The evolution of the first complex neural systems occurred in a sensory world defined by chemosensory stimuli. Despite its universality across the animal kingdom, the strategies animals use to sample for odors and orient using odors is still not clear. Odor plumes are complex structures. How animals sample their environment for odor stimuli, make decisions, and ultimately find an odorant using their sense of smell has been studied more in invertebrates and birds than mammals, yet olfaction is critical for most mammals, even humans. This dissertation will analyze the orientation and sampling strategies in two species of mammals that differ in their olfactory capacity yet are known to use odors to orient in space. It will examine olfactory navigation in both naturalistic conditions and controlled studies to understand how environmental conditions, individual differences, and olfactory cues affect search strategies, navigation behavior, and sampling behavior.

Chapter One addresses the nature of odors and olfaction, the structure of odor plumes, and a summary of our current knowledge of animal strategies for olfactory navigation through odor plumes. It also discusses how individual differences, such as sex differences and spatial cognitive abilities, may affect olfactory discrimination and subsequently, orientation.

Chapter Two investigates how a species known to be expert in olfactory navigation, the domestic dog, oriented to the outdoor scent trail of a hidden person. Search and rescue dogs were adept at following odor trails to a target person despite a number of meteorological factors affecting odor dispersion along the trail. Meteorological data collected along the odor trail revealed that hot temperatures, low humidity, and high wind speeds caused odors to disperse quickly and widely. Under these conditions, dogs searched farther from a person’s original trail. Studying the dogs’ behavior as they followed the odor trail also revealed that dogs were more likely to sample the air for odors when moving at high speeds. Some results suggested that they slow their speed and searched the ground for odors when they lost contact with the odor plume. This study demonstrated the ease in which animals can track odors over great distances to their source.

Chapter Three describes an experiment with humans that examines sniffing behavior modulation during olfactory navigation. In this experiment, humans in an indoor setting varied their sampling behaviors in response to spatial distance from an odorant as well as to stereo olfactory cues. People sniffed less frequently and longer while initially searching for the odor plume. After detecting the odor, people casted, a behavior characterized by zig zagging trajectories, when they were attempting to definitively locate the odor plume. Once the plume was found and they were following it to the source, they sniffed more frequently and had shorter sniffs. Overall, as people approached the source of the odor, sniffing intensity increased. Sniffs were always slower, shorter, and less intense when using stereo olfaction than when one nostril was blocked. Women also detected odor plumes earlier than men. This is the first study to show people modulate their sniffing patterns while navigating an odor plume.

The final experiment in Chapter Four asked whether people have a mental prototype of an odor plume’s structure. People’s movement patterns and sampling behavior were recorded as they interacted with a virtual odor plume in a virtual environment. This study revealed that people treated the virtual plume as if it were a real odor plume and exhibited similar behaviors as in the real world experiment in Chapter Three. People sampled more frequently while they searched for the stimuli, less frequently when they were following the virtual odor, and then increased their sampling frequency again if they lost contact with the stimuli. People were sensitive to as little as a 1% drop in stimulus intensity, to which they reacted by correcting their trajectory to pursue an increasing stimulus gradient instead. They were also able to successfully modulate their sampling behavior when using stereo or non-stereo cues. Overall, men performed better at this task, meaning they were able to estimate the origin of the virtual odor with higher accuracy than women.

This body of work is one of the first to investigate mammalian odor navigation. It shows that mammals have many strategies to modulate their sampling and orientation behavior to account for meteorological factors, loss of stereo cues, and individual differences. The dissertation concludes with a discussion of these three complementary experiment and suggested future studies.

Caching is the movement and storage of food items by animals for future use. Caching facilitates survival during periods of scarcity, may reduce foraging time during future searches for food, and allows animals to take advantage of periods when available food exceeds current needs. Scatter-hoarding animals store one item per cache, and must employ cognitive strategies to protect their caches. These strategies include assessing the relative value of food items, carefully hiding food items, deceptive behaviors to thwart potential pilferers, and remembering each cache location. Such decisions should be driven by economic variables, such as the value of the individual food items, the scarcity of these items, and competition and risk of pilferage by conspecifics.

My dissertation begins with a general overview of the food-storing literature and the natural caching behavior of the scatter-hoarding fox squirrel (Sciurus niger). I then describe several experiments that explored the decisions fox squirrels make when storing food. A study examining how fox squirrels adjust effort assessing and caching food based on the food item’s value (weight, perishability and nutritional content) using two different foods, hazelnuts and peanuts, is described in Chapter 2. Squirrels (n = 23) were observed during natural periods of food scarcity (summer) and abundance (fall). Assessment and investment per cache increased when resource value was higher (hazelnuts) or resources were scarcer, but decreased as experimental sessions continued. This study showed that fox squirrels’ assessment and caching behaviors were sensitive to both daily and seasonal resource abundance.

