of locomotion isrelatively uncommon in mammals, raising the questionof what advantage it might afford these heteromyidrodents. They are typically associated with sparselyvegetated habitat and must forage in the open, wherethey are potentially vulnerable to a variety of preda-tors. Bartholomew and Caswell (1951) concluded thatthe special value of bipedalism to kangaroo rats arosefrom the ability it imparts for rapidly changing direc-tion in the open and thereby lowering predation risk.Barts collaboration with the anthropologist J. B. Bird-sell in an effort to reconstruct the ecology of the pro-tohominids again raised the issue of the advantage useof this unconventional form of locomotion would pro-vide these ancestral humans (Bartholomew and Bird-sell, 1953). The two investigators concluded that bi-pedalism was important to protohominids in freeingthe hands, thereby allowing continuous and efficientmanipulation of such rudimentary tools as rocks,sticks, or bones. Bartholomew and Birdsell (1953)therefore refined the definition of man from being atool-using animal (a host of other animals employtools) to one of being the only mammal that is contin-uously dependent upon tools for survival. They con-cluded that movement by the protohominids into thisnovel dimension of behavior was importantly linkedwith the advent of bipedalism.

The second example of Barts inferential abilitiesresulted from the work with pinnipeds cited earlier.This led him to wonder about factors leading to evo-lution of polygyny in this group, one of its most con-spicuous features. He developed a model (Bartholo-mew, 1970) based on the special features of these an-imals, terrestrial partuition and offshore marine feed-ing, which have interacted with characteristicscommon to most mammals in such away as to produceboth sexual dimorphism in size and polygynous breed-ing systems. Gregariousness and exclusion of mostmales from females in rookeries were accorded keyroles. Also, large size and subcutaneous fat, character-istics serving to promote heat conservation during im-mersion of the animals, were recognized for their rolesin permitting sustained fasting and prolonged territoryoccupancy by dominant males. Barts abilities to ex-plore the full implications of the results of his research,to maintain an evolutionary perspective, and to iden-tify probable key steps in the evolution of particularclades represent important features of George A. Bar-

tholomews research legacy. They cap a remarkablerecord of scholarly accomplishment.

EDUCATION AND SERVICEIn a professorial career spanning 19471987,

George Bartholomew distinguished himself in biolog-ical instruction and is regarded at the University ofCalifornia at Los Angeles as one of the top 20 profes-sors in the history of the institution (Anonymous,2000). I had the privilege of being an undergraduatestudent in two of his courses during his early years.His lectures were models of clarity and he showed aknack for linking individual facts to larger issues inbiology. The lectures dealing with what I have referredto as experimental natural history (Dawson, 1988)were instrumental in my decision to pursue a post-graduate career in environmentally oriented physiolo-gy. For this I shall be forever grateful.

Bart has also been a spectacularly successful mentorof graduate students and postdoctoral scholars and hasdirected the theses of 42 of the former and guided 15of the latter. A. F. Bennett and C. Lowe (2005) haveconstructed an academic geneology that includes notonly these individuals, but their students as well:

(http://128.200.122.57/login.html).This reveals that more than 900 persons can trace theirintellectual lineage directly to George A. Bartholomew(A. F. Bennett, personal communication), a significantfraction of the physiological ecologists active today.Bart has always been a very approachable, supportive,and patient mentor, stimulating graduate students andpostdoctoral scholars to do their best through personalinteraction and his seminar courses. As is evident fromthe REFERENCES section of this essay, he made apoint of involving many of these individuals in hisresearch program, imparting to us a concern for defin-ing meaningful questions for investigation and for rig-orously interpreting our research results. Individualsworking with him were exposed to his graceful writingstyle and rigorous editorial standardsexcellent prep-aration for completing theses. The writing of papersresulting from research collaborations additionallyschooled us in the publication process.

