Richard G. Coss

Snake Mobbing By California Ground Squirrels: Adaptive Variation and Ontogeny

California ground squirrels (Spermophilus beecheyi) commonly live in association with and are the prey of snakes. Field observations indicate that encounters between the two may often include mobbing by the squirrel and defensive behavior by the snake. Our research had three goals : 1) to systematically observe and describe these mobbing interactions in both field and laboratory situations; 2) to compare in the laboratory the intensity of mobbing gopher, garter, and rattlesnakes by squirrels from two populations which encounter rattlesnakes (rattlesnake adapted), and one which does not (rattlesnake nonadapted) ; 3) to record and describe reactions to a garter snake by young snake-naive squirrels from rattlesnake adapted and nonadapted populations. We found the following. 1. Squirrels approached snakes, investigated them in elongate postures, bobbed their heads, flagged their tails, and sniffed snakes. Aggressively motivated squirrels kicked sand at the snakes, displayed lateral postures, pounced on, and bit them. 2. The stressful impact of this behavior upon the snake is documented by positive correlations between indices of mobbing intensity by squirrels and indices of defensive behavior by the snake. 3. Squirrels from both rattlesnake adapted populations mobbed snakes less intensely than the rattlesnake nonadapted squirrels. 4. The adult-like response of young snake-naive squirrels to a garter snake was significantly stronger than to a moving novel object, thus demonstrating that their response to the snake was based upon stimulus parameters other than novelty. 5. Snake-naive young from a rattlesnake adapted population mobbed less intensely than snake-naive young from a rattlesnake nonadapted population. 6. Snake-naive young mobbed more intensely than wild-caught adults. We proposed the following. 1. Snake mobbing may benefit ground squirrels by reducing the snakes hunting efforts in the area in which mobbing occurred. 2. The presence of venomous snakes increases the risk to the mobber, thereby favoring an adaptive attenuation in mobbing intensity. 3. Because young squirrels are often left at the burrow by foraging mothers, it is likely that first encounters with snakes often occur in the absence of adults. Under these conditions natural selection might favor predetermined epigenesis of the ability to recognize and respond appropriately to snakes. 4. Young snake-naive squirrels may not be as capable as adults of recognizing immobile snakes. Their enhanced response, relative to adults, to moving snakes may be an adaptive mechanism which permits the young to learn to recognize static snake form.

The function of dendritic spines: A review of theoretical issues

The discovery of dendritic spines in the late nineteenth century has prompted nearly 90 years of speculation about their physiological importance. Early observations that bulbous spine heads had very close approximations with the axon terminals of other neurons, confirmed later by ultrastructural study, led to ideas that spines enhance dendritic surface areas for making synaptic contacts. More recent application of cable and core-conductor theory to the anatomical study of spines has raised a number of new ideas about spine function. One important issue was derived from the theoretical treatment of spines as tiny dendrites with much higher input resistances than those of the larger parent dendrites. The high spine-stem resistance results in relative electrical isolation of the spine head; this causes large local depolarizations in the spine head. Several theoretical studies have also shown that if the spine-head input resistances are substantially higher than those of the parent dendrites, spines have the potential for modulating a host of biochemical and biophysical processes that might regulate synaptic efficacy. Empirical studies have documented that spine heads increase rapidly in size after afferent projections have been stimulated electrically and after animals have engaged in a single bout of ecologically important behavioral activity. Such spine head enlargement dilates the portion of the spine stem adjacent to the spine head and this process shortens the spine stem without appreciably altering overall spine length. Theoretical study shows that spine-stem shortening lowers the spine-head input resistance relative to the branch input resistance. This reduction in input resistance can enhance the transfer of electrical charge from the spine head to the parent dendrite, especially when the synaptic conductance is large relative to the spine-head input conductance. Spine-stem shortening also lowers the peak transient membrane potential in the spine head and this factor could delimit Ca2+ influx into the spine head via voltage-dependent Ca2+ channels. The modulation of Ca2+ influx by spine-stem shortening has the potential for regulating Ca2+-sensitive enzymatic activity in the spine head that could affect phosphorylation of cytoskeletal proteins maintaining spine shape and phosphorylation of proteins in the postsynaptic density. Finally, theoretical findings are described that examine the effects of voltage-dependent inward-current channels in the spine head and their ability to amplify the charge transfer due to transmitter-dependent synaptic conductances.

