Many animals can increase their communication efficiency by enhancing the complexity in a single sensory modality or by evolving displays that target multiple sensory modalities (Cui et al., 2016; Partan and Marler, 1999). Such multimodal signaling can be highly complex, often involving multiple underlying neuronal motor programs that need to be synchronized in order to perform well (Partan and Marler, 1999; Ryan et al., 2019; Halfwerk et al., 2019; Higham and Hebets, 2013). The production and reception of multimodal signals is often more costly in terms of energy loss or predation and parasitism risk when compared to unimodal signals (Bro-Jørgensen, 2010), and their evolution is therefore often explained through functional benefits, such as cross-modal perception by receivers, which can improve signal detection and discrimination, or enhance attention and memory time (Halfwerk et al., 2019; Hebets and Papaj, 2004; Halfwerk et al., 2014b). Contra to why, we know far less how multimodal signals evolve from unimodal ones. An important question remains whether and when multimodal signals evolve de novo, or evolve through a process of co-option, by incorporating additional cues into a unimodal display (Halfwerk et al., 2019).

Human and many animals often generate by-product cues during signaling that can influence the perception of the dominant part of the signal. A famous example in humans is the McGurk effect which shows lip movement (the by-product of pronunciation) affects speech perception (McGurk and MacDonald, 1976). Similarly, floating frogs produce water ripples when calling from the water. These ripple cues are an unintentional by-product of calling, but have become part of the sexual display, as their presence modulates receiver responses to their acoustic signal components (Halfwerk et al., 2014a). Multimodal signals can thus originate from cues associated with primary signal production, either through a physical linkage (e.g. case of call-induced water ripples) or through a temporal linkage, for example, cues generated by other non-communicative behaviors that occur around the time of signaling. Once signal receivers start to pay attention to these other cues, subsequent selection on these physically or temporally linked cues may lead to closer integration and synchronization with the primary signal and become incorporated into a new, multimodal display. Such process of co-option has been proposed for many ritualized visual displays which are predicted to have evolved from different intra- or interspecific activities such as intentional movements, protective and autonomic responses (Harper, 1991; Hödl and Amézquita, 2001). For example, comparative analyses on Anatidae (i.e. ducks) suggest that the precopulatory displays of head-dipping seem to be derived from bathing behavior (Johnsgard, 1962), which may have originally been associated in time with other sexual signaling behaviors. Physical movements are in particular likely to become integrated into sexual displays. In human and some animals, movements are often used to attract the attention of receivers (Clark and Morjan, 2001; Hugill et al., 2010) and may even serve as primary sexual displays providing reliable information on sender quality (Hugill et al., 2010; Hasson, 1997; Taylor et al., 2000).

Anurans (i.e. frogs and toads) provide a good opportunity to test whether non-communicative behaviors can be co-opted into a signal function (Preininger et al., 2013a; Starnberger et al., 2014). In some anurans, for example, arm-waving movements appear to originate from cleaning behavior due to the similarities in both displays (Pombal et al., 1994). Furthermore, many anuran species display defensive movements that are also similar with communicative visual displays of some taxa (de Sá et al., 2016; Preininger et al., 2009). Here, we hypothesized that some of these physical movements originated from anti-parasite behavior in frogs. Amphibians are often confronted with parasitism from a range of different insects, such as mosquitoes or midges (Grafe et al., 2008; Legett et al., 2018; Van Beurden, 1980; Kay et al., 1985; Ferrar, 1987). These parasites are often attracted to the frog’s mating call to collect a blood meal. In return they may transmit blood-borne diseases or endo-parasites, thus imposing a large cost to a calling frog (Bernal and de Silva, 2015; Bernal et al., 2006; Meuche et al., 2016). Some anurans are observed to perform defensive physical movements in response to these parasites.

Anurans primarily communicate with acoustic signals. Background noise generated by flowing water is an impediment to acoustic communication of torrent anuran species (Preininger et al., 2013a; Grafe et al., 2012). Multimodal displays may increase the efficiency of signal detection and perception (Hebets and Papaj, 2004), and thus are favored in complex noisy environments. Researches on some torrent frogs have showed that the coupling between physical displays (e.g. vocal sac and limb movements) with calls may direct the receiver’s attention and play an important role in conspecific interactions (Preininger et al., 2013a; Preininger et al., 2009; Grafe et al., 2012; Grafe and Wanger, 2007). Insect-evoked movements are often similar to limb movements that act as visual signal. The movements evoked by host-parasite interactions may increase the complexity of signal displays and can potentially increase female preference for acoustic signals in frogs. Thus, the parasite-host interaction may provide an important source of evolutionary raw material for ritualized visual displays in anurans, which in turn may have led to the evolution of multimodal displays in which visual movements and acoustic calls have been combined.

