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    Human magnetic sense is mediated by a light and magnetic field resonance-dependent mechanism

    SubjectsThe study comprised 34 men (19–26 years, mean 23 years; body mass index 19–31 kg/m2, mean 24 kg/m2) with no physical disabilities or mental disorders, including color blindness and claustrophobia30,31. All subjects were informed of the aims, the study procedure, and the financial compensation for participation, and were asked to follow the rules of the study. Prior to each experiment, subjects underwent short-term starvation31,54 (18–20 h; no food except pure water after lunch (12–1 pm) or dinner (6–7 pm), no later than 1 pm or 7 pm, respectively, one the day before the test), no medical treatments, and normal sleep (at least 6 h, between 10 pm the day before the test day to 8 am on the test day)31. Prior to starting each experiment, subjects were stabilized on a chair for ~ 10 min in a room next to the testing room. Based on an assessment with a pre-experiment questionnaire and the first blood glucose level, measured before starting the experiment (see “Geomagnetic orientation assay” section below), subjects who had not followed these rules were not allowed to take the test on the day and the test was postponed. The study was approved by the Institutional Review Board of Kyungpook National University and all the procedures followed the regulations for human subject research. Informed consent was obtained from all subjects.Modulation of GMFThe ambient GMF in the testing room had a total intensity 45.0 μT, inclination 53°, and declination − 7° (Daegu city, Republic of Korea); the total intensity of 50.0 μT in our previous study31 was changed due to a reconstruction of the building; 45.0 μT was maintained throughout the period of this study. To provide the subjects with various GMF-like magnetic fields (i.e., by modulating of total intensity, inclination, or direction of magnetic north), the coil system from our previous studies6,7,31 was used. It comprised three double-wrapped, orthogonal, rectangular Helmholtz coils (1.890 × 1.890 m, 1.890 × 1.800 m, and 1.980 × 1.980 m for the north–south, east–west, and vertical axes, respectively), electrically-grounded with copper mesh shielding. The subject was seated on a rotatable plastic chair with no metal components, at the center of the three-dimensional coils with his head positioned in the middle space of the vertical axis of the coils. To modulate the geomagnetic north, each pair of coils was supplied with direct current from a power supply (MK3003P; MKPOWER, Republic of Korea). The magnetic field was measured using a 3-axis magnetometer (MGM 3AXIS; ALPHALAB, USA); the field homogeneity at the position of the subject’s head was found to be 95%. The testing room was shielded by a six-sided Faraday cage comprising 10 mm thick aluminum plates, and was grounded during the entire experiment40. Background electromagnetic noise was measured inside the coils at the start and the end of each experimental day. It was attenuated by the Faraday cage more than 200-fold over the range from 500 Hz to 100 MHz as described in detail in our previous study31. The 60 Hz power frequency magnetic field was no more than 2 nT (3D NF Analyzer NFA 1000; Gigahertz Solutions, Germany). All electronic devices were placed outside the Faraday cage during the experiments, with the exception of the switch button module for GMF modulation and the antenna for generating the oscillating magnetic fields. The temperature experienced by the subjects was maintained at 25 ± 0.5 °C (Data logger 98,581; MIC Meter Industrial, Taiwan) by air circulation through the honeycomb on the ceiling of the Faraday cage31.Geomagnetic orientation assayAdopting a two-alternative forced choice (2-AFC) paradigm33,34, a geomagnetic orientation assay was conducted similar to our previous study31. Experiments were performed at 09:30–11:30 am or 1:00–5:00 pm (local time, UTC + 09:00) (each experiment: 50 min–1 h 10 min; mean ≈ 1 h, which was shorter by approximately 30 min than that in the previous study: 1 h 20 min–1 h 40 min; mean ≈ 1 h 30 min). Depending on the experiment, starved or unstarved subjects were tested individually. Prior to each experiment, the subjects were asked to remain with their heads facing the front, with eyes closed and earmuffs on during the experiment. In particular, they were asked to concentrate on sensing, if they could, the ambient geomagnetic north during the association phase, and to use the sensed information, depending on the experiment, to orient toward one of the two modulated magnetic norths (0°/180° for magnetic north–south axis or 90°/270° for magnetic east–west axis, rotated clockwise with respect to the ambient geomagnetic north) during the test phase. Subjects were instructed to avoid distracting thoughts and to think immediately “which direction is modulated magnetic north?” whenever they were distracted during the test phase, or felt they were being biased by experiences from earlier experiments. While seated on the rotatable chair, the subject’s blood glucose level was measured shortly before the first session and immediately after each session with eyes open except in the ‘dark’ experiment (Accu-Chek Guide; Roche, Germany)31. If the determined value before the first session varied by more than 15% relative to the mean (Table S2)31, the experiment was postponed and repeated at a later date (approximately 2% of experiments). The subjects were stabilized with eyes closed for 2 min before the first trial in the absence of visual, auditory, olfactory, and haptic sensory cues. For the ‘dark’ experiment (light intensity ≈ 0 lx), subjects wore home-made ‘blind’ goggles and were stabilized with eyes closed for 5 min55,56, and then asked whether they could see any light. If they could, the goggles were adjusted to prevent leakage of light, and the subject then had another 5 min of stabilization with eyes closed before starting the experiment. The subjects were illuminated with light from a filtered/non-filtered diffused light-emitting diode, depending on the experiment (Table S1). The home-made filter goggles were worn throughout the experiment, including the association and test phase, when required. The goggles contained glass filters (Tae Young Optics, Republic of Korea) to provide the eyes with particular wavelengths of light (Spectrometer USB4000-UV-VIS, Ocean Optics, USA) (Fig. S1). Each experiment consisted of 16 sequential trials for ‘no-association’ and ‘food-association’. For the food-association, a subject facing toward the ambient geomagnetic north was gently provided with a chocolate chip31 on his right palm by an experimenter, and given 30 s to eat it, while during no-association trials, food was not provided during the association phase. After a subsequent 5 s interval, the experimenter gently touched the subject’s right thenar area using a paper rod, as the cue to start the test. One of the two modulated magnetic north directions, depending on the experiment, was randomly provided 3 s before the cue for the test. Each of the modulated magnetic north directions was provided eight times for the no-association and food-association sessions. Subjects were informed of the nearly equal probability for each of the modulated magnetic north directions before each experiment. With the touch cue, subjects were asked to rotate freely toward any direction (clockwise or counterclockwise) by themselves (1–4 cycles of two-thirds rotation) and try to sense the direction of the modulated magnetic north during a 1 min period. Rotation was allowed within the rotation angle (− 30° to 210° for the magnetic north–south axis or − 120° to 120° for the east–west axis, depending on experiments, with respect to the ambient magnetic north), which was confined by the plastic stool (Fig. 1A) touching the left or right ankle of the subjects. When subjects determined the direction of the magnetic north, they stopped rotating to face toward the direction and lifted their right hand to indicate the direction to the experimenter. The direction was measured by the experimenter at 10° intervals using the scale on the walls of the Faraday cage31. A prerequisite for correct orientation was that the subject indicated the direction within the range of 30° to the both sides with respect to the magnetic cardinal directions, which was instructed to the subjects before each experiment. When the direction the subjects indicated was out of the 30° range, the trial was not included in the data and was repeated (approximately 0.63% of trials). Before the subsequent trial, the subject was gently rotated to face toward the ambient geomagnetic north and then rested for 5 s. For the ‘dark’ experiment, subjects were asked whether they could see any leaked light immediately after the last measurement of blood glucose level at the end of experiment. If the subject could see leaked light, the experiment was nullified and repeated later on (approximately 3% of experiments; 2/68). All experiments were performed in a double-blind fashion. The experimenter who conducted the orientation assay knew whether a subject was starved or not, wearing filter goggles, and food-associated or not, but did not know the random magnetic north sequences that were controlled by the personal computer (PC) system. Another experimenter responsible for analyzing the data did not know whether the subject was starved or not, the experimental conditions, including light wavelengths, or whether an oscillating magnetic field had been provided to the subjects. Thus, none of the experimenters were aware of all the subject information and data during the experiments and data analysis. The correct orientation rate was calculated by (the number of correct orientation trials/total number of trials) (raw data, Appendix S3). All the subjects participated in all the experiments performed in random order with an interval of at least 3 days between experiments. After each experiment, the subjects were asked to answer a post-experiment questionnaire about whether they closed their eyes when required during the entire period of the experiment. In cases when a subject did not maintain closed eyes, the experiment was repeated (approximately 1% of experiments). For each subject, a preliminary experiment on the “magnetic north–south axis” was conducted twice (unstarved and starved for each) with no goggles for adaption to the experimental procedure. These data were not included in the results.Experiments with oscillating magnetic fieldsExperiments with oscillating magnetic fields were performed using the standard geomagnetic orientation assay described above. To produce the oscillating magnetic fields, oscillating currents from a function generator (AFG3021; Tektronix, USA. For each magnetic field, sweep of 500 ms; interval of 1 ms. See Fig. S6A) were amplified (ENI 2100L RF power amplifier; Bell Electronics, USA) and fed into a calibrated coil antenna (30 cm diameter, 6509 loop antenna; ETS-LINDGREN, USA) mounted on a wooden frame, comprised of a single winding of coaxial cable. The oscillating magnetic fields were measured daily, before the first and after the last experiment of the day, using a spectrum analyzer (SPA-921TG; Com-Power, USA) with a calibrated loop antenna (48 cm diameter, AL-130R; Com-Power, USA) and a calibrated magnetometer (Probe HF 3061, NBM-550; Narda, Germany). Magnetic field intensities were measured on the glabella of the subjects; variations in intensity between subjects due to different seating heights were less than 10% of the average values (Table S3). The function generator and amplifier were placed outside the Faraday cage, and switched on during the dummy load control experiments with no signal from the PC system. The band widths of the monochromatic magnetic fields, i.e., 1.260 and 1.890 MHz were 0.020 and 0.019 MHz (“average”, √3 kHz), respectively, at the bottoms of the peaks. During the test phase, the maximum values of magnetic noise on the glabella of subjects including the dummy load did not exceed the following values: (1) 5 Hz–9 kHz; 2 nT/√ 2 kHz of “average” and 8 nT/√ 9 kHz of “max-hold” (0.05 nT/√ 2 kHz of “average” and 5 nT/√ 9 kHz of “max-hold” in the dummy load) (3D NF Analyzer NFA 1000; Gigahertz Solutions, Germany); (2) 9 kHz–500 kHz; 5 nT/√ 3 kHz of “average” and 8 nT/√ 3 kHz of “max-hold” (≈ 0 nT/√ 3 kHz of “average” and ≈ 1 nT/√ 3 kHz of “max-hold” in the dummy load) (the AL-130R antenna) (Fig. S6C); and (3) 500 kHz–30 MHz; 0.006 nT of 3.780 MHz harmonic in the 1.260 MHz, 0.03 nT of 5.670 MHz harmonic in the 1.890 MHz, and ≈ 0 nT in the dummy load (/√ 10 kHz of “average”) (Fig. S6B), and 0.15 nT/√ 10 kHz of “max-hold” at the same frequencies above and ≈ 0 nT in the dummy load (the AL-130R antenna).Statistical analysisTo determine the significance of orientation data from the 2-AFC paradigm, a one-sample t-test (test mean: 0.5), paired sample t-test, or two-sample t-test was performed using Origin software 11 (Origin, USA). To verify the reasonability of the t-tests, all data sets were checked using the Anderson–Darling test if the data follow a normal distribution (Appendix S4). To evaluate the difference between the means of two data sets when at least one of them did not show a normal distribution, the percentile bootstrap method57 was used (95% confidence interval, see Fig. S2, Appendices S1 and S2 for raw data). To analyze the blood glucose data, a paired sample t-test was used. Based on the results of previous study31, to describe different response groups of magnetic orientation in the 2-AFC paradigm, a principal component analysis36,37 was conducted on correct orientation rates by starved subjects, with no association/food-association under the full wavelength or  > 400 nm light conditions using SPSS 23 (IBM, USA). Following the principal component analysis calculation, the k-means clustering algorithm—one of the unsupervised learning methods—was used to objectively classify the groups58. The number of groups was two, and the distance between the center of the cluster and all points was Euclidean distance. The classification boundary was marked with the perpendicular bisector from the centers of the two groups. The first two principal components accounted for a significant portion of the total variance (73.1%; PC1 = 40.8%, PC2 = 32.3%). Statistical values are presented as mean ± SEM. More

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    Increasing salinity stress decreases the thermal tolerance of amphibian tadpoles in coastal areas of Taiwan

    Root, T. L. et al. Fingerprints of global warming on wild animals and plants. Nature 421, 57–60 (2003).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Meehl, G. A. et al. How much more global warming and sea level rise?. Science 307, 1769–1772 (2005).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Stocker, T. F. et al. (Cambridge University Press, 2013).Kopp, R. E. et al. Probabilistic 21st and 22nd century sea-level projections at a global network of tide-gauge sites. Earth’s Future 2, 383–406 (2014).ADS 
    Article 

    Google Scholar 
    Church, J. A. & White, N. J. A 20th century acceleration in global sea‐level rise. Geophys. Res. Lett. 33 (2006).Church, J. A. & White, N. J. Sea-level rise from the late 19th to the early 21st century. Surv. Geophys. 32, 585–602 (2011).ADS 
    Article 

    Google Scholar 
    Vermeer, M. & Rahmstorf, S. Global sea level linked to global temperature. Proc. Natl. Acad. Sci. 106, 21527–21532 (2009).ADS 
    CAS 
    PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    Horton, B. P., Rahmstorf, S., Engelhart, S. E. & Kemp, A. C. Expert assessment of sea-level rise by AD 2100 and AD 2300. Quatern. Sci. Rev. 84, 1–6 (2014).ADS 
    Article 

    Google Scholar 
    Day, J. W., Pont, D., Hensel, P. F. & Ibañez, C. Impacts of sea-level rise on deltas in the Gulf of Mexico and the Mediterranean: The importance of pulsing events to sustainability. Estuaries 18, 636–647 (1995).CAS 
    Article 

    Google Scholar 
    Feagin, R. A., Sherman, D. J. & Grant, W. E. Coastal erosion, global sea-level rise, and the loss of sand dune plant habitats. Front. Ecol. Environ. 3, 359–364 (2005).Article 

    Google Scholar 
    Nicholls, R. J. Planning for the impacts of sea level rise. Oceanography 24, 144–157 (2011).Article 

    Google Scholar 
    Hinkel, J. et al. Coastal flood damage and adaptation costs under 21st century sea-level rise. Proc. Natl. Acad. Sci. 111, 3292–3297 (2014).ADS 
    CAS 
    PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    Deutsch, C. A. et al. Impacts of climate warming on terrestrial ectotherms across latitude. Proc. Natl. Acad. Sci. 105, 6668–6672 (2008).ADS 
    CAS 
    PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    Duarte, H. et al. Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities. Glob. Change Biol. 18, 412–421 (2012).ADS 
    Article 

    Google Scholar 
    Licht, P. & Brown, A. G. Behavioral thermoregulation and its role in the ecolgy of the red-bellied newt, Taricha rivularis. Ecology 48, 598–611 (1967).Article 

    Google Scholar 
    Feder, M. E. & Pough, F. H. Temperature selection by the red-backed salamander, Plethodon c. cinereus (Green) (Caudata: Plethodontidae). Comp. Biochem. Physiol. Part A Physiol. 50, 91–98 (1975).CAS 
    Article 

    Google Scholar 
    Keen, W. H. & Schroeder, E. E. Temperature selection and tolerance in three species of Ambystoma larvae. Copeia 1975, 523–530 (1975).Article 

    Google Scholar 
    Hoppe, D. M. Thermal tolerance in tadpoles of the chorus frog Pseudacris triseriata. Herpetologica. 318–321 (1978).Cupp Jr, P. V. Thermal tolerance of five salientian amphibians during development and metamorphosis. Herpetologica. 234–244 (1980).Howard, J. H., Wallace, R. L. & Stauffer, J. R. Critical thermal maxima in populations of Ambystoma macrodactylum from different elevations. J. Herpetol. 17, 400–402 (1983).Article 