Rapid dendritic spine stem shortening during one-trial learning: The honeybee's first orientation flight

Our initial study of honeybees using the rapid Golgi method showed that dendritic spines on calycal interneurons had shorter stems due to spine head enlargement in bees with greater cumulative experience. This study sought to determine if spine stem shortening could be induced rapidly during the first orientation flight, a one-trial place learning event. Newly emerged bees were reared in a small broodless hive with a virgin queen and allowed to take their first orientation flight at 6 and 8 days of age. Spine profiles of 5 flyers and 5 non-flyers were traced in large scale using light microscopy and a modified camera lucida. Overall spine length and stem length were measured on these tracings using a digitizing tablet. Additional measurements of maximum spine head width, profile area, and perimeter were made using computer image analyses. Examining group differences in spine stem length as a function of overall spine length, our results revealed a clear association between rapid spine stem shortening and the first orientation flight lasting several minutes. This effect, however, was restricted to only the long spines. Flight-induced stem shortening was accompanied by elongated swelling of the spine head without an appreciable expansion of the spine perimeter.

Tiger decline caused by the reduction of large ungulate prey: evidence from a study of leopard diets in southern India

Populations of leopards and tigers in the Kalakad-Mundanthurai Tiger Reserve, India, appear to be declining. To identify the cause of this decline, we examined the diets and the relative densities of leopards and tigers, comparing scat from this park with that from the Mudumalai Wildlife Sanctuary, a park known to have high leopard and tiger densities. Results suggested that the leopard density in Mudumalai was approximately twice that in Mundanthurai. No evidence of tigers was found in Mundanthurai. Prey species found in leopard diets in the two parks was similar; albeit, mean prey weight and the proportion of large ungulates were markedly lower in the Mundanthurai leopard diet. These dietary differences are consistent with the infrequent sightings of large ungulates in Mundanthurai. Analyses of satellite data revealed that large areas of grazing land in Mundanthurai have shifted to thicket, reducing available forage for large ungulates. Since large ungulates constitute important tiger prey, the low density of ungulates in Mundanthurai might explain the apparent absence of tigers. Our findings suggest that the tiger population in the Kalakad-Mundanthurai Tiger Reserve could be enhanced via the application of habitat management for large ungulates.

Changes in morphology of dendritic spines on honeybee calycal interneurons associated with cumulative nursing and foraging experiences.

Using the rapid Golgi method, the morphology of dendritic spines was quantified in the calyxes of groups of newly emerged, nurse, and forager honeybees. These groups were studied because they represented distinct stages of behavioral development and cumulative experience which, according to recent vertebrate findings, may be associated with enlargement of the spine head and stem shortening. Measurements were made of spine density, overall spine length, stem length, maximum head width, and profile area using eyepiece micrometry and computer image analyses. The results indicated that none of the groups differed appreciably in spine density and overall spine length. Foragers did exhibit spines with markedly larger profile areas and shorter stems than those in newly emerged and nurse honeybees. However, nurses and foragers did not differ appreciably in spine head width, but both groups had markedly wider heads than the newly emerged group did. These findings suggest that elongated growth of the spine head and concomitant stem shortening is an incremental process affecting different portions of the spine population at different rates. In particular, the growth rate of most spines appears to accelerate during the foraging stage in which the diversity of sensory stimulation is greatest.