In the present study we examined the role of insect parasites in driving multimodal signal evolution in the little torrent frog (Amolops torrentis), a tropical species that breeds in noisy mountain streams and displays both day and night. Male little torrent frogs prefer to emit advertisement calls from the rocks near streams or near vegetation. Calling males are also often observed to be disturbed by various insects including midges and some other potential parasites. In order to repel these insects, they usually display limb movements that are similar to some spontaneous movements as well as to visual displays that have been reported in other torrent frogs (de Sá et al., 2016; Caldart et al., 2014). Frog-biting midges often locate male anuran hosts by exploiting their advertisement calls (Grafe et al., 2008; Bernal et al., 2006; Meuche et al., 2016). So, there may be a predictable connection between stereotyped calls and limb movements that seem to be chaotic in this species. These contents suggest that their defensive movements may act as a visual cue component in addition to the acoustic component of little torrent frogs.

Here, we evaluated whether the presence of eavesdropping parasites increases limb movements and determined whether and how these parasite-evoked physical displays influence female preference for multimodal signals. First, we filmed little torrent frogs in the field and classified their physical displays involving limb movements. Second, we assessed the link between parasitism and male limb display by quantifying the frequency of parasite interactions as well as limb movements, and tested whether calling males produced more parasite-evoked displays compared to silent males. In order to avoid assessing individual differences, we collected sufficient samples (at least 30 males in each group) to compare the defend displays between calling frogs and silent frogs inhabited in same environment. Third, we determined the effect of midge-evoked visual movements on female mate choice with and without the advertisement calls presented, and examined if there was a specific sequence of attractive limb movements and calls. Finally, we tested whether exaggerated movements play a role in mate choice by analyzing the change of male foot flagging (FF) and leg stretching (LS) displays when females approached them in the field.

Male little torrent frogs show a rich repertoire of limb displays. By performing female choice tests and observing male-female interactions in the field, we showed that several of these limb displays (AW, HFL, and LS + FF) can serve as visual signal components and influence female mate choice. All limb movements could be spontaneously generated, but their rates were increased by call-induced parasite presence. We also found calling males to produce more limb displays than silent males. Such parasite-host interactions may have important evolutionary consequences because females in our choice tests showed a strong preference for males that emitted advertisement calls accompanied by parasite-evoked movements (e.g. AW and HFL). We did not find such preference for limb movements in the absence of call playback, demonstrating that these visual components are part of a multimodal display.

Color, vocal sac, and physical movement, as visual subcomponents, can be added to acoustic signals in anuran multimodal communication (de Luna et al., 2010). For example, agonistic behaviors of male Allobates femoralis are only evoked when males are exposed to vocal sac pulsations combined with acoustic signals during playback experiments (Narins et al., 2005). More and more studies show that streamside-breeding anurans often have complex physical displays including vocal sac inflation, limb movement, as well as body movement. For example, a recent investigation found that male Brazilian torrent frogs (Hylodes japi) have 18 distinct physical displays which may be associated with different social contexts (de Sá et al., 2016). Female little torrent frogs have been shown to prefer the vocal sac movements synchronized with calls over calls only (Zhao, 2021). In the present study, we further showed that this species performed diverse common limb displays. However, we did not observe a potential visual signal related with body displays.

Stream-breeding frogs often possess abundant limb or body movements, but their communicative functions have rarely been tested (Hödl and Amézquita, 2001). Most previous work analyzed those physical movements based on field observation or video, and few researchers have experimentally explored the effect of these visual displays on female mate choice. In the present study, we experimentally examined whether limb displays can serve as visual signal and influence female choice in little torrent frogs. By video playbacks, we found females show a significant preference for males displaying with AW and HFL as compared to motionless males. FF displays are widespread in anurans, and their functions are mainly explored from the perspective of male-male competition. For instance, male Bornean ranid frogs (Staurois guttatus) significantly increase such display when conspecific advertisement calls are broadcasted from 1 to 2 m distance in the field (Grafe and Wanger, 2007). In our study, males generated more conspicuous LS and FF displays when females were at close range in the field. Because of the difficulties in obtaining male-female interaction data, we only collected four samples which were used to examine the role of LS + FF displays. Similar with results in some other species such as Staurois parvus (Preininger et al., 2013b), males also increased such movements in response to male-male closed interactions (L Zhao et al., unpublished data), indicating that LS and FF actually are used in close-range communication. Moreover, the statistical power was high and p≤0.001 for all tests. So our results about the role of the exaggerated movements may not be biased by sample size. However, playback tests and more accumulation on field data are necessary in the future.

