Coexistence of Rhinolophus affinis and Rhinolophus pearsoni revisited
Tinglei Jiang, Guanjun Lu, Keping Sun, Jinhong Luo & Jiang Feng
Acta Theriologica ISSN 0001-7051 Volume 58 Number 1 Acta Theriol (2013) 58:47-53 DOI 10.1007/s13364-012-0093-x
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Author's personal copy Acta Theriol (2013) 58:47–53 DOI 10.1007/s13364-012-0093-x
ORIGINAL PAPER
Coexistence of Rhinolophus affinis and Rhinolophus pearsoni revisited Tinglei Jiang & Guanjun Lu & Keping Sun & Jinhong Luo & Jiang Feng
Received: 4 June 2012 / Accepted: 10 August 2012 / Published online: 26 August 2012 # Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2012
Abstracts The investigation of mechanism of species coexistence promotes understanding of the mechanistic processes behind community ecology and ecosystem functions. Niche theory declares that species coexistence within a community must partition the resources of their environment. Two sympatric and morphologically similar bat species, Rhinolophus affinis and Rhinolophus pearsoni, provided a unique opportunity to test the causal mechanism of coexistence. Previous study showed that their coexistence was promoted not by the trophic and spatial niche differentiation but the relatively high abundance of prey resources, which was not in accord with the prediction of niche theory. Here, therefore, we reanalyzed the dietary composition by fecal analysis and surveyed the feeding time of both species. Our results showed that R. affinis and R. pearsoni hunt mainly mostly on Coleoptera and Lepidoptera, and there was a very high overlap (0.84) of trophic niche between the two species. However, significant difference in the duration of the activity period between both species was detected, which illustrated that temporal partitioning of prey resource use facilitated their coexistence. Additionally, our work highlighted the importance of integration of the traditional methods and next-generation sequencing methods for identifying dietary composition of carnivores, and suggested that ongoing studies of species coexistence must consider simultaneously multiple niche axes. Communicated by: Karol Zub T. Jiang : J. Feng Jilin Key Laboratory of Animal Resource Conservation and Utilization, Northeast Normal University, 5268 Renmin St., Changchun 130024, China T. Jiang : G. Lu : K. Sun : J. Luo : J. Feng (*) Key Laboratory for Wetland Ecology and Vegetation Restoration of National Environmental Protection, Northeast Normal University, 5268 Renmin St., Changchun 130024, China e-mail:
[email protected]
Keywords Bats . Niche . Coexistence . Dietary composition . Next generation sequencing
Introduction Niche theory states that species coexistence within a community must partition the resources of their environment (Leibold and McPeek 2006). In mammals, species coexistence facilitated by niche differentiation have been most intensely studied for sympatric carnivore species, and many of these investigations have illustrated niche differentiation involves prey preferences (Carbone and Gittleman 2002; Lanszki and Heltai 2010; Silva-Pereira et al. 2011), habitat partitioning (Chamberlain and Leopold 2005; Pereira et al. 2012), microhabitat differences (Johnson and Franklin 1994; Kruuk et al. 1994; Pereira et al. 2012), and temporal partitioning (De Almeida Jácomo et al. 2004). Similarly, bat assemblages usually consist of a majority of morphologically very similar species coexisting (Kunz and Fenton 2003), and mounting evidence showed that their coexistence was promoted by niche differentiation in food resources and habitat use (Aguiar and Antonini 2008; Aguirre et al. 2002; Arlettaz et al. 1997, 2000; Ashrafi et al. 2011; Bumrungsri et al. 2007; Fukui et al. 2009; Hickey et al. 1996; Jiang et al. 2008; Razgour et al. 2011; Reside and Lumsden 2011; Siemers and Swift 2006; Siemers et al. 2011; Ye et al. 2009). However, relatively few studies focused on the effect of temporal niche partitioning on bat species coexistence. Only two studies showed that coexisting bat species partitioned temporal niche in using water resources in waterlimited environments (Adams and Thibault 2006; O' Farrell and Bradley 1970). Therefore, investigations of temporal partitioning of resource use in bats can add significantly to our understanding of mechanisms of species coexistence. The situation of two sympatric and morphologically similar bat species Rhinolophus affinis and Rhinolophus
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pearsoni provided a unique opportunity to examine how temporal partitioning of resource use promote species coexistence. A previous study showed that the diets of R. affinis and R. pearsoni consisted mainly of Lepidoptera and Coleoptera, and pairwise comparisons indicated that there were no significant differences in dietary composition and prey size between both species based upon analysis of culled parts (Jiang et al. 2008). Additionally, similarity in wing shapes (relatively low wing loads, aspect ratio, and a relative high tip shape ratio) of the two bat species may imply that they cannot segregate foraging microhabitats to an extent which prevents entirely competitive interfere, which may lead to strong interspecific competition between R. affinis and R. pearsoni despite that prey resources is very abundant (Jiang et al. 2008). In this study, therefore, we reanalyzed the dietary composition by fecal analysis and monitored the emergence and return time of both species, and try to test for the existence of (1) a broad overlap in the trophic niche between R. affinis and R. pearsoni, and (2) a distinct temporal partitioning of prey resource use in the two bat species.