    Google Scholar 
    Floyd, R. B. Ontogenetic change in the temperature tolerance of larval Bufo marinus (Anura: Bufonidae). Comp. Biochem. Physiol. A Physiol. 75, 267–271 (1983).Article 

    Google Scholar 
    Floyd, R. B. Effects of photoperiod and starvation on the temperature tolerance of larvae of the giant toad, Bufo marinus. Copeia 1985, 625–631 (1985).MathSciNet 
    Article 

    Google Scholar 
    Manis, M. L. & Claussen, D. L. Environmental and genetic influences on the thermal physiology of Rana sylvatica. J. Therm. Biol 11, 31–36 (1986).Article 

    Google Scholar 
    Layne, J., Claussen, D. & Manis, M. Effects of acclimation temperature, season, and time of day on the critical thermal maxima and minima of the crayfish Orconectes rusticus. J. Therm. Biol 12, 183–187 (1987).Article 

    Google Scholar 
    Lutterschmidt, W. I. & Hutchison, V. H. The critical thermal maximum: History and critique. Can. J. Zool. 75, 1561–1574 (1997).Article 

    Google Scholar 
    Simon, M. N., Ribeiro, P. L. & Navas, C. A. Upper thermal tolerance plasticity in tropical amphibian species from contrasting habitats: Implications for warming impact prediction. J. Therm. Biol 48, 36–44 (2015).Article 
    PubMed 

    Google Scholar 
    Boutilier, R., Donohoe, P., Tattersall, G. & West, T. Hypometabolic homeostasis in overwintering aquatic amphibians. J. Exp. Biol. 200, 387–400 (1997).CAS 
    Article 
    PubMed 

    Google Scholar 
    Shoemaker, V. & Nagy, K. A. Osmoregulation in amphibians and reptiles. Annu. Rev. Physiol. 39, 449–471 (1977).CAS 
    Article 
    PubMed 

    Google Scholar 
    Viertel, B. Salt tolerance of Rana temporaria: Spawning site selection and survival during embryonic development (Amphibia, Anura). Amphibia-Reptilia 20, 161–171 (1999).Article 

    Google Scholar 
    Wu, C.-S. & Kam, Y.-C. Thermal tolerance and thermoregulation by Taiwanese rhacophorid tadpoles (Buergeria japonica) living in geothermal hot springs and streams. Herpetologica 61, 35–46 (2005).Article 

    Google Scholar 
    Gomez-Mestre, I. & Tejedo, M. Local adaptation of an anuran amphibian to osmotically stressful environments. Evolution 57, 1889–1899 (2003).Article 
    PubMed 

    Google Scholar 
    Christy, M. T. & Dickman, C. R. Effects of salinity on tadpoles of the green and golden bell frog (Litoria aurea). Amphibia-Reptilia 23, 1–11 (2002).Article 

    Google Scholar 
    Wu, C.-S. & Kam, Y.-C. Effects of salinity on the survival, growth, development, and metamorphosis of Fejervarya limnocharis tadpoles living in brackish water. Zool. Sci. 26, 476–482 (2009).Article 

    Google Scholar 
    Wu, C. S., Yang, W. K., Lee, T. H., Gomez-Mestre, I. & Kam, Y. C. Salinity acclimation enhances salinity tolerance in tadpoles living in brackish water through increased Na+, K+-ATPase expression. J. Exp. Zool. A Ecol. Genet. Physiol. 321, 57–64 (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    Alexander, L. G., Lailvaux, S. P., Pechmann, J. H. & DeVries, P. J. Effects of salinity on early life stages of the Gulf Coast toad, Incilius nebulifer (Anura: Bufonidae). Copeia 2012, 106–114 (2012).Article 

    Google Scholar 
    Bernabò, I., Bonacci, A., Coscarelli, F., Tripepi, M. & Brunelli, E. Effects of salinity stress on Bufo balearicus and Bufo bufo tadpoles: Tolerance, morphological gill alterations and Na+/K+-ATPase localization. Aquat. Toxicol. 132, 119–133 (2013).Article 
    CAS 
    PubMed 

    Google Scholar 
    Kearney, B. D., Pell, R. J., Byrne, P. G. & Reina, R. D. Anuran larval developmental plasticity and survival in response to variable salinity of ecologically relevant timing and magnitude. J. Exp. Zool. A Ecol. Genet. Physiol. 321, 541–549 (2014).Article 
    PubMed 

    Google Scholar 
    Hsu, W. T., Wu, C. S., Hatch, K., Chang, Y. M. & Kam, Y. C. Full compensation of growth in salt-tolerant tadpoles after release from salinity stress. J. Zool. 304, 141–149 (2018).Article 

    Google Scholar 
    Hsu, W.-T. et al. Salinity acclimation affects survival and metamorphosis of crab-eating frog tadpoles. Herpetologica 68, 14–21 (2012).Article 

    Google Scholar 
    Lai, J.-C., Kam, Y.-C., Lin, H.-C. & Wu, C.-S. Enhanced salt tolerance of euryhaline tadpoles depends on increased Na+, K+-ATPase expression after salinity acclimation. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 227, 84–91 (2019).CAS 
    Article 

    Google Scholar 
    Brown, M. E. & Walls, S. C. Variation in salinity tolerance among larval anurans: Implications for community composition and the spread of an invasive, non-native species. Copeia 2013, 543–551 (2013).Article 

    Google Scholar 
    Balinsky, J. B. Adaptation of nitrogen metabolism to hyperosmotic environment in Amphibia. J. Exp. Zool. A Ecol. Genet. Physiol. 215, 335–350 (1981).CAS 

    Google Scholar 
    Duellman, W. & Trueb, L. Biology of Amphibians (John Hopkins University Press, 1994).
    Google Scholar 
    Alcala, A. C. Breeding behavior and early development of frogs of Negros, Philippine Islands. Copeia 1962, 679–726 (1962).Article 

    Google Scholar 
    Gordon, M. S. & Tucker, V. A. Osmotic regulation in the tadpoles of the crab-eating frog (Rana cancrivora). J. Exp. Biol. 42, 437–445 (1965).CAS 
    Article 

    Google Scholar 
    Dunson, W. A. Tolerance to high temperature and salinity by tadpoles of the Philippine frog, Rana cancrivora. Copeia 1977, 375–378 (1977).Article 

    Google Scholar 
    Uchiyama, M., Murakami, T., Wakasugi, C. & Yoshizawa, H. Structure of the kidney in the crab-eating frog, Rana cancrivora. J. Morphol. 204, 147–156 (1990).CAS 
    Article 
    PubMed 

    Google Scholar 
    Heo, K., Kim, Y. I., Bae, Y., Jang, Y. & Borzée, A. First report of Dryophytes japonicus tadpoles in saline environment. Russ. J. Herpetol. 26, 87–90 (2019).Article 

    Google Scholar 
    Jian, C. Y., Cheng, S. Y. & Chen, J. C. Temperature and salinity tolerances of yellowfin sea bream, Acanthopagrus latus, at different salinity and temperature levels. Aquac. Res. 34, 175–185 (2003).Article 

    Google Scholar 
    Sardella, B. A., Sanmarti, E. & Kültz, D. The acute temperature tolerance of green sturgeon (Acipenser medirostris) and the effect of environmental salinity. J. Exp. Zool. A Ecol. Genet. Physiol. 309, 477–483 (2008).Article 
    PubMed 

    Google Scholar 
    Everatt, M. J., Worland, M. R., Convey, P., Bale, J. S. & Hayward, S. A. The impact of salinity exposure on survival and temperature tolerance of the Antarctic collembolan Cryptopygus antarcticus. Physiol. Entomol. 38, 202–210 (2013).Article 

    Google Scholar 
    Kerby, J. L., Richards-Hrdlicka, K. L., Storfer, A. & Skelly, D. K. An examination of amphibian sensitivity to environmental contaminants: are amphibians poor canaries?. Ecol. Lett. 13, 60–67 (2010).Article 
    PubMed 

    Google Scholar 
    Chang, Y. M., Wu, C. S., Huang, Y. S., Sung, S. M. & Hwang, W. Occurrence and reproduction of anurans in brackish water in a coastal forest in Taiwan. Herpetol. Notes 9, 291–295 (2016).
    Google Scholar 
    Peng, T. R., Hsieh, Y. H. & Liu, T. S. Hydro chemical characteristics and salinization of groundwater in Yunlin area. J. Chin. Soil Water Conserv. 32, 173–189 (2005).
    Google Scholar 
    Gosner, K. L. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183–190 (1960).
    Google Scholar 
    Phillips, S. J., Anderson, R. P., Dudík, M., Schapire, R. E. & Blair, M. E. Opening the black box: An open-source release of Maxent. Ecography 40, 887–893 (2017).Article 

    Google Scholar 
    Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).Article 

    Google Scholar 
    Groff, L. A., Marks, S. B. & Hayes, M. P. Using ecological niche models to direct rare amphibian surveys: A case study using the Oregon Spotted Frog (Rana pretiosa). Herpetol. Conserv. Biol. 9, 354–368 (2014).
    Google Scholar 
    Kumar, P. Assessment of impact of climate change on Rhododendrons in Sikkim Himalayas using Maxent modelling: limitations and challenges. Biodivers. Conserv. 21, 1251–1266 (2012).Article 

    Google Scholar 
    Pineda, E. & Lobo, J. M. Assessing the accuracy of species distribution models to predict amphibian species richness patterns. J. Anim. Ecol. 78, 182–190 (2009).Article 
    PubMed 

    Google Scholar 
    Yuan, H.-S., Wei, Y.-L. & Wang, X.-G. Maxent modeling for predicting the potential distribution of Sanghuang, an important group of medicinal fungi in China. Fungal Ecol. 17, 140–145 (2015).Article 

    Google Scholar 
    Chinathamby, K., Reina, R. D., Bailey, P. C. & Lees, B. K. Effects of salinity on the survival, growth and development of tadpoles of the brown tree frog, Litoria ewingii. Aust. J. Zool. 54, 97–105 (2006).Article 

    Google Scholar 
    Metcalfe, N. B. & Monaghan, P. Compensation for a bad start: Grow now, pay later?. Trends Ecol. Evol. 16, 254–260 (2001).Article 
    PubMed 

    Google Scholar 
    Metzger, D. C., Healy, T. M. & Schulte, P. M. Conserved effects of salinity acclimation on thermal tolerance and hsp70 expression in divergent populations of threespine stickleback (Gasterosteus aculeatus). J. Comp. Physiol. B. 186, 879–889 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Sanabria, E. et al. Effect of salinity on locomotor performance and thermal extremes of metamorphic Andean Toads (Rhinella spinulosa) from Monte Desert, Argentina. J. Therm. Biol. 74, 195–200 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Sokolova, I. M. Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr. Comp. Biol. 53, 597–608 (2013).Article 
    PubMed 

    Google Scholar 
    Kikawada, T. et al. Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid. Biochem. Biophys. Res. Commun. 348, 56–61 (2006).CAS 
    Article 
    PubMed 

    Google Scholar 
    Sanzo, D. & Hecnar, S. J. Effects of road de-icing salt (NaCl) on larval wood frogs (Rana sylvatica). Environ. Pollut. 140, 247–256 (2006).CAS 
    Article 
    PubMed 

    Google Scholar 
    Wood, L. & Welch, A. M. Assessment of interactive effects of elevated salinity and three pesticides on life history and behavior of southern toad (Anaxyrus terrestris) tadpoles. Environ. Toxicol. Chem. 34, 667–676 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Gomez-Mestre, I., Tejedo, M., Ramayo, E. & Estepa, J. Developmental alterations and osmoregulatory physiology of a larval anuran under osmotic stress. Physiol. Biochem. Zool. 77, 267–274 (2004).CAS 
    Article 
    PubMed 

    Google Scholar 
    Dent, J. N. Hormonal interaction in amphibian metamorphosis 1 2. Am. Zool. 28, 297–308 (1988).CAS 
    Article 

    Google Scholar 
    Bodensteiner, B. L. et al. Thermal adaptation revisited: How conserved are thermal traits of reptiles and amphibians?. J. Exp. Zool. Part A Ecol. Integr. Physiol. 335, 173–194 (2021).Article 

    Google Scholar 
    Rezende, E. L., Tejedo, M. & Santos, M. Estimating the adaptive potential of critical thermal limits: Methodological problems and evolutionary implications. Funct. Ecol. 25, 111–121 (2011).Article 

    Google Scholar 
    Mitchell, J. D., Hewitt, P. & Van Der Linde, T. D. K. Critical thermal limits and temperature tolerance in the harvester termite Hodotermes mossambicus (Hagen). J. Insect Physiol. 39, 523–528 (1993).Article 

    Google Scholar 
    Plummer, M. V., Williams, B. K., Skiver, M. M. & Carlyle, J. C. Effects of dehydration on the critical thermal maximum of the desert box turtle (Terrapene ornata luteola). J. Herpetol. 37, 747–751 (2003).Article 

    Google Scholar 
    Lee, S. et al. Effects of feed restriction on the upper temperature tolerance and heat shock response in juvenile green and white sturgeon. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 198, 87–95 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Blaustein, A. R. & Wake, D. B. Declining amphibian populations: A global phenomenon?. Trends Ecol. Evol. 5, 203–204 (1990).Article 

    Google Scholar 
    Kiesecker, J. M., Blaustein, A. R. & Belden, L. K. Complex causes of amphibian population declines. Nature 410, 681 (2001).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Rohr, J. R. & Raffel, T. R. Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proc. Natl. Acad. Sci. 107, 8269–8274 (2010).ADS 
    CAS 
    PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    Pounds, J. A. et al. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439, 161 (2006).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Skelly, D. & Freidenburg, L. Effects of beaver on the thermal biology of an amphibian. Ecol. Lett. 3, 483–486 (2000).Article 

    Google Scholar 
    Radchuk, V. et al. Adaptive responses of animals to climate change are most likely insufficient. Nat. Commun. 10, 1–14 (2019).CAS 
    Article 

    Google Scholar  More

  • in

    Switches, stability and reversals in the evolutionary history of sexual systems in fish

    Speijer, D., Lukeš, J. & Eliáš, M. Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life. Proc. Natl Acad. Sci. 112, 8827–8834 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bachtrog, D. et al. Sex determination: why so many ways of doing it? PLoS Biol. 12, e1001899 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Ah-King, M. & Nylin, S. Sex in an evolutionary perspective: just another reaction norm. Evolut. Biol. 37, 234–246 (2010).Article 

    Google Scholar 
    Leonard, J. L. The evolution of sexual systems in animals. In: Leonard, J.L. (ed.). Transitions between sexual systems: understanding the mechanisms of, and pathways between, dioecy, hermaphroditism and other sexual systems, 1–58 Springer (2019).Weeks, S. C., Benvenuto, C. & Reed, S. K. When males and hermaphrodites coexist: a review of androdioecy in animals. Integr. Comp. Biol. 46, 449–464 (2006).PubMed 
    Article 

    Google Scholar 
    Goldberg, E. E. et al. Macroevolutionary synthesis of flowering plant sexual systems. Evolution 71, 898–912 (2017).PubMed 
    Article 

    Google Scholar 
    Waples, R. S., Mariani, S. & Benvenuto, C. Consequences of sex change for effective population size. Proc. R. Soc. B: Biol. Sci. 285, 20181702 (2018).Article 

    Google Scholar 
    Benvenuto, C. & Weeks, S. C. Hermaphroditism and gonochorism. The Natural History of the Crustacea: Reproductive Biology VI, 197–241 (2020).
    Google Scholar 
    Mariani, S., Sala-Bozano, M., Chopelet, J. & Benvenuto, C. Spatial and temporal patterns of size-at-sex-change in two exploited coastal fish. Environ. Biol. Fishes 96, 535–541 (2013).Article 

    Google Scholar 
    Käfer, J., Marais, G. A. & Pannell, J. R. On the rarity of dioecy in flowering plants. Mol. Ecol. 26, 1225–1241 (2017).PubMed 
    Article 

    Google Scholar 
    Atz, J. Intersexuality in Fishes. In C.N. Amstrong and A.J. Marshall (eds). Intersexuality in vertebrates including man, 145–232 Academic Press, London (1964).Jarne, P. & Auld, J. R. Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals. Evolution 60, 1816–1824 (2006).PubMed 
    Article 