Frogs and toads are known to be able to see well in dim-light (Yovanovich et al., 2017). Many anurans perform behaviors only at environmental illuminations with very low levels (Buchanan, 1993). Due to their phototactic responses (Jaeger and Hailman, 1973), some video playback studies may have obtained odd results in the past. Little torrent frogs are diurnal species who can communicate with acoustic and visual signals under high-light as well as dark environments. In order to avoid possible effects from light, we set a low environmental illumination according to a natural level. In our study, females discriminated between moving and stationary stimuli. Meanwhile, more conspicuous movements (e.g. HFL) had greater attractiveness than less conspicuous movements (e.g. LSA). We thus argue that little torrent frogs actually recognize the video image as a conspecific stimulus.

Among four visual movements in our playback experiments, the attractive AW and HFL are more conspicuous than the unattractive W and LSA because the display of AW and HFL involves more occupation in terms of time and space. More conspicuous physical movements can increase receiver’s attention (Stokes and Williams, 1971; Quaranta et al., 2007), so the difference in conspicuousness may be related to the attractiveness of these movements. According to the efficacy-based hypotheses, if two signals of different modalities are generated sequentially, a signal may alert the receiver to another signal (Hebets and Papaj, 2004; Grafe et al., 2012). In this study, the AW and HFL displays tend to be emitted following advertisement calls. We show there is a pattern on the sequence of advertisement calls and limb movements that can elicit female preference, which is similar with the coupling between calls and FF in some torrent frogs (Preininger et al., 2009; Grafe et al., 2012). The LS and FF movements are the most conspicuous visual signal in little torrent frogs. Males significantly increase the two movements when females appear nearby in the wild. Such conspicuous displays, however, are not used during parasite interactions because male frogs generally perform defensive motions when parasites fall on their body (or limbs) or fly very close to their body (or limbs). Under these conditions, small and medium limb movements are sufficient, while the exaggerated motions (LS and FF) seem to be unnecessary. Therefore, the LS and FF displays are specially performed for conspecific communication, but may have evolved out of the less conspicuous limb movements.

The evolution of dynamic visual signals is often influenced by several social and environmental factors such as territorial aggression (Preininger et al., 2013a; Schuppe et al., 2017; Wu et al., 2018), diurnality (Harper, 1991), background noise (Grafe et al., 2012; Grafe and Tony, 2017), as well as predation pressure (Bradbury and Vehrencamp, 1998). Visual movements or movement-involved multimodal signals can result in senders with more chance of being seen by predators or parasites. Physical displays thus often need to increase the attention of intended receivers while limiting the eavesdropping of unintended receivers (Steinberg et al., 2014). In little torrent frogs, male limb displays increased with parasite stress, and such defensive movements can serve as visual cues. These results suggest that parasite stress can induce more visual movements and increase the complexity of audiovisual multimodal displays in little torrent frogs as a by-product. In this study, calling males had a larger parasitic risk than silent males, and we identified Corethrella spp. midges which are known to localize frog hosts by eavesdropping on their calls (Bernal and de Silva, 2015). However, more studies are needed to further examine whether and how the species is eavesdropped by sound-locating midges.