Materials and methods Study area and species
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least five droppings about 90 min after a meal. Collected pellets were air-dried for storage in paper envelopes. Subsequently we released the bats into the roost. In the laboratory, where possible, we randomly selected five pellets from each bat for the analysis. The fecal pellets were soaked in 95 % ethanol for at least 2 h and teased apart with dissecting needles on a Petri dish under a binocular microscope (XTS-30, Zoom stereo microscope; Beijing Tech Instrument Co., Ltd.; 10–90× magnification). Identification of invertebrate remains to order was conducted using several identification keys (Shiel et al. 1997; Whitaker 1988) and by comparison to a reference collection gathered in the foraging area of the bats. The proportion (percent volume) of each prey category (mainly insect orders) was estimated for the whole individual samples. We investigated the abundance and the diversity of insect species using incandescent security lights in different sites of the foraging area, which were kept from dust to dawn at those nights observing emergence and return time of bats. At every insect sampling site, automated bat detectors (UltraSoundGate 116; Avisoft Bioacoustics, Berlin, Germany) were used to confirm that bats foraged in these areas. We calculated the food–niche breadth (FNB) (Hickey et al. 1996) for the two horseshoe bats by , n X FNB ¼ 1 Pi j2 ð1Þ i¼1
Our study focused on the nursery colony of R. affinis and R. pearsoni located at Shiyan cave (114°12′E, 26°36′N) in Liping village of Jinggangshan Natural Reserve, Jiangxi Province, China, from June to August in 2009. The characteristics of weather and vegetation in this area were described in detail by Jiang et al. (2008). The Shiyan cave consists of a main cave and a side branch of only 20 m long. R. pearsoni and R. affinis roosted in the main cave and in the side branch, respectively, with the number of individuals for R. affinis and R. pearsoni of about 1,500 and 800. Therefore, we can easily observe emergence and return time of the two bat species under such conditions because the main cave and the side branch have a respective entrance. Data collection and diet analysis
where Pi is the proportion of the ith prey category of species j. The trophic niche overlap between R. affinis and R. pearsoni was calculated using Schoener’s niche overlap index (Schoener 1970): ! n X NOI ¼ 1 ð1=2Þ ð2Þ jPi j Pi k j i¼1
where Pi is the proportion of the ith prey category of species j and k. Prey resource diversity index in the environment was calculated using the Simpson index (D) (Sun 2001): D¼1
n X
ðPi Þ2
ð3Þ
i¼1
We captured bats by setting mist nets at the entrance of the main cave and the side branch once a week from June to August in 2009 as bats entered the roost after foraging. R. affinis and R. pearsoni have distinctively different noseleaves, so species identification was relatively easy based upon Csorba et al. (2003). Here, adult bats were kept individually in cloth bags until they defecated. We identified the bats as adult by inspecting epiphyseal fusions of the bats’ forearms (Racey 1974). Five pellets were considered as the minimal number of pellets. Normally, bats can excrete at
where Pi is the proportion of the ith prey category in the environment. Richness index of available insects in the environment was calculated using the Margalef richness index (d) (Margalef 1958): d ¼ ðS 1Þ=ln N
ð4Þ
where S is the number of insect categories and N is the total number of individual of all insect categories.
