Comparing cross-species regression to independent contrasts
Comparisons with previous studies are difficult because the data bases and especially comparative methodologies are fundamentally different. Most earlier studies used simple cross-species regression and thus may overestimate the strength of a relationship by failing to distinguish similarity due to common ancestry from that due to similar selection pressures (Harvey & Pagel 1991). Such was the case when we re-examined the allometric relationships using cross-species regression. Except for age of independence and haematocrit, all variables displayed a significant relationship with size (either body or brain weight), with uncorrected P-values often less than 0·0001 (see Bininda-Emonds & Gittleman 2000). Throughout the discussion, we assume our use of independent contrasts at least in part explains any different findings compared to the literature and will instead concentrate on other, more case specific causes.
Results from studies of the Carnivora using cross-species analysis vs. those using some form of phylogenetic correction (e.g. Gittleman 1986b, 1993, 1994; Elgar & Harvey 1987; Ferguson, Virgl & Larivière 1996) are not substantially different. This arises partly because many early ‘taxonomic corrections’ resemble cross-species techniques more than current ones, which account more effectively for phylogenetic effects. Also, although cross-species regression is theoretically invalid (Purvis et al. 1994), it can still give approximately correct answers when the comparative relationship is strong (Pagel 1993) and largely independent of phylogeny.
Adaptations in aquatic carnivores
Relative to their terrestrial sister taxa, aquatic carnivores possess increased (absolute) head and body lengths, decreased interbirth intervals, shorter lifespans and possibly smaller litter sizes. There were few other differences in the 20 variables we examined.
Smaller litter sizes are characteristic of K-selected species, which otters and pinnipeds are often considered to be (McLaren 1967; Hennemann, Thompson & Konecny 1983; Stirling 1983; Schmitz & Lavigne 1984). This life history trait is also associated with a tendency towards larger neonates (only weakly supported herein) and generally precocial young (Eisenberg 1981). Together, this suite of life histories provides advantages for both mother and offspring in dealing with an amphibious lifestyle. Given that dens or rookeries are often close to the water, suitable breeding sites are at a premium (Bartholomew 1970; Repenning 1976), thus competitively limiting the number of offspring that can be raised. Precociality is advantageous because of the greater risks the aquatic environment places on newborns (e.g. risk of drowning, problems with flotation) and the increased complexity of dealing with both terrestrial and aquatic habitats (only sea otter offspring will potentially never set foot on land; Kenyon 1981).
Functional explanations for the remaining two strong trends are not apparent. The result for interbirth interval may be an artefact. With few exceptions, carnivores give birth at approximately 12-month intervals. Many viverrids have shorter interbirth intervals than this and many large carnivores have longer intervals. Together, these two exceptions are sufficient to produce a positive correlation between interbirth interval and brain weight. Thus, although most aquatic species have 12-month interbirth intervals like their sister taxa, their intervals appear shorter when scaled to their relatively large brain size (see below); comparisons uncorrected for size showed no trend (Table 4). Comparative statements about interbirth interval are also often suspect due to rounding errors in the raw data (Gittleman 1989) and because the values given in the literature often do not account for the true interval where successful rearing of offspring occurs. The decreased longevity of aquatic species could derive from the truly amphibious nature of these organisms. Aquatic carnivores are therefore at greater risk from predators and other dangers associated with two very different environments, neither of which they are ideally adapted to. However, because the longevity estimates we used represent maximum, rather than average lifespans, and were often obtained from captive animals, such a functional explanation seems unlikely. Differences in animal husbandry techniques may be a partial explanation; however, in pinnipeds at least, captive vs. wild longevity values were usually comparable.
Size differences between aquatic and terrestrial carnivores influence numerous functional traits. Despite being advantageous for thermodynamic reasons, aquatic carnivores are absolutely larger than their terrestrial sister taxa for only head and body length, and generally not proportionately larger when we accounted for allometry. The significant increase in head and body length, which remains even when we corrected for size using body weight, is actually detrimental thermodynamically by making these animals less spherical, but is beneficial for locomotion due to streamlining (see Fish 1993). Therefore, other mechanisms such as increased insulation (see also Wolff & Guthrie 1985) are apparently sufficient to meet the thermoregulatory demands of the aquatic environment without changes to basal metabolic rate (BMR). The assertion that aquatic mammals have proportionately higher BMRs apparently stems from incompatible data (Lavigne et al. 1986). Early physiological studies of marine mammals used more manageably sized juveniles, whereas those of most terrestrial mammals used adults in accordance with Kleiber’s (1975) criteria (adults that are postabsorptive, non-reproductive, at rest and in thermoneutral conditions). Juveniles have elevated BMRs compared to adults (Ashwell-Erickson, Elsner & Wartzok 1979; Little 1995). Metabolic data for marine mammals meeting Kleiber’s criteria do not show elevated BMRs (Lavigne et al. 1986; but see Williams 1998).