The idea that some physical movements are the raw material of dynamic visual signals has been proposed for many years (Harper, 1991; Johnsgard, 1962). In the Panamanian golden frog (Atelopus zeteki), for instance, the conspicuous semaphore signal is supposed to originate from a standard stepping motion (Lindquist and Hetherington, 1998). However, it is largely unknown how physical movements are incorporated into communicative systems. Sexual selection is believed to be an important driver and the evolution of physical movements may be favored when females are sensitive to some movements in specific environments (Fleishman, 1992). During courtship, complex signals are often preferred by females and males frequently include sexual displays more than one channel (Andersson, 1994; Clark and Feo, 2010). So physical movements from males may be incorporated into multimodal communication systems if they tap into the sensory bias of females and are beneficial to increase the attractiveness of males (sensory exploitation process; Ryan, 1998). In our study, female little torrent frogs showed a significant preference for the conspicuous defensive movements when the advertisement calls were simultaneously broadcasted. In noisy streams, acoustic signals plus the relatively conspicuous movements may benefit animals to overcome auditory masking by flowing water (Partan, 2017). Our study experimentally shows that such incorporation of non-sexual movements may actually work to increase female preference and thus become part of a multimodal display. The associated limb movements are a by-product of fending of eavesdropping parasites, which may only increase receiver’s attention for a brief moment, but which may or may not influence mate choices in other ways (e.g. mate quality assessment). We thus do not argue that we demonstrate a multimodal evolution, but test for prerequisite conditions of a scenario in which multimodal cues evolve from unimodal one via co-option of associated cues.

The simplest movements (LSA/W) are hardly used during parasite interactions and do not induce female preference. The intermediate movements (AW/HFL) are used during parasite interactions and induce a preference. The most complex movements (LS + FF) are only used during male-female (or male-male) interactions. This observed pattern could therefore reflect the evolutionary history of the visual display, from a simple to an advanced stage, where the most complex movements are no longer used in their original context (parasite defense) but only for their new function (sexual communication). Interestingly, in many anurans such as, for example, Micrixalus saxicola and S. parvus (Preininger et al., 2013b), the most complex display also involve FF.

In conclusion, we show that calling behaviors and the levels of parasite interference are correlated and males produce diverse defensive limb movements in order to avoid those unintended receivers in little torrent frogs. By female mate choice tests, we find that relatively conspicuous defensive movements increase the attractiveness of male calls to female frogs. Thus, we suggest that parasite-host interaction may increase the complexity of audiovisual displays. For the first time, we experimentally demonstrate that movements evoked by interspecific activities may evolve via increasing female preference. Our results, together with phylogenetic studies in future, would increase our understanding toward the evolutionary origin of dynamic visual cues and the relationship between natural or sexual selection pressure and multimodal communication behavior.

Data used to generate the results are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.f1vhhmgzg.

1. 1. Zhao L
   2. Wang J
   3. Zhang H
   4. Wang T
   5. Yang Y
   6. Tang Y
   7. Halfwerk W
   8. Cui J

   (2022) Dryad Digital Repository

   The data of parasite-induced and spontaneous displays in each limb movement for calling males, silent males and males that have females nearby.

   https://doi.org/10.5061/dryad.f1vhhmgzg

1. Book

   1. Andersson M

   (1994) Sexual Selection

   Princeton, NJ: Princeton Univ. Press.

   https://doi.org/10.1515/9780691207278

   • Google Scholar
2. 1. Bernal X.E.
   2. Rand AS
   3. Ryan MJ

   (2006) Acoustic preferences and localization performance of blood-sucking flies (Corethrella Coquillett) to túngara frog calls

   Behavioral Ecology 17:709–715.

   https://doi.org/10.1093/beheco/arl003

   • Google Scholar
3. 1. Bernal XE
   2. de Silva P

   (2015) Cues used in host-seeking behavior by frog-biting midges (Corethrella spp. Coquillet

   Journal of Vector Ecology 40:122–128.

   https://doi.org/10.1111/jvec.12140

   • PubMed
   • Google Scholar
4. Book

   1. Bradbury JW
   2. Vehrencamp SL

   (1998)

   Principles of Animal Communication

   Sinauer Press.

   • Google Scholar
5. 1. Bro-Jørgensen J

   (2010) Dynamics of multiple signalling systems: animal communication in a world in flux

   Trends in Ecology & Evolution 25:292–300.

   https://doi.org/10.1016/j.tree.2009.11.003

   • PubMed
   • Google Scholar
6. 1. Buchanan BW

   (1993) Effects of enhanced lighting on the behaviour of nocturnal frogs

   Animal Behaviour 45:893–899.

   https://doi.org/10.1006/anbe.1993.1109

   • Google Scholar
7. 1. Caldart VM
   2. Iop S
   3. Cechin SZ

   (2014) Social interactions in a neotropical stream frog reveal a complex repertoire of visual signals and the use of multimodal communication

   Behaviour 151:719–739.

   https://doi.org/10.1163/1568539X-00003165

   • Google Scholar
8. 1. Clark DL
   2. Morjan CL

   (2001) Attracting female attention: the evolution of dimorphic courtship displays in the jumping spider Maevia inclemens (Araneae: Salticidae

