What is Communicated in the Antipredator Calls of Lemurs: Evidence from Playback Experiments with Ringtailed and Ruffed Lemurs

Two hypotheses of signal specificity in antipredator calls (“referential signalling” and “response urgency”) are discussed in light of prior research on ground squirrels and vervet monkeys. These hypotheses then are examined with data on responses of semi-captive ringtailed and ruffed lemurs to antipredator call playbacks. Although the responses of ringtailed lemurs support a referential-signalling interpretation of their antipredator calls, those of ruffed lemurs do not conform well to either hypothesis. Rather, ruffed lemur antipredator calls seem best viewed as “affective” signals that may only reflect underlying emotional/motivational states.     

Female Putty-Nosed Monkeys Use Experimentally Altered Contextual Information to Disambiguate the Cause of Male Alarm Calls

Many animal vocal signals are given in a wide range of contexts which can sometimes have little in common. Yet, to respond adaptively, listeners must find ways to identify the cause of a signal, or at least rule out alternatives. Here, we investigate the nature of this process in putty-nosed monkeys, a forest primate. In this species, adult males have a very restricted repertoire of vocalizations which are given in response to a wide variety of events occurring under conditions of limited visibility. We carried out a series of field playback experiments on females (N = 6) in a habituated group in Gashaka Gumti National Park, Nigeria, in which male alarm/loud calls were presented either alone, or following acoustic information that simulated the occurrence of natural disturbances. We demonstrate that listeners appear to integrate contextual information in order to distinguish among possible causes of calls. We conclude that, in many cases, pragmatic aspects of communication play a crucial role in call interpretation and place a premium on listeners'' abilities to integrate information from different sources.     

Organizational Changes to Thyroid Regulation in Alligator mississippiensis: Evidence for Predictive Adaptive Responses

During embryonic development, organisms are sensitive to changes in thyroid hormone signaling which can reset the hypothalamic-pituitary-thyroid axis. It has been hypothesized that this developmental programming is a ‘predictive adaptive response’, a physiological adjustment in accordance with the embryonic environment that will best aid an individual''s survival in a similar postnatal environment. When the embryonic environment is a poor predictor of the external environment, the developmental changes are no longer adaptive and can result in disease states. We predicted that endocrine disrupting chemicals (EDCs) and environmentally-based iodide imbalance could lead to developmental changes to the thyroid axis. To explore whether iodide or EDCs could alter developmental programming, we collected American alligator eggs from an estuarine environment with high iodide availability and elevated thyroid-specific EDCs, a freshwater environment contaminated with elevated agriculturally derived EDCs, and a reference freshwater environment. We then incubated them under identical conditions. We examined plasma thyroxine and triiodothyronine concentrations, thyroid gland histology, plasma inorganic iodide, and somatic growth at one week (before external nutrition) and ten months after hatching (on identical diets). Neonates from the estuarine environment were thyrotoxic, expressing follicular cell hyperplasia (p = 0.01) and elevated plasma triiodothyronine concentrations (p = 0.0006) closely tied to plasma iodide concentrations (p = 0.003). Neonates from the freshwater contaminated site were hypothyroid, expressing thyroid follicular cell hyperplasia (p = 0.01) and depressed plasma thyroxine concentrations (p = 0.008). Following a ten month growth period under identical conditions, thyroid histology (hyperplasia p = 0.04; colloid depletion p = 0.01) and somatic growth (body mass p<0.0001; length p = 0.02) remained altered among the contaminated sites. This work supports the hypothesis that embryonic EDC exposure or iodide imbalance could induce adult metabolic disease states, thereby stressing the need to consider the multiple environmental variables present during development.     

Decrease in Alarm Call Response Among Tufted Capuchins in Competitive Feeding Contexts: Possible Evidence for Counterdeception

Animal signals function to elicit behaviors in receivers that ultimately benefit the signaler, while receivers should respond in a way that maximizes their own fitness. However, the best response may be difficult for receivers to determine when unreliable signaling is common. “Deceptive” alarm calling is common among tufted capuchins (Cebus apella nigritus) in competitive feeding contexts, and responding to these calls is costly. Receivers should thus vary their responses based on whether a call is likely to be reliable. If capuchins are indeed able to assess reliability, I predicted that receivers will be less likely to respond to alarms that are given during competitive feeding contexts than in noncompetitive contexts, and, within feeding contexts, that individuals inside or adjacent to a food patch will be less likely to respond to alarms than those further from the resource. I tested these predictions in a group of wild capuchins by observing the reactions of focal animals to alarm calls in both noncompetitive contexts and experimental feeding contexts. Antipredator escape reactions, but not vigilance reactions, occurred significantly less often in competitive feeding contexts than in noncompetitive contexts and individuals adjacent to food patches were more likely to respond to alarm calls than were those inside or further from food patches. Although not all predictions were fully supported, the findings demonstrate that receivers vary their behavior in a way that minimizes the costs associated with “deceptive” alarms, but further research is needed to determine whether or not this can be attributed to counterdeception.     

