Skip to main content
  • Research article
  • Open access
  • Published:

Bat pollinators: a decade of monitoring reveals declining visitation rates for some species in Thailand


Bats are important pollinators, but they are difficult to study since they are volant and nocturnal. Thus, long-term studies of nectarivorous bats are scarce, despite their potential to help assess trends in bat populations and their pollination services. We used capture rates of nectarivorous bats at chiropterophilous flowers in order to examine temporal trends in bat visitation in an area that is undergoing extensive land use change. We mist-netted at five bat-pollinated plant taxa (Durio zibethinus, Musa acuminata, Oroxylum indicum, Parkia speciosa, and Sonneratia spp.) in southern Thailand over six years between 2011 and 2021. We found that the most common bat species, Eonycteris spelaea, was the main visitor at all five plant taxa and had consistent visitation rates across all study years. In contrast, two other important pollinators, Macroglossus minimus and M. sobrinus, showed 80% declines in the number of individuals netted at mangrove apple (Sonneratia spp.) and banana (Musa acuminata) flowers, respectively. These findings suggest that E. spelaea (a large, cave-roosting species with a broad diet) is more tolerant of anthropogenic change than are Macroglossus bats (small, foliage-roosting species with specialized diets), which may in turn affect the reproductive success of plants pollinated by these species. Our study demonstrates how decade-long monitoring can reveal species-specific temporal patterns in pollinator visitation, emphasizing the need for tailored conservation plans. While the conservation status of most nectarivorous bats in the area is Least Concern, our results indicate that population studies in Southeast Asia are urgently needed for updated bat species conservation assessments.


While most pollination research has focused on bees and other insects [53, 72], bats are highly important pollinators for many night-blooming plant species [19, 35]. Bat-pollinated plants are often highly specialized [59] and typically share little overlap with other pollinator groups [67]. Previous research has shown that vertebrate-pollinated plants are more dependent on their pollinators than are insect-pollinated plants, especially in the tropics [50]. Furthermore, bat-pollinated plants are more dependent on their pollinators than plants that are pollinated by other vertebrate groups, such as birds or rodents [50]. Many of these bat-pollinated plant species are ecologically and economically important [35, 60].

Despite their importance, bat pollinators are understudied, in part, because of the difficulty of studying these elusive, nocturnal, and volant animals [32]. Pollinating bats in the paleotropics present an even greater challenge, given that they do not echolocate, which precludes the use of acoustic monitoring and requires capturing individuals in order to identify them to species [23]. Thus, because they require large investments in time, energy, and funding, long-term ecological studies of bats (i.e., > 10 years sensu [32]) are scarce (but see [25, 28, 33, 47, 65]). However, multi-year studies can be informative for assessing trends in bat populations and their pollination services [23, 28, 32], especially given how quickly landscapes are changing in the Anthropocene [58, 74].

Most research examining the effects of anthropogenic stressors on pollinators has focused on insects, but bats are affected by many of the same challenges. For example, large-scale studies of insect pollinators have found that land-use type and intensity affect pollinator diversity, especially in tropical regions [42], and especially for pollinators with narrow diets [72]. Moreover, fragmentation [4, 26] and climate change [20, 49] can also negatively affect insect pollinators. Research examining how bat pollinators respond to anthropogenic change is less comprehensive, but studies published to date have highlighted similar overall patterns. Habitat loss and degradation are some of the biggest threats to bats [23, 31, 41, 46]. Similarly, Regan et al. [52] found that habitat loss due to agriculture is one of the main drivers of extinction among mammalian pollinators, most of which are bats, and that pollinating bat species tend to be more threatened than non-pollinating bat species. Moreover, flower-visiting bats exhibit dietary shifts in response to changes in landscape structure [56] and climate change can affect the distributions of nectarivorous bats and the plant species they pollinate, resulting in spatial mismatch between plants and pollinators [75]. One of the key findings among many of these studies is that the effect of anthropogenic disturbance varies by region and pollinator species [27, 41, 42, 53, 72]. Thus, research is still needed for many pollinator taxa, such as understudied bat pollinators, and multi-year studies can provide valuable information about how pollinators are responding to anthropogenic changes.

In particular, previous research has stressed the need for more bat research in understudied tropical areas such as Southeast Asia [23, 34, 41, 48]. We conducted a decade-long study on the pollinating bats of southern Thailand, collecting data in 2011–2014 and 2019–2021. The flora of this region includes many species that are pollinated by bats, including the economically important durian (Durio zibethinus L. [13]) and a critically endangered mangrove species (Sonneratia griffithii Kurz [45]). Much is known about the ecology of the flower-visiting bat species in the area [1,2,3, 10,11,12,13, 54, 56, 60,61,62,63], but we lack reliable information about their population sizes and trends. For example, the IUCN Red List [30] classifies many of the local flower-visiting bat species as Least Concern, but the lack of concrete information makes such assessments untenable. Inconsistent with these IUCN assessments, a study in Singapore estimated that 33–72% of the country’s bat species are now locally extinct, and projected that at least 23% of the bat species in Southeast Asia will be extinct by 2100 [36]. Moreover, the study area has changed substantially over the past few decades. A recent study demonstrated that, between 1995 and 2015, southern Thailand lost 21% of terrestrial forests, 26.2% of mangrove forests, and 55% of peat swamp forests, with up to 33% of remaining forests classified as highly vulnerable to future land conversion [64]. Given such extensive land-use changes, we examined bat capture rates at key chiropterophilous plant species in southern Thailand between 2011–2021 in order to assess trends in bat populations and the pollination services they provide.