   Proceedings. Biological Sciences 268:2461–2465.

   https://doi.org/10.1098/rspb.2001.1819

   • PubMed
   • Google Scholar
9. 1. Clark CJ
   2. Feo TJ

   (2010) Why do Calypte hummingbirds “sing” with both their tail and their syrinx? An apparent example of sexual sensory bias

   The American Naturalist 175:27–37.

   https://doi.org/10.1086/648560

   • PubMed
   • Google Scholar
10. 1. Cui J
    2. Song X
    3. Zhu B
    4. Fang G
    5. Tang Y
    6. Ryan MJ

    (2016) Receiver discriminability drives the evolution of complex sexual signals by sexual selection

    Evolution; International Journal of Organic Evolution 70:922–927.

    https://doi.org/10.1111/evo.12889

    • PubMed
    • Google Scholar
11. 1. de Luna AG
    2. Hödl W
    3. Amézquita A

    (2010) Colour, size and movement as visual subcomponents in multimodal communication by the frog Allobates femoralis

    Animal Behaviour 79:739–745.

    https://doi.org/10.1016/j.anbehav.2009.12.031

    • Google Scholar
12. 1. de Sá FP
    2. Zina J
    3. Haddad CFB

    (2016) Sophisticated Communication in the Brazilian Torrent Frog Hylodes japi

    PLOS ONE 11:e0145444.

    https://doi.org/10.1371/journal.pone.0145444

    • PubMed
    • Google Scholar
13. 1. Ferrar P

    (1987)

    A guide to the breeding habits and immature stages of Diptera Cyclorrhapha

    Entomonograph 8:e907.

    • Google Scholar
14. 1. Fleishman LJ

    (1992) The Influence of the Sensory System and the Environment on Motion Patterns in the Visual Displays of Anoline Lizards and Other Vertebrates

    The American Naturalist 139:36–61.

    https://doi.org/10.1086/285304

    • Google Scholar
15. 1. Grafe T.U.
    2. Wanger TC

    (2007) Multimodal Signaling in Male and Female Foot-Flagging Frogs Staurois guttatus (Ranidae): An Alerting Function of Calling

    Ethology 113:772–781.

    https://doi.org/10.1111/j.1439-0310.2007.01378.x

    • Google Scholar
16. 1. Grafe TU
    2. Mohd Saat HB
    3. Hagen N
    4. Kaluza B
    5. Hj Berudin ZB
    6. Abdul Wahab MAB

    (2008) Acoustic localisation of frog hosts by blood-sucking flies Corethrella Coquillet (Diptera: Corethrellidae) in Borneo

    Australian Journal of Entomology 47:350–354.

    https://doi.org/10.1111/j.1440-6055.2008.00667.x

    • Google Scholar
17. 1. Grafe TU
    2. Preininger D
    3. Sztatecsny M
    4. Kasah R
    5. Dehling JM
    6. Proksch S
    7. Hödl W

    (2012) Multimodal communication in a noisy environment: a case study of the Bornean rock frog Staurois parvus

    PLOS ONE 7:e37965.

    https://doi.org/10.1371/journal.pone.0037965

    • PubMed
    • Google Scholar
18. 1. Grafe TU
    2. Tony JA

    (2017) Temporal variation in acoustic and visual signalling as a function of stream background noise in the Bornean foot-flagging frog, Staurois parvus

    Journal of Ecoacoustics 1:e1.

    https://doi.org/10.22261/jea.x74qe0

    • Google Scholar
19. 1. Halfwerk W
    2. Jones PL
    3. Taylor RC
    4. Ryan MJ
    5. Page RA

    (2014a) Risky ripples allow bats and frogs to eavesdrop on a multisensory sexual display

    Science (New York, N.Y.) 343:413–416.

    https://doi.org/10.1126/science.1244812

    • PubMed
    • Google Scholar
20. 1. Halfwerk W
    2. Page RA
    3. Taylor RC
    4. Wilson PS
    5. Ryan MJ

    (2014b) Crossmodal comparisons of signal components allow for relative-distance assessment

    Current Biology 24:1751–1755.

    https://doi.org/10.1016/j.cub.2014.05.068

    • PubMed
    • Google Scholar
21. 1. Halfwerk W
    2. Varkevisser J
    3. Simon R
    4. Mendoza E
    5. Scharff C
    6. Riebel K

    (2019) Toward Testing for Multimodal Perception of Mating Signals

    Frontiers in Ecology and Evolution 7:e124.

    https://doi.org/10.3389/fevo.2019.00124

    • Google Scholar
22. Book

    1. Harper DGC

    (1991)

    Communication, in Behavioural Ecology: An Evolutionary Approach

    Oxford: Blackwell Scientific Publications.