    Google Scholar 
    Leonard, J. L. Williams’ paradox and the role of phenotypic plasticity in sexual systems. Integr. Comp. Biol. 53, 671–688 (2013).PubMed 
    Article 

    Google Scholar 
    Weeks, S. C. The role of androdioecy and gynodioecy in mediating evolutionary transitions between dioecy and hermaphroditism in the animalia. Evolution 66, 3670–3686 (2012).PubMed 
    Article 

    Google Scholar 
    Renner, S. S. The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am. J. Bot. 101, 1588–1596 (2014).PubMed 
    Article 

    Google Scholar 
    Bawa, K. S. Evolution of dioecy in flowering plants. Annu. Rev. Ecol. Syst. 11, 15–39 (1980).Article 

    Google Scholar 
    Charlesworth, B. & Charlesworth, D. A model for the evolution of dioecy and gynodioecy. Am. Nat. 112, 975–997 (1978).Article 

    Google Scholar 
    Charlesworth, D. Androdioecy and the evolution of dioecy. Biol. J. Linn. Soc. 22, 333–348 (1984).Article 

    Google Scholar 
    Pannell, J. R. The evolution and maintenance of androdioecy. In: Annual Review of Ecology and Systematics 397–425 (2002).Bull, J. & Charnov, E. On irreversible evolution. Evolution 39, 1149–1155 (1985).CAS 
    PubMed 
    Article 

    Google Scholar 
    Barrett, S. C. The evolution of plant reproductive systems: how often are transitions irreversible? Proc. R. Soc. B: Biol. Sci. 280, 20130913 (2013).Article 

    Google Scholar 
    Oyarzún, P. A., Nuñez, J. J., Toro, J. E. & Gardner, J. P. Trioecy in the marine mussel Semimytilus algosus (Mollusca, Bivalvia): stable sex ratios across 22 degrees of a latitudinal gradient. Front. Mar. Sci. 7, 348 (2020).Article 

    Google Scholar 
    Dani, K. & Kodandaramaiah, U. Plant and animal reproductive strategies: lessons from offspring size and number tradeoffs. Front. Ecol. Evol. 5, 38 (2017).Article 

    Google Scholar 
    Avise, J. & Mank, J. Evolutionary perspectives on hermaphroditism in fishes. Sex. Dev. 3, 152–163 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Dornburg, A. & Near, T. J. The Emerging phylogenetic perspective on the evolution of Actinopterygian fishes. Annu. Rev. Ecol. Evol. Syst. 52, 427–452 (2021).Article 

    Google Scholar 
    Costa, W. J., Lima, S. M. & Bartolette, R. Androdioecy in Kryptolebias killifish and the evolution of self-fertilizing hermaphroditism. Biol. J. Linn. Soc. 99, 344–349 (2010).Article 

    Google Scholar 
    Costa, W. Colouration, taxonomy and geographical distribution of mangrove killifishes, the Kryptolebias marmoratus species group, in southern Atlantic coastal plains of Brazil (Cyprinodontiformes: Rivulidae). Ichthyol. Explor. Freshw. 27, 183–192 (2016).
    Google Scholar 
    Powell, M. L., Kavanaugh, S. I. & Sower, S. A. Seasonal concentrations of reproductive steroids in the gonads of the Atlantic hagfish, Myxine glutinosa. J. Exp. Zool. Part A Comp. Exp. Biol. 301, 352–360 (2004).Article 
    CAS 

    Google Scholar 
    Pennell, M. W., Mank, J. E. & Peichel, C. L. Transitions in sex determination and sex chromosomes across vertebrate species. Mol. Ecol. 27, 3950–3963 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ghiselin, M. T. The evolution of hermaphroditism among animals. Q. Rev. Biol. 44, 189–208 (1969).CAS 
    PubMed 
    Article 

    Google Scholar 
    Eppley, S. M. & Jesson, L. K. Moving to mate: the evolution of separate and combined sexes in multicellular organisms. J. Evol. Biol. 21, 727–736 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Warner, R. R. The adaptive significance of sequential hermaphroditism in animals. Am. Nat. 109, 61–82 (1975).Article 

    Google Scholar 
    Warner, R. R., Robertson, D. R. & Leigh, E. G. Sex change and sexual selection. Science 190, 633–638 (1975).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Charnov, E. L. The Theory of Sex Allocation. Princeton University Press, USA (1982).Policansky, D. Sex change in plants and animals. Annu. Rev. Ecol. Syst. 13, 471–495 (1982).Article 

    Google Scholar 
    Benvenuto, C., Coscia, I., Chopelet, J., Sala-Bozano, M. & Mariani, S. Ecological and evolutionary consequences of alternative sex-change pathways in fish. Sci. Rep. 7, 9084 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Charnov, E. L. Natural selection and sex change in pandalid shrimp: test of a life-history theory. Am. Nat. 113, 715–734 (1979).MathSciNet 
    Article 

    Google Scholar 
    Broquet, T. et al. The size advantage model of sex allocation in the protandrous sex-changer Crepidula fornicata: role of the mating system, sperm storage, and male mobility. Am. Nat. 186, 404–420 (2015).PubMed 
    Article 

    Google Scholar 
    Erisman, B. E., Craig, M. T. & Hastings, P. A. A phylogenetic test of the size-advantage model: evolutionary changes in mating behavior influence the loss of sex change in a fish lineage. Am. Nat. 174, E83–E99 (2009).PubMed 
    Article 

    Google Scholar 
    Buxton, C. D. & Garratt, P. A. Alternative reproductive styles in seabreams (Pisces: Sparidae). Environ. Biol. Fishes 28, 113–124 (1990).Article 

    Google Scholar 
    Shapiro, D. Y. Social behavior, group structure, and the control of sex reversal in hermaphroditic fish. Adv. Study Behav. 10, 43–102 (1979).Article 

    Google Scholar 
    Stearns, S. C. Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87, 476–486 (2000).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Waples, R. S., Luikart, G., Faulkner, J. R. & Tallmon, D. A. Simple life-history traits explain key effective population size ratios across diverse taxa. Proc. R. Soc. Lond. B: Biol. Sci. 280, 20131339 (2013).
    Google Scholar 
    Martinez, A. S., Willoughby, J. R. & Christie, M. R. Genetic diversity in fishes is influenced by habitat type and life-history variation. Ecol. Evolution 8, 12022–12031 (2018).Article 

    Google Scholar 
    Harvey, P. H. & Pagel, M. D. The comparative method in evolutionary biology. (Oxford University Press, USA, 1991).Barneche, D. R., Robertson, D. R., White, C. R. & Marshall, D. J. Fish reproductive-energy output increases disproportionately with body size. Science 360, 642–645 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Brandl, S. J. & Bellwood, D. R. Pair-formation in coral reef fishes: an ecological perspective. Oceanogr. Mar. Biol.: Annu. Rev. 52, 1–80 (2014).
    Google Scholar 
    Fitzpatrick, J. L. Sperm competition and fertilization mode in fishes. Philos. Trans. R. Soc. B: Biol. Sci. 375, 20200074 (2020).Article 

    Google Scholar 
    Parker, G. A. Conceptual developments in sperm competition: a very brief synopsis. Philos. Trans. R. Soc. B: Biol. Sci. 375, 20200061 (2020).Article 

    Google Scholar 
    Warner, R. R. Sex change in fishes: hypotheses, evidence, and objections. Environ. Biol. Fishes 22, 81–90 (1988).Article 

    Google Scholar 
    Molloy, P. P., Goodwin, N. B., Côté, I. M., Reynolds, J. D. & Gage, M. J. Sperm competition and sex change: a comparative analysis across fishes. Evolution 61, 640–652 (2007).PubMed 
    Article 

    Google Scholar 
    Erisman, B. E., Petersen, C. W., Hastings, P. A. & Warner, R. R. Phylogenetic perspectives on the evolution of functional hermaphroditism in teleost fishes. Integr. Comp. Biol. 53, 736–754 (2013).PubMed 
    Article 

    Google Scholar 
    Sadovy, Y., Colin, P. & Domeier, M. Aggregation and spawning in the tiger grouper, Mycteroperca tigris (Pisces: Serranidae). Copeia 1994, 511–516 (1994).Article 

    Google Scholar 
    Muñoz, R. C. & Warner, R. R. A new version of the size-advantage hypothesis for sex change: incorporating sperm competition and size-fecundity skew. Am. Nat. 161, 749–761 (2003).PubMed 
    Article 

    Google Scholar 
    Horne, C. R., Hirst, A. G. & Atkinson, D. Selection for increased male size predicts variation in sexual size dimorphism among fish species. Proc. R. Soc. B: Biol. Sci. 287, 20192640 (2020).Article 

    Google Scholar 
    Parker, G. The evolution of expenditure on testes. J. Zool. 298, 3–19 (2016).Article 

    Google Scholar 
    Stockley, P., Gage, M., Parker, G. & Møller, A. Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am. Nat. 149, 933–954 (1997).CAS 
    PubMed 
    Article 

    Google Scholar 
    Pla, S., Benvenuto, C., Capellini, I. & Piferrer, F. A phylogenetic comparative analysis on the evolution of sequential hermaphroditism in seabreams (Teleostei: Sparidae). Sci. Rep. 10, 3606 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Vrijenhoek, R. C. Unisexual fish: model systems for studying ecology and evolution. Annu. Rev. Ecol. Syst. 25, 71–96 (1994).Article 

    Google Scholar 
    Sadovy de Mitcheson, Y. & Liu, M. Functional hermaphroditism in teleosts. Fish. Fish. 9, 1–43 (2008).Article 

    Google Scholar 
    Rabosky, D. L. et al. An inverse latitudinal gradient in speciation rate for marine fishes. Nature 559, 392 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Froese, R., Pauly, D. & Editors. FishBase. World Wide Web electronic publication. www.fishbase.org (2018).Moore, W. S. Evolutionary ecology of unisexual fishes. In: Evolutionary genetics of fishes, 329–398 (Springer, 1984).Collin, R. & Miglietta, M. P. Reversing opinions on Dollo’s Law. Trends Ecol. Evol. 23, 602–609 (2008).PubMed 
    Article 

    Google Scholar 
    Domes, K., Norton, R. A., Maraun, M. & Scheu, S. Re-evolution of sexuality breaks Dollo’s law. Proc. Natl Acad. Sci. 104, 7139–7144 (2007).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dollo, L. Les lois de l’évolution. Bull. Soc. Belge Géol. Paléont. Hydrol. 7, 164–166 (1893).
    Google Scholar 
    King, B. & Lee, M. S. Ancestral state reconstruction, rate heterogeneity, and the evolution of reptile viviparity. Syst. Biol. 64, 532–544 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Uller, T. & Helanterä, H. From the origin of sex-determining factors to the evolution of sex-determining systems. Q. Rev. Biol. 86, 163–180 (2011).PubMed 
    Article 

    Google Scholar 
    Devlin, R. H. & Nagahama, Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208, 191–364 (2002).CAS 
    Article 

    Google Scholar 
    Volff, J.-N., Nanda, I., Schmid, M. & Schartl, M. Governing sex determination in fish: regulatory putsches and ephemeral dictators. Sex. Dev. 1, 85–99 (2007).PubMed 
    Article 

    Google Scholar 
    Nagahama, Y., Chakraborty, T., Paul-Prasanth, B., Ohta, K. & Nakamura, M. Sex determination, gonadal sex differentiation and plasticity in vertebrate species. Physiol. Rev. 101, 1237–1308 (2020).PubMed 
    Article 

    Google Scholar 
    Penman, D. J. & Piferrer, F. Fish gonadogenesis. Part I: genetic and environmental mechanisms of sex determination. Rev. Fish. Sci. 16(S1), 16–34 (2008).CAS 
    Article 

    Google Scholar 
    Mank, J. E., Promislow, D. E. L. & Avise, J. C. Evolution of alternative sex-determining mechanisms in teleost fishes. Biol. J. Linn. Soc. 87, 83–93 (2006).Article 

    Google Scholar 
    Galetti, P. M., Aguilar, C. T. & Molina, W. F. An overview of marine fish cytogenetics. Hydrobiologia 420, 55–62 (2000).Article 

    Google Scholar 
    Yoshida, K. et al. Sex chromosome turnover contributes to genomic divergence between incipient stickleback species. PLoS Genet. 10, e1004223 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Ross, J. A., Urton, J. R., Boland, J., Shapiro, M. D. & Peichel, C. L. Turnover of sex chromosomes in the stickleback fishes (Gasterosteidae). PLoS Genet. 5, e1000391 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Vicoso, B. Molecular and evolutionary dynamics of animal sex-chromosome turnover. Nature Ecology & Evolution 1–10 (2019).Gamble, T. et al. Restriction site-associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems. Mol. Biol. Evol. 32, 1296–1309 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Pokorná, M. & Kratochvíl, L. Phylogeny of sex-determining mechanisms in squamate reptiles: are sex chromosomes an evolutionary trap? Zool. J. Linn. Soc. 156, 168–183 (2009).Article 

    Google Scholar 
    Furman, B. L. et al. Sex chromosome evolution: sso many exceptions to the rules. Genome Biol. Evol. 12, 750–763 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Carvalho, N. D. M. et al. Cytogenetics of Synbranchiformes: a comparative analysis of two Synbranchus Bloch, 1795 species from the Amazon. Genetica 140, 149–158 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Piferrer, F. Epigenetic mechanisms in sex determination and in the evolutionary transitions between sexual systems. Philos. Trans. R. Soc. B: Biol. Sci. 376, 20200110 (2021).Article 
    CAS 

    Google Scholar 
    Grant, S. et al. Genetics of sex determination in flowering plants. Dev. Genet. 15, 214–230 (1994).Article 

    Google Scholar 
    Harrington Jr, R. W. How ecological and genetic factors interact to determine when self-fertilizing hermaphrodites of Rivulus marmoratus change into functional secondary males, with a reappraisal of the modes of intersexuality among fishes. Copeia 389–432 (1971).Adolfi, M. C., Nakajima, R. T., Nóbrega, R. H. & Schartl, M. Intersex, Hermaphroditism, and gonadal plasticity in vertebrates: Evolution of the Müllerian duct and Amh/Amhr2 signalling. Annual Review of Animal Biosciences (2018).Adkins-Regan, E. Early organizational effects of hormones: an evolutionary perspective. In Adler, N.T. (ed.) Neuroendocrinology of reproduction: physiology and behavior, 159–228 (Springer, USA, 1981).Navara, K. J. The truth about Nemo’s dad: sex-changing behaviors in fishes. In Choosing Sexes 183–212 (Springer, Cham, 2018).Orban, L., Sreenivasan, R. & Olsson, P. E. Long and winding roads: testis differentiation in zebrafish. Mol. Cell. Endocrinol. 312, 35–41 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zohar, Y., Abraham, M. & Gordin, H. The gonadal cycle of the captivity-reared hermaphroditic teleost Sparus aurata (L.) during the first two years of life. Annales de. Biologie Anim. Biochim. Biophys. 18, 877–882 (1978).Article 

    Google Scholar 
    Chang, C.-F. & Yueh, W.-S. Annual cycle of gonadal histology and steroid profiles in the juvenile males and adult females of the protandrous black porgy, Acanthopagrus schlegelii. Aquaculture 91, 179–196 (1990).CAS 
    Article 

    Google Scholar 
    Miura, S., Nakamura, S., Kobayashi, Y., Piferrer, F. & Nakamura, M. Differentiation of ambisexual gonads and immunohistochemical localization of P450 cholesterol side-chain cleavage enzyme during gonadal sex differentiation in the protandrous anemonefish, Amphiprion clarkii. Comp. Biochem. Physiol. Part B: Biochem. Mol. Biol. 149, 29–37 (2008).Article 
    CAS 

    Google Scholar 
    Yamaguchi, S. & Iwasa, Y. Advantage for the sex changer who retains the gonad of the nonfunctional sex. Behav. Ecol. Sociobiol. 71, 39 (2017).Article 

    Google Scholar 
    Munday, P. L., Kuwamura, T. & Kroon, F. J. Bi-directional sex change in marine fishes. In: Cole, K.S. (ed.) Reproduction and sexuality in marine fishes: Patterns and processes. 241–271 (University of California Press, Berkeley, USA, 2010).Uller, T., Feiner, N., Radersma, R., Jackson, I. S. & Rago, A. Developmental plasticity and evolutionary explanations. Evol. Dev. 22, 47–55 (2020).PubMed 
    Article 

