Age differences in arousal and vigilance in California ground squirrels (Spermophilus beecheyi).

Newly emerged pup, juvenile, and adult California ground squirrels (Spermophilus beecheyi douglasii) were videorecorded at a seminatural field site in northern California. Video data revealed age differences in the budgeting of ground squirrel behavior, habitat use, and physiological arousal as indicated by morphometric analyses of tail piloerection. Adults and juveniles devoted their time to foraging in the open at feeding stations while displaying low to moderate levels of arousal, respectively. Pups remained vigilant on the fringe of covered habitats while displaying comparatively higher levels of arousal. Higher pup arousal may facilitate memory formation during early stages of development.

Recognition of heterospecific alarm vocalizations by bonnet macaques (Macaca radiata).

Recognition of heterospecific alarm vocalizations is an essential component of antipredator behavior in several prey species. The authors examined the role of learning in the discrimination of heterospecific vocalizations by wild bonnet macaques (Macaca radiata) in southern India The bonnet macaques' flight and scanning responses to playbacks of their own alarm vocalizations were compared with their responses to playbacks of vocalizations of Nilgiri langurs (Trachypithecus johnii), Hanuman langurs (Semnopithecus entellus), and sambar deer (Cervus unicolor). The study was conducted in 3 regions that differed in the frequency with which bonnet macaques encountered these species and included an urban setting. Call recognition was highest in adults and in regions where individuals were frequently exposed to the calling species; calls were not recognized by urban monkeys. Thus, age and experience are important factors in heterospecific call recognition by bonnet macaques.

California ground squirrel (Spermophilus beecheyi) blood sera inhibits crotalid venom proteolytic activity.

Some California ground squirrels (Spermophilus beecheyi) show limited necrosis following envenomation by northern Pacific rattlesnakes (Crotalus viridis oreganus). This study demonstrates that S. beecheyi blood sera inhibits venom proteases. Sera from rattlesnake-abundant habitats inhibited C. v. oreganus venom more effectively than venom from two allopatric rattlesnake species, C. v. viridis and C. atrox, suggesting evolutionary specialization. The pattern of inhibition among squirrel populations corresponds best with history of rattlesnake predation, in contrast to current rattlesnake density.

Cognitively based apparent motion: an extreme case.

An ambiguous figure is used to provide a demonstration of apparent motion in which there is no change in the retinal image or in external space.

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.

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.

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.

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 the mouth and eye features are evaluated individually (although each feature may influence the evaluation of the other) and 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'.

Calibrating the molecular clock: estimates of ground squirrel divergence made using fossil and geological time markers.

According to 5-Myr-old fossil evidence, ground squirrels within the genus Spermophilus had diverged into subgenera Spermophilus and Otospermophilus by late Miocene times. Radiometric dating has also provided a precise time for the sudden onset of a geological event, occurring 0.725 Myr ago, that initiated the complete and permanent reproductive isolation of two subspecies within the subgenus Otospermophilus. Since these two subspecies (S. beecheyi beecheyi and S. b. douglasii) readily hybridize with each other under laboratory conditions, allopatric subspeciation is unlikely to have occurred prior to 0.725 Myr ago. We employed Nei's model for estimating genetic distance in units which are linear in time, calibrated on the 0.725-Myr-ago date for initiation of S. b. subspeciation, to test its ability to generate a time scale for subgeneric divergence in keeping with the minimum estimate provided by the fossil record. This represents the most valid test to date of the utility of Nei's model for estimating genetic distance in units which are linear in time. Nei's model was found to underestimate this minimum time by 1 Myr, but it approximated this date after correcting values of D for variation in rates of evolution among loci.

Timing of dispersal in juvenile jewel fish during development is unaffected by available space.

The spatial distributions of 2 groups of sibling juvenile jewel fish were examined between 58 and 99 days of age to determine the effects of spatial experience on the timing of dispersal from a more aggregative behavioral mode. One group was provided a seminatural 1000-liter aquarium, the other with 70% less space per fish, but both groups were able to observe the same number of fish. Using a computer and digitizing tablet, distances between 1st-6th nearest neighbors were measured from time-sampled video recordings of spatial distributions in either overhead or underneath plan views. Both groups exhibited changes in aggregative behavior that were remarkably similar. Between 65 and 92 days of age, both groups showed gradual dispersal, which accelerated abruptly at 93-99 days of age. These results suggest that the timing of dispersal is regulated by developmental processes operating independently of spatial experience.

Rapid effect of biologically relevant stimulation on tectal neurons: changes in dendritic spine morphology after nine minutes are retained for twenty-four hours.

