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The Critical Importance of Old World Fruit Bats for Healthy Ecosystems and Economies

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The Critical Importance of Old World Fruit Bats for Healthy Ecosystems and Economies fevo-09-641411 March 30, 2021 Time: 11:8 # 1 REVIEW published: 06 April 2021 doi: 10.3389/fevo.2021.641411 The Critical Importance of Old World Fruit Bats for Healthy Ecosystems and Economies Sheema Abdul Aziz1*, Kim R. McConkey2, Krizler Tanalgo3,4, Tuanjit Sritongchuay3, Mary-Ruth Low1, Joon Yee Yong1, Tammy L. Mildenstein5, Christine Ely Nuevo-Diego6, Voon-Ching Lim7 and Paul A. Racey8 1 Project Pteropus, Rimba, Kuala Lumpur, Malaysia, 2 School of Environmental and Geographical Sciences, University of Nottingham Malaysia, Semenyih, Malaysia, 3 Landscape Ecology Group, Center for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, China, 4 Department of Biological Sciences, College of Science and Mathematics, University of Southern Mindanao, Cotabato, Philippines, 5 Department of Biology, Cornell College, Mount Vernon, IA, United States, 6 Bat Eco-Interactions Project, Houston, TX, United States, 7 School of Science, Monash University Malaysia, Bandar Sunway, Malaysia, 8 Centre for Ecology and Conservation, University of Exeter, Exeter, United Kingdom Despite extensive documentation of the ecological and economic importance of Old World fruit bats (Chiroptera: Pteropodidae) and the many threats they face from humans, Edited by: Anna Traveset, negative attitudes towards pteropodids have persisted, fuelled by perceptions of bats as Consejo Superior de Investigaciones being pests and undesirable neighbours. Such long-term negativity towards bats is now Científicas, Spain further exacerbated by more recent disease-related concerns, particularly associated Reviewed by: with the current COVID-19 pandemic. There remains an urgent need to investigate Ricardo Rocha, University of Cambridge, and highlight the positive and beneficial aspects of bats across the Old World. While United Kingdom previous reviews have summarised these extensively, numerous new studies conducted Merlin Tuttle, Merlin Tuttle’s Bat Conservation, over the last 36 years have provided further valuable data and insights which warrant United States an updated review. Here we synthesise research on pteropodid-plant interactions, *Correspondence: comprising diet, ecological roles, and ecosystem services, conducted during 1985- Sheema Abdul Aziz 2020. We uncovered a total of 311 studies covering 75 out of the known 201 pteropodid [email protected] species (37%), conducted in 47 countries. The majority of studies documented diet Specialty section: (52% of all studies; 67 pteropodid species), followed by foraging movement (49%; This article was submitted to Population and Evolutionary 50 pteropodid species), with fewer studies directly investigating the roles played by Dynamics, pteropodids in seed dispersal (24%; 41 pteropodid species), pollination (14%; 19 a section of the journal pteropodid species), and conflict with fruit growers (12%; 11 pteropodid species). Frontiers in Ecology and Evolution Pteropodids were recorded feeding on 1072 plant species from 493 genera and Received: 14 December 2020 Accepted: 08 March 2021 148 families, with fruits comprising the majority of plant parts consumed, followed Published: 06 April 2021 by flowers/nectar/pollen, leaves, and other miscellaneous parts. Sixteen pteropodid Citation: species have been confirmed to act as pollinators for a total of 21 plant species, and Aziz SA, McConkey KR, Tanalgo K, Sritongchuay T, Low M-R, 29 pteropodid species have been confirmed to act as seed dispersers for a total of 311 Yong JY, Mildenstein TL, plant species. Anthropogenic threats disrupting bat-plant interactions in the Old World Nuevo-Diego CE, Lim VC and include hunting, direct persecution, habitat loss/disturbance, invasive species, and Racey PA (2021) The Critical Importance of Old World Fruit Bats climate change, leading to ecosystem-level repercussions. We identify notable research for Healthy Ecosystems gaps and important research priorities to support conservation action for pteropodids. and Economies. Front. Ecol. Evol. 9:641411. Keywords: bat-plant interactions, double mutualism, ecosystem services, Palaeotropics, pollination, doi: 10.3389/fevo.2021.641411 Pteropodidae, seed dispersal Frontiers in Ecology and Evolution| www.frontiersin.org 1 April 2021| Volume 9| Article 641411 fevo-09-641411 March 30, 2021 Time: 11:8 # 2 Aziz et al. Critical Importance of Pteropodid Bats INTRODUCTION underestimated compared to the much more widely studied birds, primates, and large terrestrial mammals (Seltzer et al., Discrepancies between human perceptions of an animal, and 2013; Baker et al., 2018). Further, pteropodid species that can the importance of the animal to broader human well-being, maintain