    Google Scholar 
    Pla, S., Maynou, F. & Piferrer, F. Hermaphroditism in fish: incidence, distribution and associations with abiotic environmental factors. Rev. Fish. Biol. Fish. 31, 935–955 (2021).Article 

    Google Scholar 
    Boettiger, C., Lang, D. T. & Wainwright, P. C. rfishbase: exploring, manipulating and visualizing FishBase data from R. J. Fish. Biol. 81, 2030–2039 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Pagel, M., Meade, A. & Barker, D. Bayesian estimation of ancestral character states on phylogenies. Syst. Biol. 53, 673–684 (2004).PubMed 
    Article 

    Google Scholar 
    Pagel, M. & Meade, A. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am. Nat. 167, 808–825 (2006).PubMed 
    Article 

    Google Scholar 
    Pagel, M. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete. Proc. R. Soc. B: Biol. Sci. 255, 37–45 (1994).ADS 
    Article 

    Google Scholar 
    Currie, T. E. & Meade, A. In Modern phylogenetic comparative methods and their application in evolutionary biology, 263–286 (Springer, 2014).Furness, A. I. & Capellini, I. The evolution of parental care diversity in amphibians. Nat. Commun. 10, 1–12 (2019).CAS 
    Article 

    Google Scholar 
    Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Freckleton, R. P., Harvey, P. H. & Pagel, M. Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712–726 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Pagel, M. Inferring evolutionary processes from phylogenies. Zool. Scr. 26, 331–348 (1997).Article 

    Google Scholar 
    Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Orme, D. The caper package: comparative analysis of phylogenetics and evolution in R. https://cran.r-project.org/web/packages/caper/vignettes/caper.pdf (2018).Schiettekatte, N., Brandl, S. & Casey, J. Fishualize: Color palettes based on fish species. R package v0.2.2 (2021). More

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    Whales from space dataset, an annotated satellite image dataset of whales for training machine learning models

    Very high-resolution (VHR) satellite imagery allows us to survey regularly remote and large areas of the ocean, difficult to access by boats or planes. The interest in using VHR satellite imagery for the study of great whales (including sperm whales and baleen whales) has grown in the past years1,2,3,4,5 since Abileah6 and Fretwell et al.7 showed its potential. This growing interest may be linked to the improvement in the spatial resolution of satellite imagery, which increased in 2014 from 46 cm to 31 cm. This upgrade enhanced the confidence in the detection of whales in satellite imagery, as more details could be seen, such as whale-defining features (e.g. flukes).Detecting whales in the imagery is either conducted manually1,4,5,7, or automatically2,3. A downside of the manual approach is that it is time-demanding, with manual counter often having to view hundred and sometimes thousands of square kilometres of open ocean. The development of automated approaches to detect whales by satellite would not only speed up this application, but also reduce the possibility of missing whales due to observer fatigue and standardize the procedure. Various automated approaches exist from pixel-based to artificial intelligence. Machine learning, an application of artificial intelligence, seems to be the most appropriate automated method to detect whales efficiently in satellite imagery2,3,8,9.In machine learning an algorithm learns how to identify features by repeatedly testing different search parameters against a training dataset10,11. Concerning whales, the algorithm needs to be trained to detect the wide variety of shapes and colour characterising whales. Shapes and colour will be influenced by the type of species, the environment (e.g. various degree of turbidity), the light conditions, and the behaviours (e.g. foraging, travelling, breaching), as different behaviours will result in different postures. The larger a training dataset is, the more accurate and transferable to other satellite images the algorithm will be. At the time of writing, such a dataset does not exist or is not publicly available.Creating a large enough dataset necessary to train algorithms to detect whales in VHR satellite imagery will require the various research groups analysing VHR satellite imagery to openly share examples of whales and non-whale objects in VHR satellite imagery, which could be facilitated by uploading such data on a central open source repository, similar to the GenBank12 for DNA code or OBIS-Seamap13 for marine wildlife observations. Ideally clipped out image chips of the whale objects would be shared as tiff files, which retains most of the characteristics of the original image. However, all VHR satellites are commercially owned, except for the Cartosat-3 owned by the government of India14, which means it is not possible to publicly share image chips as tiff file. Instead, image chips could be shared in a png or jepg format, which involve loosing some spectral information. If tiff files are required, georeferenced and labelled boxes encompassing the whale objects could also be shared, including information on the satellite imagery to allow anyone to ask the commercial providers for the exact imagery.Here we present a database of whale objects found in VHR satellite imagery. It represents four different species of whales (i.e. southern right whale, Eubalaena australis; grey whale, Eschrichtius robustus; humpback whale, Megaptera novaeangliae; fin whale, Balaenoptera physalus; Fig. 1), which were manually detected in images captured by different satellites (i.e., GeoEye-1, Quickbird-2, WorldView-2, WorldView-3). We created the database by (i) first detecting whale objects manually in satellite imagery, (ii) then we classified whale objects as either “definite”, “probable” or “possible” as in Cubaynes et al.1; and (iii) finally we created georeferenced and labelled points and boxes centered around each whale object, as well as providing image chips in a png format. With this database made publicly available, we aim to initiate the creation of a central database that can be built upon.Fig. 1Database of annotated whales detected in satellite imagery covering different species and areas. Humpback whales were detected in Maui Nui, US (a); grey whales in Laguna San Ignacio, Mexico (b); fin whales in the Pelagos Sanctuary, France, Monaco and Italy (c); southern right whales were observed in three areas, off the Peninsula Valdes, Argentina (d); off Witsand, South Africa (e); and off the Auckland Islands, New Zealand (f). The dot size represents the number of annotated whales per location. Whale silhouettes were sourced from philopic.com (the grey and humpback whales silhouettes are from Chris Luh).Full size image More

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    Determinants of variability in signature whistles of the Mediterranean common bottlenose dolphin

    Wilkins, M. R., Seddon, N. R. & Safran, R. J. Evolutionary divergence in acoustic signals: causes and consequences. Trends Ecol. Evol. 28, 156–166 (2013).PubMed 
    Article 

    Google Scholar 
    Wei, C. Sound production and propagation in cetacean. In Neuroendocrine Regulation of Animal Vocalization (eds Rosenfeld, C. S. & Hoffmann, F.) 267–291 (Academic Press, 2021).Chapter 

    Google Scholar 
    Nakakara, F. Social functions of cetacean acoustic communication. Fish. Sci. 68, 298–301 (2002).Article 

    Google Scholar 
    Caldwell, M. C. & Caldwell, D. K. Vocalization of naive captive dolphins in small groups. Science 159, 1121–1123 (1968).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Caldwell, M. C., Caldwell, D. K. & Tyack, P. L. Review of the signature-whistle-hypothesis for the Atlantic bottlenose dolphin. In The bottlenose dolphin (eds Leatherwood, S. & Reeves, R. R.) 199–234 (Academic Press, 1990).Chapter 

    Google Scholar 
    Ford, J. B. Vocal traditions among resident killer whales (Orcinus orca) in coastal waters of British Columbia. Can. J. Zool. 69, 1454–1483 (1991).Article 

    Google Scholar 
    Weilgart, L. & Whitehead, H. Group-specific dialects and geographical variation in coda repertoire in South Pacific sperm whales. Behav. Ecol. Sociobiol. 40, 277–285 (1997).Article 

    Google Scholar 
    Deeck, V. B., Ford, J. K. B. & Spong, P. Dialect change in resident killer whales: implications for vocal learning and cultural transmission. Anim. Behav. 60, 629–638 (2000).Article 

    Google Scholar 
    Chen, Z. & Wiens, J. J. The origins of acoustic communication in vertebrates. Nat. Commun. 11, 369 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Morton, E. S. Sources of selection on avian sounds. Am. Nat. 109, 17–34 (1975).ADS 
    Article 

    Google Scholar 
    Irwin, D. E., Thimgan, M. P. & Irwin, J. H. Call divergence is correlated with geographic and genetic distance in greenish warblers (Phylloscopus trochiloides): A strong role for stochasticity in signal evolution?. J. Evol. Biol. 21, 435–448 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Campbell, P. et al. Geographic variation in the songs of Neotropical singing mice: Testing the relative importance of drift and local adaptation. Evol. 64, 1955–1972 (2010).
    Google Scholar 
    Connor, R. C., Wells, R. S., Mann, J. & Read, A. J. The bottlenose dolphin: Social relationships in a fission-fusion society. In Cetacean societies: Field studies of dolphins and whales (eds Mann, J. et al.) 91–126 (University of Chicago Press, Chicago, 2000).
    Google Scholar 
    Janik, V. M. & Sayigh, L. S. Communication in bottlenose dolphins: 50 years of signature whistle research. J. Comp. Physiol. A https://doi.org/10.1007/s00359-013-0817-7 (2013).Article 

    Google Scholar 
    MacFarlane, N. et al. Signature whistles facilitate reunions and/or advertise identity in Bottlenose Dolphins. JASA 141, 3543 (2017).Article 

    Google Scholar 
    Buckstaff, K. C. Effects of watercraft noise on the acoustic behaviour of bottlenose dolphins, Tursiops truncatus, in Sarasota Bay, Florida. Mar. Mam. Sci. 20, 709–725 (2004).Article 

    Google Scholar 
    Cook, M. L. H., Sayigh, L. S., Blum, J. E. & Wells, R. S. Signature-whistle production in undisturbed free-ranging bottlenose dolphins (Tursiops truncatus). Proc. R. Soc. Lond. B. 271, 1043–1049 (2004).Article 

    Google Scholar 
    Watwood, S. L., Owen, E. C. G., Tyack, P. L. & Wells, R. S. Signature whistle use by temporarily restrained and free-swimming bottlenose dolphins, Tursiops truncatus. Anim. Behav. 69, 1373–1386 (2005).Article 

    Google Scholar 
    Sayigh, L. S., Tyack, P. L., Wells, R. S., Scott, M. D. & Irvine, A. B. Sex difference in signature whistle production of free-ranging bottle-nosed dolphins, Tursiops-truncatus. Beh. Ecol. Soc. 36, 171–177 (1995).Article 

    Google Scholar 
    Tyack, P. L. & Sayigh, L. S. Vocal learning in cetaceans. In Social influences on vocal development (eds Snowdon, C. T. & Hausberger, M.) 208–233 (Cambridge University Press, 1997).Chapter 

    Google Scholar 
    Miksis, J. L., Tyack, P. & Buck, J. R. Captive dolphins, Tursiops truncatus, develop signature whistles that match acoustic features of human-made model sounds. JASA 112, 728–739 (2002).Article 

    Google Scholar 
    Fripp, D. et al. Bottlenose dolphin (Tursiops truncatus) calves appear to model their signature whistles on the signature whistles of community members. Anim. Cogn. 8, 17–26 (2005).PubMed 
    Article 

    Google Scholar 
    Janik, V. M. & Slater, P. J. B. Context-specific use suggests that bottlenose dolphin signature whistles are cohesion calls. Anim. Behav. 56, 829–838 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sayigh, L. S., Tyack, P. L., Wells, R. S. & Scott, M. D. Signature whistles of free-ranging bottlenose dolphins, Tursiops truncatus: mother offspring comparisons. Behav. Ecol. Sociobiol. 26, 247–260 (1990).Article 

    Google Scholar 
    Watwood, S. L., Tyack, P. L. & Wells, R. S. Whistle sharing in paired male bottlenose dolphins, Tursiops truncatus. Behav. Ecol. Sociobiol. 55, 531–543 (2004).Article 

    Google Scholar 
    Janik, V. M., Dehnhardt, G. & Todt, D. Signature whistle variations in a bottlenosed dolphin, Tursiops truncatus. Behav. Ecol. Sociobiol. 35, 243–248 (1994).Article 

    Google Scholar 
    Esch, H. C., Sayigh, L. S. & Wells, R. S. Quantifying parameters of bottlenose dolphin signature whistles. Mar. Mam. Sci. 24, 976–986 (2009).Article 

    Google Scholar 
    Gridley, T. Geographic and species variation in bottlenose dolphin (Tursiops spp.) signature whistle types. PhD Thesis Biology. University of St Andrews (2011).King, S. L. & Janik, V. M. Bottlenose dolphins can use learned vocal labels to address each other. Proc Natl Acad Sci USA 110, 13216–13221 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kriesell, H., Elwen, S. H., Nastasi, A. & Gridley, T. Identification and characteristics of signature whistles in wild bottlenose dolphins (Tursiops truncatus) from Namibia. PLoS ONE 9, e106317 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Luis, A. R., Couchinho, M. N. & dos Santos, M. E. Signature whistles in wild bottlenose dolphins: Long term stability and emission rates. Acta Ethol. https://doi.org/10.1007/s10211-015-0230-z (2015).Article 

    Google Scholar 
    Wang, D. W., Würsig, B. & Evans, W. E. Whistles of bottlenose dolphins: Comparisons among populations. Aquatic Mam. 21, 65–77 (1995).
    Google Scholar 
    May-Collado, L. J. & Wartzok, D. A comparison of bottlenose dolphin whistles in the Atlantic Ocean: Factors promoting whistle variation. J. Mammal. 89, 1229–1240 (2008).Article 

    Google Scholar 
    Papale, E. et al. Acoustic divergence between bottlenose dolphin whistles from the Central-Eastern North Atlantic and Mediterranean Sea. Acta Ethol. 17, 155–165 (2014).Article 

    Google Scholar 
    La Manna, G., Rako-Gospić, N., Manghi, M., Picciulin, M. & Sarà, G. Assessing geographical variation on whistle acoustic structure of three Mediterranean populations of common bottlenose dolphin (Tursiops truncatus). Beh. 154, 583–607 (2017).Article 

    Google Scholar 
    La Manna, G. et al. Whistle variation in Mediterranean common bottlenose dolphin: The role of geographical, anthropogenic, social, and behavioral factors. Ecol. Evol. 00, 1–7 (2020).
    Google Scholar 
    Natoli, A., Birkun, A., Aguilar, A., Lopez, A. & Rus Hoelzel, A. Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus) based on microsatellite and mitochon-drial DNA analyses. Proc. R. Soc. Lond. B. 272, 1217–2122 (2005).CAS 

    Google Scholar 
    Richardson, W. J., Greene, C. R., Malme, C. I. & Thomson, D. H. Marine mammals and noise (Academic Press, London, 1995).
    Google Scholar 
    Gnone, G., et al. TursioMed: An international project to assess the conservation status of the bottlenose dolphin in the Mediterranean Sea. Final Report (2019).La Manna, G. & Ronchetti, F. Relazione sul monitoraggio della presenza e distribuzione del tursiope Tursiops truncatus nell’area del nord Sardegna comprendente l’Area Marina Protetta Capo Caccia – Isola Piana. Report AMP, 42 (2018).La Manna, G., Ronchetti, F., Sarà, G., Ruiu, A. & Ceccherelli, G. Common bottlenose dolphin protection and sustainable boating: species distribution modeling for effective coastal planning. Front. Mar. Sci. 7, 542648 (2020).Article 

    Google Scholar 
    Pace, D. S. et al. An integrated approach for cetacean knowledge and conservation in the central Mediterranean Sea using research and social media data sources. Aquat. Conserv. 29, 1302–1323 (2019).Article 

    Google Scholar 
    Pace, D. S. et al. Capitoline Dolphins: Residency patterns and abundance estimate of Tursiops truncatus at the Tiber River Estuary (Mediterranean Sea). Biology 10, 275 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pulcini, M., Pace, D. S., La Manna, G., Triossi, F. & Fortuna, C. M. Distribution and abundance estimates of bottlenose dolphins (Tursiops truncatus) around Lampedusa Island (Sicily Channel, Italy). Implications for their management. J. Mar. Biol. Assoc. UK 6, 1175–1184 (2013).
    Google Scholar 
    La Manna, G., Ronchetti, F. & Sarà, G. Predicting common bottlenose dolphin habitat preference to dynamically adapt management measures from a Marine Spatial Planning perspective. Ocean Coast. Manag. 130, 317–327 (2016).Article 

