Diego Llusia

Sex and age-class differences in calls of Iberian red deer during the rut: reversed sex dimorphism of pitch and contrasting roars from farmed and wild stags

Stag rutting calls differ among subspecies of red deer Cervus elaphus. Studying sex-, age-, and subspecies-related vocal variation may highlight the forces driving this evolution. This study presents the first bioacoustical comparison of oral calls produced during the rut by Iberian red deer Cervus elaphus hispanicus stags, hinds and calves and compares the acoustics of nasal and oral calls of hinds and calves. Also, it provides the first comparison of rutting roars between farmed and wild stags. Call maximum and mean fundamental frequencies (f0max and f0mean) were higher in farmed than in wild stags. Moreover, hinds had lower f0max and f0mean compared with both farmed and wild stags. The call minimum fundamental frequency (f0min) was indistinguishable between all groups of adults, irrespective of sex, farming and nasal versus oral vocal emission. In calves, but not in hinds, oral calls had higher f0max and f0mean compared with nasal calls. The higher fundamental frequencies in farmed as compared with wild stags may have resulted from emotional arousal due to human presence at recordings or from the higher body conditions of stags reared under a farm. The comparison of our results with previously published data on various subspecies of red deer suggests that there are different pathways of vocal ontogeny in eastern and western branches of Cervus elaphus and that the acoustics of stag and hind calls are more similar within the various subspecies than they are among the subspecies.

TERRESTRIAL SOUND MONITORING SYSTEMS, A METHODOLOGY FOR QUANTITATIVE CALIBRATION

ABSTRACT We present a series of practical techniques designed to standardize, quantify and allow comparison of population information obtained from periodic automated terrestrial recordings of acoustic animals. From the experience obtained mainly from anuran monitoring systems, we discuss issues such as establishing comparable recording levels, calibrating the detection space for each station, establishing correlations with population densities and comparison with other acoustical surveys. We emphasize the need to obtain species-specific data on source levels (sound pressure levels).

Propagation of natural toad calls in a Mediterranean terrestrial environment

Propagation patterns of animal acoustic signals provide insights into the evolution of signal design to convey signalers information to potential recipients. However, propagation properties of vertebrate calls have been rarely studied using natural calls from individuals; instead playback calls broadcast through loudspeakers have been used extensively, a procedure that may involve acoustical and physical features differing from natural sounds. Measurements of the transmission characteristics of natural advertisement calls, which are simple tonal sounds, of the Iberian midwife toad, Alytes cisternasii, were carried out, and the results were compared with previously published results broadcasting recorded calls of the same species. Measurements of sound pressure level (SPL) of calls from individual male A. cisternasii revealed that the call amplitude decreases at distances of 1-8 m from the source at rates averaging 1-5 dB above spherical transmission loss in an omni-directional pattern. A comparison between SPLs of natural calls in the current study and of playback calls from a previous study showed that patterns of propagation did not differ in average values, but variance was significantly higher for natural calls. Results suggest that using broadcast signals for transmission experiments may result in a simplification of the conditions in which actual animals communicate in nature.

Call transmission efficiency in native and invasive anurans: competing hypotheses of divergence in acoustic signals

Invasive species are a leading cause of the current biodiversity decline, and hence examining the major traits favouring invasion is a key and long-standing goal of invasion biology. Despite the prominent role of the advertisement calls in sexual selection and reproduction, very little attention has been paid to the features of acoustic communication of invasive species in nonindigenous habitats and their potential impacts on native species. Here we compare for the first time the transmission efficiency of the advertisement calls of native and invasive species, searching for competitive advantages for acoustic communication and reproduction of introduced taxa, and providing insights into competing hypotheses in evolutionary divergence of acoustic signals: acoustic adaptation vs. morphological constraints. Using sound propagation experiments, we measured the attenuation rates of pure tones (0.2–5 kHz) and playback calls (Lithobates catesbeianus and Pelophylax perezi) across four distances (1, 2, 4, and 8 m) and over two substrates (water and soil) in seven Iberian localities. All factors considered (signal type, distance, substrate, and locality) affected transmission efficiency of acoustic signals, which was maximized with lower frequency sounds, shorter distances, and over water surface. Despite being broadcast in nonindigenous habitats, the advertisement calls of invasive L. catesbeianus were propagated more efficiently than those of the native species, in both aquatic and terrestrial substrates, and in most of the study sites. This implies absence of optimal relationship between native environments and propagation of acoustic signals in anurans, in contrast to what predicted by the acoustic adaptation hypothesis, and it might render these vertebrates particularly vulnerable to intrusion of invasive species producing low frequency signals, such as L. catesbeianus. Our findings suggest that mechanisms optimizing sound transmission in native habitat can play a less significant role than other selective forces or biological constraints in evolutionary design of anuran acoustic signals.