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Observation of emergence and return time of bats In summer, the standard sunset time of study area was about 19:20; thus, emergence and return time of bats were observed about once a week from 18:00 to dawn the next day by Guanjun Lu and Tinglei Jiang from early June to the end of August in 2009. The former watched the activities of R. affinis; the latter looked at that of R. pearsoni. Sunrise and sunset time was recorded using GPS (eTrex Vista) before observation. Both observers always corrected the time of their watches to avoid error. Bats emergence time was determined by surveyors’ eyes because we can rely on the faint light at dusk when bats fly away from their roost. Several individuals of both species of bats may exit and reenter the roost several times before departing for foraging grounds, which is called “light sampling” behavior (Mitchell-Jones and McLeish 2004). We defined and recorded the emergence time after sunset when one or several individuals participating in the “light sampling” behavior flew away from their roost. Before sunrise, both species of bats swarmed at the roost entrance 10 and 30 min before entering. Since R. pearsoni flew towards its roost about 2 h before sunrise after foraging, we monitored the activities of R. pearsoni using a nightscope (Zenit NVPIEZO) at the entrance of the main cave when R. pearsoni started swarming. We recorded the return time of R. pearsoni before sunrise when one or several individuals entered the cave. Normally, R. affinis returned to its roost about 30 min before sunrise, so we can rely on the faint light at dawn to determine the time of return of this species. Statistical analysis We conducted a chi-square test to test the differences in the dietary composition between R. affinis and R. pearsoni. Additionally, t tests was used to evaluate differences between the two bat species in emergence, return time, and the duration of the activity period of them in SPSS 16.0.
Results In this study, we analyzed 890 and 1,995 fecal pellets collected from 178 and 399 individuals of R. affinis and R. pearsoni, respectively. Overall, 10 prey categories were determined from fecal samples, 10 categories in the diet of R. affinis and seven in the diet of R. pearsoni. Six of ten categories were found in the diet of both species (Table 1). The diet of R. affinis consisted mainly of Coleoptera and Lepidoptera, which represented 61.38 % and 28.90 % of the average volume, respectively. R. pearsoni foraged on seven prey categories, with Coleoptera (57.74 %), Lepidoptera (24.75 %), Hemiptera (15.88 %), Hymenoptera (0.35 %),
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Orthoptera (0.39 %), Homoptera (0.42 %), and unknown (0.46 %). Interestingly, the diet of R. affinis contained Megaloptera (0.95 %), Diptera (0.36 %), Neuroptera (0.53 %), and Trichoptera (0.28 %), insects that were not found in the diet of R. pearsoni. Additionally, the average percentage of Hemiptera in the diet of R. pearsoni was found to be considerably higher to that of R. affinis (15.88 % vs. 0.36 %). The food–niche breadth of R. affinis was found to be considerably similar to that of R. pearsoni (2.16 vs. 2.38; Table 1). The trophic niche overlap index between R. affinis and R. pearsoni was 0.84 despite the chi-square test showing that dietary composition between R. affinis and R. pearsoni was significantly different (χ2 04853.22, df010, P0 0.000). A total of nine insect order and 4,123 individuals were trapped in the area. The dominant categories were Lepidoptera (41.87 %), Orthoptera (32.17 %), and Coleoptera (9.32 %). The Simpson diversity index and the Margalef richness index for all insects in the area were 0.71 and 0.96, respectively (Table 1). Overall, 14 days of the emergence and return time of R. affinis and R. pearsoni were observed except when there were heavy rains in the area. R. affinis flew away from its roost significantly earlier than R. pearsoni (11.21±2.64 min vs. 15.21±2.15 min, t04.4, df026, P00.000). However, times of return before sunrise in R. affinis was significantly later than that in R. pearsoni (32.42±8.45 min vs. 132.36± 5.54 min, t034.15, df021, P00.000). Therefore, the duration of the activity period of R. affinis was significantly longer than that of R. pearsoni (578.67± 10.36 min vs. 422.73±7.32 min, t0−48.95, df021, P00.000).
Discussion As predicted by the ecomorphological paradigm, morphological similarities between R. affinis and R. pearsoni were matched by similarities in their diets. Since R. affinis and R. pearsoni fed mainly on Coleoptera and Lepidoptera, the very high overlap (0.84) of trophic niche between the two species was detected (Table 1), suggesting that there was no significant differentiation in the trophic niche. The result was consistent with the data based upon analysis of culled parts from previous study by Jiang et al. (2008), which also confirmed our first hypothesis. Therefore, our results, with the data derived from Findley and Black (1983), suggested that morphology of the insectivorous bats was strongly predictive of their diets. Interestingly, we found that R. pearsoni ate more Hemiptera than R. affinis (15.88 % vs. 0.36 %), which may be used to explain that the chi-square test detected significant differences in dietary composition between R. affinis and R.
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Table 1 Dietary composition of Rhinolophus affinis and Rhinolophus pearsoni and the insects trapped in the environment
Rhinolophus affinis (%)
Coleoptera
The chi-square test was performed to test the difference of dietary composition between the two bat species based upon the program set by McDonald (2009)
Lepidoptera Hemiptera Hymenoptera Orthoptera Homoptera Megaloptera Diptera Neuroptera Trichoptera Unknown Chi-square test Trophic niche breadth Trophic niche overlap Simpson diversity index Richness index
61.38 28.90 0.36 3.03 1.37 1.01 0.95 0.36 0.53 0.28 1.79 χ2 04853.22, df010, P00.000 2.16
Rhinolophus pearsoni (%)
Light-trap samples in the environment N (%)
57.74
397 (9.32)
24.75 15.88 0.35 0.39 0.42 – – – – 0.46
1783 (41.87) 119 (2.79) 98 (2.3) 1370 (32.17) 133 (3.12)
2.38
78( 1.83) 119 (2.79) 96 (1.78) – – –
0.84 –
–
0.71
–
–
0.96
pearsoni (Table 1). Similarly, two studies also showed that Homoptera (>10 % volume) was the secondary important food items in the dietary composition of Rhinolophus mehelyi (Sharifi and Hemmati 2004) and Rhinolophus megaphyllus (Pavey and Burwell 1998). So, we suspected that these rhinolophid bats may prefer homopteran insects. However, obviously only further experimental investigation will help in clarifying the reasons of the preference. The presence of superabundant prey resources may allow species to coexist by dampening the interspecific competition (Christopher and Barrett 2006; González-Solís et al. 1997; Reside and Lumsden 2011). As in the previous study by Jiang et al. (2008), our results also indicated that there were high prey diversity and availability in the study area in summer (Table 1), which may promote coexistence of R. affinis and R. pearsoni as a candidate factor. In the environment, Lepidoptera (41.87 %), Orthoptera (32.17 %), and Coleoptera (9.32 %) were the frequent prey categories captured in the light traps (Table 1), which was not completely consistent with the major component of dietary compositions of R. affinis and R. pearsoni because Coleoptera was the most important prey of both species. This result illustrated that the two species may forage selectively prey. However, this may also be because that Lepidoptera is more sensitive to incandescent security lights than Coleoptera. A large number of published data on prey hunt by insectivorous bats are from stomach content, culled parts, and fecal analysis (Whitaker 1988). If bats are already dead, stomach content should be examined. Culled parts can be extremely useful in analysis of diets because it can give
accurate results. Fecal analysis can reflect basically the actual diet that bats eat every night in their normal habitats. In the previous study, Jiang et al. (2008) showed that Lepidoptera were the most frequent prey in R. affinis (70.57 %) and R. pearsoni (82.81 %) by analyzing culled parts in the flight tent. However, in this study, both species ate mainly on Coleoptera (61.38 % vs. 57.74 %). The two methods got different results, which may be because that the spectral range of incandescent security lights preferred Lepidopteran insects in the previous study. Therefore, in order to understand completely the dietary composition of insectivorous bats, a combination of these methods will be necessary. However, these traditional methods are limiting because that they may give imprecise and biased results (Pickett et al. 2012). With the development of molecular techniques, therefore, more and more studies have employed nextgeneration sequencing techniques to identify insect prey from feces of carnivores (Jarman et al. 2004; Pickett et al. 2012; Pompanon et al. 2012; Shehzad et al. 2012). The method potentially provides more accurate results for dietary studies, and thus can help researchers to fully understand the biology of a species and the functioning of ecosystems. As trophic and spatial niches, the niche theory states that the temporal niche axis should be considered as a mechanism for partitioning of resource use (Adams and Thibault 2006; De Almeida Jácomo et al. 2004). In bats, temporal niche differences in using water resources in water-limited environments can facilitate coexistence of sympatric species (Adams and Thibault 2006; O' Farrell and Bradley 1970). In
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this study, emergence and return time of R. affinis and R. pearsoni were significantly different (Fig. 1a, b), and thus lead to the conclusion that the difference in the duration of the activity period of bats between the two bat species was significant (Fig. 1c). R. affinis foraged during the whole
Fig. 1 The emergence time after sunset (a), times of return before sunrise (b), and the duration of the activity period (c) in Rhinolophus affinis and Rhinolophus pearsoni
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night (578.67±10.36 min), but the feeding time of R. pearsoni (422.73±7.32 min) is much shorter, less than that of R. affinis. Therefore, our results showed that temporal partitioning of prey resource use dampened the interspecific competition between R. affinis and R. pearsoni, and further promoted their coexistence. And we suggested that differences in the duration of the activity period between both species may also be driven more or less by relative population numbers. The number of R. affinis (abut 1,500) was nearly two times than that of R. pearsoni (about 800), so intraspecific competition between R. affinis is relatively larger, which may imply that R. affinis have to spend more time to forage for survival. However, as an alternative explanation, differences in the feeding time between R. affinis and R. pearsoni may be a by-product of the spatial niche partitioning. In bats, differentiation in spatial niche has been addressed as an important resource partitioning mechanism for species coexistence (Arlettaz et al. 1997; Davidson-Watts et al. 2006). In this study, R. affinis left earlier and returned later than R. pearsoni, which may indicate that the former have to fly to foraging habitats that are further away from the roost than that of the latter. Species of bats with similar wing shapes are expected to exploit foraging habitats in similar ways (Norberg and Rayner 1987), hence flight morphology may not contribute to differences in foraging area between R. affinis and R. pearsoni because their wing shapes are similar. However, differences in echolocation call frequencies (R. affinis vs. R. pearsoni, 85.86 ± 0.59 vs. 63.80±0.55 kHz) may promote spatial partitioning of prey resource use between the two species because foraging habitat hypothesis (Neuweiler 1998) suggests that different call frequencies adapt to different forage habitats. Therefore, differences in the feeding time between R. affinis and R. pearsoni may be a result of the different foraging distances of the two species from the roost to forage area. However, obviously only further experimental examination will help in answering the prediction. In summary, our study showed that there was a broad overlap in the trophic niche of R. affinis and R. pearsoni, but that temporal partitioning of prey resource use in both species facilitated their coexistence. Additionally, a relatively high abundance of prey may be addressed as an important candidate causal factor for their coexistence. Our work highlights integration of the traditional methods and next-generation sequencing for determining dietary ranges and components of carnivores is critical for understanding the mechanistic processes behind species coexistence and community ecology. We also suggested that ongoing studies of species coexistence must consider simultaneously trophic, temporal, and spatial niches.
Author's personal copy 52 Acknowledgments We would like to thank Guo Xinchun and Deng Guofang for their help in the field work. This project was supported by grants from the National Natural Science Foundation of China (Grant No. 31030011, 31100280), Research Fund for the Doctoral Program of Higher Education of China (20110043120015), and the Campus youth fund (10QNJJ015).
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