    Google Scholar 
    Santostasi, N. L., Bonizzoni, S., Bearzi, G., Eddy, L. & Gimenez, O. A robust design capture-recapture analysis of abundance, survival and temporary emigration of three odontocete species in the Gulf of Corinth, Greece. PLoS ONE 11, e0166650 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Bearzi, G., Bonizzoni, S. & Gonzalvo, J. Mid-distance movements of common bottlenose dolphins in the coastal waters of Greece. J. Ethol 29, 369–374 (2011).Article 

    Google Scholar 
    Bearzi, G. et al. Dolphins in a scaled-down Mediterranean: The Gulf of Corinth’s odontocetes. In Adv. Mar. Biol. Vol. 75 (eds NotarbartolodiSciara, G. et al.) 297–331 (Academic Press, 2016).
    Google Scholar 
    Pleslić, G. et al. The abundance of common bottlenose dolphins (Tursiops truncatus) in the former special marine reserve of the Cres-Lošinj Archipelago, Croatia. Aquat. Conserv. 25, 125–137 (2015).Article 

    Google Scholar 
    Rako-Gospić, N. et al. Factor associated variations in the home range of a resident Adriatic common bottlenose dolphin population. Mar. Pol. Bul. 124, 234–244 (2017).Article 
    CAS 

    Google Scholar 
    Janik, V. M., King, S. L., Sayigh, L. S. & Wells, R. S. Identifying signature whistles from recordings of groups of unrestrained bottlenose dolphins (Tursiops truncatus). Mar Mam. Sci 29, 1–14 (2013).Article 

    Google Scholar 
    La Manna, G., Manghi, M., Pavan, G., Lo Mascolo, F. & Sarà, G. Behavioural strategy of common bottlenose dolphins (Tursiops truncatus) in response to different kinds of boats in the waters of Lampedusa Island (Italy). Aquat. Conserv. 23, 745–757 (2013).
    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2015).
    Google Scholar 
    Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. & Smith, G. H. Mixed effects models and extensions in ecology with R, 579 (Springer, 2009).MATH 
    Book 

    Google Scholar 
    Garamszegi, L. Z. A simple statistical guide for the analysis of behaviour when data are constrained due to practical or ethical reasons. Anim. Beh. 120, 223–234 (2015).Article 

    Google Scholar 
    Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R Core Team. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–137 (2018).Janik, V. M. Source levels and the estimated active space of bottlenose dolphin (Tursiops truncatus) whistles in the Moray Firth, Scotland. J. Comp. Physiol. A Sens. Neural Behav. Physiol 186, 673–680 (2000).CAS 
    Article 

    Google Scholar 
    Quintana-Rizzo, E., Mann, D. A. & Wells, R. S. Estimated communication range of social sounds used by bottlenose dolphins (Tursiops truncatus). JASA 120, 1671–1683 (2006).Article 

    Google Scholar 
    Sayigh, L. S. Development and function of signature whistles of free ranging bottlenose dolphins, Tursiops truncatus. MIT/WHOI joint program (1992).Janik, V. M., Sayigh, L. S. & Wells, R. S. Signature whistle shape conveys identity information to bottlenose dolphins. PNAS 103, 8293–8297 (2006).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Papale, E., Gamba, M., Perez-Gil, M., Martin, V. M. & Giacoma, C. Dolphins adjust species-specific frequency parameters to compensate for increasing background noise. PLoS ONE 10, e0121711 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    La Manna, G., Rako-Gospić, N., Manghi, M. & Ceccherelli, G. Influence of environmental, social and behavioural variables on the whistling of the common bottlenose dolphin (Tursiops truncatus). Behav. Ecol. Sociobiol. 73, 12 (2019).Article 

    Google Scholar 
    Ballard, S. M. & Lee, K. M. The acoustics of marine sediments. JASA 13, 18–18 (2017).
    Google Scholar 
    Smolker, R. & Pepper, J. W. Whistle convergence among allied male bottlenose dolphins (Delphinidae, Tursiops sp). Ethology 105, 595–617 (1999).Article 

    Google Scholar 
    Sayigh, L. S., Esch, H. C., Wells, R. S. & Janik, V. M. Facts about signature whistles of bottlenose dolphins (Tursiops truncatus). Anim. Behav. 74, 1631–1642 (2007).Article 

    Google Scholar 
    Jourdan J., et al. Distribution and abundance of bottlenose dolphin (Tursiops truncatus) along French Provençal coast. In Proceeding of the 30th European Cetacean Society Conference, Madeira (2016).Labach, H. et al. Distribution and abundance of common bottlenose dolphin (Tursiops truncatus) over the French Mediterranean continental shelf. Mar. Mam. Sci. 2021, 1–11 (2021).
    Google Scholar 
    Terranova, F. et al. Signature whistles of the demographic unit of bottlenose dolphins (Tursiops truncatus) inhabiting the Eastern Ligurian Sea: characterisation and comparison with the literature. Eur. Zool. J. 88, 771–781 (2021).Article 

    Google Scholar  More

  • in

    Shoaling guppies evade predation but have deadlier parasites

    Everard, M., Johnston, P., Santillo, D. & Staddon, C. The role of ecosystems in mitigation and management of Covid-19 and other zoonoses. Environ. Sci. Policy 111, 7–17 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Alizon, S., Hurford, A., Mideo, N. & Van Baalen, M. Virulence evolution and the trade‐off hypothesis: history, current state of affairs and the future. J. Evolut. Biol. 22, 245–259 (2009).CAS 
    Article 

    Google Scholar 
    Cressler, C. E., McLeod, D. V., Rozins, C., Van Den Hoogen, J. & Day, T. The adaptive evolution of virulence: a review of theoretical predictions and empirical tests. Parasitology 143, 915–930 (2016).PubMed 
    Article 

    Google Scholar 
    Acevedo, M. A., Dillemuth, F. P., Flick, A. J., Faldyn, M. J. & Elderd, B. D. Virulence‐driven trade‐offs in disease transmission: a meta‐analysis. Evolution 73, 636–647 (2019).PubMed 
    Article 

    Google Scholar 
    Anderson, R. M. & May, R. M. Coevolution of hosts and parasites. Parasitology 85, 411–426 (1982).PubMed 
    Article 

    Google Scholar 
    McKay, B., Ebell, M., Dale, A. P., Shen, Y. & Handel, A. Virulence-mediated infectiousness and activity trade-offs and their impact on transmission potential of influenza patients. Proc. R. Soc. B 287, 20200496 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bonneaud, C. et al. Experimental evidence for stabilizing selection on virulence in a bacterial pathogen. Evol. Lett. 4, 491–501 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    De Roode, J. C., Yates, A. J. & Altizer, S. Virulence–transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc. Natl Acad. Sci. USA 105, 7489–7494 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fraser, C., Hollingsworth, T. D., Chapman, R., de Wolf, F. & Hanage, W. P. Variation in HIV-1 set-point viral load: epidemiological analysis and an evolutionary hypothesis. Proc. Natl Acad. Sci. USA 104, 17441–17446 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Choo, K., Williams, P. D. & Day, T. Host mortality, predation and the evolution of parasite virulence. Ecol. Lett. 6, 310–315 (2003).Article 

    Google Scholar 
    Williams, P. D. & Day, T. Interactions between sources of mortality and the evolution of parasite virulence. Proc. R. Soc. B 268, 2331–2337 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gandon, S., Jansen, V. A. & Van Baalen, M. Host life history and the evolution of parasite virulence. Evolution 55, 1056–1062 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Prado, F., Sheih, A., West, J. D. & Kerr, B. Coevolutionary cycling of host sociality and pathogen virulence in contact networks. J. Theor. Biol. 261, 561–569 (2009).PubMed 
    Article 

    Google Scholar 
    Herre, E. A. Population structure and the evolution of virulence in nematode parasites of fig wasps. Science 259, 1442–1445 (1993).CAS 
    PubMed 
    Article 

    Google Scholar 
    Boots, M. & Mealor, M. Local interactions select for lower pathogen infectivity. Science 315, 1284–1286 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Alizon, S., de Roode, J. C. & Michalakis, Y. Multiple infections and the evolution of virulence. Ecol. Lett. 16, 556–567 (2013).PubMed 
    Article 

    Google Scholar 
    Bull, J. J. & Lauring, A. S. Theory and empiricism in virulence evolution. PLoS Pathog. 10, e1004387 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Brown, S. P., Hochberg, M. E. & Grenfell, B. T. Does multiple infection select for raised virulence? Trends Microbiol. 10, 401–405 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Peacor, S. D. & Werner, E. E. The contribution of trait-mediated indirect effects to the net effects of a predator. Proc. Natl Acad. Sci. USA 98, 3904–3908 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Seppälä, O., Karvonen, A. & Valtonen, E. T. Shoaling behaviour of fish under parasitism and predation risk. Anim. Behav. 75, 145–150 (2008).Article 

    Google Scholar 
    Lopez, L. K. & Duffy, M. A. Mechanisms by which predators mediate host–parasite interactions in aquatic systems. Trends Parasitol. 37, 890–906 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rigby, M. C. & Jokela, J. Predator avoidance and immune defence: costs and trade-offs in snails. Proc. R. Soc. B 267, 171–176 (2000).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Krause, J., Ruxton, G. D., Ruxton, G. & Ruxton, I. G. Living in Groups (Oxford Univ. Press, 2002).Godin, J.-G. J. Antipredator function of shoaling in teleost fishes: a selective review. Nat. Can. 113, 241–250 (1986).
    Google Scholar 
    Gandon, S., van Baalen, M. & Jansen, V. A. The evolution of parasite virulence, superinfection, and host resistance. Am. Nat. 159, 658–669 (2002).PubMed 
    Article 

    Google Scholar 
    Magurran, A. E. Evolutionary Ecology: The Trinidadian Guppy (Oxford Univ. Press, 2005).Magurran, A. E. & Seghers, B. H. Variation in schooling and aggression amongst guppy (Poecilia reticulata) populations in Trinidad. Behaviour 118, 214–234 (1991).Article 

    Google Scholar 
    Seghers, B. H. & Magurran, A. E. Predator inspection behaviour covaries with schooling tendency amongst wild guppy, Poecilia reticulata, populations in Trinidad. Behaviour 128, 121–134 (1994).Article 

    Google Scholar 
    Huizinga, M., Ghalambor, C. & Reznick, D. The genetic and environmental basis of adaptive differences in shoaling behaviour among populations of Trinidadian guppies, Poecilia reticulata. J. Evolut. Biol. 22, 1860–1866 (2009).CAS 
    Article 

    Google Scholar 
    Stephenson, J. F., Van Oosterhout, C., Mohammed, R. S. & Cable, J. Parasites of Trinidadian guppies: evidence for sex‐ and age‐specific trait‐mediated indirect effects of predators. Ecology 96, 489–498 (2015).PubMed 
    Article 

    Google Scholar 
    Richards, E. L., Van Oosterhout, C. & Cable, J. Sex-specific differences in shoaling affect parasite transmission in guppies. PLoS ONE 5, e13285 (2010).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Johnson, M. B., Lafferty, K. D., Van Oosterhout, C. & Cable, J. Parasite transmission in social interacting hosts: monogenean epidemics in guppies. PLoS ONE https://doi.org/10.1371/journal.pone.0022634 (2011).Gotanda, K. M. et al. Adding parasites to the guppy-predation story: insights from field surveys. Oecologia 172, 155–166 (2013).PubMed 
    Article 

    Google Scholar 
    Fraser, B. A., Ramnarine, I. W. & Neff, B. D. Temporal variation at the MHC class IIB in wild populations of the guppy (Poecilia reticulata). Evolution 64, 2086–2096 (2010).PubMed 

    Google Scholar 
    Stephenson, J. F. et al. Host heterogeneity affects both parasite transmission to and fitness on subsequent hosts. Philos. Trans. R. Soc. B 372, 20160093 (2017).Article 

    Google Scholar 
    Cable, J. & Van Oosterhout, C. The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence. Int. J. Parasitol. 37, 1449–1458 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Reznick, D. N., Butler, M. J. IV, Rodd, F. H. & Ross, P. Life‐history evolution in guppies (Poecilia reticulata) 6. Differential mortality as a mechanism for natural selection. Evolution 50, 1651–1660 (1996).PubMed 

    Google Scholar 
    Bonds, M. H., Keenan, D. C., Leidner, A. J. & Rohani, P. Higher disease prevalence can induce greater sociality: a game theoretic coevolutionary model. Evolution 59, 1859–1866 (2005).PubMed 
    Article 

    Google Scholar 
    Kerr, B., Neuhauser, C., Bohannan, B. J. & Dean, A. M. Local migration promotes competitive restraint in a host–pathogen ‘tragedy of the commons’. Nature 442, 75–78 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Boots, M. & Sasaki, A. ‘Small worlds’ and the evolution of virulence: infection occurs locally and at a distance. Proc. R. Soc. B 266, 1933–1938 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wild, G., Gardner, A. & West, S. A. Adaptation and the evolution of parasite virulence in a connected world. Nature 459, 983–986 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Dargent, F., Rolshausen, G., Hendry, A., Scott, M. & Fussmann, G. Parting ways: parasite release in nature leads to sex‐specific evolution of defence. J. Evolut. Biol. 29, 23–34 (2016).CAS 
    Article 

    Google Scholar 
    Reznick, D. A., Bryga, H. & Endler, J. A. Experimentally induced life-history evolution in a natural population. Nature 346, 357–359 (1990).Article 

    Google Scholar 
    Stephenson, J. F., van Oosterhout, C. & Cable, J. Pace of life, predators and parasites: predator-induced life-history evolution in Trinidadian guppies predicts decrease in parasite tolerance. Biol. Lett. 11, 20150806 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Stephenson, J. F., Stevens, M., Troscianko, J. & Jokela, J. The size, symmetry, and color saturation of a male guppy’s ornaments forecast his resistance to parasites. Am. Naturalist 196, 597–608 (2020).Article 

    Google Scholar 
    Godin, J.-G. J. & McDonough, H. E. Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait. Behav. Ecol. 14, 194–200 (2003).Article 

    Google Scholar 
    Van Oosterhout, C., Harris, P. & Cable, J. Marked variation in parasite resistance between two wild populations of the Trinidadian guppy, Poecilia reticulata (Pisces: Poeciliidae). Biol. J. Linn. Soc. 79, 645–651 (2003).Article 

    Google Scholar 
    Hawley, D. M., Gibson, A. K., Townsend, A. K., Craft, M. E. & Stephenson, J. F. Bidirectional interactions between host social behaviour and parasites arise through ecological and evolutionary processes. Parasitology 148, 274–288 (2020).PubMed 
    Article 

    Google Scholar 
    Janecka, M. J., Rovenolt, F. & Stephenson, J. F. How does host social behavior drive parasite non-selective evolution from the within-host to the landscape-scale? Behav. Ecol. Sociobiol. 75, 1–20 (2021).Article 

    Google Scholar 
    Tao, H., Li, L., White, M. C., Steel, J. & Lowen, A. C. Influenza A virus coinfection through transmission can support high levels of reassortment. J. Virol. 89, 8453–8461 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Eshel, I. Evolutionary and continuous stability. J. Theor. Biol. 103, 99–111 (1983).Article 

    Google Scholar 
    Hurford, A., Cownden, D. & Day, T. Next-generation tools for evolutionary invasion analyses. J. R. Soc. Interface 7, 561–571 (2009).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Leimar, O. Multidimensional convergence stability. Evolut. Ecol. Res. 11, 191–208 (2009).
    Google Scholar 
    Reznick, D., Bryant, M. & Holmes, D. The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata). PLoS Biol. 4, e7 (2005).PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Stephenson, J. F. Parasite-induced plasticity in host social behaviour depends on sex and susceptibility. Biol. Lett. https://doi.org/10.1098/rsbl.2019.0557 (2019).Lopez, S. Acquired resistance affects male sexual display and female choice in guppies. Proc. R. Soc. B 265, 717–723 (1998).Article 

    Google Scholar 
    van Oosterhout, C. et al. Selection by parasites in spate conditions in wild Trinidadian guppies (Poecilia reticulata). Int. J. Parasitol. 37, 805–812 (2007).PubMed 
    Article 