Study area

This work was conducted in southern Thailand (Phatthalung, Satun, Songkhla, and Trang provinces; 6°32'–7°36' N, 99°21'–100°37' E) where nectarivorous bats and bat-pollinated plant species are common [63]. The area is dominated by rubber and oil palm plantations intermixed with other agricultural landscapes (e.g., rice paddies and fruit orchards), patches of natural habitat (e.g., lowland tropical forests and mangrove forests), and human settlements [60, 64, 68]. The climate is tropical. The average minimum temperature in our study area is 24oC, the average maximum temperature is 34°C, and the average yearly precipitation is 1,800 mm (years 1991–2020) (Climatological Center, Thai Meteorological Department,

Study species

The most common flower-visiting bat species in our study area include three nectar-specialist bat species (Eonycteris spelaea (Dobson, 1871); Macroglossus minimus (E. Geoffroy, 1810); and M. sobrinus K. Andersen, 1911) and four primarily frugivorous bat species (Cynopterus brachyotis (Müller, 1838); C. horsfieldii Gray, 1843; C. sphinx (Vahl, 1797), and Rousettus leschenaultii (Desmarest, 1820)) [63]. The nectar-specialist species have long muzzles and tongues characteristic of nectarivores [22], and forage almost exclusively on floral resources [11, 40, 62, 63]. In contrast, the primarily frugivorous species have powerful jaws and well-developed molars [21], and while they mainly forage on fruits, they have also been observed foraging at flowers [12, 40, 63].

We focused on five bat-pollinated plant taxa for this study: Durio zibethinus L., Musa acuminata Colla, Oroxylum indicum (L.) Benth. ex Kurz, Parkia speciosa Hassk., and Sonneratia L.f. species (Fig. 1). These species are some of the major food resources for nectar-feeding bats [11, 60, 62]. Durio zibethinus (Malvaceae, durian) is an economically-important fruit crop in the region that exhibits mass flowering, producing several thousand flowers in the span of about 10 days [13]. Flowers are hermaphroditic and, depending on the cultivar, can be either self-incompatible or self-compatible [13, 69]. Musa acuminata (Musaceae, banana) is a temporally dioecious, herbaceous plant species ubiquitous throughout southeast Asia [6, 29]. Each shoot produces a single inflorescence that displays 15–40 flowers per night for multiple weeks [29], and flowering individuals can be found year-round [24]. While cultivated bananas are parthenocarpic, wild plants require pollination to set fruit [5, 6]. Oroxylum indicum (Bignoniaceae, Indian trumpet flower) is a self-incompatible tree species found throughout much of Asia [54]. Flowers are hermaphroditic and only a few open per night, but flowering trees can be found year-round [55]. Parkia speciosa (Fabaceae, sator or petai) is a self-incompatible tree species that can have up to 70 capitula open per night [10]. Capitula contain 2,500–4,000 flowers, and inflorescences are either hermaphroditic or functionally staminate [10]. Sonneratia (Lythraceae, mangrove apple) is a paleotropical mangrove genus with hermaphroditic flowers and flowering tends to occur in flushes [57, 66]. Four species of Sonneratia are found in our study area (S. alba Sm., S. caseolaris (L.) Engl., S. griffithii Kurz, and S. ovata Backer, [60].

Fig. 1
figure 1

Plant study species with their main pollinators. A Durio zibethinus inflorescence with Eonycteris spelaea, (B) Sonneratia alba flower with Macroglossus minimus, (C) Musa acuminata inflorescence with Macroglossus sobrinus, (D) Oroxylum indicum inflorescence with Eonycteris spelaea, and (E) Parkia speciosa inflorescence with Eonycteris spelaea. White scale bars represent 3 cm. Photos A, D, and E were taken by Merlin Tuttle, photos B and C were taken by Alyssa Stewart

Data collection

In order to assess the frequency of each bat species at each of our plant study species, we used mist-nets (Avinet Research Supplies, Maine, USA) to catch foraging bats. We mist-netted at our plant study species for a total of 23 nights in 2011, 34 nights in 2013, 34 nights in 2014, 23 nights in 2019, 26 nights in 2020, and 20 nights in 2021 (4–10 nights per plant species per year; Supplementary Table 1). We changed mist-netting locations each night to minimize avoidance learning. Mist-netting sites differed across years but tended to be in the same general areas (e.g., netting at different houses or farms in the same village). For each plant species, we mist-netted when flowers were highly abundant (between March and May for D. zibethinus, between May and October for all other study species). For two plant species we were only able to collect data in four years of the study period (D. zibethinus: 2013, 2014, 2020, 2021; Sonneratia: 2013, 2014, 2019, 2020). Mist-nets were placed as close as possible to open flowers (from 18.30 – 24.00 h) and netting heights were similar across years (Supplementary Table 1). Nets were checked for bats every 15–30 minutes. Bat captures were used to determine the overall number of bats netted per hour (total number of bats netted divided by the total number of mist-net hours; net size: 6 x 2.6 m) for each bat species at each focal plant species. Netted bats were identified to species following Francis [21], held in breathable cloth bags to prevent repeat captures, provided with sugar water, and released after mist-nets were taken down.

