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SCHOOL OF BIOSCIENCES

Craig R. White - Abstracts

Craig White

Craig R. White
School of Biosciences
The University of Birmingham
Birmingham
B15 2TT, UK

Ph: +44 (0) 121 414 3822
Fax: +44 (0) 121 414 5925
c.r.white@bham.ac.uk

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Research

A complete list of my publications

Publications with Abstracts

The Comparative Physiology Lab Group

White, C.R. (2001) The energetics of burrow excavation by the inland robust scorpion, Urodacus yaschenkoi (Birula 1903). Australian Journal of Zoology 49, 663-674

The inland robust scorpion, Urodacus yaschenkoi (Urodacinae, Scorpionidae), is a large (~3 g) semifossorial scorpion that is widespread in arid regions of Australia. It constructs spiralling burrows up to 1 m deep in sandy soils. This study determined the net cost of transport (NCOT) by burrowing, which represents the energy used in horizontally burrowing a given distance, excluding maintenance metabolism. A mathematical model generally applicable to semi-fossorial species was developed and used to estimate the total cost of burrow construction. The model incorporates (1) horizontal NCOT, (2) the cost of moving spoil and the animal’s mass along the length of the tunnel, and (3) the cost of working against gravity to raise spoil and the animal’s mass to the surface. The total cost of burrow excavation to a depth of 47 cm was estimated to be 350–530 J. This represents approximately 2% of an adult scorpion’s yearly energy turnover. Interspecific allometric comparisons of published NCOT data from phylogenetically diverse burrowers (with body masses spanning over two orders of magnitude) showed that burrowing method and substrate are important determinants of NCOT. Specifically, the cost of constructing an open tunnel through damp or dry sand is higher than the cost of moving through wet sand or mud without forming a tunnel.


White C.R. and Seymour, R.S. (2003) Mammalian basal metabolic rate is proportional to body mass2/3. Proceedings of the National Academy of Sciences of the USA. 100, 4046-4049

The relationship between mammalian basal metabolic rate (BMR, ml of oxygen per h) and body mass (M, g) has been the subject of regular investigation for over a century. Typically, the relationship is expressed as an allometric equation of the form BMR = a M b. The scaling exponent (b) is a point of contention throughout this body of literature, within which arguments for and against geometric (b proportional to 2/3) and quarter-power (b proportional to 3/4) scaling are made and rebutted. Recently, interest in the topic has been revived by published explanations for quarter-power scaling based on fractal nutrient supply networks and four-dimensional biology. Here, a new analysis of the allometry of mammalian BMR that accounts for variation associated with body temperature, digestive state, and phylogeny finds no support for a metabolic scaling exponent of 3/4. Data encompassing five orders of magnitude variation in M and featuring 619 species from 19 mammalian orders show that BMR proportional to M2/3.


Seymour, R.S., White, C.R. and Gibernau, M. (2003) Heat reward for insect pollinators. Nature 426, 243-244

in neotropical forests, adults of many large scarab beetle species spend most of their time inside the floral chambers of heatproducing flowers, where they feed and mate throughout the night and rest during the following day, before briefly flying to another flower. Here we measure floral temperatures in Philodendron solimoesense (Araceae) in French Guiana and the respiration rates of Cyclocephala colasi beetles at floral and ambient temperatures, and show that the the beetles’ extra energy requirements for activity are 2.0–4.8 times greater outside the flower than inside it. This finding indicates that heat produced by the flower constitutes an important energy reward to pollinators, allowing them to feed and mate at a fraction of the energy cost that would be required outside the flower.


White, C.R. (2003) The influence of foraging mode and arid adaptation on the basal metabolic rates of burrowing mammals. Physiological and Biochemical Zoology 76, 122-134

Two competing but nonexclusive hypotheses to explain the reduced basal metabolic rate (BMR) of mammals that live and forage underground (fossorial species) are examined by comparing this group with burrowing mammals that forage on the surface (semifossorial species). These hypotheses suggest that the low BMR of fossorial species either compensates for the enormous energetic demands of subterranean foraging (the cost-of-burrowing hypothesis) or prevents overheating in closed burrow systems (the thermal-stress hypothesis). Because phylogentically informed allometric analysis showed that arid burrowing mammals have a significantly lower BMR than mesic ones, fossorial and semifossorial species were compared within these groups. The BMRs of mesic fossorial and semifossorial mammals could not be reliably distinguished, nor could the BMRs of large (> 77 g) arid fossorial and semifossorial mammals. This finding favours the thermal-stress hypothesis, because the groups appear to have similar BMRs despite differences in foraging costs. However, in support of the cost-ofburrowing hypothesis, small (< 77 g) arid fossorial mammals were found to have a significantly lower BMR than semifossorial mammals of the similar size. Given the high mass-specific metabolic rates of small animals, they are expected to be under severe energy and water stress in arid environments. Under such conditions, the greatly reduced BMR of small fossorial species may compensate for the enormous energetic demands of subterranean foraging.


