INTRODUCTION

Many studies of animal behavior and ecology implicitly presume that metazoans possess the ability to obtain, process, retain, and act upon information about the spatial properties of their environment, including the presence and location of resources, potential mates or competitors, and possible predators. For example, the habitat selection models described by Pulliam and Danielson (1991) assume that individuals are capable of finding the best available site among an array of choices.

In particular, foraging theory seeks to predict an animal's behavioral choices, based on its knowledge of resource availability, competition, and predation risk (Kramer 2001; Leighton, 2002; Koy and Plotnick 2007). Foragers are hypothesized to continuously compare the net energy gains and costs of continuing to forage in a currently exploited patch with those associated with searching for or moving to another patch. The resulting movements, and the potential corresponding traces, are largely a consequence of interplay of the spatial structure of the environment and the organism's ability to perceive this structure. Foraging traces, as used here, are produced both by exploiting a patch and by locating and moving to a new patch (i.e., they could include both repichnia and pascichnia).

Although vision is important in many organisms, the principal means by which marine animals of all sizes obtain this information is through chemoreception (Phillips 1978; Weissburg 2000; Riordan and Lindsay 2002). The detection of chemicals, their discrimination, and the behavioral reactions they evoke may well be the most primitive of all activities of living organisms.

Recent molecular and neurobiological studies of chemoreception have identified striking similarities in the cellular and neurobiological mechanisms of odor detection and transduction in diverse metazoan taxa, including vertebrates, arthropods, terrestrial gastropods, echinoids, and nematodes (Hildebrand and Shepard 1997; Eisthen 2002; Gaillard et al. 2004; Ache and Young 2005, Raible et al. 2006). These similarities include the functional anatomy of olfactory receptor (OR) neurons, the use of G protein-coupled receptors with seven membrane spanning domains as odorant receptors, the pathways used for olfactory signal transduction, and the nature of odor coding by receptors.

Chemoreception can be divided into contact chemoreception (also called: near-field, gustatory, or taste), in which the organism is in direct physical contact with the source of the chemicals, and distant chemoreception (also called: far-field, olfactory, smell), where chemicals (odorants) are transported through a medium to the chemosensory cells. For example, asteroids may use distant chemoreception to locate and discriminate among food sources (Brewer and Konar 2005; Thompson et al. 2005), but also employ contact chemoreception for choosing among prey items (Beddingfield and McClintock 1993). Similarly, sessile deposit feeding spionid polychaetes respond both to dissolved chemicals and to chemicals bound to particle surfaces (Riordan and Lindsay 2002).

The spatial pattern of odor distribution has been termed the "odor landscape" (Atema 1996; Moore and Crimaldi 2004). Chemicals produced by odor sources, usually due to the metabolic activities of organisms, are transported and mixed by diffusion and turbulent fluid movement. The concentrations of odorants that reach chemoreceptors depend both on the location of these sources and the nature of fluid flow between the sources and the sensing organism.

Studies of the fluid biomechanics of chemoreception have shown that scale is clearly important in how organisms perceive and move within odor landscapes (Ache and Young 2005; Moore and Crimaldi 2004; Koehl 2006). In general, microscopic organisms are in a physical realm where the odor landscape is relatively simple; resource detection and body movement are controlled by diffusion and viscosity. They react only to changes in concentration gradients experienced over time (Fenchel 2002) and move their entire bodies to detect changes in concentrations. For example, the bacterium E. coli moves through a combination of straight-line "runs" and random "tumbles," with tumbles producing a slight bias in the forward direction (Berg 2000). By increasing the length of runs, the cell can move up a chemical gradient. Smaller protozoa show similar behavior (Blackburn and Fenchel 1999). Small and simple organisms also usually have "taste" and "smell" combined, rather than separate as in more complex organisms (Ache and Young 2005).

In contrast, larger organisms, such as lobsters or snails, are in a physical realm where chemical detection and movement are controlled by turbulence and thus by spatially and temporally complex odor plumes. The "odor landscape" at these scales is thus complex and dynamic (Atema 1996; Moore and Crimaldi 2004), with odor sources potentially being located at a considerable distance from the organism. Organisms generally react to changes in concentration over space, using sensory organs that are often bilateral and are moved to detect changes in concentrations in the odor plumes and to increase the rate of fluid flow past them (Webster et al. 2001).

Although little studied, it is likely that the odor landscape for mobile infaunal organisms is also dominated by movement within chemical gradients, since they are not exposed to turbulent flow conditions. Movement in chemical gradients by the soil nematode C. elegans is characterized by straight runs and reorienting turns (Pierce-Shimomura et al. 1999). As in bacteria, the number of turns decreases as an animal moves up a gradient. Experiments with spionids by Riordan and Lindsay (2002) also suggest that contact chemoreception with sediment particles is important for infaunal forms.

In this paper, I describe a simulation model for foraging that demonstrates the importance of distant chemoreception in spatially complex and patchy environments. These results are then discussed in the context of changes in environmental complexity and animal evolution associated with the Ediacaran-Cambrian transition.