In addition to his direct interactions with students,George Bartholomew has contributed to the education-al process by producing some valuable instructionalmaterials. These include chapters in two textbooks,one for introductory students in biology (Gordon etal., 1976) and the other for seniors and even graduatestudents in this field (Gordon et al., 1982). The chap-ters in the latter book, which is especially relevant tothe interests of integrative and comparative biologists,deal, respectively, with the general features of energymetabolism and with body temperature and energymetabolism and are notable among textbook chaptersin providing valuable reference information for re-searchers in physiological ecology, as well as students.Thirty-two educational films provide a further impor-tant part of the Bartholomew educational legacy. These



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analyze significant behaviors and processes of animalsand illustrate a number of biological principles. Theextensive film series on the Galapagos Islands as anevolutionary laboratory are especially noteworthy.

Barts fairness and calm good judgment have alsoallowed him to contribute important service to a num-ber of groups. He was been Chair of the Departmentof Zoology at UCLA and also participated in severalboards or committees at the national level. These in-clude advisory panels for the National Science Foun-dation, the Board of Trustees of the California Acad-emy of Sciences, and the Council of the SmithsonianInstitution. Additionally, he served as a Scientific Ad-visor to U.S. Marine Mammal Commission. He orga-nized and served as Chief Scientist of R/V Alpha Helixexpeditions to New Guinea and the Galapagos Islands,facilitating the research of groups of colleagues andgraduate students while conducting his own research.His service to scientific societies includes terms asVice President of the American Ornithologists Unionand President of the predecessor of the Society of In-tegrative and Comparative Biology, the American So-ciety of Zoologists.

CONCLUDING STATEMENTProfessor George A. Bartholomew has played a ma-

jor role in shaping ecologically oriented physiologicalstudies of animals in the period from just after WorldWar II until the present. His importance to physiolog-ical ecology and to the Society of Integrative andComparative Biology results from contributions at sev-eral levels.. An inspiring teacher, effective graduatementor, and innovative and productive researcher,George A. Bartholomew has maintained a clear visionof what can be accomplished by realizing that biologyis a continuum and has strived to work at interfacesbetween disciplines. His holistic view of biology andhis recognition of the ultimate connection of organis-mal studies with enquiries conducted at other levels ofbiological integration have made him a voice of reasonin elucidating the drawbacks for creative scholarshipof excessive disciplinary fractionation. Perhaps we cangive him no higher accolade than recognizing him asa truly broad scholar who has had a major impact onhis many students and postdoctoral scholars as well ason their students, on ecologically oriented physiology,and on comparative and integrative biology generally.The George A. Bartholomew Award provides a tan-gible indication of the esteem in which Bart is held bycolleagues in the Division of Comparative Biochem-istry and Physiology and throughout the SICB.

REFERENCESAnonymous. 2000. The Bruin century. UCLA Today 20(9).Bartholomew, G. A., Jr. 1942. The fishing activities of double-crest-

ed cormorants on San Francisco Bay. Condor 44:1321.Bartholomew, G. A., Jr. 1943a. The daily movements of cormorants

on San Francisco Bay. Condor 45:318.Bartholomew, G. A., Jr. 1943b. Contests of double-crested cormo-

rants for perching sites. Condor 45:186195.Bartholomew, G. A., Jr. 1949. The effect of light intensity and day

length on reproduction in the English sparrow. Bull. Mus.Comp. Zool. 101:433476.

Bartholomew, G. A., Jr. 1950. Reoccupation by the elephant seal ofLos Coronados Islands, Baja California, Mexico. J. Mamm. 31:98.

Bartholomew, G. A., Jr. 1951. Spring, summer, and fall censuses ofthe pinnipeds on San Nicolas Island, California. J. Mamm. 32:1521.

Bartholomew, G. A., Jr. 1952. Reproductive and social behavior ofthe northern elephant seal. U. Calif. Publ. Zool. 47:369472.

Bartholomew, G. A. 1956. Temperature regulation in the macropodmarsupial, Setonix brachyurus. Physiol. Zool. 29:2640

Bartholomew, G. A. 1958. The role of physiology in the distributionof terrestrial vertebrates. In Zoogeography, pp. 8195. AAAS,Washington, D.C.