Ontogenetic and Sex Differences Influence Alarm Call Responses in Mammals: a Meta‐Analysis

Animals respond to alarm calls by increasing their antipredator behavior; however, responses may consistently differ by age or sex. Although several adaptive explanations have been proposed to account for age‐dependent antipredator behavior, similar explanations are rarely extended to sex‐specific responses. Furthermore, no attempts have been made to quantitatively estimate the direction or magnitude of these differences across studies. Here, we use meta‐analysis to discover overall trends in the literature, as well as differences owing to experimental or population parameters. Across our sample of available studies (unfortunately biased toward rodents and primates), males respond more than females, and young respond more than adults. Furthermore, young of quickly maturing species display more adult‐like antipredator behavior than young of slowly maturing species, suggesting that young must develop antipredator behavior at a pace consistent with the length of their ontogenetic period (a.k.a. juvenile/sub‐adult period, defined as the time between birth and attainment of sexual maturity). We review previously proposed explanations for such age differences, namely, that longer ontogenetic periods may provide juveniles with time to develop behavior through learning and experience, or, maturation rates may influence age‐specific selection pressures and the consequent evolution of age‐specific behavioral strategies. We evaluate our results in light of these hypotheses, although our conclusions are limited by the number and taxonomic bias of available studies. We therefore suggest ways in which future studies may tease apart the relative importance of learning and experience vs. age‐specific adaptive behavior, and draw attention to opportunities for research on age‐ and sex‐specific alarm call responses.     

Biogeography of Dwarf Lemurs: Genetic Evidence for Unexpected Patterns in Southeastern Madagascar

Seven species of dwarf lemurs (Cheirogaleus spp.) are currently recognized after a recent revision of the genus. During a field study in southeastern Madagascar, we observed 3 distinct morphotypes of Cheirogaleus resembling Cheirogaleus medius, C. major and C. crossleyi. In particular, for Cheirogaleus crossleyi southeastern Madagascar was far away from the known distribution range of the species when referring to the recent revision of the genus. In order to clarify the taxonomic status of the 3 morphotypes, we compared field samples from southeastern Madagascar to museum specimens from several locations in Madagascar and to field samples from Kirindy/CFPF, western Madagascar by genetic analyses using the mitochondrial cytochrome b gene. Genetic data yield strong support for 2 of the 3 morphotypes to represent Cheirogaleus medius and C. major. The third morphotype is genetically closely related to Cheirogaleus crossleyi, albeit more distantly than the other 2 morphotypes to the respective reference samples. The genetic distance is related to a considerable geographic distance between the location of our field study and the origin of the respective reference specimen, because Cheirogaleus crossleyi had been reported only from northern Madagascar. Our field observations indicate an isolated population in southeastern Madagascar. We propose to identify them as Cheirogaleus crossleyi and discuss the population genetic and biogeographic considerations supporting this conclusion.     

Functionally Referential Alarm Calls in Tamarins (Saguinus fuscicollis and Saguinus mystax) – Evidence from Playback Experiments

Studies on primate vocalisation have revealed different types of alarm call systems ranging from graded signals based on response urgency to functionally referential alarm calls that elicit predator‐specific reactions. In addition, alarm call systems that include both highly specific and other more unspecific calls have been reported. There has been consistent discussion on the possible factors leading to the evolution of different alarm call systems, among which is the need of qualitatively different escape strategies. We studied the alarm calls of free‐ranging saddleback and moustached tamarins (Saguinus fuscicollis and Saguinus mystax) in northeast Peru. Both species have predator‐specific alarm calls and show specific non‐vocal reactions. In response to aerial predators, they look upwards and quickly move downwards, while in response to terrestrial predators, they look downwards and sometimes approach the predator. We conducted playback experiments to test if the predator‐specific reactions could be elicited in the absence of the predator by the tamarins’ alarm calls alone. We found that in response to aerial alarm call playbacks the subjects looked significantly longer upwards, and in response to terrestrial alarm call playbacks they looked significantly longer downwards. Thus, the tamarins reacted as if external referents, i.e. information about the predator type or the appropriate reaction, were encoded in the acoustic features of the calls. In addition, we found no differences in the responses of S. fuscicollis and S. mystax whether the alarm call stimulus was produced by a conspecific or a heterospecific caller. Furthermore, it seems that S. fuscicollis terrestrial alarm calls were less specific than either S. mystax terrestrial predator alarms or either species’ aerial predator alarms, but because of the small sample size it is difficult to draw a final conclusion.     