    • Google Scholar
23. 1. Hasson O

    (1997) Towards a General Theory of Biological Signaling

    Journal of Theoretical Biology 185:139–156.

    https://doi.org/10.1006/jtbi.1996.0258

    • PubMed
    • Google Scholar
24. 1. Hebets EA
    2. Papaj DR

    (2004) Complex signal function: developing a framework of testable hypotheses

    Behavioral Ecology and Sociobiology 57:197–214.

    https://doi.org/10.1007/s00265-004-0865-7

    • Google Scholar
25. 1. Higham JP
    2. Hebets EA

    (2013) An introduction to multimodal communication

    Behavioral Ecology and Sociobiology 67:1381–1388.

    https://doi.org/10.1007/s00265-013-1590-x

    • Google Scholar
26. Book

    1. Hödl W
    2. Amézquita A

    (2001)

    Visual Signaling in Anuran Amphibians, in Anuran Communication

    Washington: Smithsonian Institution Scholarly Press.

    • Google Scholar
27. 1. Hugill N
    2. Fink B
    3. Neave N

    (2010) The role of human body movements in mate selection

    Evolutionary Psychology 8:66–89.

    https://doi.org/10.1177/147470491000800107

    • PubMed
    • Google Scholar
28. 1. Jaeger RG
    2. Hailman JP

    (1973) Effects of intensity on the phototactic responses of adult anuran amphibians: A comparative survey

    Zeitschrift Fur Tierpsychologie 33:352–407.

    https://doi.org/10.1111/j.1439-0310.1973.tb02103.x

    • PubMed
    • Google Scholar
29. 1. Johnsgard PA

    (1962)

    Evolutionary trends in the behaviour and morphology of the Anatidae

    Wildfowl 13:e19.

    • Google Scholar
30. 1. Kato H
    2. Uezato H
    3. Sato H
    4. Bhutto AM
    5. Soomro FR
    6. Baloch JH
    7. Iwata H
    8. Hashiguchi Y

    (2010) Natural infection of the sand fly Phlebotomus kazeruni by Trypanosoma species in Pakistan

    Parasites & Vectors 3:e10.

    https://doi.org/10.1186/1756-3305-3-10

    • PubMed
    • Google Scholar
31. 1. Kay BH
    2. Boreham PF
    3. Fanning ID

    (1985) Host-feeding patterns of Culex annulirostris and other mosquitoes (Diptera: Culicidae) at Charleville, southwestern Queensland, Australia

    Journal of Medical Entomology 22:529–535.

    https://doi.org/10.1093/jmedent/22.5.529

    • PubMed
    • Google Scholar
32. 1. Legett HD
    2. Baranov VA
    3. Bernal XE

    (2018) Seasonal variation in abundance and diversity of eavesdropping frog-biting midges (Diptera, Corethrellidae) in a neotropical rainforest

    Ecological Entomology 43:226–233.

    https://doi.org/10.1111/een.12492

    • Google Scholar
33. 1. Lindquist ED
    2. Hetherington TE

    (1998) Semaphoring in an earless frog: the origin of a novel visual signal

    Animal Cognition 1:83–87.

    https://doi.org/10.1007/s100710050012

    • PubMed
    • Google Scholar
34. 1. McDonald JJ
    2. Teder-Sälejärvi WA
    3. Hillyard SA

    (2000) Involuntary orienting to sound improves visual perception

    Nature 407:906–908.

    https://doi.org/10.1038/35038085

    • PubMed
    • Google Scholar
35. 1. McGurk H
    2. MacDonald J

    (1976) Hearing lips and seeing voices

    Nature 264:746–748.

    https://doi.org/10.1038/264746a0

    • PubMed
    • Google Scholar
36. 1. Meuche I
    2. Keller A
    3. Ahmad Sah HH
    4. Ahmad N
    5. Grafe TU

    (2016) Silent listeners: can preferences of eavesdropping midges predict their hosts’ parasitism risk?