Bartholomew, G. A. 1964. The roles of physiology and behaviourin the maintenance of homeostasis in the desert environment.In G. M. Hughes (ed.), Homeostasis and feedback mechanisms,Symp. Soc. Exp. Biol 18:729. Cambridge University Press,Cambridge, U. K.

Bartholomew, G. A. 1966a. Interaction of physiology and behaviorunder natural conditions. In R. I. Bowman (ed.), The Galapa-gos, pp. 3945. University of California Press, Berkeley andLos Angeles.

Bartholomew, G. A. 1966b. The role of behavior in the temperatureregulation of the masked booby. Condor 68:523535.

Bartholomew, G. A. 1966c. A field study of temperature relationsin the Galapagos marine iguana. Copeia 1966:241250.

Bartholomew, G. A. 1970. A model for the evolution of pinnipedpolygyny. Evolution 24:546559.

Bartholomew, G. A. 1972. The water economy of seed-eating birdsthat survive without drinking. In Proc. XVth Internat. Ornithol.Congr., pp. 237254. E. J. Brill, Leiden.

Bartholomew, G. A. 1981. A matter of size: An examination ofendothermy in insects and terrestrial vertebrates. In B. Heinrich(ed.), Insect thermoregulation, pp. 4578. John Wiley & Sons,New York.

Bartholomew, G. A. 1982a. Scientific innovation and creativity: Azoologists point of view. Amer. Zool. 22:227235.

Bartholomew, G. A. 1982b. Physiological control of body temper-ature. In C. Gans and F. H. Pough (eds.), Biology of the Reptilia,Vol. 12, pp. 167211. Academic Press, London and New York.

Bartholomew, G. A. 1986. The role of natural history in contem-porary biology. BioScience 36:324329.

Bartholomew, G. A. 1987. Interspecific comparison as a tool forecological physiologists. In M. E. Feder, A. F. Bennett, W. W.Burggren, and R. B. Huey (eds.), New directions in ecologicalphysiology, pp. 1137. Cambridge University Press, Cambridge,U.K.

Bartholomew, G. A. 2005. Integrative biology: An organismic bi-ologists point of view. Integr. Comp. Biol. 45:330332.

Bartholomew, G. A. and M. C. Barnhart. 1984. Tracheal gases, re-spiratory gas exchange, body temperature and flight in sometropical cicadas. J. Exp. Biol. 111:131144.

Bartholomew, G. A., A. F. Bennett, and W. R. Dawson. 1976. Swim-ming, diving, and lactate production of the marine iguana, Am-blyrhynchus cristatus. Copeia 1976:709720.

Bartholomew, G. A., Jr. and J. B. Birdsell. 1953. Ecology and theprotohominids. Am. Anthropologist 55:481498.

Bartholomew, G. A. and T. J. Cade. 1957a. The body temperatureof the American kestrel, Falco sparverius. Wilson Bull. 69:149154.

Bartholomew, G. A. and T. J. Cade. 1957b. Temperature regulation,hibernation, and aestivation in the little pocket mouse, Perog-nathus longimembris. J. Mamm. 38:6071.

Bartholomew, G. A. and T. J. Cade. 1963. The water economy ofland birds. Auk 80:504539.

Bartholomew, G. A. and T. M. Casey. 1977a. Body temperature andoxygen consumption during rest and activity in relation to bodysize in some tropical beetles. J. Therm. Biol. 2:173176.

Bartholomew, G. A. and T. M. Casey. 1977b. Endothermy duringterrestrial activity in large beetles. Science: 195:882883.

Bartholomew, G. A. and T. M. Casey. 1978. Oxygen consumption



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of moths during rest, pre-flight warm-up, and flight in relationto body size and wing morphology. J. Exp. Biol. 76:1125.

Bartholomew, G. A. and H. H. Caswell, Jr. 1951. Locomotion inkangaroo rats and its adaptive significance. J. Mamm. 32:155169.

Bartholomew, G. A. and W. R. Dawson. 1952. Body temperaturesin nestling western gulls. Condor 54:5860.