    Google Scholar 
    Pérez-Jvostov, F., Hendry, A. P., Fussmann, G. F. & Scott, M. E. Are host–parasite interactions influenced by adaptation to predators? A test with guppies and Gyrodactylus in experimental stream channels. Oecologia 170, 77–88 (2012).PubMed 
    Article 

    Google Scholar 
    Eiben, A. E. & Smith, J. E. Introduction to Evolutionary Computing (Springer, 2003).Carnell, R. lhs: Latin hypercube samples v.1.1.1 (R-Project, 2020).Iooss, B., Da Veiga, S., Janon, A. & Pujol, G. Sensitivity: Global sensitivity analysis of model outputs v.1.25.0 (R-Project, 2021).Wright, D. & Krause, J. Repeated measures of shoaling tendency in zebrafish (Danio rerio) and other small teleost fishes. Nat. Protoc. 1, 1828–1831 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Friard, O. & Gamba, M. BORIS: a free, versatile open‐source event‐logging software for video/audio coding and live observations. Methods Ecol. Evol. 7, 1325–1330 (2016).Article 

    Google Scholar 
    Griffiths, S. W. & Magurran, A. E. Sex and schooling behaviour in the Trinidadian guppy. Anim. Behav. 56, 689–693 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Magurran, A., Seghers, B., Carvalho, G. & Shaw, P. Behavioural consequences of an artificial introduction of guppies (Poecilia reticulata) in N. Trinidad: evidence for the evolution of anti-predator behaviour in the wild. Proc. R. Soc. B 248, 117–122 (1992).Article 

    Google Scholar 
    Sievers, C. et al. Reasons for the invasive success of a guppy (Poecilia reticulata) population in Trinidad. PLoS ONE 7, e38404 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mohammed, R. S. et al. Parasite diversity and ecology in a model species, the guppy (Poecilia reticulata) in Trinidad. R. Soc. Open Sci. 7, 191112 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lyles, A. M. Genetic Variation and Susceptibility to Parasites: Poeclia reticulata Infected with Gyrodactylus turnbulli. PhD dissertation, Princeton Univ. (1990).Fraser, B. A. & Neff, B. D. Parasite mediated homogenizing selection at the MHC in guppies. Genetica 138, 273 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Reznick, D. & Endler, J. A. The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36, 160–177 (1982).PubMed 

    Google Scholar 
    El‐Sabaawi, R. W. et al. Assessing the effects of guppy life history evolution on nutrient recycling: from experiments to the field. Freshw. Biol. 60, 590–601 (2015).Article 

    Google Scholar 
    Liley, N. & Luyten, P. Geographic variation in the sexual behaviour of the guppy, Poecilia reticulata (Peters). Behaviour 95, 164–179 (1985).Article 

    Google Scholar 
    Reznick, D. N. et al. Eco-evolutionary feedbacks predict the time course of rapid life-history evolution. Am. Nat. 194, 671–692 (2019).PubMed 
    Article 

    Google Scholar  More

  • in

    A trait database and updated checklist for European subterranean spiders

    Zanne, A. E. et al. Fungal functional ecology: bringing a trait-based approach to plant-associated fungi. Biol. Rev. 95, 409–433 (2020).PubMed 
    Article 

    Google Scholar 
    Põlme, S. et al. FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Divers. 105, 1–16 (2020).Article 

    Google Scholar 
    Fraser, L. H. TRY—A plant trait database of databases. Glob. Chang. Biol. 26, 189–190 (2020).ADS 
    PubMed 
    Article 

    Google Scholar 
    Kattge, J. et al. TRY plant trait database – enhanced coverage and open access. Glob. Chang. Biol. 26, 119–188 (2020).ADS 
    PubMed 
    Article 

    Google Scholar 
    Oliveira, B. F., São-Pedro, V. A., Santos-Barrera, G., Penone, C. & Costa, G. C. AmphiBIO, a global database for amphibian ecological traits. Sci. Data 4, 170123 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lecocq, T. et al. TOFF, a database of traits of fish to promote advances in fish aquaculture. Sci. Data 6, 301 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jones, K. E. et al. PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90, 2648 (2009).Article 

    Google Scholar 
    Parr, C. L. et al. GlobalAnts: a new database on the geography of ant traits (Hymenoptera: Formicidae). Insect Conserv. Divers. 10, 5–20 (2017).Article 

    Google Scholar 
    Homburg, K., Homburg, N., Schäfer, F., Schuldt, A. & Assmann, T. Carabids.org – a dynamic online database of ground beetle species traits (Coleoptera, Carabidae). Insect Conserv. Divers. 7, 195–205 (2014).Article 

    Google Scholar 
    Lowe, E. C. et al. Towards establishment of a centralized spider traits database. J. Arachnol. 48 (2020).Tobias, J. A. et al. AVONET: morphological, ecological and geographical data for all birds. Ecol. Lett. 25, 581–597 (2022).PubMed 
    Article 

    Google Scholar 
    Mammola, S., Carmona, C. P., Guillerme, T. & Cardoso, P. Concepts and applications in functional diversity. Funct. Ecol. 35, 1869–1885 (2021).Article 

    Google Scholar 
    de Bello, F. et al. Handbook of trait-based ecology: from theory to R tools. (Cambridge University Press, 2021).Edwards, K. F. et al. Evolutionarily stable communities: a framework for understanding the role of trait evolution in the maintenance of diversity. Ecol. Lett. 21, 1853–1868 (2018).PubMed 
    Article 

    Google Scholar 
    McGill, B. J., Enquist, B. J., Weiher, E. & Westoby, M. Rebuilding community ecology from functional traits. Trends Ecol. Evol. 21, 178–185 (2006).PubMed 
    Article 

    Google Scholar 
    Violle, C., Reich, P. B., Pacala, S. W., Enquist, B. J. & Kattge, J. The emergence and promise of functional biogeography. Proc. Natl. Acad. Sci. 111, 13690–13696 (2014).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kosman, E., Burgio, K. R., Presley, S. J., Willig, M. R. & Scheiner, S. M. Conservation prioritization based on trait‐based metrics illustrated with global parrot distributions. Divers. Distrib. 25, 1156–1165 (2019).Article 

    Google Scholar 
    Cadotte, M. W., Carscadden, K. & Mirotchnick, N. Beyond species: functional diversity and the maintenance of ecological processes and services. J. Appl. Ecol. 48, 1079–1087 (2011).Article 

    Google Scholar 
    de Bello, F. et al. Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers. Conserv. 19, 2873–2893 (2010).Article 

    Google Scholar 
    Ficetola, G. F., Canedoli, C. & Stoch, F. The Racovitzan impediment and the hidden biodiversity of unexplored environments. Conserv. Biol. 33, 214–216 (2019).PubMed 
    Article 

    Google Scholar 
    Mammola, S. et al. Collecting eco-evolutionary data in the dark: Impediments to subterranean research and how to overcome them. Ecol. Evol. 11, 5911–5926 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mammola, S. et al. Fundamental research questions in subterranean biology. Biol. Rev. 95, 1855–1872 (2020).PubMed 
    Article 

    Google Scholar 
    Cardoso, P. Diversity and community assembly patterns of epigean vs. troglobiont spiders in the Iberian Peninsula. Int. J. Speleol. 41, 83–94 (2012).Article 

    Google Scholar 
    Fernandes, C. S., Batalha, M. A. & Bichuette, M. E. Does the cave environment reduce functional diversity? PLoS One 11, e0151958 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Saccò, M. et al. New light in the dark – a proposed multidisciplinary framework for studying functional ecology of groundwater fauna. Sci. Total Environ. 662, 963–977 (2019).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Mammola, S. & Isaia, M. Spiders in caves. Proceedings of the Royal Society B: Biological Sciences 284, 20170193 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Parimuchová, A. et al. The food web in a subterranean ecosystem is driven by intraguild predation. Sci. Rep. 11, 4994 (2021).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Bloom, T. et al. Discovery of two new species of eyeless spiders within a single Hispaniola cave. J. Arachnol. 42, 148–154 (2014).Article 

    Google Scholar 
    Mammola, S., Cardoso, P., Ribera, C., Pavlek, M. & Isaia, M. A synthesis on cave-dwelling spiders in Europe. J. Zool. Syst. Evol. Res. 56, 301–316 (2018).Article 

    Google Scholar 
    Mammola, S. et al. Continental data on cave-dwelling spider communities across Europe (Arachnida: Araneae). Biodivers. Data J. 7, e38492 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Milano, F. et al. Spider conservation in Europe: a review. Biol. Conserv. 256, 109020 (2021).Article 

    Google Scholar 
    Pekár, S. et al. The World Spider Trait database (WST): a centralised global open repository for curated data on spider traits. Database 2021, baab064 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ledesma, E., Jiménez-Valverde, A., de Castro, A., Aguado-Aranda, P. & Ortuño, V. M. The study of hidden habitats sheds light on poorly known taxa: spiders of the Mesovoid Shallow Substratum. Zookeys 841, 39–59 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    World Spider Catalog. World Spider Catalog. Version 23.0. Natural History Museum Bern 10.24436/2 (2022).Nentwig, W. et al. Araneae – Spider of Europe. 10.24436/1 (2021).Malumbres-Olarte, J. et al. Habitat filtering and inferred dispersal ability condition across-scale species turnover and rarity in Macaronesian island spider assemblages. J. Biogeogr. 48, 3131–3144 (2021).Article 

    Google Scholar 
    Nentwig, W., Gloor, D. & Kropf, C. Spider taxonomists catch data on web. Nature 528, 479 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Mammola, S. et al. Environmental filtering and convergent evolution determine the ecological specialization of subterranean spiders. Funct. Ecol. 34, 1064–1077 (2020).Article 

    Google Scholar 
    Mammola, S. et al. Ecological speciation in darkness? Spatial niche partitioning in sibling subterranean spiders (Araneae: Linyphiidae: Troglohyphantes). Invertebr. Syst. 32, 1069–1082 (2018).Article 

    Google Scholar 
    Huber, B. A. Cave-dwelling pholcid spiders (Araneae, Pholcidae): A review. Subterr. Biol. 26, 1–18 (2018).ADS 
    Article 

    Google Scholar 
    Arnedo, M. A., Oromí, P., Múrria, C., Macías-Hernández, N. & Ribera, C. The dark side of an island radiation: systematics and evolution of troglobitic spiders of the genus Dysdera Latreille (Araneae:Dysderidae) in the Canary Islands. Invertebr. Syst. 21, 623–660 (2007).Article 

    Google Scholar 
    Ubick, D., Paquin, P., Cushing, P. E. & Duperre, N. Spiders of North America: An Identification Manual. (Amer Arachnological Society, 2007).Cardoso, P., Pekár, S., Jocqué, R. & Coddington, J. A. Global patterns of guild composition and functional diversity of spiders. PLoS One 6, e21710 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Smithers, P. The early life history and dispersal of the cave spider Meta menardi (Latreille, 1804) (Araneae: Tetragnathidae). Bull. Br. arachnol. Soc 13, 213–216 (2005).
    Google Scholar 
    Mammola, S., Hormiga, G., Arnedo, M. A. & Isaia, M. Unexpected diversity in the relictual European spiders of the genus Pimoa (Araneae:Pimoidae). Invertebr. Syst. 30, 566–587 (2016).Article 

    Google Scholar 
    Sket, B. Can we agree on an ecological classification of subterranean animals? J. Nat. Hist. 42, 1549–1563 (2008).Article 

    Google Scholar 
    Trajano, E. & de Carvalho, M. R. Towards a biologically meaningful classification of subterranean organisms: A critical analysis of the schiner-racovitza system from a historical perspective, difficulties of its application and implications for conservation. Subterr. Biol. 22, 1–26 (2017).Article 

    Google Scholar 
    Martínez, A. & Mammola, S. Specialized terminology reduces the number of citations to scientific papers. Proc. R. Soc. B Biol. Sci. 288, 20202581 (2021).Article 

    Google Scholar 
    Mammola, S. Finding answers in the dark: caves as models in ecology fifty years after Poulson and White. Ecography 42, 1331–1351 (2019).Article 

    Google Scholar 
    Mammola, S. et al. Quantifying troglomorphism in hyperspace. Arpha Conf. Abstr. 5, e82941 (2022).Wickham, H. ggplot2: Elegant Graphics for Data Analysis. (Springer-Verlag, 2016).Palacio, F. X. et al. A protocol for reproducible functional diversity analyses. EcoEvoRxiv https://doi.org/10.32942/osf.io/yt9sb (2022).Article 

    Google Scholar 
    Gower, J. C. A General Coefficient of Similarity and Some of Its Properties. Biometrics 27, 857–871 (1971).Article 

    Google Scholar 
    de Bello, F., Botta-Dukát, Z., Lepš, J. & Fibich, P. Towards a more balanced combination of multiple traits when computing functional differences between species. Methods Ecol. Evol. 12, 443–448 (2021).Article 

    Google Scholar 
    Paradis, E. & Schliep, K. Ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Oksanen, J. et al. R Package vegan: community ecology package. R package version 2.5-3 (2018).R Core Team. R: A language and environment for statistical computing. (2021).Mammola, S. A trait database for European subterranean spiders, Figshare, https://doi.org/10.6084/m9.figshare.16574255 (2022).Cardoso, P. & Pekar, S. arakno – An R package for effective spider nomenclature, distribution, and trait data retrieval from online resources. J. Arachnol. 50, 30–32 (2022).Article 

    Google Scholar 
    Johnson, T. F., Isaac, N. J. B., Paviolo, A. & González-Suárez, M. Handling missing values in trait data. Glob. Ecol. Biogeogr. 30, 51–62 (2021).Article 

    Google Scholar 
    Podani, J., Kalapos, T., Barta, B. & Schmera, D. Principal component analysis of incomplete data – A simple solution to an old problem. Ecol. Inform. 61, 101235 (2021).Article 

    Google Scholar 
    Cardoso, P., Mammola, S., Rigal, F. & Carvalho, J. C. BAT: Biodiversity Assessment Tools. R package version 2.6.0 (2021).Cardoso, P., Rigal, F. & Carvalho, J. C. BAT – Biodiversity Assessment Tools, an R package for the measurement and estimation of alpha and beta taxon, phylogenetic and functional diversity. Methods Ecol. Evol. 6, 232–236 (2015).Article 

    Google Scholar 
    De Bello, F. et al. Quantifying the relevance of intraspecific trait variability for functional diversity. Methods Ecol. Evol. 2, 163–174 (2011).Article 

    Google Scholar 
    Violle, C. et al. The return of the variance: intraspecific variability in community ecology. Trends Ecol. Evol. 27, 244–252 (2012).PubMed 
    Article 

    Google Scholar 
    Gentile, G., Bonelli, S. & Riva, F. Evaluating intraspecific variation in insect trait analysis. Ecol. Entomol. 46, 11–18 (2020).Article 

    Google Scholar 
    Wong, M. K. L. & Carmona, C. P. Including intraspecific trait variability to avoid distortion of functional diversity and ecological inference: Lessons from natural assemblages. Methods Ecol. Evol. 12, 946–957 (2021).Article 

    Google Scholar 
    Mammola, S., Piano, E., Malard, F., Vernon, P. & Isaia, M. Extending Janzen’s hypothesis to temperate regions: a test using subterranean ecosystems. Funct. Ecol. 33, 1638–1650 (2019).Article 

    Google Scholar 
    Kratochvíl, J. Araignées cavernicoles des îles Dalmates. Přírodovědné práce ústavů Československé Akad. Věd v Brně 12, 1–59 (1978).
    Google Scholar 
    Denny, M. The fallacy of the average: on the ubiquity, utility and continuing novelty of Jensen’s inequality. J. Exp. Biol. 220, 139–146 (2017).PubMed 
    Article 

    Google Scholar 
    Mammola, S. et al. Cave_dwelling_spiders_Europe. Figshare https://doi.org/10.6084/m9.figshare.8224025.v1 (2019).Darwin, C. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle of life. (John Murray, 1859).Wong, M. K. L., Guénard, B. & Lewis, O. T. Trait-based ecology of terrestrial arthropods. Biol. Rev. 94, 999–1022 (2019).PubMed 
    Article 

    Google Scholar 
    Lučić, I. Interview with Boris Sket: nothing has a sense in speleobiology, without a comparison of cave animals with the ‘normal’ epigean ones. Acta Carsologica 50, 5–9 (2021).Article 

