Threat-Sensitive Responses to Predator Attacks in a Damselfly

The threat sensitivity hypothesis predicts that prey species assess and adjust their behavior flexibly in accordance with the magnitude of the threat imposed by a predator. We tested this hypothesis with regard to escape behavior and thanatosis (feigning of death to escape predation) in larvae of the damselfly Ischnura elegans. We manipulated the perceived predation threat of the larvae by changing three factors: lamellae autotomy (an escape strategy where animals sacrifice a body part when grasped by a predator; lamellae present or absent), kairomone type (odors released by predators; control, dragonfly kairomones or fish kairomones), and population of origin (fishpond or fishless pond). We demonstrated that thanatosis increased survival both when confronted with dragonfly and fish predators. We could show, for the first time, costs of past autotomy to be predator‐dependent: larvae without lamellae suffered higher predation mortality but only in the presence of a dragonfly predator and not in the presence of a fish predator. This is in accordance with the observed reduced escape speed of larvae after autotomy, which may affect escape probability toward dragonfly predators but not to the very fast fish predators. Unexpectedly, kairomone type did not affect the escape response of the larvae. In accordance with the threat sensitivity hypothesis, after an unsuccessful attack, larvae without lamellae had a higher frequency to enter thanatosis than larvae with lamellae and larvae from the fishpond showed longer thanatosis durations than larvae from the fishless pond. Consistent with the hypothesis, the reaction of the larvae to a simulated attack depended jointly on lamellae status and population. In fishless ponds, larvae with lamellae swam away more frequently than larvae without lamellae; in fishponds both groups almost never swam away and relied mostly upon immobility. Given the obvious benefits of adaptively varying escape responses we hypothesize this threat sensitivity to be widespread. Moreover, we argue that former inconsistencies between studies with regard to escape behavior may have been partly because of such adaptive variation.     

Contextual Information and Differential Responses to Alarm Whistles in California Ground Squirrels

In the field, we videotaped the reactions of squirrels to playbacks of 1, 3 and 5 whistle vocalizations at two sound intensities differing by 10 dB. The squirrels reacted by running to boulders or burrows and freezing. As time progressed following playbacks, freezing declined and squirrels resumed feeding, locomotion and grooming. With increasing numbers of whistles, squirrels were more likely to run and less likely to mount a boulder. With more high intensity whistles, squirrels froze quadrupedally more and bipedally less. Freezing postures did not vary as a function of the number of low-intensity whistles. Walking was suppressed least by 1 and 3 whistles at low intensity, and inhibited most by all high-intensity whistles as well as by the low-intensity 5-whistle playback. When the squirrel was on a boulder, quadrupedal freezing was more common than bipedal freezing. Off the boulder, the two freezing postures were equally likely. We propose that squirrels assessed risk from information encoded in the whistle(s) and contextual to it, and varied their reactions as a function of apparent risk.     

Effects of Nickel Chloride on Myocardial Contractile Properties in Active Ground Squirrels with Different Responses to Hypothermia

Biophysics - The effects of 1.5 mM nickel chloride on the contraction force, the force–frequency relation, and post-rest potentiation in the myocardium were studied in active Urocitellus...     

How Rearing History Affects Alarm-call Responses of Belding's Ground Squirrels (Spermophilus beldingi, Sciuridae)