Bartholomew, G. A. and W. R. Dawson. 1954. Temperature regu-lation in young pelicans, herons, and gulls. Ecology 35:466472.

Bartholomew, G. A. and W. R. Dawson. 1958. Body temperaturesin California and Gambels quail. Auk 75:150156.

Bartholomew, G. A. and W. R. Dawson. 1979. Thermoregulatorybehavior during incubation in Heermanns gulls. Physiol. Zool.52:422437.

Bartholomew, G. A., W. R. Dawson, and R. C. Lasiewski. 1970.Thermoregulation and heterothermy in some of the smaller fly-ing foxes (Megachiroptera) of New Guinea. Z. vergl. Physiol.70:196209.

Bartholomew, G. A. and R. J. Epting. 1975a. Rates of post-flightcooling in sphinx moths. In D. M. Gates and R. B. Schmerl(eds.), Perspectives in biophysical ecology, pp. 405415.Springer-Verlag, New York.

Bartholomew, G. A. and R. J. Epting. 1975b. Allometry of post-flight cooling rates in moths: a comparison with vertebrate ho-meotherms. J. Exp. Biol. 63:603613.

Bartholomew, G. A. and D. L. Goldstein. 1984. The energetics ofdevelopment in a very large altricial bird, the brown pelican. InR. S. Seymour (ed.), Respiration and metabolism of embryonicvertebrates. Perspectives in vertebrate science, Vol. 3, pp. 347357. Dr. W. Junk, Dordrecht, Boston, Lancaster.

Bartholomew, G. A. and B. Heinrich. 1973. A field study of flighttemperatures in moths in relation to body weight and wing load-ing. J. Exp. Biol. 58:123135.

Bartholomew, G. A. and B. Heinrich. 1978. Endothermy in Africandung beetles during flight, ball making, and ball rolling. J. Exp.Biol. 73:6583.

Bartholomew, G. A., Jr. and P. G. Hoel. 1953. Reproductive behaviorof the Alaska fur seal, Callorhinus ursinus. J. Mamm. 34:417436.

Bartholomew, G. A., T. R. Howell, and T. J. Cade, 1957. Torpidityin the white-throated swift, Anna hummingbird, and poor-will.Condor 59:145155.

Bartholomew, G. A. and J. W. Hudson. 1960. Aestivation in theMohave ground squirrel Citellus mohavensis. In C. P. Lymanand A. R. Dawe (eds.), Mammalian hibernation, Bull. Mus.Comp. Zool. 124:193208.

Bartholomew, G. A. and J. W. Hudson. 1961. Desert ground squir-rels. Sci. Amer. 205:107116.

Bartholomew, G. A. and J. W. Hudson. 1962. Hibernation, estiva-tion, temperature regulation, evaporative water loss, and heartrate of the pygmy possum, Cercaertus nanus. Physiol. Zool. 35:94107.

Bartholomew, G. A., J. W. Hudson, and T. R. Howell. 1962. Bodytemperature, oxygen consumption, evaporative water loss, andheart rate in the poor-will. Condor 64:117125.

Bartholomew, G. A. and R. C. Lasiewski. 1965. Heating and coolingrates, heart rate and simulated diving in the Galapagos marineiguana. Comp. Biochem. Physiol. 16:573582.

Bartholomew, G. A., R. C. Lasiewski, and E. C. Crawford, Jr. 1968.Patterns of gular flutter in cormorants, pelicans, owls, anddoves. Condor 70:3134.

Bartholomew, G. A., P. Leitner. and J. E. Nelson. 1964. Body tem-perature, oxygen consumption, and heart rate in three speciesof Australian flying foxes. Physiol. Zool. 37:179198.

Bartholomew, G. A. and J. R. B. Lighton. 1985. Ventilation andoxygen consumption during rest and locomotion in a tropicalcockroach, Blaberus giganteus. J. Exp. Biol. 118:449454.

