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(1985) 207491-509 ! Brain Size, Development and Metabolism In WZooLLond.(A) (1985) 207,491-509 Peter M. Bennett and Paul H. Harvey* School of Biological Sciences, University of Sussex, Palmer, Brighton BN1 9QG, U.K. (Accepted 12 March 1985) (With 11 figures in the text) ! BrainRecent size, hypotheses development that variation and in brain metabolism size among birds in and birds mammals and result mammals from differences Indices of embryonic and post-embryonic brain growth are defined. Precocial birds and mammals have high embryonic brain growth indices which arc compensated for by low post- iin metabolicembryonic allocation indices during(with the ontogeny exception ofare Homo tested. sapiens). In contrast, altricial birds and mammals have low embryonic and high post-embryonic indices. Altricial birds have relatively small brains at hatching and develop relatively large brains as adults, but among mammals there is no equivalent correlation between variation in adult relative brain sizes and state of neonatal development. Compensatory brain development in both birds and mammals is associated with compensatory parental metabolic allocation. In comparison with altricial development, precocial development is characterized by higher levels of brain growth and parental metabolic allocation prior to hutching or birth and lower levels subsequently. Differences between degrees of postnatal investment by the parents in the young of precocial birds versus precocial mammals may result in the different patterns of adult brain size associated with precociality versus altriciality in the two groups. The allometric exponent scaling brain on body size dilTcrs among taxonomic levels in birds. The exponent is higher for some parts ofthe brain than others, irrespective of taxonomic level. Unlike mammals, the exponents for birds do not show a general increase with taxonomic level. These patterns call into question recent interpretations of the allometric exponent in birds, and the reason for changes in exponent with taxonomic level. Contents Introduction 4-'- H y p o t h e s e s a n d t e s t s 4 9 . M a t e r i a l s a n d m e t h o d s 4 9 - W e i g h t s a n d r a t e s 4 9 ' Developmental classification 49 A n a l y s i s 4 9 R e s u l t s 4 9 Brain size and metabolism in birds 49 Brain size and development in birds 49 Brain size and development in mammals 49 I n t e r - o r d e r c o m p a r i s o n s 5 0 Discussion 50 R e f e r e n c e s 5 0 A p p e n d i x 5 0 Present address: Department of Zoology, University of Oxford. South Parks Road. Oxford OX1 3PS 0022 -5460 (85/012491 + 19S0300/0 © 1985 The Zoological Society of London ■ j ^^r^ Tjj 492 P. M. BENNETT AND P. H. HARVEY Introduction The selective forces responsible for the evolution of differences in brain size among vertebr remain poorly understood. Larger-bodied species have larger brains, and this is presum*!? necessary in order to integrate the activities of their various parts. After controlling for this gen i effect of body size, a number of authors have identified certain ecological and behavioui correlates of relative brain size among mammals. These differences have often been interpr id i to mean that species with more complex behaviour patterns are selected to have h brains (Bauchot & Stephan, 1966, 1969; Pirlot & Stephan, 1970; Jerison, 1973- Ksenber/* j Wilson, 1978, 1981; Clutton-Brock & Harvey, 1980; Mace, Harvey & Clutton'-Brock I98n 1981). However, elsewhere we have pointed out that these correlates of relative brain <••« i y little evidence II state of development ofthe young at hatching was found to be a strong'correlate of ^nation in relative brain size among birds. In this paper, we investigate recent hypotheses that varia tion in relative brain size among birds and mammals may result from energetic constraint (Martin, 1981, 1983; Armstrong, 1982, 1983; Hofman, 1983) linked to developmental process, < (Martin, 1981, 1983). processes Hypotheses and tests The idea that brain size is somehow linked to metabolism has been encouraged by the realization that the allometric exponent linking brain to body size is around 0-75 for mammals (Bauchot, 1978; Martin, 1981; Armstrong, 1983; Martin & Harvey, 1984) and 0-56 across species of birds or reptiles (Martin, 1981). Basal metabolic rates (measured as oxygen consump. tion or heat production per unit body weight per unit time) have been found to increase with approximately) the 0-75 power of body weight within each of these taxonomic groups (Hemmingsen, 1950, 1960; Kleiber, 1961; Lasiewski & Dawson, 1967). The similarity- of the bramrbody and the metabolism:body exponents of 0-75 for mammals suggests a possible relationship between brain size and metabolism. Two recent hypotheses have been proposed to account for the relationship. The first hypothesis is due to Armstrong (1982, 1983) and Hofman (1983), who plotted brain size against adult body metabolism across species of mammals. They found a linear