Juvenile, but not adult, Belding’s ground squirrels (Spermophilus beldingi) exhibit markedly different responses to alarm calls as a function of their environment. Compared with same-aged, free-living juveniles, captive juveniles (housed in large outdoor enclosures) are more likely to respond to playbacks, to exhibit more exaggerated initial responses (e.g. enter a burrow vs. freeze) and to remain alert longer following playbacks of alarm and non-alarm calls. Two studies were conducted to identify the factors contributing to these response differences. Postemergent rearing environments (such as the opaque enclosure walls that limited visual and auditory stimulation in captivity, or the increased number of conspecifics and natural alarm calls that free-living juveniles experienced) could not account for the majority of response differences between captive and free-living juveniles (Study 1). To determine if the attenuated responses of free-living juveniles were due to foraging pressures, we compared the behaviours of food-provisioned captive juveniles with those of non-provisioned captive juveniles. Although sample sizes were small, no differences were evident in the development or expression of responses as a function of foraging pressure. Next, the development of captive juveniles was compared with that of juveniles reared in the field but housed in captivity after emergence (Study 2). Differences in the response patterns of field-reared and captive-reared animals matched the differences reported previously, as the responses of field-reared animals observed in captivity mirrored those of free-living juveniles that remained in the field. Thus, the differences in alarm-call responses originally observed between captive and free-living juveniles are attributed to their pre-emergent, but not post-emergent, rearing histories. Captive pups experienced levels of auditory, visual, tactile, and olfactory stimulation that were greater than those typically experienced by free-living pups. The increased exposure to conspecific alarm calls may have primed captive pups to respond more often and more intensely to the auditory stimuli they heard as juveniles. Sensitivity to early rearing environments may be adaptive for young ground squirrels if it facilitates the development of antipredator behaviour patterns that are appropriate for the local predator environment (e.g. openness of habitat, frequency of predators, availability of refuges).     

Antipredator Responses to a Previously Neutral Sound by Free-living Adult Golden-mantled Ground Squirrels, Spermophilus lateralis (Sciuridae)

I investigated whether free-living adult golden-mantled ground squirrels ( Spermophilus lateralis ) could learn to associate a novel sound with the appearance of a predator. Using a classical conditioning protocol, I presented adult squirrels with a novel tone followed by the appearance of a model hawk. After repeated trials, I again measured the squirrels' behavioral responses to the tone and compared them with their pretraining responses. Individuals that experienced the tone paired with the hawk responded with antipredator behavior of longer duration after pairing than before and these responses were indistinguishable from responses to natural, conspecific alarm calls. By examining the process, rather than simply the pattern, of call recognition ontogeny, this study provides new evidence for a mechanism by which animals can develop the ability to respond to both conspecific and heterospecific calls.     

Responses of Terrestrial Antarctic Ecosystems to Climate Change

Antarctic terrestrial biota are generally limited by the inexorably linked environmental factors of low summer temperature and lack of available water. However, in parts of the Antarctic, both these factors are changing rapidly on contemporary timescales. Terrestrial biota have concurrently been faced with changes in the timing of UV-B maxima associated with spring ozone depletion. The region of the Antarctic Peninsula and Scotia Arc has experienced one of the most rapid rates of environmental warming seen worldwide over the last 30–50 years. Together with local changes in precipitation, this has resulted in a rapid reduction in extent and thinning of many ice-fields and glaciers, exposing new terrain for colonisation while, at the same time, altering patterns of water availability in terrestrial habitats. The rapid development of communities on newly-exposed ground is also facilitated by the existence of soil propagule banks, which contain propagules of both local and exotic origin. In this paper we collate and review evidence from a range of observational and manipulative studies that investigate the effect of climate change, especially increased temperature, on the processes of colonisation and subsequent community development by plants in the Antarctic. Biological changes that have been associated with climate change are visible in the form of expansions in range and local population numbers amongst elements of the flora. Environmental manipulation experiments further demonstrate the possibility of large and rapid species and community responses to climate amelioration, with many resident biota responding positively, at least in the absence of increased competition from exotic colonists. Manipulation studies are also starting to elucidate more subtle responses to climate changes, at levels ranging from cell biochemistry to habitat and food web structure. Integrating such subtle responses is vital to improving our ability to understand the consequences of climate change, as these may lead to much greater consequential impacts on communities and ecosystems.      