    Behavioral Ecology 27:995–1003.

    https://doi.org/10.1093/beheco/arw002

    • Google Scholar
37. 1. Narins PM
    2. Grabul DS
    3. Soma KK
    4. Gaucher P
    5. Hödl W

    (2005) Cross-modal integration in a dart-poison frog

    PNAS 102:2425–2429.

    https://doi.org/10.1073/pnas.0406407102

    • PubMed
    • Google Scholar
38. 1. Partan S
    2. Marler P

    (1999) Communication goes multimodal

    Science (New York, N.Y.) 283:1272–1273.

    https://doi.org/10.1126/science.283.5406.1272

    • PubMed
    • Google Scholar
39. 1. Partan SR

    (2017) Multimodal shifts in noise: switching channels to communicate through rapid environmental change

    Animal Behaviour 124:325–337.

    https://doi.org/10.1016/j.anbehav.2016.08.003

    • Google Scholar
40. 1. Pombal JP
    2. Sazima I
    3. Haddad CFB

    (1994) Breeding Behavior of the Pumpkin Toadlet, Brachycephalus ephippium (Brachycephalidae

    Journal of Herpetology 28:516.

    https://doi.org/10.2307/1564972

    • Google Scholar
41. 1. Preininger D
    2. Boeckle M
    3. Hödl W

    (2009) Communication in Noisy Environments II: Visual Signaling Behavior of Male Foot-flagging Frogs staurois Latopalmatus

    Herpetologica 65:166–173.

    https://doi.org/10.1655/08-037R.1

    • Google Scholar
42. 1. Preininger D
    2. Boeckle M
    3. Freudmann A
    4. Starnberger I
    5. Sztatecsny M
    6. Hödl W

    (2013a) Multimodal signaling in the Small Torrent Frog (Micrixalus saxicola) in a complex acoustic environment

    Behavioral Ecology and Sociobiology 67:1449–1456.

    https://doi.org/10.1007/s00265-013-1489-6

    • PubMed
    • Google Scholar
43. 1. Preininger D
    2. Boeckle M
    3. Sztatecsny M
    4. Hödl W
    5. Navas CA

    (2013b) Divergent Receiver Responses to Components of Multimodal Signals in Two Foot-Flagging Frog Species

    PLOS ONE 8:e55367.

    https://doi.org/10.1371/journal.pone.0055367

    • PubMed
    • Google Scholar
44. 1. Quaranta A
    2. Siniscalchi M
    3. Vallortigara G

    (2007) Asymmetric tail-wagging responses by dogs to different emotive stimuli

    Current Biology 17:R199–R201.

    https://doi.org/10.1016/j.cub.2007.02.008

    • PubMed
    • Google Scholar
45. 1. Reichert MS
    2. Höbel G

    (2015) Modality interactions alter the shape of acoustic mate preference functions in gray treefrogs

    Evolution; International Journal of Organic Evolution 69:2384–2398.

    https://doi.org/10.1111/evo.12750

    • PubMed
    • Google Scholar
46. 1. Rosenthal GG
    2. Rand AS
    3. Ryan MJ

    (2004) The vocal sac as a visual cue in anuran communication: an experimental analysis using video playback

    Animal Behaviour 68:55–58.

    https://doi.org/10.1016/j.anbehav.2003.07.013

    • Google Scholar
47. 1. Rowe C

    (1999) Receiver psychology and the evolution of multicomponent signals

    Animal Behaviour 58:921–931.

    https://doi.org/10.1006/anbe.1999.1242

    • PubMed
    • Google Scholar
48. 1. Ryan MJ

    (1998) Sexual selection, receiver biases, and the evolution of sex differences

    Science (New York, N.Y.) 281:1999–2003.

    https://doi.org/10.1126/science.281.5385.1999

    • PubMed
    • Google Scholar
49. 1. Ryan MJ
    2. Page RA
    3. Hunter KL
    4. Taylor RC

    (2019) ‘Crazy love’: nonlinearity and irrationality in mate choice

    Animal Behaviour 147:189–198.

    https://doi.org/10.1016/j.anbehav.2018.04.004

    • Google Scholar
50. 1. Schuppe ER
    2. Fuxjager MJ
    3. Williams T

    (2017) High‐speed displays encoding motor skill trigger elevated territorial aggression in downy woodpeckers

    Functional Ecology 32:450–460.