relationship with a slope of one, which accords with the interpretation that adult mammals have been selected to allocate a constant proportion of their bodies' basal metabolism to the brain. But there is some scatter around the line, with primates having larger brains for their body metabolism than have ! other mammals. Both authors attempt to explain this by arguing that primates have higher cerebral metabolic rates than other mammals. Primates allocate 9-20% of their body metabolism to the brain, compared with 5% for other mammals. However, if primates have relatively large brains for whatever reason) they will concomitantly require a higher proportion of body metabolism to maintain their brains. Consequently, this argument makes no predictions about why primates (or, likewise, Homo within the primates) have relatively large brains (see also Harvey & Bennett, 1983). A second hypothesis linking brain size to metabolism in mammals has been proposed by Martin (1981, 1983), who takes into account the finding that, while the brain:body exponent is 0-75 lor mammals, it is about 0-56 for birds and reptiles. Since the basal metabolism: body size exponent X * -' iX ■■ 1 BRA,N SIZE. DEVELOPMENT AND METABOLISM IN BIRDS AND MAMMALS 493 WSheen e in founda direct to linkapproximate between 0-75the brain for all size three of classes,an adult heand argued its own.metabolic that 'there is rate no case (Martn for El"stead.qgl). 'it insteau,is the mothers u» metabolici nartitinn turnover which,na bothof mresources d.rect terms (throughbetween the nrthc adult brain (Martin, i^oj>;. ima "j^i""'j *■• r — - ^1ftoto size should scale with the 0-75 power on mother's body size and. therefore, ft 3ad" TW It second brain size prediction should is scale necessary isometrically to produce (with the an 0-75 exponent scaling of adultone) brainon neonatal size on brainadult b0vvyhenMartin (1981) attempted to test for the predicted relationships in mammals, he found that /results were complicated by variation in the state of development ofthe young at birth For tH ' Livc- sequencesizes, precocial of prolonged mammals intrauterine tend to have growth, relatively neonates long ofgestation precocial periods. mammals Probably (e.g nrimates ungulates and cetaceans) have relatively larger brains at birth than do neonates oi dear mammals (e.g. insectivores and most carnivores). When the two groups were taken irately Martin demonstrated the predicted relationships between neonatal brain size adult hran size and adult body size. However, precocial mammals seemed to have relatively larger ins, both as neonates and as adults, than altricial mammals. The relationship between large lit relative brain size and precocial development contrasts with Eisenberg s (1981) finding ,hat in a different sample of mammalian species, there was no correlation between adult elat'ive brain size and the state of development of the young at birth. This difference may result from > 'tin's sample being biased by unequal representation of species from different mammalian orders. A high proportion of the precocial species in his sample are primates and species belonging to this order tend to have relatively large brains as adults. But several other orders are underrepresented in the sample and species from some of these tend to be precocial and have relatively small brain sizes as adults (e.g. Artiodactyla or Penssodactyla- see Martin & Harvey, 1984). An assessment of the generality of the correlation, or lack of correlation between precociality and large neonatal and adult brain sizes is necessary for mammals. The ontogeny of brain development has already been examined in primates (Martin, 1983; Martin - Harvey, 1984; Harvey, Martin &Clutton-Brock, In press). A negative relationship exists between indices of foetal and post-natal brain growth. Folivorous primates have low foetal brain growth indices. Folivorous mammals tend to have lower basal metabolic rates than mammals of other dietetic groups (McNab, 1978, 1980). The suggestion that low foetal brain growth is .. associated with low adult metabolic rates lends support to Martin's theory. Furthermore, adult folivorous primates have relatively small brains. If folivorous primates do, indeed, have low \ metabolic rates, this may account for the dietary correlation which had previously been seen as lendina support to the sensory complexity interpretation of variation in relative brain size i (Clutton-Brock & Harvey, 1980). Preliminary results are in the predicted direction (see Harvey I & Benr-tt, 1983). Similarly, a relationship between diet and relative brain size in bats (Eisen- berg & Wilson, 1978) can also be accounted for by a correlation between diet and metabolic rates and another between metabolic rates and brain size (Armstrong, 1983). Martin (1981) went on to argue that, since birds and most reptiles are oviparous, in these groups it is the metabolism of the egg that provides for embryonic brain development.
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