Behavioral responses to predator and heterospecific alarm calls are habitat-specific in Eurasian tree sparrows.

Acoustic communication plays a vital role in predator-prey interactions. Although habitat structure has been shown to affect anti-predator tactics, little is known about how animals vary their behaviors in response to predator calls or heterospecific alarm calls in different environments. Here we used sound playbacks to test the responses of Eurasian tree sparrows (Passer montanus) foraging in harvested/unharvested rice paddy and open residential area. In the first experiment, we tested their behavioral responses to dove calls, male common cuckoo (Cuculus canorus) calls, hawk-like calls mimicked by female common cuckoo, sparrowhawk (Accipiter nisus) calls, and human yell calls produced to scare birds (predator signal playbacks). In the second experiment, we tested their behavioral responses to the Japanese tit's (Parus minor) territorial songs and alarm calls (heterospecific alarm signal playbacks). Results showed that the tree sparrows had less fleeing in unharvested ripe rice paddy than in harvested rice paddy and open residential area. In predator signal playbacks, call type affected the escape behavior of sparrows in unharvested rice paddy and open residential area but not harvested rice paddy. In alarm signal playbacks, tit alarm calls evoked more fleeing than territorial songs in harvested rice paddy and open residential area but not unharvested rice paddy. These results suggest that anthropogenic habitat changes may influence avian anti-predator tactics.

Auditory sensitivity and tympanic middle ear in a vocal and a non-vocal frog.

The tympanic middle ear is important for anuran hearing on land. However, many species have partly or entirely lost their tympanic apparatus. Previous studies have compared hearing sensitivities in species that possess and lack tympanic membranes capable of sound production and acoustic communication. However, little is known about how these hearing abilities are comparable to those of mutant species. Here, we compared the eardrum and middle ear anatomies of two sympatric sibling species from a noisy stream habitat, namely the "non-vocal" Hainan torrent frog (Amolops hainanensis) and the "vocal" little torrent frog (Amolops torrentis), the latter of which is capable of acoustic communication. Our results showed that the relative (to head size) eardrum diameter of A. hainanensis was smaller than that of A. torrentis, although the absolute size was not smaller. Unlike A. torrentis, the tympanic membrane area of A. hainanensis was not clearly differentiated from the surrounding skin. The middle ear, however, was well-developed in both species. We measured the auditory brainstem responses (ABRs) of A. hainanensis and compared the ABR thresholds and latencies to those previously obtained for A. torrentis. Our results suggested that these two species exhibited significant differences in hearing sensitivity. A. hainanensis (smaller relative eardrum, nonvocal) had higher ABR thresholds and longer initial response times than A. torrentis (larger relative eardrum, vocal) at lower frequencies. Neurophysiological responses from the brain were obtained for tone pips between 800 Hz and 7,000 Hz, with peak sensitivities found at 3,000 Hz (73 dB SPL) for A. hainanensis, and at 1,800 Hz (61 dB SPL) for A. torrentis. Our results suggest that the non-vocal A. hainanensis has lower hearing sensitivity than its vocal sister species (i.e., A. torrentis), which may be related to differences in tympanic or inner ear structure and morphology.

Response to comment on 'Parasite defensive limb movements enhance acoustic signal attraction in male little torrent frogs'.

Recently we showed that limb movements associated with anti-parasite defenses can enhance acoustic signal attraction in male little torrent frogs (Amolops torrentis), which suggests a potential pathway for physical movements to become co-opted into mating displays (Zhao et al., 2022). Anderson et al. argue for alternative explanations of our results and provide a reanalysis of part of our data (Anderson et al., 2023). We acknowledge some of the points raised and provide an additional analysis in support of our hypothesis.

Geographical variation of the acoustic signals in the spot-legged treefrog (Polypedates megacephalus) of Hainan Island.

Geographical divergence in acoustic signals is often affected by multiple selective pressures. Environmental factors are expected to shape signals by adjusting for greater propagation efficiency. Nevertheless, such habitat-driven hypotheses have not been well-examined with multi-signal and multi-habitat types included simultaneously. In this study, we evaluated call similarity of the spot-legged treefrog (Polypedates megacephalus), characterized by multiple call types, from 11 geographic populations across Hainan Island. We also examined multiple factors (i.e. body mass, temperature, altitude, and vegetation) among different acoustical geographic clusters, and tested whether the variation in acoustic length and frequency among different habitats was in accordance with the prediction derived from the acoustic adaptation hypothesis. We showed that P. megacephalus from Hainan Island included 3 acoustic geographic clusters: the northeastern flatlands, the southwest mountains, and the hills around the mountains. We also showed that environmental factors (i.e. altitude and vegetation) varied across these 3 acoustically distinct areas. Moreover, the duration of the different call types supported the hypothesis that they should have optimal transmission in their own habitats. Thus, our results reveal the roles of ecological selection in the geographical divergence of anuran acoustic signals.