plant populations in degraded areas regularly forage is perhaps most profoundly unbalanced for bats. Old World in isolated trees (Schmelitschek et al., 2009), and can be key fruit bats (family Pteropodidae; Simmons and Cirranello, 2020; to catalysing restoration in disturbed habitats (Sritongchuay also referred to as “pteropodids”) are particularly threatened, et al., 2014; Oleksy et al., 2015). A comprehensive understanding facing multiple environmental pressures not only as a result of bat-plant interactions in the Old World is essential for of exclusion from statutory protection policies, but also due defining their importance, and their benefits to humans – to a lack of necessary conservation attention, even for legally which can help foster a much-needed and more favourable protected species (Aziz et al., 2016). In addition, the COVID- balance in public opinion, and direct research to important 19 pandemic is the latest and worst disease-related concern to gaps in knowledge. have reinforced long-held fears and negative attitudes towards The goal of this paper is to synthesise the breadth of bats (López-Baucells et al., 2018; Rocha et al., 2020; Tuttle, 2020; our latest knowledge on pteropodid diet and pteropodid-plant Zhao, 2020). Bats are persecuted due to misguided fears of viral interactions, building from previous reviews and spanning transmission (Tuttle, 2018; Rocha et al., 2020; Lu et al., 2021), more than three decades of research (1985–2020). We use the noise, smell and mess associated with roosts in residential this dataset to: (i) describe the confirmed and potential areas (Aziz et al., 2017a), and for their consumption of fruit ecological roles that pteropodids perform, by evaluating studies crops (Aziz et al., 2016); the latter has even induced mass culls on diet, foraging movement, pollination, and seed dispersal; of ∼50% of the endemic flying fox (Pteropus niger) population (ii) summarise the main threats to these roles; and (iii) in Mauritius (Florens and Baider, 2019). Fruit bats also continue identify the most critical research gaps. This review thus to be intensively harvested for consumption (Mildenstein et al., covers the current state of knowledge regarding pteropodid- 2016), despite often dwindling populations, and despite zoonotic plant interactions. disease concerns. The 201 species of pteropodids range from Africa, the eastern Mediterranean, Madagascar, Indian Ocean islands, METHODS across South and Southeast Asia, southern East Asia including Hong Kong and Taiwan, and throughout islands of the In this review of more recent bat-plant interaction studies, we Pacific from the Ryukyu Archipelago, to coastal eastern included interactions described in post-1985 reviews along with Australia (including Christmas Island), Melanesia, Micronesia, the many new studies since. We also included studies that and Polynesia excluding New Zealand and Hawai’i (Mickleburgh investigated ecosystem services and disservices by pteropodids et al., 1992). Available data on the status of species suggest (Zhang et al., 2007). serious population declines for many, mainly due to habitat loss With the exception of Pacific island nations and and overhunting, with 37% of assessed species being threatened Papua New Guinea, data have been organised according to (IUCN, 2020). Pteropodid declines will also result in plant country and geopolitical regions (United Nations, 2020). We declines, with ecosystem-wide repercussions. grouped together island nations of the regions Melanesia, Complex inter-relationships between Pteropodid bats and Micronesia, and Polynesia as “The Pacific.” For Africa, we treated plants over millennia have resulted in “bat flowers” and “bat insular and continental nations as separate regions. fruits” that are reliant on bats for pollination and/or seed dispersal Although this review covers all pteropodids across their (Marshall, 1983). Bat-plant interactions were first recorded in range, for which the common term “fruit bats” is sometimes 1772 and compiled in the mid-1980s (Marshall, 1983, 1985), used, we use the terms “large pteropodid” and “large fruit bat” to showing how pteropodids carry out vital ecological functions refer only to species with either body weight ≥250 g or forearm in diverse habitats, and are thus essential for the healthy length >110 mm (following Pierson and Rainey, 1992; Kunz and functioning of ecosystems and economies (Marshall, 1985; Fujita Pierson, 1994), which includes the genera Acerodon, Aproteles, and Tuttle, 1991; Mickleburgh et al., 1992; Richards, 1995; Desmalopex, Dobsonia, Eidolon, Hypsignathus, Pteralopex, Lacher et al., 2019). On faunally depauperate islands, pteropodids Pteropus, and Styloctenium (Pierson and Rainey, 1992; Kunz and play keystone roles as principal pollinators and seed dispersers Pierson, 1994; genera list compiled by Mildenstein,
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