Statistical analysis

All analyses were performed in R 4.2.2 [51]. To examine trends in bat visitation throughout our study period, we examined bat capture rates at each plant species across years using linear mixed modeling (LMM, function lmer, package “lme4”; [8]). Separate analyses were conducted for each focal plant species. We included capture rate (bats per hour) as the response variable; bat species, year, and their interaction as fixed factors; and site as a random factor. Factor significance was assessed using the joint_test function (package “emmeans”; [37]) and, when significant, factor levels were compared using Tukey’s post-hoc test (function emmeans, package “emmeans”; [37]) with a Holm-Bonferroni correction to control for multiple comparisons. We also compared bat capture rates across two time periods, pooling data collected in 2011–2014 and data collected in 2019–2021. The models were set up and analyzed in the same way as above, except that we used time period as a fixed factor instead of year. All graphs were created using the “ggplot2” package [71].


LMM results revealed that capture rates at flowers differed among bat species at all five plant study species, but overall capture rates at each plant species did not change across years (Table 1). However, there was a significant interaction between bat species and year for banana (M. acuminata), Indian trumpet flower (O. indicum), and mangrove apple (Sonneratia spp.) (Table 1). At durian (D. zibethinus) flowers, E. spelaea was the most frequent visitor followed by R. leschenaultii, and both were netted significantly more often than the remaining bat species (Fig. 2; Supplementary Figure 1). At sator (P. speciosa) flowers, E. spelaea was the only regular visitor and was netted significantly more often than the remaining bat species (Fig. 2). For the other three plant taxa, post-hoc results were more complicated, given the significant interaction between bat species and year. At banana flowers, multiple bat species were common visitors in 2011-2014, including its known pollinators E. spelaea and M. sobrinus (Supplementary Figure 2). However, in 2019–2021, only E. spelaea was a regular visitor while M. sobrinus visits were rare (Supplementary Figure 2). At Indian trumpet flowers, E. spelaea was the dominant visitor across all years, while C. horsfieldii was a relatively common visitor in years 2011–2014 but was rarely netted in 2019–2021 (Supplementary Figure 2). At mangrove apple flowers, E. spelaea and M. minimus were equally dominant visitors in 2013–2014, while only E. spelaea was regularly netted in 2019–2020 (Supplementary Figure 2).

Table 1 Linear mixed model results (F-ratio, degrees of freedom (df), and p-values (P)) showing the effect of two main factors (bat species and year) and their interaction on the number of bats netted per hour at the flowers of five bat-pollinated plant taxa. Significant predictors are highlighted in bold
Fig. 2
figure 2

Results of LMM showing the number of bats netted per hour for seven flower-visiting bat species at five bat-pollinated plant taxa between 2011-–2021. Points show actual data; lines and shaded areas show linear regression lines and 95% confidence intervals, respectively. Note: Only data for the known pollinators of each plant taxa are shown in color, all other bat species are shown in grey; the full color figure is shown in Supplementary Figure 1.

Comparing data pooled into two time periods (2011–2014 versus 2019–2021) via LMM revealed similar results: bat species was significantly different for all plant taxa, time period was not significant for any plant taxon, and the interaction between bat species and time period was significant for banana (M. acuminata), Indian trumpet flower (O. indicum), and mangrove apple (Sonneratia spp.) (Supplementary Table 2). For durian (D. zibethinus) and sator (P. speciosa) flowers, the number of bats netted for each bat species generally did not differ between the two periods (Fig. 3; Supplementary Figure 3). For banana flowers, the numbers of M. sobrinus and C. sphinx bats netted were significantly lower in 2019-2021 than in 2011-2014 (an 80.2% and a 73.8% decrease, respectively; Fig. 3; Supplementary Figure 3). For Indian trumpet flowers, the number of C. horsfieldii bats netted was significantly lower in 2019–2021 than in 2011–2014 (a 91.1% decrease; Fig. 3; Supplementary Figure 3). For mangrove apple flowers, the number of M. minimus bats netted was significantly lower in 2019–2021 than in 2011–2014 (an 81.4% decrease; Fig. 3; Supplementary Figure 3).

