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Plenty of Room at the Bottom?

Tiny animals solve problems of housing and maintaining oversized brains, shedding new light on nervous-system evolution

William G. Eberhard, William T. Wcislo

Problems Measuring Behavior

The idea that grade changes are associated with differences in behavioral capabilities in different species stems from an assumed correlation between brain size and behavioral capabilities. Comparative studies have often been confounded by the use of imprecise, difficult-to-define behavioral metrics such as intelligence. And an important question remains unanswered: How do we quantify and compare behavior in biologically meaningful ways across different taxa? The size of an animal’s behavioral repertoire has sometimes been used as a quantitative measure of a species’ behavioral complexity. This intuitively appealing idea suffers from several problems. In a pioneering study relating behavior to head and brain size in ants, Blaine Cole, now at the University of Houston, highlighted some of them. Such a metric relies on subjective decisions to distinguish specific behaviors, and faces a problem common in artificial classification systems. Observers who are “splitters” will recognize a larger number of behaviors than those who are “lumpers.” In addition, repertoire comparisons rely on a number of unverified assumptions: that each behavior is equally demanding in terms of neural system processing, that behaviors called the same thing in different species are equally demanding and that rare behaviors, which are more likely to be missed by observers, are not drivers of brain evolution. It’s also assumed that the speed and precision with which a given behavior is performed is the same in different species and that the environmental influences shaping behavioral expression are minimal. It also makes the unlikely supposition that laboratory colonies will reveal the full repertoire of important behaviors.

These problems have led some researchers to adopt other metrics, such as the frequency of mistakes when making decisions, or the degree of precision in adjusting behavior to other variables. These traits can be compared more consistently across diverse species. Behavioral precision, the ability to accurately and consistently reproduce the same behavior, has been hypothesized to be less developed in relatively small-brained animals. Mistakes or imprecision might arise in smaller animals in several ways. For one, they have fewer sensory receptors, and thus should have decreased sensory input and hence less reliable information about the environment. They have less thorough processing of sensory inputs because of fewer interneurons or dendrites. Motor output or coordination among different limbs may be compromised by reduced feedback from proprioceptors, which sense stimuli from within a body, or from increased noise in the nervous system. The available data from tiny orb weaving spiders do not suggest behavioral limitations and are not consistent with the size-limitation hypothesis. Tiny spiders are morphologically modified to house a relatively enlarged brain, suggesting that they have adopted strategies consistent with the over-sized brain alternative we have described. The generality of this finding is currently unknown, however, because of the lack of comparative data. Other behaviors have not yet been thoroughly explored in spiders and other tiny animals. One that might be meaningfully compared among different species is the ability to learn and remember different types of lessons.

Finally, the use of overly inclusive measurements, such as overall brain size, rather than measurements of regions involved directly in behavioral tasks, can confound comparisons among species. Bats, for example, rely on hearing to a greater extent than we do. Due to body size differences, our subcortical auditory brain region is vastly larger than that of bats, so overall size is not informative. Relative size, however, reveals that the subcortical auditory region of the bat brain comprises 1.6 percent of total brain volume, versus 0.015 percent in humans. The problem of associating behavior with particular brain regions is exacerbated by cultural differences among scientific disciplines. Studies on behavior often take a comparative approach and include data from diverse species. Neurobiological studies are more often focused on a very small number of so-called model organisms that are studied under laboratory conditions, where they express a much smaller range of behaviors than in nature. Indeed, one recent study showed that approximately 75 percent of the research efforts of neuroscientists, as judged by numbers of publications, were directed at only three species—the mouse, the rats, and the human. When compared with a recent estimate of 7.7 million animal species worldwide, that is about 3.9 x 10-5 percent of animal biodiversity.

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