Resistance of California ground squirrels (Spermophilus Beecheyi) to the venom of the northern Pacific rattlesnake (Crotalus Viridis Oreganus): A study of adaptive variation

Recent studies have documented natural resistance to snake venom in a number of diverse mammalian species. The present paper documents for the first time variation in such resistance within one single species, the California ground squirrel (Spermophilus beecheyi). This species is a frequent prey of the northern Pacific rattlesnake (Crotalus viridis oreganus) in certain habitats. Venom resistance was tested directly in two populations of ground squirrels by injection of 1-40 mg/kg venom doses. One population was obtained from a habitat with a high rattlesnake density; the other population came from a rattlesnake-free habitat. Dramatic differences in the response to venom between these populations were manifested, based on a variety of criteria, such as mortality, necrosis and healing time. Resistance to venom was also examined by LD50 tests in groups of mice pre-injected with ground squirrel sera from three rattlesnake-adapted California populations and a non-adapted Arctic population (S. parryii) from snake-free central Alaska. The California ground squirrel sera were 3.3-5.3 times more effective in the in vivo neutralization of venom than the sera from Arctic ground squirrels. Moreover, the level of protection by the sera as reflected by the LD50 values was highly correlated (P less than 0.005) with the level of in vitro squirrel serum-venom binding as quantified by radioimmunoassay (RIA). A subsequent RIA revealed that binding levels of sera from 14 California ground squirrel populations correlated significantly (P less than 0.025) with local rattlesnakes densities; i.e. sera pools from populations sympatric with rattlesnakes exhibited the highest binding, whereas populations living in habitats where rattlesnakes are rare or absent typically exhibited the lowest binding levels, several of which approximated the Arctic control. Taken together, these results demonstrate intraspecific variation that is probably the result of differential natural selection due to northern Pacific rattlesnakes. This intraspecific variation should be taken into consideration when testing for natural resistance in wild-caught species.

Perceptual Determinants of Gaze Aversion By the Lesser Mouse Lemur (Microcebus Murinus), the Role of Two Facing Eyes

Captive lesser mouse lemurs (Microcebus murinus) were observed to avert their heads during face-to-face encounters. Based on evidence obtained from other vertebrate species, predominantly among the Primates, it was assumed that the facing orientation and direction of gaze of an adversary was the provocative agent eliciting gaze aversion by mouse lemurs. A more precise examination of the perceptual determinants of gaze aversion employed models presenting various combinations of eyelike concentric circles. Presented side-by-side in paired comparisons, it was predicted that a model presenting two horizontally placed concentric circles, which schematically resemble two facing eyes, would elicit less visual inspection, i.e., more visual avoidance, than models presenting less physiognomic arrangements of concentric circles. Using a special model-viewing apparatus, Experiment I examined the gaze behavior of 28 mouse lemurs in their peak activity period to determine the response-eliciting effectiveness of 5 models varying in the number of concentric circles. Experiment 2 examined 50 lemurs, some of which were in seasonally and artificially induced torpor. Three models differing in the spatial orientation of two concentric circles were investigated in an attempt to control for contour complexity. Both the bout frequency and duration of model fixation were measured using head orientation as the response criterion. The following results were obtained: 1. For the over-all paired comparisons in both experiments, the model presenting two horizontally positioned concentric circles was the only model which elicited significantly fewer bouts of longer fixation. 2. Because of a lack of homogeneity in model fixation, due to intense fear in some lemurs, the lemurs were separated into homogeneous subgroups using statistical criteria in the first experiment and behavioral criteria in the second. Only the largest subgroups comprising relatively calm mouse lemurs exhibited differential model fixation at a significant level. In both experiments, these particular subgroups looked significantly less at the critical model exhibiting two schematic facing eyes than at any of the other models. In conjunction with observations of dyadic interactions among mouse lemurs, the experimental findings suggest the following: 1. Two schematic facing eyes viewed out of context with a predator or conspecific are a provocative source of stimulation eliciting less visual inspection which could be considered analogous to bouts of gaze aversion observed among interacting lemurs. 2. In concordance with laboratory observations of attenuated gaze aversion by frightened mouse lemurs, the more fear-motivated lemurs in the present experiments exhibited reduced differential model inspection. The affinity between these findings implies, perhaps, that fear-motivation increases the tendency to engage in less selective investigative gazing as the animal shifts into a protective behavior mode. This as well as any other functional interpretation of the role of gaze behavior during agonistic encounters, however, awaits further experimental support.