Fig. 3
figure 3

A comparison of the number of bats netted per hour (mean ± SE) for seven nectar-feeding bat species at five bat-pollinated plant taxa between 2011–2014 (teal) and 2019–2021 (orange). Significant differences between the two time periods are denoted with asterisks (one asterisk, P < 0.05; two asterisks, P < 0.01). Abbreviations: C. bra, Cynopterus brachyotis; C. hor, Cynopterus horsfieldii; C. sph, Cynopterus sphinx; E. spe, Eonycteris spelaea; M. min, Macroglossus minimus; M. sob, Macroglossus sobrinus; R. les, Rousettus leschenaultii


Between 2011 and 2021, we observed declines in the number of bats netted at floral resources for some bat species, with results varying by plant taxon. The strictly nectarivorous species, which are the main pollinators of chiropterophilous plants in southern Thailand [60], exhibit different patterns, with some species maintaining consistent visitation rates over the past decade and others exhibiting significant declines. The primarily frugivorous species had low visitation rates across all plant taxa and across all years, making it difficult to assess long-term patterns, and they contribute little towards the pollination of chiropterophilous plant species in southern Thailand [60]. Thus, we focus our discussion on the strictly nectarivorous species.

Eonycteris spelaea is an important pollinator of diverse plant species in southern Thailand [10, 11, 13, 54, 60], and the findings of this study demonstrate that the number of E. spelaea netted at five bat-pollinated plant taxa has remained consistent or even increased (though not significantly) over the past decade (Figs. 2, 3). These findings suggest that E. spelaea is relatively tolerant of the changes in land use that occurred in the study area (e.g., agricultural intensification and urbanization, [64]). Indeed, we commonly netted E. spelaea in banana and durian orchards, as well as at flowering plants next to houses and on university campuses. The ubiquity of E. spelaea across diverse anthropogenic habitats indicates that this species is relatively undisturbed by artificial lighting and human activity, which may be due to its relatively large size (45-75 g; [21], A. Stewart, pers. obs.) that potentially makes it less wary of predation than smaller bat species. Eonycteris spelaea can even persist in limestone caves in Kuala Lumpur, Malaysia, one of the largest cities in southeast Asia [38, 43]. Thus, this bat species may actually benefit from some land use changes, as many bat-pollinated plant species are intentionally cultivated by humans (e.g., durian and sator) and others thrive in the sunny, open habitats maintained by humans (e.g., Indian trumpet flower and wild banana).

In contrast, we observed significant declines for two other important bat pollinators, M. minimus and M. sobrinus (Figs. 2, 3). Previous work has shown that Macroglossus bats are the main pollinators of banana and mangrove apple flowers in southern Thailand [45, 60]. The findings of this study show that the number of M. sobrinus netted at banana flowers dropped 80% when comparing data from 2011–2014 and 2019–2021 (Fig. 3). Similarly, the number of M. minimus bats netted at mangrove apple flowers dropped 81% between 2011–2014 and 2019–2021 (Fig. 3). Several factors have likely contributed to these declines. We hypothesize that Macroglossus bats are more affected than E. spelaea is by ongoing habitat loss and degradation, since Macroglossus species roost in vegetation [57, 73] while E. spelaea roosts in caves [1]. Kingston [33] studied insectivorous bats in Malaysia and also reported cave-roosting species to be more resilient to forest loss and degradation than foliage-roosting species. Macroglossus minimus bats may be particularly affected by land conversion as they primarily roost in mangroves [57], and Thailand has already lost over half of its mangrove forest cover [9]. Moreover, Macroglossus bats are less than half the size of E. spelaea [21] and have shorter lifespans [7] and much smaller foraging ranges; average home range has been estimated to be 5.8 ha for M. minimus [73] and 518 ha for E. spelaea [2]. Since E. spelaea has a long life span and foraging range, it can presumably visit the same resource-rich sites for several years, while smaller bats with shorter life spans and foraging ranges may be more affected by habitat change and more likely to relocate. Winfree et al. [72] also found that dietary specialists, such as Macroglossus bats, are more sensitive to changes in land use than are dietary generalists, such as E. spelaea. Finally, Macroglossus bats appear to be less tolerant of human disturbance, which may make them less likely to roost in and forage at cultivated banana plants, and shrinking areas of natural habitat may contribute to the significant declines observed in this study.

Pollinator declines are troubling not only for the pollinator species themselves, but also for the plant species that depend on them for pollination. The observed declines in the number of Macroglossus bats caught at banana and mangrove apple flowers are likely to affect plant reproductive success given that the former are primarily pollinated by M. sobrinus and the latter by M. minimus [60]. While cultivated bananas are parthenocarpic, wild bananas require pollination to reproduce [5], and wild bananas can be an important source of genetic diversity, particularly given the susceptibility of many clonal banana cultivars to disease [16]. Reduced pollinator visitation to mangrove apple flowers is of even greater concern given that these ecologically important species depend on pollinators to reproduce, particularly for the critically endangered S. griffithii [45] and the near threatened S. ovata [44]. Thus, the observed reduction in pollinator visitation, combined with intensive mangrove deforestation and other land conversion in southern Thailand [64], is likely to have substantial effects on the reproductive success of these plant species and further research is necessary to monitor changes in wild banana and mangrove apple reproduction.