White, C.R. and Seymour, R.S. (2004) Does BMR contain a useful signal? Mammalian BMR allometry and correlations with a selection of physiological, ecological and life-history variables. Physiological and Biochemical Zoology 77, 929-941

Basal metabolic rate (BMR, mL oxygen h-1) is a useful measurement only if standard conditions are realised. We present an analysis of the relationship between mammalian body mass (M, g) and BMR that accounts for variation associated with body temperature, digestive state and phylogeny. In contrast to the established paradigm that BMR is proportional to M 3/4, data from 619 species, representing 19 mammalian orders and encompassing five orders of magnitude variation in M, show that BMR is proportional to M 2/3. If variation associated with body temperature and digestive state are removed, the BMRs of eutherians, marsupials and birds do not differ and no significant allometric exponent heterogeneity remains between orders. The usefulness of BMR as a general measurement is supported by the observation that, after the removal of body mass effects, the residuals of BMR are significantly correlated with the residuals for a variety of physiological and ecological variables, including maximum metabolic rate, field metabolic rate, resting heart rate, lifespan, litter size, and population density.


White, C.R. and Seymour, R.S. (2005) Allometric Scaling of Mammalian Metabolism. Journal of Experimental Biology 208, 1611-1619

The importance of size as a determinant of metabolic rate (MR) was first suggested by Sarrus and Rameaux over 160 years ago. Max Rubner’s (1883) finding of a proportionality between MR and body surface area in dogs was consistent with Sarrus and Rameaux’s fomulation and suggested a proportionality between MR and body mass (M) raised to the power of 2/3. However, interspecific analyses compiled during the first half of the 20th century concluded that mammalian basal MR (BMR, mL oxygen h-1) was proportional to M 3/4, a viewpoint that persisted for seven decades, even leading to its common application to non-mammalian groups. Beginning in 1997, the field was re-invigorated by three new theoretical explanations for 3/4-power BMR scaling. However, the debate over which theory accurately explains 3/4 power scaling may be premature, because some authors maintain that there is insufficient evidence to adopt an exponent of 3/4 over 2/3. If progress toward understanding the non-isometric scaling of BMR is ever to be made, it is first essential to know what the relationship actually is. We re-examine previous investigations of BMR scaling by standardising units and recalculating regression statistics. The proportion of large herbivores in a data set is positively correlated both with the scaling exponent (b, where BMR = a M b) and the coefficient of variation (CV: the standard deviation of ln-ln residuals) of the relationship. Inclusion of large herbivores therefore both inflates b and increases variation around the calculated trendline. This is related to the long fast duration required to achieve the postabsorptive conditions required for determination of BMR, and because peak postfeeding resting MR (RMRpp) scales with an exponent of 0.75 +/- 0.03 (95% CI). Large herbivores are therefore less likely to be postabsorptive when MR is measured, and are likely to have a relatively high MR if not postabsorptive.
    The 3/4 power scaling of RMRpp is part of a wider trend where, with the notable exception of cold-induced maximum MR (b = 0.65 +/- 0.05), b is positively correlated with the elevation of the relationship (higher MRs scale more steeply). Thus exercise induced maximum MR (b = 0.87 +/- 0.05) scales more steeply than RMRpp, field MR (b = 0.73 +/- 0.04), thermoneutral resting MR (RMRt, b = 0.712 +/- 0.013) and BMR. The implication of this observation is that contamination of BMR data with non-basal measurements is likely to increase the BMR scaling exponent even if the contamination is randomly distributed with respect to M. Artificially elevated scaling exponents can therefore be accounted for by the inclusion of measurements that fail to satisfy the requirements for basal metabolism, which are strictly defined (adult, non-reproductive, postabsorptive animals resting in a thermoneutral environment during the inactive circadian phase). Similarly, a positive correlation between M and body temperature (Tb) and between Tb and mass-independent BMR contributes to elevation of b. While not strictly a defined condition for the measurement of BMR, the normalisation of BMR measurements to a common Tb (36.2 ºC) to achieve standard metabolic rate (SMR) further reduces the CV of the relationship. Clearly the value of the exponent depends on the conditions under which the data are selected. The exponent for true BMR is 0.686 (+/- 0.014), Tb normalised SMR is 0.675 (+/- 0.013) and RMRt is 0.712 (+/- 0.013).