Bartholomew, G. A. and J. R. B. Lighton. 1986a. Endothermy andenergy metabolism of a giant tropical fly Pantophthalmus ta-baninus. J. Comp. Physiol. B 156:461468.

Bartholomew, G. A. and J. R. B. Lighton. 1986b. Oxygen con-

sumption during hover-feeding in free-ranging Anna humming-birds Calypte anna. J. Exp. Biol. 123:191200.

Bartholomew, G. A., J. R. B. Lighton, and D. H. Feener, Jr. 1988.Energetics of trail running, load carriage, and emigration in thecolumn-raiding army ant Eciton hamatum. Physiol. Zool. 61:5768.

Bartholomew, G. A., J. R. B. Lighton, and G. N. Louw. 1985. En-ergetics of locomotion and patterns of respiration in tenebrionidbeetles from the Namib Desert. J. Comp. Physiol. B 155:155162.

Bartholomew, G. A. and R. E. MacMillen. 1960. The water require-ments of mourning doves and their use of sea water and NaClsolutions. Physiol. Zool. 33:171178.

Bartholomew, G. A. and R. E. MacMillen. 1961. Oxygen consump-tion, estivation, and hibernation in the kangaroo mouse, Micro-dipodops pallidus. Physiol. Zool. 34:177183.

Bartholomew, G. A. and M. Rainy. 1971. Regulation of body tem-perature in the rock hyrax, Heterohyrax brucei. J. Mamm. 52:8195.

Bartholomew, G. A. and C. H. Trost. 1970. Temperature regulationin the speckled mousebird, Colius striatus. Condor 72:141146.

Bartholomew, G. A. and V. A. Tucker. 1963. Control of changes inbody temperature, metabolism, and circulation by the agamidlizard, Amphibolurus barbatus. Physiol. Zool. 36:199218.

Bartholomew, G. A. and V. A. Tucker. 1964. Size, body temperature,thermal conductance, oxygen consumption, and heart rate inAustralian varanid lizards. Physiol. Zool. 37:341354.

Bartholomew, G. A., V. A. Tucker, and A. K. Lee. 1965. Oxygenconsumption, thermal conductance, and heart rate in the Aus-tralian skink Tiliqua scincoides. Copeia 1965:169173.

Bartholomew, G. A., C. M. Vleck, and T. L Bucher. 1983. Energymetabolism and nocturnal hypothermia in two tropical passerinefrugivores, Manacus vitellinus and Pipra mentalis. Physiol.Zool. 56:370379.

Bartholomew, G. A. and D. Vleck. 1979. The relation of oxygenconsumption to body size and to heating and cooling in theGalapagos marine iguana, Amblyrhynchus cristatus. J. Comp.Physiol. 132:285288.

Bartholomew, G. A., D. Vleck, and C. M. Vleck. 1981. Instanta-neous measurements of oxygen consumption during pre-flightwarm-up and post-flight cooling in sphingid and saturniidmoths. J. Exp. Biol. 90:1732.

Bartholomew, G. A., F. N. White, and T. R. Howell. 1976. Thethermal significance of the nest of the sociable weaver Phile-tairus socius: Summer observations. Ibis 118:402410.

Bartholomew, G. A. and F. Wilkie. 1956. Body temperature in thenorthern fur seal, Callorhinus ursinus. J. Mamm. 37:327337.

Bell, G. P., G. A. Bartholomew, and K. A. Nagy. 1986. The rolesof energetics, water economy, foraging behavior, and geother-mal refugia in the distribution of the bat, Macrotus californicus.J. Comp. Physiol. B 156:441450.

Bennett, A. F., W. R. Dawson, and G. A. Bartholomew. 1975. Effectsof activity and temperature on aerobic and anaerobic metabo-lism of the Galapagos marine iguana. J. Comp. Physiol. 100:317329.

Bennett, A. F., and C. Lowe. 2005. The academic geneology ofGeorge A. Bartholomew. Integr. Comp. Biol. 45:231233.

Brown, J. H. and G. A. Bartholomew. 1969. Periodicity and ener-getics of torpor in the kangaroo mouse, Microdipodops pallidus.Ecology 50:705709.