Flight from a threatening stimulus was used as a natural analog of tetanizing electrical stimulation to determine whether brief, intense stimulation can alter dendritic spine morphology. Juvenile jewel fish were pretreated in a dark, sound-proofed room for 48 h, at which time unstimulated controls were sacrificed by hypothermic anesthesia. Remaining fish were forced to flee for 9 min and then either sacrificed immediately (9-min stimulated group) or returned to the dark for 24 h (24 h recovery group). Morphometric quantification of dendritic spines on the basal 120 micrometers of the apical dendrites of tectal pyriform interneurons revealed substantial changes in 3 measures of spine shape: spine head width, overall spine length, and spine stem length. Compared with unstimulated controls, 9 min of stimulation changed the relative frequencies of spine head width, overall spine length and spine stem length. Morphological effects were evident after 24 h, and changes in relative spine length and spine stem length frequencies were more pronounced in the upper strata of neurons 24 h after stimulation. Thus brief, biologically relevant stimulation can cause both immediate and persistent changes in spine morphology; this plasticity is discussed in the context of related anatomical studies.

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.

Effects of chronic crowding stress on midbrain development: changes in dendritic spine density and morphology in jewel fish optic tectum.

This study investigates the effects of a biologically relevant stressor, crowding, on the development of neurons in the major teleostean brain area, the optic tectum. Adult jewel fish were reared for approximately 4 years under conditions of moderate density (3.3 liter/fish), or under uncrowded control conditions (25 liter/fish). Quantitative morphometric measures of Golgi-stained tissue were used to test whether long-term crowding at moderate density produced developmental deficits lasting beyond the juvenile period. Chronic crowding did not affect body size or gross tectal growth. However, crowding significantly decreased the density of dendritic spine formation on apical dendrites of pyriform interneurons in the basal region of the tectum (stratum album centrale). Additionally, the shapes of spines on this segment of the apical dendrite were altered by crowding: relative frequencies of overall spine length and spine stem length changed significantly. These results are interpreted in the context of cytoarchitectural changes produced by more extreme developmental stressors in previous studies.

Jewel fish retain juvenile schooling pattern after crowded development.

Juvenile jewel fish were crowded between 100 and 160 days of age (15 fish/3.6 liters) in a double-walled aquarium sharing water flow with uncrowded siblings (15 fish/69.4 liters). Photographs of schooling in a 73-liter aquarium were made after 30 and 60 days of crowding. Distances maintained between each fish and its 1st-5th nearest neighbors and orientation angles between 1st nearest neighbors were measured. After 30 days, crowded juveniles maintained significant nonrandomly aggregated distances to their 1st-5th neighbors, spacing significantly closer than uncrowded siblings. After 60 days, crowded juveniles maintained both closer, nonrandom distances to 1st-5th neighbors and significantly more parallel orientation to 1st nearest neighbors. Thus, whereas uncrowded juveniles followed the normal developmental pattern of dispersion, crowded siblings retained juvenile spacing behavior.

Short-term juvenile crowding arrests the developmental formation of dendritic spines on tectal interneurons in jewel fish.

Development of jewel fish tectal interneurons was measured as a function of crowded development. The number of dendritic spines on the apical dendrites of pyriform interneurons was counted in the stratum album centrale plexiform layer because previous research indicated that this was the region in which both social deprivation and acute juvenile crowding produced neuronal deficits. Results showed that 100- and 130-day-old uncrowded juveniles had spine densities equivalent to 160-day-old juveniles crowded at 15 fish/3.6 liter for 60 days. Thus, no spine formation occurred after the onset of crowding. Sibling 160-day-old juveniles reared in the uncrowded condition (1 fish/4.6 liter) had already acquired the normal complement of spines exhibited by 4-year-old adults reared at low density (1 fish/25 liter). These results show that acute crowding can arrest the normal course of neuronal development in juvenile jewel fish.

Plasticity of dendritic spine formation: a state-dependent stochastic process.

This study proposes that plasticity of dendritic spine formation may be modeled as distribution patterns imbedded in a spine length-dependent and density-dependent stochastic process. Modeling the jewel fish tectal interneuron revealed a critical 10-36 micron region where spine length plasticity was predicted to be most detectable. This hypothesis was tested by comparing neurons sampled from jewel fish reared for 4 years in a crowded environment (1 fish/5.64 l) with uncrowded controls (1 fish/25 l). The interaction between fish groups and the location of spine length differences was significant (p less than 0.01) within the basal 10-30 micron dendritic segment. Spine head widths were also significantly smaller (p less than 0.01) in the crowded fish over the entire dendrite. These findings suggest two modes of neuronal plasticity: (1) plasticity of spine length during formation, and (2) plasticity in spine head width after the spine is formed.

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.

Crowded jewel fish show changes in dendritic spine density and spine morphology.

This study demonstrates that neuronal development can be adversely affected by short-term crowding. Compared with uncrowded siblings (15 fish/73-litre), juvenile jewel fish (15 fish/3.6-litre) crowded for 60 days exhibited 50-58% fewer dendritic spines and spines with narrower heads on pyriform interneurons in deep tectal strata. These findings indicate that crowded environments can produce aberrant neuronal development similar to that seen in socially deprived jewel fish.