It is important to note that the observed declines in the number of bats netted at floral resources does not necessarily indicate declines in population size. One possible alternative explanation is that differences in flowering intensity across years may be responsible for the observed declines. We think this explanation is unlikely given that the two plant species where declines were observed (banana and mangrove apple) exhibit steady-state flowering throughout all or most of the year, and flowering intensity appeared similar across study years (A. Stewart, pers. obs.); however, it is possible that other changes in food resources (e.g., nectar volume or concentration) are influencing bat foraging. Another potential explanation could be that foliage-roosting bats such as M. minimus and M. sobrinus are moving deeper into forests, farther away from human activity, and thus were netted less often at the human-cultivated plants (e.g., durian and sator) and sun-loving species (e.g., Indian trumpet flower and wild banana) that were the focus of this study. This possibility could also explain the significant declines in C. sphinx netted at banana flowers and C. horsfieldii netted at Indian trumpet flowers (Fig. 3), given that Cynopterus bats also roost in foliage [14]. However, contrary to this hypothesis, a recent study in Indonesia found that M. minimus bats were twice as abundant in plantations than in forests because of the relative abundance of banana plants [70], and Cynopterus bats are generally reported to be tolerant of human disturbance [14, 15, 39]. This explanation is still troubling given current deforestation rates in Thailand [17, 64], even in national parks and other protected areas [18], which means that even natural refuges are shrinking. While current IUCN Red List reports state that Eonycteris, Macroglossus, and Cynopterus bats are of Least Concern, the findings of this research indicate that population studies of nectarivorous bats in southeast Asia are urgently needed for updated species conservation assessments.

Availability of data and materials

The data used in this study are openly available in Mendeley Data at (


  1. Acharya PR, Racey PA, McNeil D, Sotthibandhu S, Bumrungsri S. Timing of cave emergence and return in the dawn bat (Eonycteris spelaea, Chiroptera: Pteropodidae) in southern Thailand. Mammal Study. 2015;40(1):47–52.

    Article  Google Scholar 

  2. Acharya PR, Racey PA, Sotthibandhu S, Bumrungsri S. Home-range and foraging areas of the dawn bat Eonycteris spelaea in agricultural areas of Thailand. Acta Chiropterologica. 2015;17(2):307–19.

    Article  Google Scholar 

  3. Acharya PR, Racey PA, Sotthibandhu S, Bumrungsri S. Feeding behaviour of the dawn bat (Eonycteris spelaea) promotes cross pollination of economically important plants in Southeast Asia. J Pollinat Ecol. 2015;15(7):44–50.

    Article  Google Scholar 

  4. Aizen MA, Feinsinger P. Bees not to be? Responses of insect pollinator faunas and flower pollination to habitat fragmentation. In: Bradshaw G, Marquet P, editors. How Landscapes Change. Berlin: Springer; 2003. p. 111–29.

    Chapter  Google Scholar 

  5. Amah D, Turner DW, Gibbs DJ, Waniale A, Gram G, Swennen R. Overcoming the fertility crisis in bananas (Musa spp.). In: Kema GHJ, Drenth A, editors. Achieving Sustainable Cultivation of Bananas. Cambridge: Burleigh Dodds Science Publishing Limited; 2021. p. 257–306.

  6. Andersson L. Musaceae. In: Kubitzki K, editor. Flower Plants - Monocotyledons. Springer Berlin Heidelberg; 1998. p. 296–301.

  7. Austad S, Fischer K. Mammalian aging, metabolism, and ecology: evidence from the bats and marsupials. J Gerontol. 1991;46(2):B47-53.

    Article  CAS  PubMed  Google Scholar 

  8. Bates D, Maechler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67(1):1–48.

    Article  Google Scholar 

  9. Bukoski JJ, Dronova I, Potts MD. Net loss statistics underestimate carbon emissions from mangrove land use and land cover change. Ecography. 2022;4:e05982.

    Article  ADS  Google Scholar 

  10. Bumrungsri S, Harbit A, Benzie C, Carmouche K, Sridith K, Racey P. The pollination ecology of two species of Parkia (Mimosaceae) in southern Thailand. J Trop Ecol. 2008;24(5):467–75.

    Article  Google Scholar 

  11. Bumrungsri S, Lang D, Harrower C, Sripaoraya E, Kitpipit K, Racey PA. The dawn bat, Eonycteris spelaea Dobson (Chiroptera: Pteropodidae) feeds mainly on pollen of economically important food plants in Thailand. Acta Chiropterologica. 2013;15(1):95–104.

    Article  Google Scholar 

  12. Bumrungsri S, Leelapaibul W, Racey PA. Resource partitioning in sympatric Cynopterus bats in lowland tropical rain forest Thailand. Biotropica. 2007;39(2):241–8.

    Article  Google Scholar 

  13. Bumrungsri S, Sripaoraya E, Chongsiri T, Sridith K, Racey PA. The pollination ecology of durian (Durio zibethinus, Bombacaceae) in southern Thailand. J Trop Ecol. 2009;25(1):85–92.

    Article  Google Scholar 

  14. Campbell P, Reid NM, Zubaid A, Adnan AM, Kunz TH. Comparative roosting ecology of Cynopterus (Chiroptera: Pteropodidae) fruit bats in peninsular Malaysia. Biotropica. 2006;38(6):725–34.