Bucher, T. L. and G. A. Bartholomew. 1984. Analysis of variationin gas exchange, growth patterns, and energy utilization in aparrot and other avian embryos. In R. S. Seymour (ed.), Res-piration and metabolism of embryonic vertebrates. Perspectivesin Vertebrate Science, Vol. 3, pp. 359372. Dr. W. Junk, Dor-drecht, Boston, Lancaster.

Bucher, T. L., M. J. Ryan, and G. A. Bartholomew. 1982. Oxygenconsumption during resting, calling, and nest building in thefrog Physalaemus pustulosus. Physiol. Zool. 55:1022.

Bucher, T. L., G. A. Bartholomew, W. Z. Trivelpiece, and N. J.Volkmann. 1986. Metabolism, growth, and activity in Adelieand emperor penguin embryos. Auk 103:485493.



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Cade, T. J. and G. A. Bartholomew. 1959. Sea-water and salt utili-zation by savannah sparrows. Physiol. Zool. 37:230238.

Chappell, M. A. and G. A. Bartholomew. 1981a. Standard operativetemperatures and thermal energetics of the antelope groundsquirrel Ammospermophilus leucurus. Physiol. Zool. 54:8193.

Chappell, M. A. and G. A. Bartholomew. 1981b. Activity and ther-moregulation of the antelope ground squirrel Ammospermophi-lus leucurus in winter and summer. Physiol. Zool. 54:215223.

Dawson, W. R. 1988. An experimental natural history of some ter-restrial vertebrates. Am. Zool. 28:11811188.

Dawson, W. R., G. A. Bartholomew, and A. F. Bennett. 1977. Areappraisal of the aquatic specializations of the Galapagos ma-rine iguana (Amblyrhynchus cristatus). Evolution 31:891897.

Feder, M. E., A. F. Bennett, and R. B. Huey. 2000. Evolutionaryphysiology. Ann. Rev. Ecol. Syst. 31:315341.

Fry, F. E. J. 1947. Effects of environment on animal activity. Pub.Ont. Fish Res. Lab. No. 68, pp. 162.

Garland, T., Jr. and P. A. Carter. 1994. Evolutionary physiology.Ann. Rev. Physiol. 56:579621.

Gordon, M. S., G. A. Bartholomew, J. D. OConnor, and E. C. Ol-son. 1976. Zoology. Macmillan Publishing Co., New York.

Gordon, M. S., G. A. Bartholomew, A. D. Grinnell, C. B. Jrgensen,and F. N. White. 1982. Animal physiology, 4th ed. MacMillan,New York.

Heinrich, B. 1981. Insect thermoregulation. John Wiley and Sons,New York.

Heinrich, B. and G. A. Bartholomew. 1971. An analysis of pre-flightwarm up in the sphinx moth Manduca sexta. J. Exp. Biol. 55:223239.

Heinrich, B. and G. A. Bartholomew. 1979. Roles of endothermyand size in inter- and intraspecific competition for elephant dungin an African dung beetle, Scarabaeus laevistriatus. Physiol.Zool. 52:484496.

Howell, T. R. and G. A. Bartholomew. 1959. Further experimentson torpidity in the poor-will. Condor 61:180185.

Howell, T. R. and G. A. Bartholomew. 1961a. Temperature regula-tion in Laysan and black-footed albatrosses. Condor 63:185197.

Howell, T. R. and G. A Bartholomew. 1961b. Temperature regula-tion in nesting Bonin Island petrels, wedge-tailed shearwaters,and Christmas Island shearwaters. Auk 78:343354.

Howell, T. R. and G. A. Bartholomew. 1962a. Temperature regula-tion in the red-tailed tropic bird and the red-footed booby. Con-dor 64:618.

Howell, T. R. and G. A. Bartholomew. 1962b. Temperature regula-tion in the sooty tern, Sterna fuscata. Ibis 104:98105.