Avian Alarm Calls Do Not Induce Anti-Predator Response in Three Anuran Species.

Many species produce alarm calls in response to predators, and the anti-predator signals are often used by other species. Eavesdropping on heterospecific alarm calls has been widely found in bird and mammal species. Other taxa, such as reptiles and amphibians, however, receive limited attention at present. Here, we selected three types of alarm calls of Japanese Tits (Parus minor) that were evoked by the Siberian Chipmunk (Eutamias sibiricus), Eurasian Sparrow Hawk (Accipiter nisus), and model snake (Elaphe spp.), respectively, and then carried out playback experiments to test whether three frog species changed their behaviors in response to the three treatments of Japanese Tit calls while the tit's territory song was used as a control. The results showed that Little Torrent Frogs (Amolops torrentis), Ornamented Pygmy Frogs (Microhyla fissipes) and Spot-legged Treefrogs (Polypedates megacephalus) did not jump off their positions in response to the same four acoustic signals. They also did not change their calling behaviors in response to the alarm calls of Japanese Tits. This study found no evidence that these anuran species can eavesdrop on heterospecific tits' alarm signals.

Parasite defensive limb movements enhance acoustic signal attraction in male little torrent frogs.

Many animals rely on complex signals that target multiple senses to attract mates and repel rivals. These multimodal displays can however also attract unintended receivers, which can be an important driver of signal complexity. Despite being taxonomically widespread, we often lack insight into how multimodal signals evolve from unimodal signals and in particular what roles unintended eavesdroppers play. Here, we assess whether the physical movements of parasite defense behavior increase the complexity and attractiveness of an acoustic sexual signal in the little torrent frog (Amolops torrentis). Calling males of this species often display limb movements in order to defend against blood-sucking parasites such as frog-biting midges that eavesdrop on their acoustic signal. Through mate choice tests we show that some of these midge-evoked movements influence female preference for acoustic signals. Our data suggest that midge-induced movements may be incorporated into a sexual display, targeting both hearing and vision in the intended receiver. Females may play an important role in incorporating these multiple components because they prefer signals which combine multiple modalities. Our results thus help to understand the relationship between natural and sexual selection pressure operating on signalers and how in turn this may influence multimodal signal evolution.

Noise constrains the evolution of call frequency contours in flowing water frogs: a comparative analysis in two clades.

BACKGROUND: The acoustic adaptation hypothesis (AAH) states that signals should evolve towards an optimal transmission of the intended information from senders to intended receivers given the environmental constraints of the medium that they traverse. To date, most AAH studies have focused on the effect of stratified vegetation on signal propagation. These studies, based on the AAH, predict that acoustic signals should experience less attenuation and degradation where habitats are less acoustically complex. Here, we explored this effect by including an environmental noise dimension to test some AAH predictions in two clades of widespread amphibians (Bufonidae and Ranidae) that actively use acoustic signals for communication. By using data from 106 species in these clades, we focused on the characterization of the differences in dominant frequency (DF) and frequency contour (i.e., frequency modulation [FM] and harmonic performances) of mating calls and compared them between species that inhabit flowing-water or still-water environments. RESULTS: After including temperature, body size, habitat type and phylogenetic relationships, we found that DF differences among species were explained mostly by body size and habitat structure. We also showed that species living in lentic habitats tend to have advertisement calls characterized by well-defined FM and harmonics. Likewise, our results suggest that flowing-water habitats can constrain the evolutionary trajectories of the frequency-contour traits of advertisement calls in these anurans. CONCLUSIONS: Our results may support AAH predictions in frogs that vocalize in noisy habitats because flowing-water environments often produce persistent ambient noise. For instance, these anurans tend to generate vocalizations with less well-defined FM and harmonic traits. These findings may help us understand how noise in the environment can influence natural selection as it shapes acoustic signals in affected species.

Photosensitive MRI biosensor for BCRP-Targeted uptake and light-induced inhibition of tumor cells.