Another important problem facing scatter-hoarding animals is how to maximize the retrieval of stored food items while minimizing the risk of pilferage by competitors. One defense against theft could be the spatial placement of caches. I describe a study examining whether the spatial distribution of caches is dependent on nut species in Chapter 3. I measured four key variables of the cache decision: distance and direction traveled, the use of distinct cache areas by nut species, and density of caches. Fox squirrels (n = 48) were tested in 50 sessions, and the geographical coordinates of over 900 cache locations were recorded. Results suggested that squirrels distribute caches using three heuristics: matching the distance traveled before caching to the value of the food item, systematically covering a caching area, and matching cache density to minimize pilferage risk to the highest valued food items. Squirrels spatially chunked their caches by nut species, but only when foraging from a single location. This first demonstration of spatial chunking in a scatter-hoarder underscores the cognitive demand of scatter-hoarding.

I describe a final field study in Chapter 4. A pilot study revealed that there was a high level of pilfering (25%) among a population of fox squirrels. Nineteen fox squirrels cached 294 hazelnuts with passive integrated transponder tags implanted in them. Variables collected included assessment and cache investment and protection behaviors; cache location, substrate, and conspicuousness of each cache; how long each cache remained in its original location, and the location where the cache was finally consumed. polymer chain reaction (PCR) analysis of hair samples obtained from 14 of the subjects was used to determine relatedness among this group of squirrels, and its potential impact on behavior. Results suggest that cache protection behaviors and the lifespan of a cache are dependent on the conspicuousness of a cache. Squirrels may mitigate some of the costs of pilfering by caching closer to the caches of related squirrels than to those of non-related squirrels.

In Chapter 5, I describe a model of the antagonistic relationship between food storing animals and their competitors using agent-based simulations where caching, memory size, and pilfering co-evolve. During periods of food abundance and scarcity, individuals could consume or store found items, retrieve old caches, or pilfer others’ caches. In the absence of pilfering, selection is strongest for longer memory. As pilfering increases, shorter memory may be more adaptive, because old caches are likely to be depleted. Contrary to common thought that social interactions enhance cognition, these findings demonstrate how competition may constrain rather than promote some cognitive abilities.

Finally, in Chapter 6, I argue that my research demonstrates that food assessment and cache investment strategies of fox squirrels represent a complex suite of behaviors. These behaviors allow squirrels to maximize the benefits of periods of excess food in the environment, while increasing the likelihood of retrieving nuts later, when food in the environment is scarce. Competition via pilfering influences these food-storing decisions and outcomes, and in some cases, may impair the cognitive abilities of food-storing animals. I discuss the overall implications of this work, and potential directions for future research.

Dogs (Canis familiaris) are strongly responsive to human influence in general, and they also readily form preferences for specific humans, yet these lines of inquiry have not often been combined. The goal of this dissertation was to advance a more specific theory regarding the nature of the dog-human bond - that it is one characterized by dependency - and to investigate whether such bonds would influence dogs to use social strategies to solve non-social problems.

In Chapter 1, I describe the features of the relationship between the dog as a species and humans, and how this inter-species relationship is reflected in the dog's attentiveness to humans and tendency to solve problems by attending to human behavior. After describing the dog's abilities in this domain, I go on to explore the phenomenon from the perspective of two of Tinbergen's four levels of analysis: phylogeny and ontogeny. To do this, I compare the dog's reading of human social cues with that of related canid species, and I then explore within-species differences among canines. Finally, I advance a new theory that dogs can be described as uniquely dependent on humans, and I explore various specific situations in which this dependency can explain the dog's problem solving strategy choices.

In Chapter 2, I explore experimentally whether the presence of social information provided by familiar versus unfamiliar humans would influence the dog's performance when choosing between two potential food sources. This study included a number of conditions; in some conditions, a familiar person indicated a container that gave food and a stranger indicated a container that did not; in other conditions this was reversed. Results show that dogs consistently chose the container indicated by or nearest to their owner, even when this container never yielded a food reward. In contrast, in two other conditions, dogs chose at chance: a control condition in which both humans were strangers, and a condition in which the owner and stranger sat reading books and provided no social signal to the dog. These results support the dependency hypothesis in showing that the dog's performance is either facilitated or hindered, depending on whether a familiar human provides accurate or inaccurate signals.

In Chapter 3, I explore the boundary conditions of the effect of familiarity on dogs' performance when choosing between potential food sources, by examining whether a brief period of familiarization with a new person would be enough for a dog to establish a preference for that person's social signal over that of a stranger. Results were not significant; some individual dogs showed a preference for a food container indicated by the familiar person, whereas others did not, but this effect was not significant at the group level. Future studies should incrementally increase the period of time used to familiarize the dog and the new person, to establish how long it takes for such a preference to form in the dog. Such findings would establish whether dogs can quickly become influenced by the information of a familiar person, without that particular dog needing to be in a state of actual dependency on that particular person, or whether dogs need a longer time period, and an actual level of dependence on a person, for this effect to occur. If actual dependency is not required, this would indicate that dependent-like responses in dogs are an automatic part of their responsiveness to familiar people, owing to such a strategy having resulted in fitness benefits over the history of the species, regardless of whether those familiar people actually materially provision the dog.