Overall, the large lack of differences among aquatic and non-aquatic carnivores is striking. Within fissipeds, life history traits are independent of ecological factors such as diet, zonation, habitat and activity pattern (Gittleman 1986b, 1993). With few exceptions (see above; also delayed ages at sexual maturity in some otters compared to terrestrial mustelids; Gittleman 1984, 1986b), our comparative tests provide another example of how little ecological factors influence carnivore life history patterns.
The similarity in haematology between aquatic and non-aquatic taxa might occur because these variables are interdependent and vary within narrow limits across all mammals to maintain optimal oxygen transport (Hawkey 1977). A more critical adaptation for aquatic species may be increasing oxygen stores through either increased blood volume or increased oxygen capacity of both blood and haemoglobin (Lenfant 1969; Lapennas & Reeves 1982; Hochachka 1992). However, there were insufficient data, particularly for terrestrial species, to test this hypothesis.
In conclusion, the effects of aquatic living as a general selective force is often a simplification and may obscure important functional differences within terrestrial (e.g. cursorial vs. arboreal species) and aquatic forms (Gittleman 1986b; Boness & Bowen 1996). Further comparative analyses are needed to isolate which key factors led to the transition between terrestrial and aquatic living and why these factors were so important.
We interpret two findings as indirect support for aquatic species also possessing proportionately larger brains for their size (see Wirz 1950; Stephan 1972). First, when corrected for body weight, brain weight showed a weak trend to increased values in aquatic forms (with P-values generally below 0·10), whereas correcting for brain weight indicated a weak trend to decreased body weight. Secondly, opposing patterns were seen in the size-corrected analysis depending on whether body or brain weight was used as the size estimator. Correcting for body weight revealed the same trends as the uncorrected analysis, but correcting for the proportionately larger brain weight caused most of the positive trends to disappear or occasionally reverse. In other words, using brain weight as a size estimator makes aquatic carnivores appear larger than they really are (in terms of body size), thereby causing variables displaying allometric effects to appear smaller.
The adaptive explanation for relatively larger brains in aquatic carnivores relates to the need for such species to process information in a complex three-dimensional environment (see Estes 1989), a form of the perceptual complexity hypothesis (see Eisenberg & Wilson 1978; Mace, Harvey & Clutton-Brock 1980; Harvey & Krebs 1990). Consistent with this is that aquatic carnivores are actually amphibious. Relatively larger brains may help to process information in two very different environments, each with specific sensory cues and cognitive demands. The amphibious nature of aquatic carnivores also explains why they retain small olfactory lobes (Fish 1898; Hubbard 1968; Gittleman 1991), structures that are absent or nearly so in the fully aquatic cetaceans (Jerison 1973). For example, in all pinnipeds, and otariids in particular, identification of newborns and pups by their mothers is based primarily on smell (King 1983; Boness & Bowen 1996). Further comparative work is needed on whether olfactory bulbs and possibly other brain components are transitional characters representing key evolutionary shifts from terrestrial to amphibious to aquatic forms (see also Barton, Purvis & Harvey 1995).
Although only a limited number of aquatic–terrestrial comparisons exist within the Carnivora, the ecological and morphological variability found in this group makes our study a valuable initial test of the questions we seek to answer: (1) to identify adaptations characterizing aquatic carnivores (relative to their terrestrial sister taxa) and (2) to determine if adaptation to an aquatic lifestyle is gradual or discrete. Our inclusion of ‘semi-aquatic’ species in order to test our second question supported the idea that exploitation of aquatic resources at even partial levels correlates with possession of what have been previously thought of as ‘aquatic adaptations’ (Stein 1988, 1989; Fish & Stein 1991). The semi-aquatic species did not display a greater tendency to contradict the proposed hypotheses or display a contrary trend to the remaining forms than did the fully aquatic pinnipeds and otters.
Increases in sample size within carnivores are not possible (beyond obtaining more information for the poorly known aquatic civets Cynogale and Osbornictis). Similar comparative analyses should test how well the ‘aquatic adaptation’ hypotheses apply across other mammals and vertebrates in general. Unfortunately, answering this question may not be easy. For instance, there are many aquatic mammals: cetaceans, sirenians, hippopotamus, platypus, some shrews, some marsupials and numerous rodents. However, the identity of their non-aquatic sister taxa is often unknown or contentious, particularly for rodents (see Parker 1990; Nowak 1991). Furthermore, even when the sister taxa are well agreed upon, such as artiodactyls for cetaceans or proboscideans for sirenians (Irwin, Kocher & Wilson 1991; Novacek 1992; Arnason & Gullberg 1996; Stanhope et al. 1996), the age of both divergences (≥ 60 million years; Novacek 1992; Arnason & Gullberg 1996; Lavergne et al. 1996) presents special problems. In each case, the accuracy of the contrast depends on obtaining extensive species data and well-resolved phylogenies for both sister groups. As well, the long divergence times mean that any differences might have accrued for selective forces other than the adaptations to an aquatic environment.