Antipredator Behavioral Responses of Native and Exotic Tadpoles to Novel Predator

Factors related to the invasion process, such as high abundance of invaders, residence time, and functional distinctiveness, are well documented, but less attention has been given to the effects of antipredator strategy of invasive species during colonization. In this study, we explored the antipredator strategy of an introduced species by comparing the predator avoidance behaviors of two native anuran species and one introduced(exotic) species in the presence of different predators. The two native anuran species used in the study were Black-spotted Pond Frog Rana nigromaculata and Terrestrial Frog Rana limnocharis. The introduced(invasive) species used was American bullfrog Lithobates catesbeianus. Chinese pond turtle Chinemys reevesii, Red-backed rat snake Elaphe rufodorsata, and Big-headed turtle Platysternon megacephalum were used as predator species. Chinese pond turtles and Red-backed rat snakes are native predators of Black-spotted Pond Frogs and Terrestrial Frogs, while Big-headed turtles are novel(unfamiliar) to the two frogs. All three predator species are novel(unfamiliar) to the American bullfrog. The results show that tadpoles of the two native species displayed behaviors of recognizing the two native predators, but did not display the capability of identifying the novel predator. Results from our study also suggest that American bullfrog tadpoles exhibited strong antipredator behavioral responses by displaying the capability of identifying unfamiliar predators without cohabitation history and prior exposure to them. Such antipredator behavioral responses could have resulted in more favorable outcomes for an invading species during the invasive introductory process.     

The Metabolic Responses to Aerial Diffusion of Essential Oils

Anxiety disorders are the most prevalent psychiatric disorders and affect a great number of people worldwide. Essential oils, take effects through inhalation or topical application, are believed to enhance physical, emotional, and spiritual well-being. Although clinical studies suggest that the use of essential oils may have therapeutic potential, evidence for the efficacy of essential oils in treating medical conditions remains poor, with a particular lack of studies employing rigorous analytical methods that capture its identifiable impact on human biology. Here, we report a comprehensive gas chromatography time-of-flight mass spectrometry (GC-TOFMS) based metabonomics study that reveals the aromas-induced metabolic changes and the anxiolytic effect of aromas in elevated plus maze (EPM) induced anxiety model rats. The significant alteration of metabolites in the EPM group was attenuated by aromas treatment, concurrent with the behavioral improvement with significantly increased open arms time and open arms entries. Brain tissue and urinary metabonomic analysis identified a number of altered metabolites in response to aromas intervention. These metabolic changes included the increased carbohydrates and lowered levels of neurotransmitters (tryptophan, serine, glycine, aspartate, tyrosine, cysteine, phenylalanine, hypotaurine, histidine, and asparagine), amino acids, and fatty acids in the brain. Elevated aspartate, carbohydrates (sucrose, maltose, fructose, and glucose), nucleosides and organic acids such as lactate and pyruvate were also observed in the urine. The EPM induced metabolic differences observed in urine or brain tissue was significantly reduced after 10 days of aroma inhalation, as noted with the loss of statistical significance on many of the metabolites in the aroma-EPM group. This study demonstrates, for the first time, that the metabonomics approach can capture the subtle metabolic changes resulting from exposure to essential oils and provide the basis for pinpointing affected pathways in anxiety-related behavior, which will lead to an improved mechanistic understanding of anxiolytic effect of essential oils.     

Taste and Physiological Responses to Glucosinolates: Seed Predator versus Seed Disperser

In contrast to most other plant tissues, fleshy fruits are meant to be eaten in order to facilitate seed dispersal. Although fleshy fruits attract consumers, they may also contain toxic secondary metabolites. However, studies that link the effect of fruit toxins with seed dispersal and predation are scarce. Glucosinolates (GLSs) are a family of bitter-tasting compounds. The fleshy fruit pulp of Ochradenus baccatus was previously found to harbor high concentrations of GLSs, whereas the myrosinase enzyme, which breaks down GLSs to produce foul tasting chemicals, was found only in the seeds. Here we show the differential behavioral and physiological responses of three rodent species to high dose (80%) Ochradenus’ fruits diets. Acomys russatus, a predator of Ochradenus’ seeds, was the least sensitive to the taste of the fruit and the only rodent to exhibit taste-related physiological adaptations to deal with the fruits’ toxins. In contrast, Acomys cahirinus, an Ochradenus seed disperser, was more sensitive to a diet containing the hydrolyzed products of the GLSs. A third rodent (Mus musculus) was deterred from Ochradenus fruits consumption by the GLSs and their hydrolyzed products. We were able to alter M. musculus avoidance of whole fruit consumption by soaking Ochradenus fruits in a water solution containing 1% adenosine monophosphate, which blocks the bitter taste receptor in mice. The observed differential responses of these three rodent species may be due to evolutionary pressures that have enhanced or reduced their sensitivity to the taste of GLSs.     

