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      Insectivorous bat reproduction and human cave visitation in Cambodia: A perfect conservation storm?

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          Abstract

          Cave roosting bats represent an important component of Southeast Asian bat diversity and are vulnerable to human disturbance during critical reproductive periods (pregnancy, lactation and weaning). Because dramatic growth of cave tourism in recent decades has raised concerns about impacts on cave bats in the region, we assessed the reproductive phenology of two insectivorous species ( Hipposideros larvatus sensu lato and Taphozous melanopogon) at three caves in Cambodia for 23 months in 2014–2016 and evaluated human visitation to these sites between 2007 and 2014. Despite the differing foraging strategies employed by the two taxa, the temporal consistency observed in proportions of pregnant, lactating and juvenile bats indicates that their major birth peaks coincide with the time of greatest cave visitation annually, particularly for domestic visitors and namely during the Cambodian new year in April. They also reflect rainfall patterns and correspond with the reproductive phenology of insectivorous cave bats in Vietnam. These findings were predictable because 1) insect biomass and thus food availability for insectivorous bats are optimal for ensuring survival of young following this period, and 2) the Khmer new year is the most significant month for religious ceremonies and thus domestic cave visitation nationally, due to the abundance of Buddhist shrines and temples in Cambodian caves. While the impact of visitor disturbance on bat population recruitment cannot be empirically assessed due to lack of historical data, it is nonetheless likely to have been considerable and raises a conservation concern. Further, because growing evidence suggests that insectivorous cave bats exhibit reproductive synchrony across continental Southeast Asia where countless cave shrines are heavily frequented during April in Theravada Buddhist countries (e.g., Myanmar, Thailand, Cambodia and Laos), our results may have wider applicability in the region. We consequently advocate for increased emphasis on sustainable cave management practices in Cambodia and further investigations to determine whether our findings present a broader concern for cave bat conservation in Southeast Asia.

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          Conservation relevance of bat caves for biodiversity and ecosystem services

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            Rainfall, food abundance and timing of parturition in African bats

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              Effects of Cave Tours on Breeding Myotis velifer

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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                30 April 2018
                2018
                : 13
                : 4
                : e0196554
                Affiliations
                [1 ] Centre for Biodiversity Conservation, Royal University of Phnom Penh, Phnom Penh, Cambodia
                [2 ] Epidemiology and Public Health Unit, Institut Pasteur du Cambodge, Phnom Penh, Cambodia
                [3 ] UPR AGIRs, CIRAD-ES, Montpellier, France
                [4 ] Fauna & Flora International, Phnom Penh, Cambodia
                [5 ] Harrison Institute, Kent, United Kingdom
                University of Western Ontario, CANADA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-0439-2446
                Article
                PONE-D-17-42248
                10.1371/journal.pone.0196554
                5927413
                29709036
                d35cca9f-3795-4fda-b889-87b17cc88894
                © 2018 Lim et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 18 December 2017
                : 16 April 2018
                Page count
                Figures: 4, Tables: 0, Pages: 13
                Funding
                This study was supported by the Southeast Asian Bat Research & Conservation Unit (USA National Science Foundation, grant no. 1051363), US Agency for International Development (Helping Address Rural Vulnerabilities and Ecosystem STability Recovery Program, prime contract #AID-442-C-11-00001), Columbus Zoo and Aquarium Conservation Fund (USA), European Commission Innovate program (ComAcross project, grant no. DCI-ASIE/2013/315-047) and Aviesan Sud and Fondation Total (SouthEast Asia Encephalitis project). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Bats
                People and Places
                Geographical Locations
                Asia
                Cambodia
                Medicine and Health Sciences
                Women's Health
                Maternal Health
                Pregnancy
                Medicine and Health Sciences
                Women's Health
                Obstetrics and Gynecology
                Pregnancy
                People and Places
                Population Groupings
                Religious Faiths
                Buddhism
                Medicine and Health Sciences
                Endocrinology
                Endocrine Physiology
                Lactation
                Biology and Life Sciences
                Physiology
                Endocrine Physiology
                Lactation
                Medicine and Health Sciences
                Physiology
                Endocrine Physiology
                Lactation
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Lactation
                Medicine and Health Sciences
                Physiology
                Reproductive Physiology
                Lactation
                Earth Sciences
                Seasons
                Social Sciences
                Anthropology
                Cultural Anthropology
                Religion
                Social Sciences
                Sociology
                Religion
                Engineering and Technology
                Structural Engineering
                Built Structures
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                All relevant data are included within the paper and its Supporting Information files.

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