Cultural ecosystem services constitute a growing field of research that is characterized by an increasing number of publications from various academic disciplines. We conducted a semiquantitative review of publications explicitly dealing with cultural ecosystem services. Our aims were: (1) to provide an overview of the current state of research, (2) to classify the diversity of research approaches by identifying clusters of publications that address cultural ecosystem services in similar ways, and (3) to highlight some important challenges for the future of cultural ecosystem services research. We reviewed 107 publications and extracted 20 attributes describing their type and content, including methods, scales, drivers of change, and trade-offs between services. Using a cluster analysis on a subset of attributes we identified five groups of publications: Group 1, conceptual focus, deals with theoretical issues; Group 2, descriptive reviews, consists mostly of desktop studies; Group 3, localized outcomes, deals with case studies coming from different disciplines; Group 4, social and participatory, deals mainly with assessing preferences and perceptions; and Group 5, economic assessments, provides economic valuations. Emerging themes in cultural ecosystem services research relate to improving methods for cultural ecosystem services valuation, studying cultural ecosystem services in the context of ecosystem service bundles, and more clearly articulating policy implications. Based on our findings, we conclude that: (1) cultural ecosystem services are well placed as a tool to bridge gaps between different academic disciplines and research communities, (2) capitalizing on the societal relevance of cultural ecosystem services could help address real-world problems, and (3) cultural ecosystem services have the potential to foster new conceptual links between alternative logics relating to a variety of social and ecological issues.

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Cultural Ecosystem Services: A Literature Review and Prospects for Future Research

Caves and other subterranean habitats with their often strange (even bizarre) inhabitants have long been objects of fascination, curiosity, and debate. The question of how such organisms have evolved, and the relative roles of natural selection and genetic drift, has engaged subterranean biologists for decades. Indeed, these studies continue to inform the general theory of adaptation and evolution. Subterranean ecosystems generally exhibit little or no primary productivity and, as extreme ecosystems, provide general insights into ecosystem function. The Biology of Caves and other Subterranean Habitats offers a concise but comprehensive introduction to cave ecology and evolution. Whilst there is an emphasis on biological processes occurring in these unique environments, conservation and management aspects are also considered. The monograph includes a global range of examples from more than 25 countries, and case studies from both caves and non-cave subterranean habitats; it also provides a clear explanation of specialized terms used by speleologists. This accessible text will appeal to researchers new to the field and to the many professional ecologists and conservation practitioners requiring a concise but authoritative overview. Its engaging style will also make it suitable for undergraduate and graduate students taking courses in cave and subterranean biology. Its more than 650 references, 150 of which are new since the first edition, provide many entry points to the research literature.

The Biology of Caves and Other Subterranean Habitats

White-nose syndrome (WNS), an emerging infectious disease that has killed over 5.5 million hibernating bats, is named for the causative agent, a white fungus (Geomyces destructans (Gd)) that invades the skin of torpid bats. During hibernation, arousals to warm (euthermic) body temperatures are normal but deplete fat stores. Temperature-sensitive dataloggers were attached to the backs of 504 free-ranging little brown bats (Myotis lucifugus) in hibernacula located throughout the northeastern USA. Dataloggers were retrieved at the end of the hibernation season and complete profiles of skin temperature data were available from 83 bats, which were categorized as: (1) unaffected, (2) WNS-affected but alive at time of datalogger removal, or (3) WNS-affected but found dead at time of datalogger removal. Histological confirmation of WNS severity (as indexed by degree of fungal infection) as well as confirmation of presence/absence of DNA from Gd by PCR was determined for 26 animals. We demonstrated that WNS-affected bats aroused to euthermic body temperatures more frequently than unaffected bats, likely contributing to subsequent mortality. Within the subset of WNS-affected bats that were found dead at the time of datalogger removal, the number of arousal bouts since datalogger attachment significantly predicted date of death. Additionally, the severity of cutaneous Gd infection correlated with the number of arousal episodes from torpor during hibernation. Thus, increased frequency of arousal from torpor likely contributes to WNS-associated mortality, but the question of how Gd infection induces increased arousals remains unanswered.

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Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome

Bats are an ecologically and taxonomically diverse group accounting for roughly a fifth of mammalian diversity worldwide. Many of the threats bats face (e.g., habitat loss, bushmeat hunting, and climate change) reflect the conservation challenges of our era. However, compared to other mammals and birds, we know significantly less about the population status of most bat species, which makes prioritizing and planning conservation actions challenging. Over a third of bat species assessed by the International Union for Conservation of Nature (IUCN) are considered threatened or data deficient, and well over half of the species have unknown or decreasing population trends. That equals 988 species, or 80% of bats assessed by IUCN, needing conservation or research attention. Delivering conservation to bat species will require sustained efforts to assess population status and trends and address data deficiencies. Successful bat conservation must integrate research and conservation to identify stressors and their solutions and to test the efficacy of actions to stabilize or increase populations. Global and regional networks that connect researchers, conservation practitioners, and local stakeholders to share knowledge, build capacity, and prioritize and coordinate research and conservation efforts, are vital to ensuring sustainable bat populations worldwide.