Responses of Male and Female Black Grouse to Male Vocal Display

The evolution of leks may be explained by several hypotheses. The ‘female preference’ hypothesis, which states that females favour males that have aggregated, has recently gained some empirical support. Low-quality, unattractive males may, however, settle near attractive males, as predicted by the ‘hotshot’ hypothesis. We tested whether black grouse Tetrao tetrix females use auditory cues to find the preferred leks, and whether males respond to vocal display emitted on leks. We conducted a playback experiment with male vocal display (rookooing) on leks, where the visiting females and displaying males were counted. The number of males tended to increase more on playback leks. Specifically, the number of 1-year-old males was greater on playback sites than on control sites. Also, the number of females, in relation to the lek size before the start of the experiment tended to increase. In addition, we used aviary playback trials to test whether females distinguish between single-male and multi-male displays. In a choice test, females showed greater preference for the ‘multi-male’ tape. The tendency for increased male numbers on playback leks resulted from increased visits of young, mobile males which were attracted to leks that they perceived to be large. This suggests a ‘hotshot’-type mechanism in the settlement of young males. Because females also responded to the supplemented auditory advertisement, or directly to the increased number of males, the ‘female preference’ hypothesis is also supported. Females may, at least in part, base their decision of which lek to visit on auditory cues, but visual contact to males may be also needed.     

Placement, Retrieval, and Memory of Caches by Thirteen-Lined Ground Squirrels

Mechanisms governing placement and retrieval of scatter hoards were investigated in 13-lined ground squirrels ( Spermophilus tridecemlineatus ). The squirrels used several placement tactics, including relatively deep burial of seeds, avoidance of prominent objects, and cryptic placement, which would reduce chance discovery by competitors but that might also increase the difficulty of retrieval for the hoarder. Nevertheless, scatter hoards were unfailingly retrieved within a day or two after placement, despite experimental elimination or displacement of local sensory cues emanating from the sites. Artificial caches placed close to true caches were not discovered, indicating that recovery attempts were quite precise. These results imply that 13-lined ground squirrels rely heavily on spatial memory for retrieval and are the first experimental demonstration of the importance of memory for cache recovery in a natural population of mammals.     

Phylogeny and Evolutionary History of the Ground Squirrels (Rodentia: Marmotinae)

Although ground squirrels (Spermophilus) and prairie dogs (Cynomys) are among the most intensively studied groups of mammals with respect to their ecology and behavior, a well-resolved phylogeny has not been available to provide a framework for comparative and historical analyses. We used complete mitochondrial cytochrome b sequences to construct a phylogeny that includes all 43 currently recognized species in the two genera, as well as representatives of two closely related genera (Marmota and Ammospermophilus). In addition, divergence times for ground squirrel lineages were estimated using Bayesian techniques that do not assume a molecular clock. All methods of phylogenetic analysis recovered the same major clades, and showed the genus Spermophilus to be paraphyletic with respect to both Marmota and Cynomys. Not only is the phylogeny at odds with previous hypotheses of ground squirrel relationships, but it suggests that convergence in morphology has been a common theme in ground squirrel evolution. A well-supported basal clade, including Ammospermophilus and two species in the subgenus Otospermophilus, diverged from all other ground squirrels an estimated 17.5 million years ago. Between 10 and 14 million years ago, a relatively rapid diversification gave rise to lineages leading to marmots and to several distinct groups of ground squirrels. The Eurasian ground squirrels diverged from their North American relatives during this period, far earlier than previously hypothesized. This period of diversification corresponded to warming climate and spread of grasslands in western North America and Eurasia. Close geographic proximity of related forms suggests that most species evolved in or near their current ranges.     