    https://doi.org/10.1111/1365-2435.13010

    • Google Scholar
51. 1. Starnberger I
    2. Preininger D
    3. Hödl W

    (2014) From uni- to multimodality: towards an integrative view on anuran communication

    Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 200:777–787.

    https://doi.org/10.1007/s00359-014-0923-1

    • PubMed
    • Google Scholar
52. 1. Steinberg DS
    2. Losos JB
    3. Schoener TW
    4. Spiller DA
    5. Kolbe JJ
    6. Leal M

    (2014) Predation-associated modulation of movement-based signals by a Bahamian lizard

    PNAS 111:9187–9192.

    https://doi.org/10.1073/pnas.1407190111

    • PubMed
    • Google Scholar
53. 1. Stokes A
    2. Williams HW

    (1971) Courtship feeding in gallinaceous birds

    The Auk 88:543–559.

    https://doi.org/10.2307/4083958

    • Google Scholar
54. 1. Taylor PW
    2. Hasson O
    3. Clark DL

    (2000) Body postures and patterns as amplifiers of physical condition

    Proceedings. Biological Sciences 267:917–922.

    https://doi.org/10.1098/rspb.2000.1090

    • PubMed
    • Google Scholar
55. 1. Van Beurden EK

    (1980)

    Mosquitoes (Mimomyia elegans (Taylor)) feeding on the introduced toad Bufo marinus (Linnaeus): implications for control of a toad pest

    Australian Zoologist 20:501–504.

    • Google Scholar
56. 1. Wu YY
    2. Ramos JA
    3. Qiu X
    4. Peters RA
    5. Qi Y

    (2018) Female–female aggression functions in mate defence in an Asian agamid lizard

    Animal Behaviour 135:215–222.

    https://doi.org/10.1016/j.anbehav.2017.11.023

    • Google Scholar
57. 1. Yovanovich CAM
    2. Koskela SM
    3. Nevala N
    4. Kondrashev SL
    5. Kelber A
    6. Donner K

    (2017) The dual rod system of amphibians supports colour discrimination at the absolute visual threshold

    Philosophical Transactions of the Royal Society B 372:e20160066.

    https://doi.org/10.1098/rstb.2016.0066

    • PubMed
    • Google Scholar
58. 1. Zhao L
    2. Wang J
    3. Yang Y
    4. Zhu B
    5. Brauth SE
    6. Tang Y
    7. Cui J

    (2017) An exception to the matched filter hypothesis: A mismatch of male call frequency and female best hearing frequency in A torrent frog

    Ecology and Evolution 7:419–428.

    https://doi.org/10.1002/ece3.2621

    • PubMed
    • Google Scholar
59. 1. Zhao L
    2. Sun X
    3. Chen Q
    4. Yang Y
    5. Wang J
    6. Ran J
    7. Brauth SE
    8. Tang Y
    9. Cui J

    (2018) Males increase call frequency, not intensity, in response to noise, revealing no Lombard effect in the little torrent frog

    Ecology and Evolution 8:11733–11741.

    https://doi.org/10.1002/ece3.4625

    • PubMed
    • Google Scholar
60. 1. Zhao L

    (2021)

    Behavioral and neurogenomic responses to acoustic and visual sexual cues are correlated in female torrent frogs

    Asian Herpetological Research 12:88–99B.

    • Google Scholar

Author details

1. Longhui Zhao

   1. CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China
   2. Ministry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, China

   Contribution

   Data curation, Formal analysis, Methodology, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-8746-2803

2. Jichao Wang

   Ministry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, China

   Contribution

   Data curation, Investigation

   Competing interests

   No competing interests declared

3. Haodi Zhang

   CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China

   Contribution

   Data curation, Investigation

   Competing interests

   No competing interests declared

4. Tongliang Wang

   Ministry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, China

   Contribution

   Data curation, Resources

   Competing interests

   No competing interests declared

5. Yue Yang

   CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

6. Yezhong Tang

   CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China

   Contribution

   Methodology, Writing – original draft

   Competing interests

   No competing interests declared

7. Wouter Halfwerk

   Department of Ecological Sciences, Vrije Universiteit Amsterdam, De Boelelaan, Amsterdam, Netherlands

   Contribution

   Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

8. Jianguo Cui

   CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China

   Contribution

   Conceptualization, Funding acquisition, Methodology, Writing – original draft, Writing – review and editing

   For correspondence

   cuijg@cib.ac.cn

   Competing interests

   No competing interests declared

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