The Effects of Starvation on Crayfish Responses to Alarm Odor

The effect of starvation on responses to alarm odor was tested with individuals of an invasive and a native species of crayfish. I predicted that chemical predator cues would inhibit feeding less in starving than well-fed animals, and that this decrease would be stronger in a native compared with an invasive species. Individuals were exposed to food odor and then alarm odor after 3 and 10 d of starvation. The inhibition of food-related behavior patterns was similar on the 2 d of testing for individuals of the invasive species, Orconectes rusticus. Individuals of O. virilis showed a significant reduction in the effects of alarm odor detection on day 10 compared with day 3 of starvation. The lack of a change in responses to alarm odors between days of testing by individuals of O. rusticus may be because they are more responsive to alarm odors than individuals of O. virilis. This behavioral difference could contribute to the successful range extension of O. rusticus.     

The Sound of Danger: Threat Sensitivity to Predator Vocalizations,Alarm Calls,and Novelty in Gulls

The threat sensitivity hypothesis predicts that organisms will evaluate the relative danger of and respond differentially to varying degrees of predation threat. Doing so allows potential prey to balance the costs and benefits of anti-predator behaviors. Threat sensitivity has undergone limited testing in the auditory modality, and the relative threat level of auditory cues from different sources is difficult to infer across populations when variables such as background risk and experience are not properly controlled. We experimentally exposed a single population of two sympatric gull species to auditory stimuli representing a range of potential threats in order to compare the relative threat of heterospecific alarm calls, conspecific alarms calls, predator vocalizations, and novel auditory cues. Gulls were able to discriminate among a diverse set of threat indicators and respond in a graded manner commensurate with the level of threat. Vocalizations of two potential predators, the human voice and bald eagle call, differed in their threat level compared to each other and to alarm calls. Conspecific alarm calls were more threatening than heterospecfic alarm calls to the larger great black-backed gull, but the smaller herring gull weighed both equally. A novel cue elicited a response intermediate between known threats and a known non-threat in herring gulls, but not great black-backed gulls. Our results show that the relative threat level of auditory cues from different sources is highly species-dependent, and that caution should be exercised when comparing graded and threshold threat sensitive responses.     

Molecular Evidence of Reproductive Isolation in Sympatric Sibling Species of Mouse Lemurs

Recent morphological and molecular phylogenetic studies of mouse lemurs (Microcebus) living in the western and southern regions of Madagascar have shown that specific diversity had been considerably underestimated. In large part, this underestimate was due to the lack of sufficient specimens from given localities to assess properly the level of phenotypic variation within and between populations. The accurate delineation of specific boundaries has no doubt been confounded by the diminutive size, nocturnal habits, and subtle morphological variation characteristic of mouse lemurs, which can make field identification of individuals problematic. We illustrate the use of molecular phylogenetic analysis to reveal reproductive isolation in two sympatric mouse lemur species, Microcebus murinus and M. griseorufus. Their documentation in the Berenty Private Reserve in the extreme south of Madagascar verifies the historically-broad distribution of Microcebus griseorufus, a species recently resurrected from synonomy.     

Responses of Quercus ilex from Different Provenances to Experimentally Imposed Water Stress

Responses of Quercus ilex L. seedlings from three different localities in Italy to experimentally imposed drought stress were analysed. Predawn (Ψ_pd) and midday (Ψ_m) leaf water potential of stressed seedlings decreased on an average until −4.0 and −4.2 MPa, respectively, in the severe water stress. At the end of the severe water stress the relative water content (RWC) was 72.5 – 83.6 % and the photosynthetic rates (P_N) near zero. The critical threshold value of Ψ_pd for complete stomatal closure was from −4.0 to −4.5 MPa. The leaf damage after the severe water stress was significantly greater in seedlings originated from the acorns of climax area (45 % total leaf injured area and 40 % fallen leaves) than in the other seedlings (on an average 20.5 % total leaf injured area and 21 % fallen leaves). This revised version was published online in July 2006 with corrections to the Cover Date.     

Age Differences in the Response of Willow Tits (Parus montanus) to Conspecific Alarm Calls

Predation is an important mortality factor in wintering birds. To counter this, birds produce alarm calls in the presence of predators which serve to warn conspecifics. In social hierarchical bird flocks, adults survive the winter better than juveniles and therefore survival strategies probably vary with social status. This study examined the differential responses to alarm calls by free-living willow tits, Parus montanus, in dominance-structured winter flocks in Finland. To explore the age-dependent differences in response to conspecific alarm calls, a series with three alarm calls was played to focal adults and juveniles while they sat in the middle section of a spruce branch. Immediately after the playback, juvenile willow tits moved more often, flew longer distances and changed branches more often than did adults. Previous mammal studies have shown that juveniles are more likely to flee than adults after hearing conspecific alarm calls. The current study demonstrates that similar age-dependent responses to conspecific alarm calls occur in birds also. These findings reflect an increased vulnerability to predators or lack of experience of young birds.     