White, C.R. (2005) The allometry of burrow geometry. Journal of Zoology 265, 395-403

The allometric relationship between body mass and burrow cross-sectional area for burrowing animals holds across greater than six orders of magnitude variation in body mass, and includes species separated by more than 500 million years of evolution from two phyla (Arthropoda and Chordata), seven classes (Arachnida, Insecta, Malacostraca, Osteichthyes, Amphibia, Reptilia, and Mammalia) and both terrestrial and marine habitats. Only birds, which construct relatively large burrows, and vermiform animals, which construct relatively narrow burrows, are separated from the remaining burrowing species. No difference is found between fossorial (burrowing animals that forage beneath the soil surface) and semi-fossorial (burrowing animals that forage terrestrially) mammals, suggesting that subterranean foragers do not modify burrow cross-sectional area to increase energy yields. However, solitary fossorial mammals do construct significantly larger nest chambers than semi-fossorial and colonial fossorial mammals. These large nest chambers probably assist in maintaining body temperature by providing a better thermally insulated microenvironment. This offsets the thermoregulatory problems faced by these animals, which are characterised by low, labile body temperatures and poor thermoregulatory ability. Colonial fossorial mammals, on the other hand, construct nest chambers that are the same relative size as those constructed by semi-fossorial mammals and probably maintain homeothermy by huddling with endothermic nest-mates.


Taggart, D.A., Shimmin, G.A., Ratcliff, J.R., Steele, V.R., Dibben, R., Dibben, J., White, C. and Temple-Smith, P.D. (2005) Seasonal changes in the testis, accessory glands and ejaculate characteristics of the southern hairy-nosed wombat, Lasiorhinus latifrons, (Marsupialia: Vombatidae). Journal of Zoology 26, 95-104

Most mammals exhibit seasonal variation in the reproductive capacity of one or both sexes. While the female southern hairy-nosed wombat Lasiorhinus latifrons is a known seasonal breeder, the extent of seasonality in the male has not been documented. To examine this, gross body measurements including scrotal diameter and the dimensions of the accessory gland bulge were recorded and male reproductive tracts were examined between 1993 and 2000. Testes, epididymides and accessory glands from all males were dissected free of connective tissue and weighed. In addition, matched semen samples were collected over four time points in 2000 corresponding to the breeding season (September), immediately post-breeding season (November), during the non-breeding season (January), and immediately before the onset of the next breeding season (June) as determined from female reproductive status. Semen was collected by electro-ejaculation and analysed for volume, sperm number and motility characteristics. Ejaculate volume, total ejaculate sperm number, percentage motile sperm, and the sperm motility rating and index were all significantly elevated in September and significantly lower in November and January. This correlated with a significant increase in body weight, peri-cloacal gland width, and the weights of the prostate, Cowper's glands, urethral bulb and crus penis. The data confirm that male reproduction in the southern hairy-nosed wombat, like that of the female, is highly seasonal with a peak in reproductive capacity occurring in August–September and a reduction by November.

Martin, G.R., Jarrett, N., Tovey, P. and White, C.R. (In Press) Visual fields in Flamingos: chick-feeding versus filter feeding. Naturwissenschaften

In birds, the position and extent of the region of binocular vision appears to be determined by feeding ecology. Of prime importance is the degree to which vision is used for the precise control of bill position when pecking or lunging at prey. In birds that do not require such precision (probe and filter-feeders), the bill falls outside the binocular field which extends above and behind the head, thus providing comprehensive visual coverage. Flamingos Phoenicopteridae are highly specialised filter-feeders. They employ a unique technique that does not require accurate bill positioning in which the inverted head is placed between the feet. Feeding flamingos often walk forwards with the head pointing “backwards”. Using an ophthalmoscopic reflex technique we show that in Lesser Flamingos Phoeniconaias minor visual fields are in fact the same as those of birds that feed by precision pecking and that feeding flamingos are blind in the direction of their walking. We suggest that this is due to the requirement for accurate bill placement when flamingos feed their chicks with “crop- milk”. We propose that chick feeding may be the ultimate determinant of visual field topography in birds, not feeding ecology.











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