    Google Scholar 
    McGill, B. J. The what, how and why of doing macroecology. Glob. Ecol. Biogeogr. 28, 6–17 (2019).Article 

    Google Scholar 
    Muscarella, R. & Uriarte, M. Do community-weighted mean functional traits reflect optimal strategies? Proc. R. Soc. B Biol. Sci. 283, 20152434 (2016).Article 

    Google Scholar 
    Petchey, O. L. & Gaston, K. J. Functional diversity (FD), species richness and community composition. Ecol. Lett. 5, 402–411 (2002).Article 

    Google Scholar 
    Mammola, S. & Cardoso, P. Functional diversity metrics using kernel density n-dimensional hypervolumes. Methods Ecol. Evol. 11, 986–995 (2020).Article 

    Google Scholar 
    Mammola, S. et al. Local- versus broad-scale environmental drivers of continental β-diversity patterns in subterranean spider communities across Europe. Proc. R. Soc. B Biol. Sci. 286, 20191579 (2019).Article 

    Google Scholar 
    Graco-Roza, C. et al. Distance decay 2.0 – a global synthesis of taxonomic and functional turnover in ecological communities. Glob. Ecol. Biogeogr, in press (available at https://doi.org/10.1101/2021.03.17.435827) (2022).Gallagher, R. V. et al. A guide to using species trait data in conservation. One Earth 4, 927–936 (2021).ADS 
    Article 

    Google Scholar 
    Chichorro, F., Juslén, A. & Cardoso, P. A review of the relation between species traits and extinction risk. Biol. Conserv. 237, 220–229 (2019).Article 

    Google Scholar 
    Chichorro, F. et al. Species traits predict extinction risk across the Tree of Life. bioRxiv 2020.07.01.183053 (2020).Violle, C. et al. Functional rarity: the ecology of outliers. Trends Ecol. Evol. 32, 356–367 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Carmona, C. P. et al. Erosion of global functional diversity across the tree of life. Sci. Adv. 7, eabf2675 (2021).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Loreau, M. et al. Biodiversity as insurance: from concept to measurement and application. Biol. Rev. 96, 2333–2354 (2021).PubMed 
    Article 

    Google Scholar 
    Sánchez-Fernández, D., Galassi, D. M. P., Wynne, J. J., Cardoso, P. & Mammola, S. Don’t forget subterranean ecosystems in climate change agendas. Nat. Clim. Chang. 11, 458–459 (2021).ADS 
    Article 

    Google Scholar 
    Borges, P. A. V. et al. Volcanic caves: Priorities for conserving the Azorean endemic troglobiont species. Int. J. Speleol. 41, 101–112 (2012).Article 

    Google Scholar 
    Rabelo, L. M., Souza-Silva, M. & Ferreira, R. L. Priority caves for biodiversity conservation in a key karst area of Brazil: comparing the applicability of cave conservation indices. Biodivers. Conserv. 27, 2097–2129 (2018).Article 

    Google Scholar 
    Nitzu, E. et al. Assessing preservation priorities of caves and karst areas using the frequency of endemic cave-dwelling species. Int. J. Speleol. 47, 43–52 (2018).Article 

    Google Scholar 
    Pipan, T., Deharveng, L. & Culver, D. C. Hotspots of subterranean biodiversity. Diversity 12, 209 (2020).Article 

    Google Scholar 
    Fattorini, S., Fiasca, B., Di Lorenzo, T., Di Cicco, M. & Galassi, D. M. P. A new protocol for assessing the conservation priority of groundwater-dependent ecosystems. Aquat. Conserv. Mar. Freshw. Ecosyst. 30, 1483–1504 (2020).Article 

    Google Scholar 
    Iannella, M. et al. Getting the ‘most out of the hotspot’ for practical conservation of groundwater biodiversity. Glob. Ecol. Conserv. e01844 (2021).Mazel, F. et al. Prioritizing phylogenetic diversity captures functional diversity unreliably. Nat. Commun. 9, 2888 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Cadotte, M. W. & Tucker, C. M. Difficult decisions: Strategies for conservation prioritization when taxonomic, phylogenetic and functional diversity are not spatially congruent. Biol. Conserv. 225, 128–133 (2018).Article 

    Google Scholar 
    Hanson, J. O. et al. Global conservation of species’ niches. Nature 580, 232–234 (2020).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Pollock, L. J. et al. Protecting biodiversity (in all its complexity): new models and methods. Trends Ecol. Evol. 35, 1119–1128 (2020).PubMed 
    Article 

    Google Scholar 
    Mammola, S. et al. Scientists’ warning on the conservation of subterranean ecosystems. Bioscience 69, 641–650 (2019).Article 

    Google Scholar 
    Wynne, J. J. et al. A conservation roadmap for the subterranean biome. Conserv. Lett. 14, e12834 (2021).Article 

    Google Scholar 
    Mammola, S. et al. Towards evidence-based conservation of subterranean ecosystems. Biol. Rev., early view at https://doi.org/10.1111/brv.12851 (2022).Culver, D. C. & Pipan, T. The biology of caves and other subterranean habitats. (Oxford University Press, USA, 2014).Culver, D. C. & Pipan, T. Shallow Subterranean Habitats: Ecology, Evolution, and Convervation. (Oxford University Press, USA, 2014).Sobral, M. All traits are functional: an evolutionary viewpoint. Trends Plant Sci. 26, 674–676 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Pipan, T. & Culver, D. C. The unity and diversity of the subterranean realm with respect to invertebrate body size. J. Cave Karst Stud. 79, 1–9 (2017).Article 

    Google Scholar 
    Elgar, M. A., Ghaffar, N. & Read, A. F. Sexual dimorphism in leg length among orb-weaving spiders: a possible role for sexual cannibalism. J. Zool. 222, 455–470 (1990).Article 

    Google Scholar 
    Deeleman-Reinhold, C. L. Revision of the cave-dwelling and related spiders of the genus Troglohyphantes Joseph (Linyphiidae), with special reference to the Yugoslav species. Opera Acad. Sci. Artium Slov. 23 (1978).Isaia, M. & Pantini, P. New data on the spider genus Troglohyphantes (Araneae, Linyphiidae) in the Italian Alps, with the description of a new species and a new synonymy. Zootaxa 2690, 1–18 (2010).Article 

    Google Scholar 
    Hagstrum, D. W. Carapace width as a tool for evaluating the rate of development of spiders in the laboratory and the field. Ann. Entomol. Soc. Am. 64, 757–760 (1971).Article 

    Google Scholar 
    Pavlek, M. & Mammola, S. Niche-based processes explaining the distributions of closely related subterranean spiders. J. Biogeogr. 48, 118–133 (2020).Article 

    Google Scholar 
    Mammola, S. Modelling the future spread of native and alien congeneric species in subterranean habitats – The case of meta cave-dwelling spiders in Great Britain. Int. J. Speleol. 46, 427–437 (2017).Article 

    Google Scholar 
    Novak, T. et al. Niche partitioning in orbweaving spiders Meta menardi and Metellina merianae (Tetragnathidae). Acta Oecologica 36, 522–529 (2010).ADS 
    Article 

    Google Scholar 
    Lunghi, E. Occurrence of the Black lace-weaver spider, Amaurobius ferox, in caves. Acta Carsologica 49, 119–124 (2020).Article 

    Google Scholar 
    Isaia, M. & Chiarle, A. Taxonomic notes on Cybaeus vignai Brignoli, 1977 (Araneae, Cybaeidae) and Dysdera cribrata Simon, 1882 (Araneae, Dysderidae) from the Italian Maritime Alps. Zoosystema 37, 45–56 (2015).Article 

    Google Scholar 
    Ledford, J. et al. Phylogenomics and biogeography of leptonetid spiders (Araneae: Leptonetidae). Invertebr. Syst. 35, 332–349 (2021).
    Google Scholar 
    Isaia, M., Mammola, S., Mazzuca, P., Arnedo, M. A. & Pantini, P. Advances in the systematics of the spider genus Troglohyphantes (Araneae, Linyphiidae). Syst. Biodivers. 15, 307–326 (2017).Article 

    Google Scholar 
    Hajer, J. & Řeháková, D. Spinning activity of the spider Trogloneta granulum (Araneae, Mysmenidae): web, cocoon, cocoon handling behaviour, draglines and attachment discs. Zoology 106, 223–231 (2003).PubMed 
    Article 

    Google Scholar 
    Huber, B. A., Pavlek, M. & Komnenov, M. Revision of the spider genus Stygopholcus (Araneae, Pholcidae), endemic to the Balkan Peninsula. Eur. J. Taxon. 752, 1–60 (2021).
    Google Scholar 
    Huber, B. A. Revision of the spider genus Hoplopholcus Kulczyński (Araneae, Pholcidae). Zootaxa 4726, 1–94 (2020).Article 

    Google Scholar 
    Cardoso, P. & Scharff, N. First record of the spider family symphytognathidae in Europe and description of Anapistula ataecina sp. n. (araneae). Zootaxa 2246, 45–57 (2009).Article 

    Google Scholar 
    Wang, C., Ribera, C. & Li, S. On the identity of the type species of the genus Telema (Araneae, Telemidae). Zookeys 251, 11–19 (2012).Article 

    Google Scholar 
    Hesselberg, T., Simonsen, D. & Juan, C. Do cave orb spiders show unique behavioural adaptations to subterranean life? A review of the evidence. Behaviour 1–28 (2019). More

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    Increased abundance of a common scavenger affects allocation of carrion but not efficiency of carcass removal in the Fukushima Exclusion Zone

    Lim, N., Kelt, D. A., Lim, K. K. & Bernard, H. Vertebrate scavengers control abundance of diarrheal-causing bacteria in tropical plantations. Zool. Stud. 59, 1–10 (2020).
    Google Scholar 
    Beasley, J. C., Olson, Z. H. & DeVault, T. L. Ecological role of vertebrate scavengers. In: Carrion Ecology, Evolution and their Applications. (eds Benbow, E.M., Tomberlin, J. & Tarone, A.) 107–127 (CRC Press, 2015).
    Ogada, D. L., Keesing, F. & Virani, M. Z. Dropping dead: Causes and consequences of vulture population declines worldwide. Ann. N. Y. Acad. Sci. 1249, 57–71 (2012).ADS 
    PubMed 
    Article 

    Google Scholar 
    Reid, W. V. et al. Ecosystems and Human Well-Being-Synthesis: A Report of the Millennium Ecosystem Assessment (Island Press, 2005).
    Google Scholar 
    Wilson, E. E. & Wolkovich, E. M. Scavenging: How carnivores and carrion structure communities. Trends Ecol. Evol. 26, 129–135 (2011).PubMed 
    Article 

    Google Scholar 
    Moleón, M., Sánchez-Zapata, J. A., Selva, N., Donázar, J. A. & Owen-Smith, N. Inter-specific interactions linking predation and scavenging in terrestrial vertebrate assemblages. Biol. Rev. 89, 1042–1054. https://doi.org/10.1111/brv.12097 (2014).Article 
    PubMed 

    Google Scholar 
    Fonseca, C. R. & Ganade, G. Species functional redundancy, random extinctions and the stability of ecosystems. J. Ecol. 89, 118–125 (2001).Article 

    Google Scholar 
    Mori, A. S., Furukawa, T. & Sasaki, T. Response diversity determines the resilience of ecosystems to environmental change. Biol. Rev. 88, 349–364. https://doi.org/10.1111/brv.12004 (2013).Article 
    PubMed 

    Google Scholar 
    Huijbers, C. M. et al. Limited functional redundancy in vertebrate scavenger guilds fails to compensate for the loss of raptors from urbanized sandy beaches. Divers. Distrib. 21, 55–63 (2015).Article 

    Google Scholar 
    Ceballos, G. et al. Accelerated modern human–induced species losses: Entering the sixth mass extinction. Sci. Adv. 1, e1400253 (2015).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Buechley, E. R. & Şekercioğlu, Ç. H. The Avian scavenger crisis: Looming extinctions, trophic cascades, and loss of critical ecosystem functions. Biol. Cons. 198, 220–228 (2016).Article 

    Google Scholar 
    Hill, J. E., DeVault, T. L., Wang, G. & Belant, J. L. Anthropogenic mortality in mammals increases with the human footprint. Front. Ecol. Environ. 18, 13–18. https://doi.org/10.1002/fee.2127 (2019).Article 

    Google Scholar 
    Sebastián-González, E. et al. Scavenging in the Anthropocene: Human impact drives vertebrate scavenger species richness at a global scale. Glob. Change Biol. 25, 3005–3017 (2019).ADS 
    Article 

    Google Scholar 
    Sebastián-González, E. et al. Network structure of vertebrate scavenger assemblages at the global scale: Drivers and ecosystem functioning implications. Ecography 43, 1–13. https://doi.org/10.1111/ecog.05083 (2020).Article 

    Google Scholar 
    Marneweck, C. J., Katzner, T. E. & Jachowski, D. S. Predicted climate-induced reductions in scavenging in eastern North America. Glob. Change Biol. 27, 3383–3394. https://doi.org/10.1111/gcb.15653 (2021).Article 

    Google Scholar 
    Mokany, K., Ash, J. & Roxburgh, S. Functional identity is more important than diversity in influencing ecosystem processes in a temperate native grassland. J. Ecol. 96, 884–893. https://doi.org/10.1111/j.1365-2745.2008.01395.x (2008).Article 

    Google Scholar 
    Gagic, V. et al. Functional identity and diversity of animals predict ecosystem functioning better than species-based indices. Proc. R. Soc. B Biol. Sci. 282, 20142620 (2015).Article 

    Google Scholar 
    Mateo-Tomás, P., Olea, P. P., Selva, N. & Sánchez-Zapata, J. A. Species and individual replacements contribute more than nestedness to shape vertebrate scavenger metacommunities. Ecography 42, 365–375 (2019).Article 

    Google Scholar 
    Sebastián-González, E. et al. Functional traits driving species role in the structure of terrestrial vertebrate scavenger networks. Ecology https://doi.org/10.1002/ecy.3519 (2021).Article 
    PubMed 

    Google Scholar 
    DeVault, T. L., Rhodes, O. E. Jr. & Shivik, J. A. Scavenging by vertebrates: Behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102, 225–234 (2003).Article 

    Google Scholar 
    Allen, M. L., Elbroch, L. M., Wilmers, C. C. & Wittmer, H. U. The comparative effects of large carnivores on the acquisition of carrion by scavengers. Am. Nat. 185, 822–833 (2015).PubMed 
    Article 

    Google Scholar 
    Moleón, M., Sánchez-Zapata, J. A., Sebastián-González, E. & Owen-Smith, N. Carcass size shapes the structure and functioning of an African scavenging assemblage. Oikos 124, 1391–1403 (2015).Article 

    Google Scholar 
    Gutiérrez-Cánovas, C. et al. Large home range scavengers support higher rates of carcass removal. Funct. Ecol. 34, 1921–1932 (2020).Article 

    Google Scholar 
    Walker, M. A. et al. Factors influencing scavenger guilds and scavenging efficiency in Southwestern Montana. Sci. Rep. https://doi.org/10.1038/s41598-021-83426-3 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Winfree, R., Fox, J., Williams, N. M., Reilly, J. R. & Cariveau, D. P. Abundance of common species, not species richness, drives delivery of a real-world ecosystem service. Ecol. Lett. 18, 626–635. https://doi.org/10.1111/ele.12424 (2015).Article 
    PubMed 

    Google Scholar 
    Mateo-Tomás, P., Olea, P. P., Moleón, M., Selva, N. & Sánchez-Zapata, J. A. Both rare and common species support ecosystem services in scavenger communities. Glob. Ecol. Biogeogr. 26, 1459–1470. https://doi.org/10.1111/geb.12673 (2017).Article 

    Google Scholar 
    Butler, J. R. A. & du Toit, J. T. Diet of free-ranging domestic dogs (Canis familiaris) in rural Zimbabwe: Implications for wild scavengers on the periphery of wildlife reserves. Anim. Conserv. 5, 29–37. https://doi.org/10.1017/s136794300200104x (2002).Article 

    Google Scholar 
    DeVault, T. L., Olson, Z. H., Beasley, J. C. & Rhodes, O. E. Jr. Mesopredators dominate competition for carrion in an agricultural landscape. Basic Appl. Ecol. 12, 268–274 (2011).Article 