Riboflavin and its derivatives are the most important coenzymes in vivo metabolism, and are closely related to life activities. In this paper, the first photolysis 129Xe biosensor was developed by combining cryptophane-A with riboflavin moiety, which showed photosensitivity recorded by hyperpolarized 129Xe NMR/MRI technology with an obvious chemical shift change of 5.3 ppm in aqueous solution. Cellular fluorescence imaging confirmed that the biosensor could be enriched in MCF-7 cells, and MTT assays confirmed that the cytotoxicity was enhanced after irradiation. Findings suggested that the biosensor has a potential application in tumor targeting and the inhibition of tumor cell proliferation after photodegradation.

An intracellular diamine oxidase triggered hyperpolarized 129Xe magnetic resonance biosensor.

Here, a novel method was developed for suppressing 129Xe signals in cucurbit[6]uril (CB6) until the trigger is activated by a specific enzyme. Due to its noncovalent interactions with amino-groups and CB6, putrescine dihydrochloride (Put) was chosen for blocking interactions between 129Xe and CB6. Upon adding diamine oxidase (DAO), Put was released from CB6 and a 129Xe@CB6 Hyper-CEST signal emerged. This proposed 129Xe biosensor was then tested in small intestinal villus epithelial cells.

Investigation of the potential risk of coal fire to local environment: A case study of Daquanhu coal fire, Xinjiang region, China.

Underground coal fires are disasters associated with coal mining activities. This study, attempts to investigate the impact of coal fires on the soil and atmosphere by measuring heavy metal concentration and borehole gas emissions for the Daquanhu coal fire zone. Different methods and equipment were used in this study, such as remote sensing, determination of the surface temperature and vegetation, field meteorological surveys, air/smoke analysis, flame photometry, atomic absorption spectrophotometry, atomic fluorescence spectrophotometry, and alkali diffusion. The results show that the surface temperature of the Daquanhu coal fire zone was reduced with a progress in coal fire extinction since 2015. Surface vegetation grew better in 2016 than in other years. The mercury (Hg) content in the western part of the fire zone is much higher than that in other parts of the fire zone. The arsenic (As) content in the eastern part is much higher than that of other parts. Data show that the estimated total amount of gas emissions during fire extinction is ~31,500 kg for CO, 489 kg for SO2, 12,885 kg for NO, 576 kg for NO2, and 20,295 kg for NOx. The intensity of the gas emissions during extinction is notably higher than that before extinction. The results also indicate coal fire's potential risk to adjacent communities, especially the risks associated with borehole injection of large amounts of possible harmful slurry, which needs to be taken seriously.

Males increase call frequency, not intensity, in response to noise, revealing no Lombard effect in the little torrent frog.

Noise is one of the main factors that can influence the processes of sound communication across a wide range of animal groups. Although the effects of ambient noise on animal communication, including anthropogenic noise, have received increasing attention, few studies have examined changes in the fine structure of acoustic signals produced by vocalizing species in constantly noisy environments. Here, we used natural recordings to determine the associations between stream noise and call parameters in the little torrent frog (Amolops torrentis). We also used playbacks of stream noise recorded in natural habitats and playbacks of white noise to examine how male vocal signals change with increasing noise levels. The results show that noise intensity has a significant effect on male call frequency, but not on call amplitude or other call characteristics. Based on this evidence, we suggest that in streamside species stream noise drives males to alter call frequency and call as loudly as possible in order to improve discriminability. These findings provide insights into the role played by ecological selection in the evolution of noise-dependent anuran vocal plasticity.

Correction to: Sometimes noise is beneficial: stream noise informs vocal communication in the little torrent frog Amolops torrentis.

[This corrects the article DOI: 10.1007/s10164-017-0515-y.].

Sometimes noise is beneficial: stream noise informs vocal communication in the little torrent frog Amolops torrentis.

Many kinds of environmental noise can interfere with acoustic communication and efficient decision making in terrestrial species. Here we identified an exception to this generalization in a streamside species, the little torrent frog (Amolops torrentis) which communicates in a stream noise environment. To determine whether stream noise can act as a cue regarding the microhabitat characteristics of senders, we performed phonotaxis experiments using stimulus pairs constructed with synthetic male calls (high or low dominant frequency) and stream noise with varied signal-to-noise ratios. We found that females prefer calls with high amplitude stream noise added compared to those with low amplitude stream noise added for both high and low dominant frequency stimulus pairs; however, stream noise itself was not attractive in the absence of calls. These results show that stream noise can function as a cue that may be used by females for enhancing the attractiveness of calls. Stream noise associates closely with rocks, topographies and vegetation and may thus provide useful microhabitat information for signal receivers, thereby acting on sexual selection. These data therefore contribute to our understanding of how the perception of mate attractiveness in heterogeneous ecological environments can evolve.