Comparison of Antipredator Responses of Two Related Water Striders to a Common Predator

This study compares the antipredator responses of two congeneric water striders that live in different habitats yet share a common predator. Aquarius nebularis and A. remigis are stream-dwelling species of water striders found in close association in central Kentucky. Aquarius nebularis typically inhabit third- and fourth-order streams that support diverse and complex fish communities; A. remigis inhabit adjacent first- and second-order tributaries that tend to have either no fish or relatively few fish patchily distributed. The ecological conditions for these two species are distinctly different, yet the green sunfish (Lepomis cyanellus) is a surface-feeding predator and a potential risk to both species. In experimental pools with sunfish, an initial fish strike caused A. remigis to move to the edge of the pool and become inactive. For the rest of the observation period, A. remigis reduced behaviour patterns that attract predators such as skating on open water, mating and male–male aggression. The proportion of A. remigis missing from sunfish pools was 5 times higher than in pools lacking fish, suggesting that 20% of water striders were killed by predation. In contrast, an initial fish strike caused A. nebularis to exhibit a burst of activity as individuals erratically skated over the open water. They then resumed the less active pre-attack behaviours a short time later. Aquarius nebularis showed none of the antipredator behaviours typical for A. remigis. Furthermore, the proportion of A. nebularis missing from sunfish pools did not differ from that in pools without fish. Although antipredator behaviour has been examined for relatively few species of water striders, this study suggests that the behaviour of the most commonly studied species, A. remigis, may not be indicative for water striders in general., Corresponding author: James J. Krupa, School of Biological Sciences, University of Kentucky, Lexington, KY 40506-0225, U.S.A. E-mail: bio149@pop.uky.edu bio149@pop.uky.edu     

Expression Profiling and Structural Characterization of MicroRNAs in Adipose Tissues of Hibernating Ground Squirrels

Micro RNAs（mi RNAs） are small non-coding RNAs that are important in regulating metabolic stress. In this study, we determined the expression and structural characteristics of 20 mi RNAs in brown（BAT） and white adipose tissue（WAT） during torpor in thirteen-lined ground squirrels. Using a modified stem-loop technique, we found that during torpor, expression of six mi RNAs including let-7a, let-7b, mi R-107, mi R-150, mi R-222 and mi R-31 was significantly downregulated in WAT（P 〈 0.05）, which was 16%–54% of euthermic non-torpid control squirrels,whereas expression of three mi RNAs including mi R-143, mi R-200 a and mi R-519 d was found to be upregulated by 1.32–2.34-fold. Similarly, expression of more mi RNAs was downregulated in BAT during torpor. We detected reduced expression of 6 mi RNAs including mi R-103 a, mi R-107, mi R-125 b, mi R-21, mi R-221 and mi R-31（48%–70% of control）, while only expression of mi R-138 was significantly upregulated（2.91 ± 0.8-fold of the control, P 〈 0.05）. Interestingly,mi RNAs found to be downregulated in WAT during torpor were similar to those dysregulated in obese humans for increased adipogenesis, whereas mi RNAs with altered expression in BAT during torpor were linked to mitochondrial b-oxidation. mi RPath target prediction analysis showed that mi RNAs downregulated in both WAT and BAT were associated with the regulation of mitogen-activated protein kinase（MAPK） signaling, while the mi RNAs upregulated in WAT were linked to transforming growth factor b（TGFb） signaling. Compared to mouse sequences, no unique nucleotide substitutions within the stem-loop region were discovered for the associated pre-mi RNAs for the mi RNAs used in this study, suggesting no structure-influenced changes in pre-mi RNA processing efficiency in the squirrel. As well, the expression of mi RNA processingenzyme Dicer remained unchanged in both tissues during torpor. Overall, our findings suggest that changes of mi RNA expression in adipose tissues may be linked