Temperature-induced shifts in hibernation behavior in experimental amphibian populations

Phenological shifts are primary responses of species to recent climate change. Such changes might lead to temporal mismatches in food webs and exacerbate species vulnerability. Yet insights into this phenomenon through experimental approaches are still scarce, especially in amphibians, which are particularly sensitive to changing thermal environments. Here, under controlled warming conditions, we report a critical, but poorly studied, life-cycle stage (i.e., hibernation) in frogs inhabiting subtropical latitudes. Using outdoor mesocosm experiments, we examined the effects of temperature (ambient vs. + ~2.2/2.4 °C of pre-/post-hibernation warming) and food availability (normal vs. 1/3 food) on the date of entrance into/emergence from hibernation in Pelophylax nigromaculatus. We found temperature was the major factor determining the hibernation period, which showed a significant shortening under experimental warming (6–8 days), with delays in autumn and advances in spring. Moreover, the timing of hibernation was not affected by food availability, whereas sex and, particularly, age were key factors in the species’ phenological responses. Specifically, male individuals emerged from hibernation earlier, while older individuals also entered and emerged from hibernation earlier. We believe that this study provides some of the first experimental evidence for the effect of climate warming on the timing of amphibian hibernation.

Neither convergence nor divergence in the advertisement call of sympatric congeneric Neotropical treefrogs

Sympatric species communicating by means of sounds share the same acoustic space, which may cause masking interference affecting the signal recognition processes. This should be especially problematic in congeneric species that tend to exhibit similar acoustic signals and behavioural traits. Thus, congeneric species in sympatry would presumably experience diversification pressures that lead to more intense call divergences than in congeneric species in allopatry. However, recent studies showed cases of signal convergence in sympatry, presenting opposite hypotheses such as convergence by adaptation to a common habitat. Therefore, to test these hypotheses, we analysed the advertisement calls and geographic distribution of 10 species of Sphaenorhynchus (i.e. a monophyletic genus of Neotropical hylids), which occur in sympatry with at least one congeneric species. Using two similarity analyses: multivariate comparison [unweighted pair group method with arithmetic mean (UPGMA)] and spectrogram cross-correlation (SPCC), and two thresholds of grouping (high and low), we searched for association between species distribution (sympatric and allopatric) and call similarity (grouped and ungrouped). Although assuming different principles, both UPGMA and SPCC methods provided extremely similar results. Sympatric species tend to be less often grouped by call similarity than allopatric species, with 0–15% of sympatric species grouped for both similarity methods. However, associations between variables were not confirmed by frequency distributions in contingency tables or by similarity values in the pairs of sympatric and allopatric species. Consequently, neither call divergence nor convergence in sympatry was supported by these results, fostering further investigation about other potential mechanisms underlying anuran call evolution, and suggesting a possible random distribution of call variables in the acoustic space.

Effects of temperature on the song parameters of the Moroccan bushcricket Eugaster spinulosa (Orthoptera, Tettigoniidae)

Acoustic signals are important for inter- and intraspecific interactions in many species. Their information potential depends largely on species characteristics. Here we describe quantitatively the song of Eugaster spinulosa (Johannson 1763), (Orthoptera, Tettigoniidae) and analyse the relationships of song parameters with temperature. To the best of our knowledge there are no previous descriptions available of the song of any species in the genus. Songs of seven males from the mountains of Jebilet, Marrakech (Morocco), were recorded in a semi-anechoic chamber for 105 days. Using automated thermal tables, individuals were exposed to a daily cycle of temperatures between 17.5 and 41.5°C. The calling song of Eugaster spinulosa is broader in frequency (2–28 kHz) than the song of other tettigoniids. It consists of extended series of separately audible echemes, which are polysyllabic and comprise a variable number of broadband syllables, usually between 5 and 10. The stridulatory activity of Eugaster spinulosa showed a wide thermal plasticity (ranging over 24°C between thermal thresholds). In addition to changes in temporal features, we found that an increase in temperature reduced the number of syllables per echeme.