    Article  Google Scholar 

  15. Chan AAQ, Aziz SA, Clare EL, Coleman JL. Diet, ecological role and potential ecosystem services of the fruit bat, Cynopterus brachyotis, in a tropical city. Urban Ecosyst. 2021;24(2):251–63.

    Article  Google Scholar 

  16. Dita M, Barquero M, Heck D, Mizubuti ESG, Staver CP. Fusarium wilt of banana: Current knowledge on epidemiology and research needs toward sustainable disease management. Front Plant Sci. 2018;9:1468.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Estoque RC, Ooba M, Avitabile V, Hijioka Y, DasGupta R, Togawa T, et al. The future of Southeast Asia’s forests. Nat Commun. 2019;10(1):1829.

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  18. Ferraro PJ, Hanauer MM, Miteva DA, Canavire-Bacarreza GJ, Pattanayak SK, Sims KRE. More strictly protected areas are not necessarily more protective: evidence from Bolivia, Costa Rica, Indonesia, and Thailand. Environ Res Lett. 2013;8(2):025011.

    Article  ADS  Google Scholar 

  19. Fleming TH, Geiselman C, Kress WJ. The evolution of bat pollination: a phylogenetic perspective. Ann Bot. 2009;104(6):1017–43.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Forrest JRK. Insect pollinators and climate change. In: Johnson S, Jones H, editors. Global Climate Change and Terrestrial Invertebrates. Chichester: John Wiley & Sons, Ltd.; 2017. p. 71–91.

    Google Scholar 

  21. Francis CM. A field guide to the mammals of Thailand and Southeast Asia. London: New Holland Publishers Ltd; 2008. p. 392.

    Google Scholar 

  22. Freeman PW. Nectarivorous feeding mechanisms in bats. Biol J Linn Soc. 1995;56(3):439–63.

    Article  Google Scholar 

  23. Frick WF, Kingston T, Flanders J. A review of the major threats and challenges to global bat conservation. Ann NY Acad Sci. 2020;1469:5–25.

    Article  ADS  PubMed  Google Scholar 

  24. Gould E. Foraging behavior of Malaysian nectar-feeding bats. Biotropica. 1978;10(3):184–93.

    Article  Google Scholar 

  25. Griffiths SR, Lumsden LF, Bender R, Irvine R, Godinho LN, Visintin C, et al. Long-term monitoring suggests bat boxes may alter local bat community structure. Aust Mammal. 2018;41(2):273–8.

    Article  Google Scholar 

  26. Hadley AS, Betts MG. The effects of landscape fragmentation on pollination dynamics: Absence of evidence not evidence of absence. Biol Rev. 2012;87(3):526–44.

    Article  PubMed  Google Scholar 

  27. Hughes AC, Satasook C, Bates PJJ, Bumrungsri S, Jones G. The projected effects of climatic and vegetation changes on the distribution and diversity of Southeast Asian bats. Glob Chang Biol. 2012;18(6):1854–65.

    Article  ADS  Google Scholar 

  28. Ingersoll TE, Sewall BJ, Amelon SK. Improved analysis of long-term monitoring data demonstrates marked regional declines of bat populations in the eastern United States. PLoS One. 2013;8(6):e65907.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  29. Itino T, Kato M, Hotta M. Pollination ecology of the two wild bananas, Musa acuminata subsp. halabanensis and M. salaccensis: chiropterophily and ornithophily. Biotropica. 1991;23(2):151–8.

    Article  Google Scholar 

  30. IUCN. The IUCN Red List of Threatened Species. 2022. Available from:

  31. Jung K, Threlfall CG. Urbanisation and its effects on bats—A global meta-analysis. In: Voigt C, Kingston T, editors. Bats in the Anthropocene: Conservation of Bats in a Changing World. New York: Springer Nature; 2016. p. 13–33.

    Chapter  Google Scholar 

  32. Kerth G. Long-term field studies in bat research: importance for basic and applied research questions in animal behavior. Behav Ecol Sociobiol. 2022;76(6):75.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Kingston T. Response of bat diversity to forest disturbance in Southeast Asia: Insights from long-term research in Malaysia. In: Adams R, Pedersen S, editors. Bat Evolution, Ecology, and Conservation. New York: Springer Science+Business Media; 2013. p. 169–85.

    Chapter  Google Scholar 

  34. Kingston T. Research priorities for bat conservation in Southeast Asia: a consensus approach. Biodivers Conserv. 2008;19(2):471–84.

    Article  Google Scholar 

  35. Kunz TH, Braun de Torrez E, Bauer D, Lobova T, Fleming TH. Ecosystem services provided by bats. Ann N Y Acad Sci. 2011;1223(1):1–38.

  36. Lane D, Kingston T, Lee B. Dramatic decline in bat species richness in Singapore, with implications for Southeast Asia. Biol Conserv. 2006;131(4):584–93.

    Article  Google Scholar 

  37. Lenth R. emmeans: estimated marginal means, aka least-squares means. 2022. Available from:

  38. Lim VC, Clare EL, Littlefair JE, Ramli R, Bhassu S, Wilson JJ. Impact of urbanisation and agriculture on the diet of fruit bats. Urban Ecosyst. 2018;21(1):61–70.

