The incredible nonshrinking carnivores

The "island rule" is the prediction that small bodied animals should evolve larger sizes on islands, while large bodied animals should evolve to be smaller. Carnivores include a large range of sizes, from the "small" species that are supposed to evolve larger body sizes on islands, up to the "big" species that are supposed to shrink. Shai Meiri et al. (2005) studied the body sizes of carnivore faunas on islands compared to the sizes and degree of isolation of the islands, to see if they followed these predicted patterns.

They don't.

There is no systematic relationship in either direction. Small carnivores, like weasels, do not increase in body size on islands. Large carnivores, like wolves and bears, do not decrease. Some exceptions have long been known -- for example, the Kodiak bear is substantially larger than continental brown bears. But Meiri et al. (2005) found no predictable relationship for carnivores at all.

That might be informative as a test for the mechanisms of island dwarfing (or island gigantism). One of the proposed mechanisms of dwarfing is lack of predation -- a factor that is much less important for large carnivores than for large herbivores. So the lack of systematic dwarfing among large carnivores suggests that a reduction in predation rates may in fact important to body size selection on large island herbivores.

Raia and Meiri (2006) went farther with these observations, proposing that a reduction in predation rates made it possible for island herbivores to reproduce successfully at a smaller body size. Additionally, a reduced investment in growth makes it possible to invest more in reproduction. If true, then it is not the limits to resources that select for smaller body size, but the direct advantages of faster reproduction. Here is their abstract:

The island rule is the phenomenon of the miniaturization of large animals and the gigantism of small animals on islands, with mammals providing the classic case studies. Several explanations for this pattern have been suggested, and departures from the predictions of this rule are common among mammals of differing body size, trophic habits, and phylogenetic affinities. Here we offer a new explanation for the evolution of body size of large insular mammals, using evidence from both living and fossil island faunal assemblages. We demonstrate that the extent of dwarfism in ungulates depends on the existence of competitors and, to a lesser extent, on the presence of predators. In contrast, competition and predation have little or no effect on insular carnivore body size, which is influenced by the nature of the resource base. We suggest dwarfism in large herbivores is an outcome of the fitness increase resulting from the acceleration of reproduction in low-mortality environments. Carnivore size is dependent on the abundance and size of their prey. Size evolution of large mammals in different trophic levels has different underlying mechanisms, resulting in different patterns. Absolute body size may be only an indirect predictor of size evolution, with ecological interactions playing a major role.

A population that reproduces at a smaller body size can maintain a faster intrinsic rate of growth, all other things being equal. Raia and Meiri note that life history selection and resource limitation are not mutually exclusive. In fact, if resources were globally reduced, it would not alter the prediction that smaller body size would be favored under a tradeoff regime with reduced predation. It might intensify this selection in contrast to a continental area with low predation, or a larger island with low predation, however, leading to an area effect.

The discussion of this paper includes a consideration of islands, including Sicily and Sardinia, which prehistorically had multiple faunas with different size characteristics. In these and other examples of repeated colonizations, the size evolution of the large herbivores appeared to be determined by the effect of competition from other herbivores and predation by carnivores:

First, in cases of repeated colonization of the same species in different islands, size change follows the competition/predation regime regardless of phylogeny. Second, island identity and hence its area, isolation, and, arguably, total resources are not significant predictors of ungulate size evolution. Admittedly, we did not test explicitly for the effect of island area and isolation in fossil ungulates because these data are not available in most cases. Yet, it is worth noting that elephants from Crete (8300 km2), Cyprus (9200 km2), Rhodos (1400 km2), Sicily (25,700 km2), and Tylos (61 km2) were of comparable size although these islands are (and certainly were) different in area by more than two orders of magnitude. In addition, the two youngest Crete deer, living along with at least four other deer species, were larger than their mainland counterparts, although inhabiting a relatively small island (Raia and Meiri 2006:1738).

Carnivores have body size adaptations that are highly dependent on the actual prey animals present. Raia and Meiri note that carnivores that rely on abundant energy-dense resources like salmon runs exhibit gigantism wherever they live, while carnivores that lose a large prey animal on islands apparently dwarf (they give the example of island foxes that dwarfed on the Channel Islands in the absence of rabbits). In other words, carnivores have body size adaptations that relate more strictly to their prey-finding and hunting ability, while herbivores scale in ways that reflect their ability to use low-quality resources in competition with smaller, more selective herbivores.

Hence, for a carnivore, isolation on an island is a roll of the dice. The carnivore might end up on an island where its large prey species are absent, and shrink. Or it may end up losing its larger carnivore competitors and adopt a larger prey size, or gain access to rich food sources that would be dominated by larger carnivores in other contexts.

Of course, as for most hypotheses, the devil is in the details. With so many factors here to compare, it is probably no wonder that a combination could be found to explain the variance in sizes on different islands.

What I find most compelling about their account is that they can explain why the same herbivores evolved differently on the same island in successive colonizations. The interdependence of competition, predation, and life history tradeoffs also makes the theory more extensible to continental faunas with different local mixes of species or resources. They posit an ordering to the evolution of small size in herbivores colonizing islands:

Our data suggest that body size on islands evolves according to prevailing ecological conditions. In Pleistocene Mediterranean islands, there were several cases of a mainland species repeatedly colonizing islands. SR varied from 0.23 to 0.82 in E. antiquus, from 0.6 to 1.35 for the C. elaphus, from 0.47 to 0.91 for Praemegaceros verticornis, and so on. Similarly, SR often varies in carnivores on different islands (e.g., in Paradoxurus hermaphroditus it ranges from 1.1 to 0.88). The direction of this variation agrees with the influence of biological interactionmainly competition in the case of ungulates and resource base in the case of carnivoresand contradicts the notion of an optimal size. Instead, smaller sizes may be selected for in insular ungulates because resources that are no longer needed for antipredator behavior and interspecific competition can be safely reallocated to reproduction (Brown 1995; Raia et al. 2003; Lomolino 2005), resulting in lower adult body mass (Roff 2000; Stearns et al. 2000; Charnov 2001). However, once the smallest size classes were occupied, new species evolved larger body size. This should be not viewed as maladaptive. We argue that species arriving later simply faced different conditions, for which the size they attained was probably adaptive (Case 1978). Indeed, larger size allows the inclusion of new (lower quality but often superabundant) resources, at least in herbivores (Demment and Van Soest 1985; Illius and Gordon 1992; Clauss and Hummel 2005). Competition with smaller species is thus reduced. The only clear disadvantage of larger-sized ungulates seems to be an extended growth period (Raia and Meiri 2006:1739).

This "ordering" effect in colonization and body size should be testable with reference to fossil samples (it is consistent with the samples from Mediterranean islands that they apply in this paper).

So if this general hypothesis is correct, then not only the fact of dwarfing, but also the extent of dwarfing is informative about the ecology of particular islands. Where there is a paleontological record, it should be possible to identify the important competitive interactions leading to body size adaptations. Also, the order of arrival may be very important to ultimate body sizes in the evolving fauna.

References:

Meiri S, Dayan T, Simberloff D. 2005. Area, isolation and body size evolution in insular carnivores. Ecology Letters 8:1211-1217. doi:10.1111/j.1461-0248.2005.00825.x

Raia P, Meiri S. 2006. The island rule in large mammals: paleontology meets ecology. Evolution 60:1731-1742. doi:10.1554/05-664.1