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Using Pharmacological Manipulation and High-precision Radio Telemetry to Study the Spatial Cognition in Free-ranging Animals

An animal&#39;s ability to perceive and learn about its environment plays a key role in many behavioral processes, including navigation, migration, ...

Washington College

Pitvipers (Viperidae: Crotalinae) possess unique sensory organs, the facial pits, capable of sensing subtle fluctuations in thermal radiation. Prey acquisition has long been regarded as the sole function of the facial pits. However, the ability to sense thermal radiation could also direct thermoregulatory behavior by remotely sensing nearby surface temperatures. Using a series of behavioral arenas of varying spatial complexity and ecological relevance, we surveyed the ability of the western diamondback rattlesnake Crotalus atrox to direct successful thermoregulatory movements with either functional or disabled facial pits. We found that western diamondback rattlesnakes could base thermoregulatory decisions on thermal radiation cues when their pits were functional, but not when blocked. Our results indicate that the facial pit is part of a generalized sense, and suggest thermoregulation as an alternative hypothesis to prey acquisition for the origin of facial pits.

Thermoregulation is the pits: use of thermal radiation for retreat site selection by rattlesnakes.

Pitvipers (Viperidae: Crotalinae) possess thermal radiation receptors, the facial pits, which allow them to detect modest temperature fluctuations within their environments. It was previously thought that these organs were used solely to aid in prey acquisition, but recent findings demonstrated that western diamondback rattlesnakes (Crotalus atrox) use them to direct behavioral thermoregulation, suggesting that facial pits might be general purpose organs used to drive a suite of behaviors. To investigate this further, we conducted a phylogenetic survey of viperine thermoregulatory behavior cued by thermal radiation. We assessed this behavior in 12 pitviper species, representing key nodes in the evolution of pitvipers and a broad range of thermal environments, and a single species of true viper (Viperidae: Viperinae), a closely related subfamily of snakes that lack facial pits but possess a putative thermal radiation receptor. All pitviper species were able to rely on their facial pits to direct thermoregulatory movements, while the true viper was unable to do so. Our results suggest that thermoregulatory behavior cued by thermal radiation is a universal role of facial pits and probably represents an ancestral trait among pitvipers. Further, they establish behavioral thermoregulation as a plausible hypothesis explaining the evolutionary origin of the facial pit.

Heat in evolution's kitchen: evolutionary perspectives on the functions and origin of the facial pit of pitvipers (Viperidae: Crotalinae).

It is commonly assumed that the facial pit of pitvipers forms relatively sharp images and can detect small differences in environmental surface temperatures. We have visualized the temperature contrast images formed on the facial pit membrane using a detailed optical and heat transfer analysis, which includes heat transfer through the air in the pit chambers as well as via thermal infrared radiation. We find the image on the membrane to be poorly focused and of very low temperature contrast. Heat flow through the air in the pit chambers severely limits sensitivity, particularly for small animals with small facial pit chambers. The aperture of the facial pit appears to be larger than is optimal for detecting small targets such as prey at 0.5 m. Angular resolution (i.e. sharpness) and image strength and contrast vary complexly with the size of the pit opening. As a result, the patterns of natural background temperatures obscure prey items and other environmental features, creating false patterns. Consequently, snakes cannot simply target the strongest signal to strike prey. To account for observed behavioral capabilities, the sensory endings on the pit membrane apparently must respond to temperature contrasts of 0.001 degrees C or less. While neural image sharpening likely enhances imaging performance, it appears important for foraging snakes to select ambush sites offering uniform backgrounds and strong thermal contrasts. As the ancestral facial pit was likely less sensitive than the current organ, objects with strong thermal signals, such as habitat features, were needed to drive the evolution of this remarkable sense.

The imaging properties and sensitivity of the facial pits of pitvipers as determined by optical and heat-transfer analysis.

The severity of the environment often influences animal cognition [1-6], as does the rate of change within that environment [7-10]. Rapid alteration of habitat places limitations on basic resources such as energy, water, nesting sites, and refugia [8, 10]. How animals respond to these situations provides insight into the mechanisms of cognition and the role of behavior in adaptation [11-13]. We tested the hypothesis that learning plays a role in the navigation of the painted turtle (Chrysemys picta) within a model of environmental change. We radiotracked experienced and naive turtles at different developmental stages from two different populations as they sought out new habitats when their pond was destroyed. Our data suggest that the ability of turtles to navigate is facilitated in part by experience during a critical period. Resident adults repeatedly used specific routes with exceptional precision, while translocated adults failed to find water. Naive juveniles (1-3 years old) from both populations used the same paths taken by resident adults; the ability to follow paths was lost by age 4. We also used laboratory behavioral assays to examine the possible cues facilitating this precise navigation. Turtles responded to manipulation of the local ultraviolet environment, but not the olfactory environment. This is the first evidence to suggest that learning during a critical period may be important for how animals respond to changing environments. Our work emphasizes the need for the examination of learning in navigation and the breadth of critical learning periods across vertebrates.