    Article  Google Scholar 

  39. Lim VC, Ramli R, Bhassu S, Wilson JJ. Pollination implications of the diverse diet of tropical nectar-feeding bats roosting in an urban cave. PeerJ. 2018;2018(3):e4572.

    Article  Google Scholar 

  40. Marshall AG. Old World phytophagous bats (Megachiroptera) and their food plants: a survey. Zool J Linn Soc. 1985;83(4):351–69.

    Article  Google Scholar 

  41. Meyer CFJ, Struebig MJ, Willig MR. Responses of tropical bats to habitat fragmentation, logging, and deforestation. In: Voigt C, Kingston T, editors. Bats in the Anthropocene: Conservation of Bats in a Changing World. New York: Springer Nature; 2016. p. 63–103.

    Chapter  Google Scholar 

  42. Millard J, Outhwaite CL, Kinnersley R, Freeman R, Gregory RD, Adedoja O, et al. Global effects of land-use intensity on local pollinator biodiversity. Nat Commun. 2021;12(1):2902.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  43. Nordin J, Chew TH, Lim LS, Shamsir MS. Temporal changes of bat diversity in the urban habitat island of Batu Caves, Malaysia. IOP Conference Series. 2021;736(1):012051.

    Google Scholar 

  44. Nuevo Diego CE, Stewart AB, Bumrungsri S. Pollinators increase reproductive success of a self-compatible mangrove, Sonneratia ovata, in southern Thailand. Trop Nat Hist. 2019;19(2):88–102.

    Google Scholar 

  45. Nuevo Diego CE, Stewart AB, Bumrungsri S. Pollinators necessary for the reproductive success of critically endangered mangrove Sonneratia griffithii. Aquat Bot. 2021;169:103340.

    Article  Google Scholar 

  46. Pereira MJR, Fonseca C, Aguiar LMS. Loss of multiple dimensions of bat diversity under land-use intensification in the Brazilian cerrado. Hystrix. 2018;29(1):25.

    Google Scholar 

  47. Pettit JL, O’Keefe JM. Impacts of white-nose syndrome observed during long-term monitoring of a midwestern bat community. J Fish Wildl Manag. 2017;8(1):69–78.

    Article  Google Scholar 

  48. Racey PA. Bat conservation: Past, present and future. In: Bat Evolution, Ecology, and Conservation. 2013. 517–32.

  49. Rafferty NE. Effects of global change on insect pollinators: multiple drivers lead to novel communities. Curr Opin Insect Sci. 2017;23:22–7.

    Article  PubMed  Google Scholar 

  50. Ratto F, Simmons BI, Spake R, Zamora-Gutierrez V, MacDonald MA, Merriman JC, et al. Global importance of vertebrate pollinators for plant reproductive success: a meta-analysis. Front Ecol Environ. 2018;16(2):82–90.

    Article  Google Scholar 

  51. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2022. Available from:

  52. Regan EC, Santini L, Ingwall-King L, Hoffmann M, Rondinini C, Symes A, et al. Global trends in the status of bird and mammal pollinators. Conserv Lett. 2015;8(6):397–403.

    Article  Google Scholar 

  53. Silva VHD, Gomes IN, Cardoso JCF, Bosenbecker C, Silva JLS, Cruz-Neto O, et al. Diverse urban pollinators and where to find them. Biol Conserv. 2023;281:110036.

    Article  Google Scholar 

  54. Srithongchuay T, Bumrungsri S, Sripao-raya E. The pollination ecology of the late-successional tree, Oroxylum indicum (Bignoniaceae) in Thailand. J Trop Ecol. 2008;24(5):477–84.

    Article  Google Scholar 

  55. Sritongchuay T, Bumrungsri S, Meesawat U, Mazer SJ. Stigma closure and re-opening in Oroxylum indicum (Bignoniaceae): causes and consequences. Am J Bot. 2010;97(1):136–43.

    Article  PubMed  Google Scholar 

  56. Sritongchuay T, Hughes AC, Bumrungsri S. The role of bats in pollination networks is influenced by landscape structure. Glob Ecol Conserv. 2019;20:e00702.

    Google Scholar 

  57. Start AN, Marshall AG. Nectarivorous bats as pollinators of trees in West Malaysia. In: Burley J, Styles B, editors. Tropical trees: variation, breeding, and conservation. London: Academic Press; 1976. p. 141–50.

    Google Scholar 

  58. Steffen W, Crutzen PJ, McNeill JR. The anthropocene: Are humans now overwhelming the great forces of nature? Ambio. 2007;36(8):614–21.

    Article  ADS  CAS  PubMed  Google Scholar 

  59. Stewart AB, Diller C, Dudash MR, Fenster CB. Pollination-precision hypothesis: support from native honey bees and nectar bats. New Phytol. 2022;235(4):1629–40.

    Article  CAS  PubMed  Google Scholar 

  60. Stewart AB, Dudash MR. Flower-visiting bat species contribute unequally toward agricultural pollination ecosystem services in southern Thailand. Biotropica. 2017;49(2):239–48.