Synthetic rainfall vibrations evoke toad emergence

Toads occupy underground refugia during periods of daily or seasonal inactivity, emerging only during rainfall [1]. We test the hypothesis that rainfall-induced vibrations in soil are the cues that trigger the emergence of toads from underground. Using playback experiments in the absence of natural rainfall in native habitats, we observed that two Iberian toad species (Pelobates cultripes and Bufo calamita) emerged significantly earlier than controls when exposed to low-frequency soil vibrations that closely mimic those of rainfall. Our results suggest that detection of abiotic seismic events are biologically relevant and widespread in arid-zone anurans. These findings provide insights into the evolutionary role played by the two low-frequency-tuned inner-ear organs in anuran amphibians - the amphibian papilla and sacculus, both detectors of weak environmental vibrational cues.

Acoustic communities reflects lateral hydrological connectivity in riverine floodplain similarly to macroinvertebrate communities

Recent studies revealed that information on ecological patterns and processes can be investigated using sounds emanating from animal communities. In freshwater environments, animal communities are strongly shaped by key ecological factors such as lateral connectivity and temperature. We predict that those ecological factors are linked to acoustic communities formed by the collection of sounds emitted underwater. To test this prediction, we deployed a passive acoustic monitoring during 15 days in six floodplain channels of the European river Rhône. The six channels differed in their temperature and level of lateral connectivity to the main river. In parallel, we assessed the macroinvertebrate communities of these six channels using classical net sampling methods. A total of 128 sound types and 142 animal taxa were inventoried revealing an important underwater diversity. This diversity, instead of being randomly distributed among the six floodplain channels, was site-specific. Generalized mixed-effects models demonstrated a strong effect of both temperature and lateral connectivity on acoustic community composition. These results, congruent with macroinvertebrate community composition, suggest that acoustic communities reflect the interactions between animal communities and their environment. Overall our study strongly supports the perspectives offered by acoustic monitoring to describe and understand ecological patterns in freshwater environments.

The advertisement calls of Brazilian anurans: Historical review, current knowledge and future directions

Advertisement calls are often used as essential basic information in studies of animal behaviour, ecology, evolution, conservation, taxonomy or biodiversity inventories. Yet the description of this type of acoustic signals is far to be completed, especially in tropical regions, and is frequently non-standardized or limited in information, restricting the application of bioacoustics in science. Here we conducted a scientometric review of the described adverstisement calls of anuran species of Brazil, the world richest territory in anurans, to evaluate the amount, standard and trends of the knowledge on this key life-history trait and to identify gaps and directions for future research strategies. Based on our review, 607 studies have been published between 1960 to 2016 describing the calls of 719 Brazilian anuran species (68.8% of all species), a publication rate of 10.6 descriptions per year. From each of these studies, thirty-one variables were recorded and examined with descriptive and inferential statistics. In spite of an exponential rise over the last six decades in the number of studies, described calls, and quantity of published metadata, as revealed by regression models, clear shortfalls were identified with regard to anuran families, biomes, and categories of threat. More than 55% of these species belong to the two richest families, Hylidae or Leptodactylidae. The lowest percentage of species with described calls corresponds to the most diverse biomes, namely Atlantic Forest (65.1%) and Amazon (71.5%), and to the IUCN categories of threat (56.8%), relative to the less-than-threatened categories (74.3%). Moreover, only 52.3% of the species have some of its calls deposited in the main scientific sound collections. Our findings evidence remarkable knowledge gaps on advertisement calls of Brazilian anuran species, emphasizing the need of further efforts in standardizing and increasing the description of anuran calls for their application in studies of the behaviour, ecology, biogeography or taxonomy of the species.