The role of age-specific learning and experience for turtles navigating a changing landscape.

We are currently experiencing shifts in climate at rates not previously recorded. One important aspect of this change is a tendency toward extremes--extremes in temperature and moisture, both within and among years. Numerous studies focus on the physiological consequences of environmental change, especially in terms of ectothermic taxa's thermal regime and use of habitat. For many species, though, cognitive responses may be a means of response to environmental perturbation. However, the effects of environmental change on the general mechanisms of cognitive processes and their implications for larger phenomena are seldom examined. Moreover, at a larger scale, we do not fully understand the features of the environment that might select for cognitive enhancements or their mechanisms, making us unable to accurately predict which species might experience the most severe response to environmental change and in which environments. This symposium brought together scientists from numerous disciplines to examine the role of cognition in how organisms cope with changing environments. We cover topics from the perspectives of the physiological mechanisms underlying and driving cognition to the complexity of individual behavioral responses in changing environments to emergent large-scale processes influencing species' abilities to respond to such change. Our ultimate goals are to explore how animals use cognition to cope with rapid environmental change, how such coping mechanisms "scale up" to affect ecological and evolutionary patterns, and how we might determine which features of the environment have been (and will become) most important for the conservation of biodiversity.

Thinking about Change: An Integrative Approach for Examining Cognition in a Changing World.

The ability to learn about the spatial environment plays an important role in navigation, migration, dispersal, and foraging. However, our understanding of both the role of cognition in the development of navigation strategies and the mechanisms underlying these strategies is limited. We tested the hypothesis that complex navigation is facilitated by spatial memory in a population of Chrysemys picta that navigate with extreme precision (±3.5 m) using specific routes that must be learned prior to age three. We used scopolamine, a muscarinic acetylcholine receptor antagonist, to manipulate the cognitive spatial abilities of free-living turtles during naturally occurring overland movements. Experienced adults treated with scopolamine diverted markedly from their precise navigation routes. Naive juveniles lacking experience (and memory) were not affected by scopolamine, and thereby served as controls for perceptual or non-spatial cognitive processes associated with navigation. Further, neither adult nor juvenile movement was affected by methylscopolamine, a form of scopolamine that does not cross the blood-brain barrier, a control for the peripheral effects of scopolamine. Together, these results are consistent with a role of spatial cognition in complex navigation and highlight a cellular mechanism that might underlie spatial cognition. Overall, our findings expand our understanding of the development of complex cognitive abilities of vertebrates and the neurological mechanisms of navigation.

Pharmacological evidence is consistent with a prominent role of spatial memory in complex navigation.

Animals inhabiting changing environments show high levels of cognitive plasticity. Cognition may be a means by which animals buffer the impact of environmental change. However, studies examining the evolution of cognition seldom compare populations where change is rapid and selection pressures are strong. We investigated this phenomenon by radiotracking experienced and naïve Eastern painted turtles (Chrysemys picta) as they sought new habitats when their pond was drained. Resident adults repeatedly used specific routes to permanent water sources with exceptional precision, while adults translocated to the site did not. Naïve 1-3 y olds from both populations used the paths taken by resident adults, an ability lost by age 4. Experience did not, however, influence the timing of movement or the latency to begin navigation. This suggests that learning during a critical period may be important for how animals respond to changing environments, highlighting the importance of incorporating cognition into conservation.

Article	Year
Thermoregulation is the pits: use of thermal radiation for retreat site selection by rattlesnakes. The Journal of experimental biology\| PubMed ID: 12819261	2003
Heat in evolution's kitchen: evolutionary perspectives on the functions and origin of the facial pit of pitvipers (Viperidae: Crotalinae). The Journal of experimental biology\| PubMed ID: 15531644	2004
The imaging properties and sensitivity of the facial pits of pitvipers as determined by optical and heat-transfer analysis. The Journal of experimental biology\| PubMed ID: 17690227	2007
The role of age-specific learning and experience for turtles navigating a changing landscape. Current biology : CB\| PubMed ID: 25578905	2015
Thinking about Change: An Integrative Approach for Examining Cognition in a Changing World. Integrative and comparative biology\| PubMed ID: 26113667	2015
Pharmacological evidence is consistent with a prominent role of spatial memory in complex navigation. Proceedings. Biological sciences\| PubMed ID: 26865305	2016
Turtles outsmart rapid environmental change: The role of cognition in navigation. Communicative & integrative biology\| PubMed ID: 27065017	2015

Aaron R. Krochmal

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