The risky environments hypothesis

In a comprehensive review of mammalian development, Eisenberg (1981) suggested links between reproductive duration, encephalisation and predation risks. Studies of different mammalian groups have emphasised the importance of environmental risks in patterns of infant development and associated life history traits (pinnipeds: Trillmich 1989, 1996; carnivores: Gittleman and Oftedal, 1987). Promislow and Harvey (1990) clearly demonstrated the importance of early mortality as a pacer of life history events in mammals. In particular, they noted the association between juvenile mortality and gestation length, duration of maternal investment (age at weaning) and growth rate to weaning independent of body size. Theoretical analyses by Charnov (1991; Charnov and Berrigan, 1993) emphasise the importance of mortality in determining the switch between individual investment in growth and investment in reproduction. These 'strategies for maturation' (e.g. Pagel and Harvey, 1993) appear to be sensitive to the resources available for growth and the risks of mortality, and also may select for adult body size itself, an argument recently developed by Koz-lowski and Weiner (1997).

Janson and van Schaik (1993) have explored the concept of ecological risk in relation to the evolution of primate juvenile periods through mortality induced by food shortages imposed by the physical or social environment. Although their hypotheses relate specifically to the post-weaning period, these illustrate the importance of ecological variation affecting growth rates among primates and touch on the issue of predation avoidance as a specific problem for the smaller-bodied immatures.

There are, as yet, few data to test the relationship between growth, weaning ages, environmental variability and mortality among primates. The original study is that of Ross (1988; see also Chapter 4), which notes the influence of ecological predictability on reproductive rates and mortality among primates. Further support for the concept that ecological variation mediates species growth patterns has been provided by Leigh's (1994a) finding that folivorous primates have rapid growth over a short duration in comparison to frugivores. Among New World primates, several studies have noted the sensitivity of interbirth intervals (Fedigan and Rose, 1995) and maternal investment and allocare (Tardif, 1994; Ross and MacLarnon, 1995) to ecological variability or risk. Growth rates among small New World monkeys are unrelated to foraging risks but may be sensitive to predation risk, at least for squirrel monkeys (Garber and Leigh, 1997). Differences in growth rates among apes, again, may be a function of the degree of ecological risk or of energy derived from the diet (Leigh and Shea,

1996). In general, the overall pattern appears to suggest that risky environments, either through predation or unpredictable variation in food supply, should maximise growth rates at some cost to the mother in terms of future reproduction.

Estimates of infant mortality were not available for the interspecific sample examined here, but when a general predation risk category was assigned (Hill, 1995; Hill and Lee, 1998), relative birth mass was greater under high risks (ANOVA, F = 3.27, df = 1, p = 0.05), while relative weaning mass tended to be lower (ANOVA, F = 2.8, df = 1, p = 0.075) (Fig. 5.4A). However, neither relative growth rates nor relative duration of lactation were associated with predation risk. Thus, a mass strategy may play a greater role in predation risk aversion than does a time strategy.

When growth variables were compared between Ross' (1988) dichotomy of predictable or unpredictable environments, there were some slight effects of environment on the residual growth rate (F134 = 2.0, p = 0.17) and residual brain growth rate (F19 = 3.9, p = 0.08; Fig. 5.4B), with higher relative growth rates when environments were unpredictable. There was also an interaction with predation risk for relative brain growth (F2>9 = 9.44, p = 0.013), with rapid relative brain growth in unpredictable environments with high predation, and low relative brain growth in predictable environments with low predation. The sample size, however, is too small to reach any definitive conclusions. Relative growth rate also appeared to be lowest in predictable environments with low predation risks, and highest in unpredictable environments with high predation risks (Interaction F12 = 2.45, p = 0.102; Fig. 5.4C). Although crude, grossly over-simplistic, and of low significance, there is at least some suggestion that environmental risk affects primate growth strategies - with predation influencing mass, while environmental quality affects the tempo of events, as suggested by Leigh (1994a).

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