    Google Scholar 
    Ogada, D. L., Torchin, M. E., Kinnaird, M. F. & Ezenwa, V. O. Effects of vulture declines on facultative scavengers and potential implications for mammalian disease transmission. Conserv. Biol. 26, 453–460. https://doi.org/10.1111/j.1523-1739.2012.01827.x (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    Morales-Reyes, Z. et al. Scavenging efficiency and red fox abundance in Mediterranean mountains with and without vultures. Acta Oecol. 79, 81–88. https://doi.org/10.1016/j.actao.2016.12.012 (2017).ADS 
    Article 

    Google Scholar 
    Inagaki, A. et al. Vertebrate scavenger guild composition and utilization of carrion in an East Asian temperate forest. Ecol. Evol. 10, 1223–1232 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Blazquez, M., Sanchez-Zapata, J. A., Botella, F., Carrete, M. & Eguía, S. Spatio-temporal segregation of facultative avian scavengers at ungulate carcasses. Acta Oecol. 35, 645–650 (2009).ADS 
    Article 

    Google Scholar 
    Inger, R., Cox, D. T. C., Per, E., Norton, B. A. & Gaston, K. J. Ecological role of vertebrate scavengers in urban ecosystems in the UK. Ecol. Evol. 6, 7015–7023. https://doi.org/10.1002/ece3.2414 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hill, J. E., DeVault, T. L., Beasley, J. C., Rhodes, O. E. Jr. & Belant, J. L. Effects of vulture exclusion on carrion consumption by facultative scavengers. Ecol. Evol. 8, 2518–2526. https://doi.org/10.1002/ece3.3840 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Olson, Z., Beasley, J., DeVault, T. L. & Rhodes, O. E. Jr. Scavenger community response to the removal of a dominant scavenger. Oikos 121, 77–84 (2012).Article 

    Google Scholar 
    Pardo-Barquín, E., Mateo-Tomás, P. & Olea, P. P. Habitat characteristics from local to landscape scales combine to shape vertebrate scavenging communities. Basic Appl. Ecol. 34, 126–139. https://doi.org/10.1016/j.baae.2018.08.005 (2019).Article 

    Google Scholar 
    Turner, K. L., Conner, L. M. & Beasley, J. C. Effect of mammalian mesopredator exclusion on vertebrate scavenging communities. Sci. Rep. 10, 1–9 (2020).Article 
    CAS 

    Google Scholar 
    Ohashi, H. et al. Differences in the activity pattern of the wild boar Sus scrofa related to human disturbance. Eur. J. Wildl. Res. 59, 167–177. https://doi.org/10.1007/s10344-012-0661-z (2013).Article 

    Google Scholar 
    Saito, M. & Koike, F. Distribution of wild mammal assemblages along an urban–rural–forest landscape gradient in warm-temperate East Asia. PLoS ONE 8, e65464. https://doi.org/10.1371/journal.pone.0065464 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gaynor, K. M., Hojnowski, C. E., Carter, N. H. & Brashares, J. S. The influence of human disturbance on wildlife nocturnality. Science 360, 1232–1235. https://doi.org/10.1126/science.aar7121 (2018).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Tsunoda, M. et al. Human disturbance affects latrine-use patterns of raccoon dogs. J. Wildl. Manag. 83, 728–736. https://doi.org/10.1002/jwmg.21610 (2019).Article 

    Google Scholar 
    Watabe, R. & Saito, M. U. Effects of vehicle-passing frequency on forest roads on the activity patterns of carnivores. Landsc. Ecol. Eng. 17, 225–231. https://doi.org/10.1007/s11355-020-00434-7 (2021).Article 

    Google Scholar 
    Luna, Á., Romero-Vidal, P. & Arrondo, E. Predation and scavenging in the city: A review of spatio-temporal trends in research. Diversity 13, 46. https://doi.org/10.3390/d13020046 (2021).Article 

    Google Scholar 
    Huijbers, C. M., Schlacher, T. A., Schoeman, D. S., Weston, M. A. & Connolly, R. M. Urbanisation alters processing of marine carrion on sandy beaches. Landsc. Urban Plan. 119, 1–8 (2013).Article 

    Google Scholar 
    Fukushima Prefectural Government. Transition of evacuation designated zones. https://www.pref.fukushima.lg.jp/site/portal-english/en03-08.html. (2019). Accessed 20 Apr 2022.Steinhauser, G., Brandl, A. & Johnson, T. E. Comparison of the Chernobyl and Fukushima nuclear accidents: A review of the environmental impacts. Sci. Total Environ. 470, 800–817 (2014).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Center for International Earth Science Information Network (CIESIN)—Columbia University. (NASA Socioeconomic Data and Applications Center (SEDAC), Palisades, NY, 2018).Lyons, P. C., Okuda, K., Hamilton, M. J., Hinton, T. G. & Beasley, J. C. Rewilding of Fukushima’s human evacuation zone in the presence of radioactive stressors. Front. Ecol. Environ. 18, 127–134 (2020).Article 

    Google Scholar 
    Deryabina, T. G. et al. Long-term census data reveal abundant wildlife populations at Chernobyl. Curr. Biol. 25, R824–R826. https://doi.org/10.1016/j.cub.2015.08.017 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Webster, S. C. et al. Where the wild things are: Influence of radiation on the distribution of four mammalian species within the Chernobyl Exclusion Zone. Front. Ecol. Environ. 14, 185–190. https://doi.org/10.1002/fee.1227 (2016).Article 

    Google Scholar 
    Schlichting, P. E., Love, C. N., Webster, S. C. & Beasley, J. C. Efficiency and composition of vertebrate scavengers at the land–water interface in the Chernobyl Exclusion Zone. Food Webs 18, e00107. https://doi.org/10.1016/j.fooweb.2018.e00107 (2019).Article 

    Google Scholar 
    Newsome, T. M. et al. Monitoring the dead as an ecosystem indicator. Ecol. Evol. 11, 5844–5856. https://doi.org/10.1002/ece3.7542 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Turner, K. L., Abernethy, E. F., Mike Conner, L., Rhodes, O. E. Jr. & Beasley, J. C. Abiotic and biotic factors modulate carrion fate and vertebrate scavenging communities. Ecology 98, 2413–2424 (2017).PubMed 
    Article 

    Google Scholar 
    Ruzicka, R. E. & Conover, M. R. Does weather or site characteristics influence the ability of scavengers to locate food?. Ethology 118, 187–196 (2012).Article 

    Google Scholar 
    Paula, J. J. S. et al. Camera-trapping as a methodology to assess the persistence of wildlife carcasses resulting from collisions with human-made structures. Wildl. Res. 41, 717–725. https://doi.org/10.1071/WR14063 (2015).Article 

    Google Scholar 
    Selva, N., Jędrzejewska, B., Jędrzejewski, W. & Wajrak, A. Factors affecting carcass use by a guild of scavengers in European temperate woodland. Can. J. Zool. 83, 1590–1601 (2005).Article 

    Google Scholar 
    Nakama, S., Yoshimura, K., Fujiwara, K., Ishikawa, H. & Iijima, K. Temporal decrease in air dose rate in the sub-urban area affected by the Fukushima Dai-ichi Nuclear Power Plant accident during four years after decontamination works. J. Environ. Radioact. 208–209, 106013. https://doi.org/10.1016/j.jenvrad.2019.106013 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    Ministry of the Environment of Japan. Off-Site Environmental Remediation in Affected Areas in Japan. http://josen.env.go.jp/en/decontamination/ (2020). Accessed 20 Apr 2022.Japan Meteorological Agency. Climate in Namie in 2018: Monthly Overview Data. http://www.data.jma.go.jp/obd/stats/etrn/view/monthly_a1.php?prec_no=36&block_no=0295&year=2018&month=7&day=&view=p1 (2018). Accessed 1 Apr 2019.De Vault, T. L., Brisbin, J., Lehr, I., Rhodes, J. & Olin, E. Factors influencing the acquisition of rodent carrion by vertebrate scavengers and decomposers. Can. J. Zool. 82, 502–509 (2004).Article 

    Google Scholar 
    Kane, A., Healy, K., Guillerme, T., Ruxton, G. D. & Jackson, A. L. A recipe for scavenging in vertebrates—The natural history of a behaviour. Ecography 40, 11. https://doi.org/10.1111/ecog.02817 (2017).Article 

    Google Scholar 
    Natusch, D. J. D., Lyons, J. A. & Shine, R. How do predators and scavengers locate resource hotspots within a tropical forest?. Aust. Ecol. 42, 742–749. https://doi.org/10.1111/aec.12492 (2017).Article 

    Google Scholar 
    Japan Aerospace Exploration Agency. High-resolution land use land cover map of Japan (ver.16.09). https://www.eorc.jaxa.jp/ALOS/en/lulc/lulc_index.htm (2011). Accessed 1 Apr 2019.Newkirk, E. S. CPW Photo Warehouse. http://cpw.state.co.us/learn/Pages/ResearchMammalsSoftware.aspx (2016). Accessed 1 Apr 2019.Therneau, T. M. A Package for Survival Analysis in R. R package version 3.3-1 (2022).Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. https://doi.org/10.18637/jss.v067.i01 (2015).Article 

    Google Scholar 
    Anderson, D. et al. Introgression dynamics from invasive pigs into wild boar following the March 2011 natural and anthropogenic disasters at Fukushima. Proc. R. Soc. B Biol. Sci. 288, 20210874. https://doi.org/10.1098/rspb.2021.0874 (2021).CAS 
    Article 

    Google Scholar 
    Ishiniwa, H., Onuma, M. & Tamaoki, M. Behavior of Radionuclides in the Environment III 463–472 (Springer, 2022).Book 

    Google Scholar 
    Nemoto, Y. et al. Effects of 137Cs contamination after the TEPCO Fukushima Dai-ichi Nuclear Power Station accident on food and habitat of wild boar in Fukushima Prefecture. J. Environ. Radioact. 225, 106342. https://doi.org/10.1016/j.jenvrad.2020.106342 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Olson, Z. H., Beasley, J. C. & Rhodes, O. E. Jr. Carcass type affects local scavenger guilds more than habitat connectivity. PLoS ONE 11, e0147798 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    DeVault, T. L., Seamans, T. W., Linnell, K. E., Sparks, D. W. & Beasley, J. C. Scavenger removal of bird carcasses at simulated wind turbines: Does carcass type matter?. Ecosphere. https://doi.org/10.1002/ecs2.1994 (2017).Article 

    Google Scholar 
    Sugiura, S., Tanaka, R., Taki, H. & Kanzaki, N. Differential responses of scavenging arthropods and vertebrates to forest loss maintain ecosystem function in a heterogeneous landscape. Biol. Cons. 159, 206–213 (2013).Article 

    Google Scholar 
    Enari, H. & Enari, H. S. Not avian but mammalian scavengers efficiently consume carcasses under heavy snowfall conditions: A case from northern Japan. Mamm. Biol. 101, 419–428. https://doi.org/10.1007/s42991-020-00097-9 (2021).Article 

    Google Scholar 
    Selva, N., Jedrzejewska, B., Jedrzejewski, W. & Wajrak, A. Scavenging on European bison carcasses in Bialowieza primeval forest (eastern Poland). Ecoscience 10, 303–311 (2003).Article 

    Google Scholar 
    Jojola-Elverum, S. M., Shivik, J. A. & Clark, L. Importance of bacterial decomposition and carrion substrate to foraging brown treesnakes. J. Chem. Ecol. 27, 1315–1331. https://doi.org/10.1023/a:1010357024140 (2001).CAS 
    Article 
    PubMed 

    Google Scholar 
    Abernethy, E. F., Turner, K. L., Beasley, J. C. & Rhodes, O. E. Jr. Scavenging along an ecological interface: Utilization of amphibian and reptile carcasses around isolated wetlands. Ecosphere 8, e01989. https://doi.org/10.1002/ecs2.1989 (2017).Article 

    Google Scholar 
    Sugiura, S. & Hayashi, M. Functional compensation by insular scavengers: The relative contributions of vertebrates and invertebrates vary among islands. Ecography 41, 1173–1183 (2018).Article 

    Google Scholar 
    Matsuo, R. & Ochiai, K. Dietary overlap among two introduced and one native sympatric carnivore species, the raccoon, the masked palm civet, and the raccoon dog, in Chiba Prefecture, Japan. Mammal Study 34, 187–194 (2009).Article 

    Google Scholar 
    Drygala, F. & Zoller, H. Diet composition of the invasive raccoon dog (Nyctereutes procyonoides) and the native red fox (Vulpes vulpes) in north-east Germany. Hystrix Italian J. Mammal. 24, 190–194 (2014).
    Google Scholar 
    Elmeros, M. et al. The diet of feral raccoon dog (Nyctereutes procyonoides) and native badger (Meles meles) and red fox (Vulpes vulpes) in Denmark. Mammal Res. 63, 405–413. https://doi.org/10.1007/s13364-018-0372-2 (2018).Article 

    Google Scholar 
    Sekizawa, R., Ichii, K. & Kondo, M. Satellite-based detection of evacuation-induced land cover changes following the Fukushima Daiichi nuclear disaster. Remote Sensing Lett. 6, 824–833 (2015).Article 

    Google Scholar 
    Ishihara, M. & Tadono, T. Land cover changes induced by the great east Japan earthquake in 2011. Sci. Rep. 7, 45769–45769. https://doi.org/10.1038/srep45769 (2017).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Focardi, S., Materassi, M., Innocenti, G. & Berzi, D. Kleptoparasitism and scavenging can stabilize ecosystem dynamics. Am. Nat. 190, 398–409 (2017).PubMed 
    Article 

    Google Scholar 
    Osugi, S., Trentin, B. E. & Koike, S. Impact of wild boars on the feeding behavior of smaller frugivorous mammals. Mamm. Biol. 97, 22–27 (2019).Article 

    Google Scholar 
    Duľa, M. & Krofel, M. A cat in paradise: Hunting and feeding behaviour of Eurasian lynx among abundant naive prey. Mamm. Biol. 100, 685–690. https://doi.org/10.1007/s42991-020-00070-6 (2020).Article 

    Google Scholar 
    Smith, J. B., Laatsch, L. J. & Beasley, J. C. Spatial complexity of carcass location influences vertebrate scavenger efficiency and species composition. Sci. Rep. 7, 10250. https://doi.org/10.1038/s41598-017-10046-1 (2017).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Moleón, M. et al. Carrion availability in space and time. In Carrion Ecology and Management (eds Olea, P.P., Mateo-Tomás, P. & Sánchez-Zapata, J.A.) 23–44 (Springer International Publishing, 2019).
    DeVault, T. L. & Rhodes, O. E. Jr. Identification of vertebrate scavengers of small mammal carcasses in a forested landscape. Acta Theriol. 47, 185–192 (2002).Article 

    Google Scholar 
    Bumann, G. B. & Stauffer, D. F. Scavenging of ruffed grouse in the Appalachians: Influences and implications. Wildl. Soc. Bull. 1973–2006(30), 853–860 (2002).
    Google Scholar 
    Young, A., Stillman, R., Smith, M. J. & Korstjens, A. H. An experimental study of vertebrate scavenging behavior in a Northwest European woodland context. J. Forensic Sci. 59, 1333–1342. https://doi.org/10.1111/1556-4029.12468 (2014).Article 
    PubMed 

    Google Scholar 
    Abernethy, E. F. et al. Carcasses of invasive species are predominantly utilized by invasive scavengers in an island ecosystem. Ecosphere 7 (2016).DeVault, T. L. & Krochmal, A. R. Scavenging by snakes: An examination of the literature. Herpetologica 58, 429–436 (2002).Article 

    Google Scholar 
    Shivik, J. A. & Clark, L. Ontogenetic shifts in carrion attractiveness to brown tree snakes (Boiga irregularis). J. Herpetol. 33, 334–336. https://doi.org/10.2307/1565737 (1999).Article 

    Google Scholar 
    Campobasso, C. P., Di Vella, G. & Introna, F. Factors affecting decomposition and Diptera colonization. Forensic Sci. Int. 120, 18–27 (2001).CAS 
    PubMed 
    Article 

    Google Scholar  More