Hudson, J. W. and G. A. Bartholomew. 1964. Terrestrial animals indry heat: Estivators. In D. B. Dill (ed.), Handbook of physiol-ogy, Sect. 4, Adaptation to the environment, pp. 541550.American Physiological Society, Washington, D.C.

Kenagy, G. J. and G. A. Bartholomew. 1985. Seasonal reproductivepatterns in five coexisting California desert rodent species. Ecol.Monogr. 55:371397.

Kingsolver, J. G. and R. B. Huey. 2003. Introduction: The evolution

of morphology, performance, and fitness. Integr. Comp. Biol.43:361366.

Lasiewski, R. C. and G. A. Bartholomew. 1966. Evaporative coolingin the poor-will and the tawny frogmouth. Condor 68:253262.

Lasiewski, R. C., W. R. Dawson, and G. A. Bartholomew. 1970.Temperature regulation in the little Papuan frogmouth, Podar-gus ocellatus. Condor 72:332338.

Lighton, J. R. B. and G. A. Bartholomew. 1988. Standard energymetabolism of a desert harvester ant Pogonomyrmex rugosus:Effects of temperature, body mass, group size, and humidity.Proc. Nat. Acad. Sci. U.S.A. 85:47654769.

Lighton, J. R. B., G. A. Bartholomew, and D. H. Feener, Jr. 1987.Energetics of locomotion and load carriage and a model of theenergy cost of foraging in the leaf-cutting ant Atta colombicaGuer. Physiol. Zool. 60:524537.

Morgan, K. R. and G. A. Bartholomew. 1982. Homeothermic re-sponse to reduced ambient temperature in a scarab beetle. Sci-ence 216:14091410.

Nicolson, S. W., G. A. Bartholomew, and M. K. Seely. 1984. Eco-logical correlates of locomotion speed, morphometrics, andbody temperature in three Namib Desert tenebrionid beetles. S.Afr. J. Zool. 19:131134.

Pennycuick, C. J. and G. A. Bartholomew. 1973. Energy budget ofthe lesser flamingo (Phoeniconaias minor Geoffrey). E. Afr.Wildl. J. 11:199207.

Peterson, R. S. and G. A. Bartholomew. 1967. The natural historyof the California sea lion. Spec. Pub. No. 1. American Societyof Mammalogists.

Poulson, T. L. and G. A. Bartholomew. 1962. Salt balance in thesavannah sparrow. Physiol. Zool. 35:109119.

Ryan, M. J., G. A. Bartholomew, and A. S. Rand. 1983. Energeticsof reproduction in a neotropical frog Physalaemus pustulosus.Ecology 64:14561462.

Seymour, R. S., G. A. Bartholomew, and M. C. Barnhart. 1983.Respiration and heat production by the inflorescence of Philo-dendron selloum Koch. Planta 157:336343.

Seymour, R. S., M. C. Barnhart, and G. A. Bartholomew. 1984.Respiratory gas exchange during thermogenesis in Philoden-dron selloum Koch. Planta 161:229232.

Smith, N. G., D. L. Goldstein, and G. A. Bartholomew. 1986. Islong-distance migration possible for soaring hawks using onlystored fat? Auk 103:607611.

Smyth, M. and G. A. Bartholomew. 1966. The water economy ofthe black-throated sparrow and the rock wren. Condor 68:447458.

Vleck, D., T. T. Gleeson, and G. A. Bartholomew. 1981. Oxygenconsumption during swimming in Galapagos marine iguanasand its ecological correlates. J. Comp. Physiol. 141:531536.

White, F. N., G. A. Bartholomew, and T. R. Howell. 1975. Thethermal significance of the nest of the sociable weaver Phile-tairus socius: Winter observations. Ibis 117:171179.

White, F. N., G. A. Bartholomew, and J. L. Kinney. 1978. Physio-logical and ecological correlates of tunnel nesting in the Euro-pean bee-eater Merops apiaster. Physiol. Zool. 51:140154.



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dawson - 2005 - george a. bartholomew's contributions to integrative and comparative biology

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