A review of the major threats and challenges to global bat conservation

Human welfare is significantly linked to ecosystem services such as the suppression of pest insects by birds and bats. However, effects of biocontrol services on tropical cash crop yield are still largely unknown. For the first time, we manipulated the access of birds and bats in an exclosure experiment (day, night and full exclosures compared to open controls in Indonesian cacao agroforestry) and quantified the arthropod communities, the fruit development and the final yield over a long time period (15 months). We found that bat and bird exclusion increased insect herbivore abundance, despite the concurrent release of mesopredators such as ants and spiders, and negatively affected fruit development, with final crop yield decreasing by 31% across local (shade cover) and landscape (distance to primary forest) gradients. Our results highlight the tremendous economic impact of common insectivorous birds and bats, which need to become an essential part of sustainable landscape management.

Bats and birds increase crop yield in tropical agroforestry landscapes

Ecosystem services are the benefits obtained from the environment that increase human well-being. Economic valuation is conducted by measuring the human welfare gains or losses that result from changes in the provision of ecosystem services. Bats have long been postulated to play important roles in arthropod suppression, seed dispersal, and pollination; however, only recently have these ecosystem services begun to be thoroughly evaluated. Here, we review the available literature on the ecological and economic impact of ecosystem services provided by bats. We describe dietary preferences, foraging behaviors, adaptations, and phylogenetic histories of insectivorous, frugivorous, and nectarivorous bats worldwide in the context of their respective ecosystem services. For each trophic ensemble, we discuss the consequences of these ecological interactions on both natural and agricultural systems. Throughout this review, we highlight the research needed to fully determine the ecosystem services in question. Finally, we provide a comprehensive overview of economic valuation of ecosystem services. Unfortunately, few studies estimating the economic value of ecosystem services provided by bats have been conducted to date; however, we outline a framework that could be used in future studies to more fully address this question. Consumptive goods provided by bats, such as food and guano, are often exchanged in markets where the market price indicates an economic value. Nonmarket valuation methods can be used to estimate the economic value of nonconsumptive services, including inputs to agricultural production and recreational activities. Information on the ecological and economic value of ecosystem services provided by bats can be used to inform decisions regarding where and when to protect or restore bat populations and associated habitats, as well as to improve public perception of bats.

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Ecosystem services provided by bats

Crop pests eaten by bats in organic pecan orchards

Native predators provide undervalued pest suppression services to agriculture. Studies of pest consumption by insectivorous bats tend to focus upon single species in large, centralized colonies, while bats dispersed in small groups within the agricultural matrix often go unnoticed. Pecan trees, Carya illinoinensis, and the destructive pecan nut casebearer (PNC) moth, Acrobasis nuxvorella, comprise a tightly linked host–parasite system in a widespread agroecosystem native to North America. Here we use a quantitative polymerase chain reaction (qPCR) assay of fecal DNA to document predation on PNC moths by an assemblage of sympatric bat species across episodic peaks in PNC abundance. Although five species of bats consume PNC moths, greater predation by a solitary tree-roosting bat (eastern red bat, Lasiurus borealis) than other species is suggested by a higher frequency of PNC occurrence and quantity of PNC gene copies in fecal samples. Consumption of PNC by bats during all documented peaks in moth activity suggests that predation pressure occurs throughout the PNC season. Our results highlight the need to consider multi-species assemblages and different foraging strategies when assessing pest suppression services, particularly in agroforestry or tree crops. Assessing the diet of only common or easily captured species limits our ability to accurately document pest consumption by bats.

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Sympatric Bat Species Prey Opportunistically on a Major Moth Pest of Pecans

ABSTRACT: Mosquitoes affect human health and well-being globally through their roles as disease-causing pathogen vectors. Utilizing genetic techniques, we conducted a large-scale dietary study of three bat species common to the southeastern U.S.A., Lasiurus seminolus (Seminole bat), Nycticeius humeralis (evening bat), and Myotis austroriparius (southeastern myotis). Through next-generation sequencing of a 180 bp portion of cytochrome oxidase subunit I (COI) of mitochondrial DNA from 180 bat guano samples, we documented consumption of 17 species of mosquitoes by bats, including six endemic arbovirus vectors. Culex quinquefasciatus, Culex coronator, Culiseta melanura, Culex salinarius, Culex erraticus, and Coquillettidia perturbans were consumed by 51.3%, 43.7%, 27.2%, 22.8%, 18.0%, and 12.7% of bats sampled, respectively. Consumption of two of these mosquito species was explained by spatial variables reflecting the prevalence of mosquito larval habitat, five were explained by bat traits (bat mass, bat species), and two were explained by these factors plus temporal variables (maximum daily temperature, time since sunset, date), making it challenging to offer specific guidance on how best to promote bats as a means of reducing arbovirus vector species. Our results show that common bat species of the southeastern U.S.A. consume endemic, but not exotic, arbovirus mosquito vectors. Future studies are needed to understand the impact of bat consumption on mosquito numbers and public health.

Elizabeth Braun de Torrez

Papers

Ecosystem services provided by bats

Crop pests eaten by bats in organic pecan orchards

Sympatric Bat Species Prey Opportunistically on a Major Moth Pest of Pecans

Consumption of endemic arbovirus mosquito vectors by bats in the southeastern United States