Finally, in Chapter 4, I explore the influence of variations in the relationship between specific dogs and owners on the dog's food-choice strategies by examining whether "closeness to owner" could predict the strength of the dog's preference for a food container indicated by the owner, among dogs tested in Chapters 2 and 3. I measured closeness by creating an owner-report survey which owners completed online. Factor analysis of a large community sample of owners revealed that this set of questions yielded two discrete scales: Owner-Initiated Closeness and Dog-Initiated Closeness. I examined correlations between these two scales and the performance of dogs tested in the previous chapters. Results were generally not significant; closeness scores did not explain variation in the strength of the dog's preference for their owner's signal. Future studies should explore more detailed ways of measuring closeness (e.g., by observing dogs and owners in their homes), and should examine whether dependence specifically, rather than closeness, might better explain differences in performance between dogs.

Laboratory mice are the most commonly studied mammal today and they are frequently used as models of human disease. In the last decades, the mouse has become a popular model for understanding genes, brains and behavior. Therefore, it is of great importance that we develop a detailed understanding of the cognitive phenotype of the animal that we so frequently utilize in the laboratory. Sex differences are an important consideration in this phenotype. Sex differences in spatial behavior are seen in a number of species, suggesting a male advantage in all things spatial and a female advantage in object recognition memory. These data are consistent among humans and rats, but inconsistent in the mouse. The goals of this study were to discover whether mice would exhibit similar sex differences in a series of tasks designed to assess cue use at different spatial resolutions. The first experiment offers an assessment of cue use in a navigation task. Specifically looking at the use of geometry and large distal cues in the testing environment. The second experiment looks at the details of object recognition. The last experiment tests both object recognition and location memory, to look more closely at the nature of the sex difference with respect to proximal cues. We housed the mice in conditions that were more ethologically valid to allow a better comparison of our data to humans, as well as enriched laboratory animals and wild caught animals that must organize their behavior in much more complex environments than those provided in the lab. The navigation task revealed a male reliance on geometry and a female flexibility in the use of multiple sets of cues. The standard object recognition tasks all demonstrated a female advantage in discriminating the novel from the familiar object. Female mice distinguished novel from familiar objects when these objects had many similar features, while male mice only discriminated between them if the objects were unlike one another. Frequently, female mice also exhibited greater attention to the objects. The male mice demonstrated an advantage only when the change provided new directional information. The female mice displayed evidence of attention to the relationships between unique cues and the features encompassed within them. This is consistent with current literature on rats and humans and suggests that mice also exhibit sex difference in cue use strategies. This suggests that, with attention to ethologically valid housing and testing, mice are an appropriate model of mammalian behavior and cognition.

Spatial memory is critical to the survival of all mobile animals. Using spatial memory animals find and keep valuable resources such as shelter, food and companionship. In a series of three studies, I explored spatial strategies and the use of multiple landmarks from comparative, computational and developmental perspectives.

In the first study, I examined the spatial strategies and landmark use of a diurnal mammalian species, the fox squirrel, Sciurus niger. Free-ranging fox squirrels showed a large degree of flexibility both in their use of landmarks and in their use of spatial strategies. Furthermore, their use of landmarks appeared to be sensitive both to changes in the test apparatus and the season in which they were tested. In the second study, I further explored fox squirrel spatial strategies from a computational modeling perspective. Given the squirrels' use of the majority strategy, we specifically investigated the suitability of using a Bayesian model to characterize the squirrels' spatial decisions. The resulting model provides a unifying framework for illustrating different strategies of landmark integration, and a tool for investigating the circumstances under which particular landmarks are used. I show that the best fitting models changed depending on the season at testing and the details of the task. These analyses support my previous claims that squirrels adopt flexible strategies in landmark use.

In the third study, I investigated whether human children develop similar flexible spatial strategies as the fox squirrels and what types of allocentric landmarks they might be using to construct such spatial strategies. In particular, we were interested in the initial development of such strategies when children first begin to use non-coincident, allocentric landmarks. Thus, all studies were conducted using 3 and 4 year old children since it is at this age that children begin to robustly use non-coincident, allocentric landmarks. I found that 3 year old children rely on a less flexible, hierarchical strategy based on their preferred landmark, but that by four years of age they begin to develop more flexible spatial strategies, similar to those of adult free-ranging fox squirrels.

In sum, both behavioral data and the results of Bayesian modeling support the conclusion that a free-ranging diurnal, mammal uses a flexible, spatial strategy to orient in its environment and that environmental factors may change the expression of such a strategy depending both on the season and properties of the experimental apparatus. At the age of four, human children have begun to develop similar flexible strategies, not long after they have begun to use non-coincident, allocentric landmarks. These results, taken together, suggest that both humans and animals have developed similar strategies to deal with spatial problems and that these strategies develop along with use of more distal landmarks in human children.