Ultrastructural and Photometric Evidence for Light-Induced Changes in Chloroplast Structure in vivo

Photometric evidence for a reversible, red-light induced transmission decrease in excised leaf tissue or the thalli of certain marine algae has been obtained under conditions which correspond to the occurrence of a light-induced shrinkage of chloroplasts within the cells. Evidence supporting this conclusion is: A) The kinetics of the nonspecific transmission changes are similar to those observed in chloroplasts in vitro. B) The magnitude of the response is larger than could be accounted for by any known pigment which absorbs at 546 mμ. C) The light-induced transmission changes are optimal at pH 5.5 to 6.5 in the presence of electron flow cofactors and weak acid anions, conditions which are optimal for light-induced chloroplast shrinkage in isolated chloroplasts. D) Examination of chloroplast ultrastructure in dark incubated and illuminated chloroplasts reveals a flattening of the chloroplast structure and shrinkage.     

Evidence for Two Separate Purinergic Responses in Paramecium tetraurelia: XTP Inhibits Only the Oscillatory Responses to GTP

The purine nucleotide GTP causes a complex behavioral response and two distinct electrophysiological responses in the ciliated protozoan Paramecium tetraurelia. One of the two electrophysiological responses is an oscillating current that is responsible for the repeated backward swimming episodes that constitute the behavioral response to GTP. The second electrophysiological response is a sustained current whose relationship to the first is unknown. Here we show that the purine nucleotide XTP can completely block both the behavioral response to GTP and its associated oscillating current, but not the sustained current induced by GTP. Notably, XTP alone causes a sustained current similar to that induced by GTP. We believe the data support the notion that P. tetraurelia possesses two distinct signal transduction pathways sensitive to purine nucleotides: one specific for GTP that leads to oscillating currents and behavior, and a second pathway activated by GTP and other purine nucleotides that leads to a sustained current. Received: 22 August 1997/Revised: 20 January 1998     

Regulation by Photoperiod of Seasonal Changes in Body Mass and Reproductive Function in Gray Mouse Lemurs (Microcebus murinus): Differential Responses by Sex

Microcebus murinus exhibits highly seasonal biological rhythms to cope with extreme seasonality in availability of resources. To study the role of daylength on seasonal changes in body mass and reproductive function, we exposed male and female gray mouse lemurs to natural, constant, or alternating light cycles for 2 years under constant environmental conditions. When exposed to either constant short (SD: 10 h light/day), long (LD: 14 h light/day), or intermediate (ID: 12 h light/day) daylength, males and females maintained a constant body mass with no spontaneous cyclic variation. We only observed typical seasonal body mass changes in subjects exposed to alternating periods of SD and LD, the weight gain being triggered by SD, whereas weight loss occurred under LD. Reproductive activity in females proceeded from an endogenous rhythm that was expressed under constant daylengths. In contrast, changes in reproductive activity in males depended on daylength variation. In both sexes, SD and LD have direct inhibitory or stimulatory effects on reproductive activity. In females, daylength regulates breeding season by synchronizing an endogenous sexual rhythm with the season, whereas in males, the perception of a critical photoperiod is used to determine the subsequent onset or arrest of their breeding season. These sexual differences in the effect of daylength could be related to sex-specific differences in reproductive constraints.     

The Sound of Arousal: The Addition of Novel Non-linearities Increases Responsiveness in Marmot Alarm Calls

Vocal structure should reflect vocal function. While much attention has focused on quantifying attributes of harmonic vocalizations, the vocalizations of many species also may contain non-linear phenomena such as warbles, subharmonics, biphonation, and deterministic chaos or noise. The function of these non-linearities remains enigmatic. In some species, harmonic vocalizations abruptly become 'noisy' when individuals are physiologically aroused and the sudden onset of these non-linearities could signal arousal or fear to receivers. One untested functional hypothesis is that vocalizations containing non-linearities are more variable from one rendition to the next, and thus are harder to habituate to. In some situations, reducing the likelihood of habituation could be important. Signals that are highly evocative are more difficult to habituate to. Thus, we conducted playback experiments to foraging yellow-bellied marmots ( Marmota flaviventris ) to determine whether the addition of white noise (a non-linear acoustic phenomenon) to alarm calls elicited a greater response than control calls without the non-linearity or control calls with silence, rather than noise, added to them. Marmots spent less time foraging after hearing calls that included noise than after normal or control calls. This result is consistent with the unpredictability hypothesis and suggests that the adaptive value of non-linearities is to prevent habituation.     

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.