Male-male competition and female choice are differentially affected by male call acoustics in the serrate-legged small treefrog, Kurixalus odontotarsus.

BACKGROUND: The evolution of exaggerated vocal signals in anuran species is an important topic. Males and females have both evolved the ability to discriminate communication sounds. However, the nature of sexual dimorphism in cognition and sensory discrimination and in the evolution and limitation of sexual signal exaggeration remain relatively unexplored. METHODS: In the present study, we used male calls of varied complexity in the serrate-legged small treefrog, Kurixalus odontotarsus, as probes to investigate how both sexes respond to variations in call complexity and how sex differences in signal discrimination play a role in the evolution of sexual signal exaggeration. The compound calls of male K. odontotarsus consist of a series of one or more harmonic notes (A notes) which may be followed by one or more short broadband notes (B notes). RESULTS: Male playback experiments and female phonotaxis tests showed that increasing the number of A notes in stimulus calls elicits increased numbers of response calls by males and increases the attractiveness of the stimulus calls to females. The addition of B notes, however, reduces male calling responses. Moreover, call stimuli which contain only B notes suppress spontaneous male calling responses. Phonotaxis experiments show that females prefer calls with greater numbers of A notes and calls containing both A notes and B notes, but do not prefer calls with only B notes. DISCUSSION: Male-male competition and female choice appear to have played different roles in the evolution and limitation of signal complexity in K. odontotarsus. These results provide new insights into how exaggerated compound signals evolve and how signal complexity may be limited in anurans.

An exception to the matched filter hypothesis: A mismatch of male call frequency and female best hearing frequency in a torrent frog.

The matched filter hypothesis proposes that the tuning of auditory sensitivity and the spectral character of calls will match in order to maximize auditory processing efficiency during courtship. In this study, we analyzed the acoustic structure of male calls and both male and female hearing sensitivities in the little torrent frog (Amolops torrentis), an anuran species who transmits acoustic signals across streams. The results were in striking contradiction to the matched filter hypothesis. Auditory brainstem response results showed that the best hearing range was 1.6-2 kHz consistent with the best sensitive frequency of most terrestrial lentic taxa, yet completely mismatched with the dominant frequency of conspecific calls (4.3 kHz). Moreover, phonotaxis tests show that females strongly prefer high-frequency (4.3 kHz) over low-frequency calls (1.6 kHz) regardless of ambient noise levels, although peripheral auditory sensitivity is highest in the 1.6-2 kHz range. These results are consistent with the idea that A. torrentis evolved from nonstreamside species and that high-frequency calls evolved under the pressure of stream noise. Our results also suggest that female preferences based on central auditory system characteristics may evolve independently of peripheral auditory system sensitivity in order to maximize communication effectiveness in noisy environments.

Bigger Is Not Always Better: Females Prefer Males of Mean Body Size in Philautus odontotarsus.

Most species are believed to evolve larger body sizes over evolutionary time. Previous studies have suggested that sexual selection, through male-male competition and female choice, favors larger males. However, there is little evidence of selection against large size. The female serrate-legged small treefrogs (Philautus odontotarsus) must carry passive males from leks to breeding grounds over relatively long distances after amplexus to find a suitable place to lay eggs. The costs of large male size may therefore decrease mating success due to reduced agility and/or higher energy requirements. Thus, we hypothesized that selection would not favor larger males in P. odontotarsus. Females can assess male body size on the basis of the dominant frequency of male calls in frogs. To assess female P. odontotarsus preferences for a potential mate's body size, male calls of high, average and low dominant frequency were played back to the females in phonotaxis experiments. Results showed that most females prefer the advertisement call with average dominant frequency. In addition, we compared the body mass distribution of amplectant males with that of single males in nature. The body masses of amplectant males are more narrowly distributed in the intermediate range than that of single males. The phonotaxis results and the data of actual female preferences in the field show that females strongly prefer potential mates of mean body sizes, consistent with the view that, in this species at least, larger males are not always perceived as better by females. In the present study, P. odontotarsus provides an example of an amphibian species in which large size does not have an advantage in mating success for males. Instead, our results provide evidences that stabilizing selection favors the optimal intermediate size of males.