Age differences in the response of California ground squirrels (Spermophilus beecheyi) to avian and mammalian predators.

The antipredator behavior of juvenile and adult California ground squirrels (Spermophilus beecheyi) was videotaped in Experiment 1 to measure the effects of age on assessment of a briefly presented live dog and a model red-tailed hawk (Buteo jamaicensis) in simulated flight. Adult squirrels treated the hawk as more dangerous than the dog, whereas juvenile squirrels showed less differentiation of the predator types. Juvenile squirrels also perceived the dog as a more immediate danger than adult squirrels did. For Experiment 2, the red-tailed hawk model was compared with models of a nonthreatening turkey vulture (Cathartes aura) and crow (Corvus brachyrhynchos). Neither age class differentiated the avian models; however, the adult squirrels treated these birds as more threatening than the juvenile squirrels did. Both studies suggest that learning may contribute to predator assessment.

Thatcher and the Cheshire Cat: Context and the Processing of Facial Features

As has been noted before, a face made gruesome by the inversion of its mouth will not be so perceived when the entire construction is inverted. Results are presented which suggest that this is because (a) the mouth and eye features are evaluated individually (although each feature may influence the evaluation of the other) and (b) the mouth, whether normal or inverted, tends to have its uppermost part assigned as ‘top’, providing for either a pleasant smiling-mouth expression or a gruesome ‘biting-intention’ expression. However, the gruesomeness of an inverted mouth is attenuated when eyes are shown below it (producing an inverted smiling face) which suggests that the location of other facial features can also influence the assignments of ‘top’.

Differential color brightness as a body orientation cue

The effects of context on perceptual learning were examined in a visual search task involving words from semantically distinct categories. Subjects were trained for a total of 8000 trials in five conditions consisting of a variably mapped (VM) condition, a consistently mapped (CM) condition, and three context conditions in which the consistency of the targets and distractors was dependent on the joint occurrence of specific target/distractor sets. The results of the training phase of the experiment showed that performance in the context conditions improved more than in the VM condition, indicating some benefit of context in the absence of total consistency, but there was less improvement than in the CM condition. After training, the subjects completed 3200 trials in five transfer conditions in which the targets and distractors of the original CM and context conditions were reversed and a new CM condition was added. In the transfer phase of the experiment there was a significant increase in RT (200 ms), indicative of negative transfer, when the CM target and distractor set were reversed. The switching of VM items to CM improved performance (50 ms). Little effect of target/distractor reversal in the cycle conditions implied that context was not used to learn or maintain relationships among specific targets and distractors. The data suggest that in the absence of traditional consistency, context plays an important role in facilitating performance. The results from the training and transfer phases of the experiment are interpreted from a hybrid-connectionist model of human information processing. The importance of contextual information in real-world tasks is discussed.Ninety male and female college students reclining on their backs in the dark were disoriented when positioned on a rotating platform under a slowly rotating disk that filled their entire visual field. Half of the disk was painted with a brighter value (~69% higher luminance level) of the color on the other half The effects of red, blue, and yellow were examined. Subjects wearing frosted goggles viewed the illuminated disk for three rotations. The disk was stopped when the subjects felt that they were right side up. A significant proportion of subjects selected the disk position in which the brighter side of each of the three colors filled their upper visual field. These results suggest that color brightness as well as lighting variation could provide space station crew members with body orientation cues as they move around.