    Article  Google Scholar 

  61. Stewart AB, Dudash MR. Field evidence of strong differential pollen placement by Old World bat-pollinated plants. Ann Bot. 2017;119(1):73–9.

    Article  PubMed  Google Scholar 

  62. Stewart AB, Dudash MR. Foraging strategies of generalist and specialist Old World nectar bats in response to temporally variable floral resources. Biotropica. 2018;50(1):98–105.

    Article  Google Scholar 

  63. Stewart AB, Makowsky R, Dudash MR. Differences in foraging times between two feeding guilds within Old World fruit bats (Pteropodidae) in southern Thailand. J Trop Ecol. 2014;30(3):249–57.

    Article  Google Scholar 

  64. Tantipisanuh N, Gale GA. Identification of areas highly vulnerable to land conversion: a case study from southern Thailand. Environ Manage. 2022;69(2):323–32.

    Article  PubMed  Google Scholar 

  65. Toffoli R, Calvini M. Long term trends of hibernating bats in North-Western Italy. Biologia. 2021;76(2):633–43.

    Article  Google Scholar 

  66. Tomlinson PB. Sonneratiaceae. In: Tomlinson PB, editor. The Botany of Mangroves. Cambridge: Cambridge University Press; 1994. p. 367–74.

    Google Scholar 

  67. Tripp EA, Manos PS. Is floral specialization an evolutionary dead-end? Pollination system transitions in Ruellia (Acanthaceae). Evolution. 2008;62(7):1712–37.

    Article  PubMed  Google Scholar 

  68. Wayo K, Leonhardt SD, Sritongchuay T, Bumrungsri S. Homing ability in a tropical Asian stingless bee is influenced by interaction between release distances and urbanisation. Ecol Entomol. 2022;47(4):536–43.

    Article  Google Scholar 

  69. Wayo K, Phankaew C, Stewart AB, Bumrungsri S. Bees are supplementary pollinators of self-compatible chiropterophilous durian. J Trop Ecol. 2018;34(1):41–52.

    Article  Google Scholar 

  70. Wibowo A, Basukriadi A, Nurdin E, Benhard G. Ecology and microhabitat model of long-tongued fruit bat Macroglossus minimus (Chiroptera: Pteropididae) in karst ecosystem of Klapanunggal, Bogor, West Java Indonesia. Int J Trop Drylands. 2022;6(1):11–5.

    Article  Google Scholar 

  71. Wickham H. ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag; 2016.

    Book  Google Scholar 

  72. Winfree R, Bartomeus I, Cariveau DP. Native pollinators in anthropogenic habitats. Annu Rev Ecol Evol Syst. 2011;42:1–22.

    Article  Google Scholar 

  73. Winkelmann JR, Bonaccorso FJ, Goedeke EE, Ballock LJ. Home range and territoriality in the least blossom bat, Macroglossus minimus Papua New Guinea. J Mammal. 2003;84(2):561–70.

    Article  Google Scholar 

  74. Winkler K, Fuchs R, Rounsevell M, Herold M. Global land use changes are four times greater than previously estimated. Nat Commun. 2021;12(1):2501.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  75. Zamora-Gutierrez V, Rivera-Villanueva AN, Martínez Balvanera S, Castro-Castro A, Aguirre-Gutiérrez J. Vulnerability of bat–plant pollination interactions due to environmental change. Glob Chang Biol. 2021;27(14):3367–82.

    Article  CAS  PubMed  Google Scholar 

Download references


We are very grateful to Piyaporn Suksai, Yingnapa Jesamor, Darunee Kaewngam, Pongsin Inpaen, Nittaya Ruadreo, Venus Saksongmuang, Sittiwa Srilopan, and Yanisa Olaranont for all of their help with fieldwork. We also thank two anonymous reviewers for their constructive comments and suggestions.


Open access funding provided by Mahidol University Research during 2011-2014 was supported by a National Science Foundation Graduate Research Fellowship awarded to ABS. Research during 2019-2021 (Grant No. RGNS63-176 awarded to ABS) was supported by the Office of the Permanent Secretary, Ministry of Higher Education, Science, Research and Innovation (OPS MHESI); Thailand Science Research and Innovation (TSRI); and the Faculty of Science, Mahidol University.

Author information

Authors and Affiliations



ABS, MRD, and SB conceived the ideas and designed the methodology; ABS, SS, KW, and PH collected the data; ABS analyzed the data and wrote the first draft of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Corresponding author

Correspondence to Alyssa B. Stewart.

Ethics declarations

Ethics approval and consent to participate

All work was conducted with permission from Thailand’s Department of National Parks, the National Research Council of Thailand, the Institutional Animal Care and Use Committee at the University of Maryland (protocols 615373 and 318146), and the Institutional Animal Care and Use Committee at the Faculty of Science, Mahidol University (protocol MUSC62-019-483).

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit The Creative Commons Public Domain Dedication waiver ( applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stewart, A.B., Srilopan, S., Wayo, K. et al. Bat pollinators: a decade of monitoring reveals declining visitation rates for some species in Thailand. Zoological Lett 10, 5 (2024).

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: