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Bats Are Acoustically Attracted to Mutualistic Carnivorous Plants

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Bats Are Acoustically Attracted to Mutualistic Carnivorous Plants Report Bats Are Acoustically Attracted to Mutualistic Carnivorous Plants Graphical Abstract Authors Michael G. Scho¨ ner, Caroline R. Scho¨ ner, Ralph Simon, ..., Se´ bastien J. Puechmaille, Liaw Lin Ji, Gerald Kerth Correspondence [email protected] In Brief To maintain mutualisms, plants specifically appeal to their animal partners’ perception. Scho¨ ner et al. now show that Paleotropical carnivorous plants have reflective structures that are acoustically attractive for mutualistic bats. This phenomenon can similarly be found in a few Neotropical bat-pollinated flowers. Highlights d A carnivorous plant features an ultrasound reflector attractive for mutualistic bats d This reflector enables the bats to easily find and identify the plant’s pitchers d The bats fertilize these Paleotropical plants with feces in exchange for roosts d Such reflectors were convergently acquired in Neotropical bat-pollinated plants Scho¨ ner et al., 2015, Current Biology 25, 1–6 July 20, 2015 ª2015 Elsevier Ltd All rights reserved http://dx.doi.org/10.1016/j.cub.2015.05.054 Please cite this article in press as: Scho¨ ner et al., Bats Are Acoustically Attracted to Mutualistic Carnivorous Plants, Current Biology (2015), http:// dx.doi.org/10.1016/j.cub.2015.05.054 Current Biology Report Bats Are Acoustically Attracted to Mutualistic Carnivorous Plants Michael G. Scho¨ ner,1,4,* Caroline R. Scho¨ ner,1,4 Ralph Simon,2,4 T. Ulmar Grafe,3 Se´ bastien J. Puechmaille,1 Liaw Lin Ji,3 and Gerald Kerth1 1Zoological Institute and Museum, Ernst-Moritz-Arndt-Universita¨ t Greifswald, Johann-Sebastian-Bach-Straße 11-12, 17489 Greifswald, Germany 2Department of Sensor Technology, Friedrich-Alexander-Universita¨ t Erlangen-Nu¨ rnberg, Paul-Gordan-Straße 3-5, 91052 Erlangen, Germany 3Department of Biology, Faculty of Science, Universiti Brunei Darussalam, Tungku Link, Gadong 1410, Brunei Darussalam 4Co-first author *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.05.054 SUMMARY partners regularly separate, they require species-specific mech- anisms to find each other again. This is also true for the carnivo- Mutualisms between plants and animals shape rous pitcher plant Nepenthes hemsleyana (Nepenthaceae), the world’s ecosystems [1, 2]. In such interactions, which recently was reported to have a mutualistic interaction achieving contact with the partner species is impera- with the insectivorous bat Kerivoula hardwickii (Vespertilionidae). tive. Plants regularly advertise themselves with signals This bat fertilizes the plant with its feces while roosting inside the that specifically appeal to the partner’s perceptual pitchers. The bat droppings enhance the nitrogen intake of preferences [3–5]. For example, many plants have N. hemsleyana by 34% on average [10]. In turn, the pitcher plants provide the bats with roosts that are free of parasites, have a sta- acquired traits such as brightly colored, fragrant ble microclimate, and offer enough roosting space for one or two flowers that attract pollinators with visual, olfactory, bats while at the same time preventing the bats from falling into or—in the case of a few bat-pollinated flowers—even the digestive fluid due to their unique morphological shape and acoustic stimuli in the form of echo-reflecting struc- low fluid level [11]. Finding and identifying N. hemsleyana tures [6–9]. However, acoustic attraction in plants is pitchers that grow in the dense Bornean peat swamp forests, rare compared to other advertisements and has never however, is a challenging task for echolocating bats: they have been found outside the pollination context and only in to distinguish echoes of the pitchers from those of the cluttered the Neotropics. We hypothesized that this phenome- surroundings [13, 14]. The situation is further complicated by non is more widespread and more diverse as plant- the fact that the bats need to distinguish the rare [11, 15] bat interactions also occur in the Paleotropics. In N. hemsleyana pitchers from the more common and similarly Borneo, mutualistic bats fertilize a carnivorous pitcher shaped pitchers of sympatric Nepenthes species, which are unsuitable for roosting [10]. plant while roosting in its pitchers [10, 11]. The In the Neotropics, a few bat-pollinated plants found an efficient pitcher’s orifice features a prolonged concave struc- solution to attract bats by developing floral ultrasound reflectors ture, which we predicted to distinctively reflect the [7, 9], which enabled them to exploit the bats’ echolocation bats’ echolocation calls for a wide range of angles. system. However, such reflectors have never been described This structure should facilitate the location and identi- for plants outside the Neotropics, probably because in the Pale- fication of pitchers even within highly cluttered sur- otropics, chiropterophilous plants are pollinated by fruit bats roundings. Pitchers lacking this structure should be (Pteropodidae) that are unlikely to use echolocation for foraging less attractive for the bats. Ensonifications of the [16, 17]. We hypothesized that this phenomenon can also be pitchers around their orifice revealed that this structure found in the Paleotropics. If so, bat-dependent plants such as indeed acts as a multidirectional ultrasound reflector. N. hemsleyana should have echo-reflecting structures making it In behavioral experiments where bats were confronted easier for bats to localize and identify pitchers. Pitchers lacking such reflectors should be more difficult to find. Additionally, the with differently modified pitchers, the reflector’s pres- bats should have echolocation calls that facilitate the finding of ence clearly facilitated the finding and identification of targets even within highly cluttered surroundings. pitchers. These results suggest that plants have con- vergently acquired reflectors in the Paleotropics and Do Pitcher Plants Have Ultrasound Reflectors? the Neotropics to acoustically attract bats, albeit for To test whether a certain pitcher structure serves as an effective completely different ecological reasons. reflector that acoustically stands out in cluttered environments and guides the bats to their target, we measured ultrasound RESULTS AND DISCUSSION echoes of pitchers from different angles using a biomimetic sonar head. We sampled pitchers of both N. hemsleyana and How mutualisms evolve or how these interactions are main- its closest relative, Nepenthes rafflesiana (Figure S1), which tained is still not sufficiently understood [12]. Particularly, if does not host bats, and ensonified them in the elevation plane Current Biology 25, 1–6, July 20, 2015 ª2015 Elsevier Ltd All rights reserved 1 Please cite this article in press as: Scho¨ ner et al., Bats Are Acoustically Attracted to Mutualistic Carnivorous Plants, Current Biology (2015), http:// dx.doi.org/10.1016/j.cub.2015.05.054 Figure 1. Echo Reflectance of Nepenthes hemsleyana and Nepenthes rafflesiana Pitchers for the Elevation Plane Given in Spectral Target Strength (A and B) Target strength (TS; mean from 40 to 160 kHz) of N. hemsleyana (A) and N. rafflesiana (B) pitchers (n = 9), respectively, for different angles of sound incidence in the elevation plane. The red- dish areas indicate where bats typically approach (see also Figures S1, S2, and S3A). Note that within this area (0 to 30), the TSs of N. hemsleyana pitchers significantly exceed the TSs of N. rafflesiana pitchers. the spectral contents of the pitchers’ echoes and found that directional spec- tral information of N. hemsleyana pitchers (from À40 to 110; each species n = 9; Figure 1) and the azimuth clearly differs from that of N. rafflesiana (as exemplarily shown in (horizontal circular) plane (90 on either side of the pitchers’ the spectral directional plots in Figures 2B and 2C). Sliding- orifice; each species n = 8; Figure 2A). window comparisons (27) of the spectra of N. hemsleyana We analyzed the mean spectral target strength (TS), which is a and N. rafflesiana pitchers (n = 8 each) revealed significant measure of acoustic backscattering of an object, for the whole spectral differences between the species within an angular frequency area of 40–160 kHz. For the measurements in the range of 20 to 25 on either side of the pitcher’s orifice, angles elevation plane, we found a clear peak for N. hemsleyana at which the back wall is ensonified (Figure 2D; see Supple- pitchers (Figure 1) for angles where the sonar beam ensonified mental Information). Thus, the bats could use the pitchers’ spe- the exposed and prolonged inner back wall at the pitcher’s cies-specific spectral pattern to identify them, especially during orifice. This concave structure is lacking in N. rafflesiana lateral approaches, while the significantly increased TS of (Figure S1A) and other sympatric Nepenthes species (e.g., N. hemsleyana pitchers helps the pitchers to acoustically stand N. ampullaria, N. bicalcarata; Figure S1B). Consequently, within out in cluttered surroundings. this area, N. hemsleyana pitchers have significantly higher TS than N. rafflesiana pitchers (Wilcoxon signed-rank test: V = Are the Bats’ Echolocation Calls Suited to Detect 11.0, p < 0.001; compare Figures 1A, 1B, and S3A). Interestingly, Pitchers in Highly Cluttered Space? this was also the area where the bats usually approached the Bats in the genus Kerivoula generally have relatively short, high- pitchers (0 to 30, data not shown; Figure S2). When ensonifying pitched calls [18] covering a very large bandwidth, which further the pitchers from steeper angles (>30), the sonar beam pointed increases when
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    Index α-amy gene family, 119 acid rain, 228–32 allergens, 201, 206 α-ketoglutarate, 175 acidosis, 223 Allium cepa see onion ABA see abscisic acid actinomorphic flowers, 194, 302 allantoic acid, 54 ABA-binding/receptor proteins, 80–81 action potential, 161–2 allantoin, 54 ABC model, 195 action spectrum (pl. spectra), 87, 90–91, 170, allelopathy, 260, 302 ABCE model, 195–6, 214 192, 302 Alopecurus myosuroides see black grass ABI genes/ABI proteins, 106, 115 actin, 15, 35 alpine environment, 218, 237 Abies lasiocarpa see subalpine fir actin filament/microfilament, 15, 34–6, 212 alternation of generations, 5, 11–13, 94 abscisic acid, 26, 75, 79–81, 139, 163, 204 active transport (across membranes), 134–6, alternative intron splice sites, 70 antagonizes cytokinins, 79 139 alternative oxidase, 47 antagonizes GA, 79, 106, 115–16, 119 acyl carrier protein/ACP, 48–9 alternative poly-adenylation sites, 70 in control of cell division, 41 acyl transferase, 49 alternative transcription start sites, 70 inhibition of flowering, 80 adaptation, 124, 128–9, 162, 181–2, 187, 214, alternative translation start sites, 71 inhibition of germination, 116 235–59, 270–271 aluminium interaction with ethylene, 109 concept, 216, 235 hyperaccumulators, 255 involvement in abscission, 187 aequorin, 85 tolerance, 252–5 involvement in stomatal closure, 224 aeration, 130, 222 toxicity, 133, 230–232, 254 involvement in stress responses, 224–6, 238 aerenchyma, 130, 240–243, 302 Alzheimer’s disease, 255 modes of action/signalling pathways, 80, 225 Aesculus hippocastanum see horse
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