The Role of Claw Colouration in Fiddler Crabs' Mate Choice
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bioRxiv preprint doi: https://doi.org/10.1101/2021.02.06.430085; this version posted March 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 1 The role of claw colouration in fiddler crabs’ mate choice: Private 2 communication channel or handicap? 3 4 Diogo Jackson Aquino Silva1, Marilia Fernandes Erickson1, Raiane dos Santos Guidi1 5 and Daniel Marques Almeida Pessoa1* 6 1Laboratory of Sensory Ecology, Department of Physiology and Behaviour, Federal University 7 of Rio Grande do Norte. 8 *Corresponding Author: Daniel Marques de Almeida Pessoa. Avenida Senador Salgado Filho, 9 s/n, Campus Universitario Lagoa Nova, UFRN, CB, DFS. Bairro Lagoa Nova. Natal-RN, 10 Brazil. 59078-970. E-mail: [email protected]. 11 12 Declarations of interest: none 13 14 Abstract 15 Colour cues play an important role in sexual selection and conspecific recognition. Literature 16 shows that conspecifics might enjoy their everyday chat, without ever worrying about 17 occasional eavesdroppers (e.g., predators), when information interchange evolves into a private 18 communication channel. Yet, when signalling is converted into foraging cues by predators, 19 their prey must pay the due cost for sustaining conversation. For that matter, fiddler crabs draw 20 attention for having flashy enlarged claws that could potentially attract the attention of many 21 predators. Surprisingly, the costs associated with claw colouration in fiddler crabs are still 22 poorly understood and have never been studied in American species. Here, we initially examine 23 whether hypertrophied claws of American thin-fingered fiddler crabs (Leptuca leptodactyla) 24 reflect UV-light and how conspecific females react to these cues. Then we test two alternative 25 hypotheses concerning the role of claw colouration in fiddler crabs’ mate choice: a) that claw bioRxiv preprint doi: https://doi.org/10.1101/2021.02.06.430085; this version posted March 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 2 26 colouration evolved into a private communication channel, which could have significantly 27 lowered signalling costs for males; b) that claw colouration is conspicuous to potential 28 reproductive partners, as well as to predators, making colour signalling by males very costly 29 (i.e., a handicap). Thereafter, we measured the reflectance spectra from several enlarged claws 30 and modelled their chromatic contrast against the background spectrum, considering the visual 31 systems of conspecific fiddler crabs and two kinds of predators (terns and plovers). We also 32 tested female conspecifics’ preference towards enlarged claws that reflected UV-light or other 33 colour cues, by artificially altering claw colouration. Our results show a clear female preference 34 for UV reflecting males. We also found that natural enlarged claws should be highly detectable 35 by avian predators, refuting the private communication channel hypothesis. Furthermore, since 36 female fiddler crabs select the most flamboyant claws from the sandy background, claw 37 colouration in fiddler crabs can be understood as an honest signal. 38 Keywords: Animal communication; terns; plovers; colour vision; handicap principle; 39 ocypodidae; runaway selection; signal honesty; spectrophotometry; ultraviolet signal. 40 41 42 HIGHLIGHTS 43 1) The hypertrophied claws of male Leptuca leptodactyla reflect UV light. 44 2) Female fiddler crabs display a natural preference for UV light cues. 45 3) Conspicuous claws function as handicaps and may honestly signal individual quality. 46 4) Male enlarged claws are more conspicuous to birds than to crabs. 47 5) Our data refute the presence of a private communication channel in L. leptodactyla. 48 49 50 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.06.430085; this version posted March 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 3 51 INTRODUCTION 52 The evolution of animal colouration has been associated with numerous functional 53 drivers, such as social signalling, antipredator defence, parasitic exploitation, 54 thermoregulation, and protective colouration (Cuthill et al. 2017). Among these drivers, the use 55 of colour signals for intra and interspecific recognition, intrasexual competition, and mate 56 choice have received special attention from researchers that study different animal taxa 57 (Higham and Winter 2015). Yet, when we consider the study of the functional significance of 58 colouration, an especially colourful group that has received far less attention, at least when 59 compared to other arthropods (e.g., insects and spiders), is Brachyura (crabs) (Caro 2018), a 60 promising taxon on which to test some key evolutionary drivers of external appearance (Zeil 61 and Hemmi 2006; Caro 2018). 62 Among Brachyura, fiddler crabs have attracted the scientific interest for some time, 63 and, for that matter, it is a group that already offers a substantial theoretical framework on 64 which working hypotheses may be formulated. To wit, literature has established these animals 65 present an array of agonistic and sexual visual displays based on size (Oliveira and Custodio 66 1998), posture (Schöne 1968; Murai and Backwell 2006), movement (Byers et al. 2010) and 67 colour (Detto 2007) cues. Such visual cues are thought to relay information concerning 68 individual reproductive status (Crane 1975) and quality (Latruffe et al. 1999), and to allow intra 69 and interspecific recognition (Dyson et al. 2020). 70 Typically, male fiddler crabs have a brightly coloured (Dyson and Backwell 2016) and 71 hypertrophied claw that can be used either as a weapon, in male-male disputes, or as an 72 ornament, for female attraction (Crane 1975). Since fiddler crabs express two different kinds 73 of visual pigments, which are responsible for absorbing light in the UV (300-400 nm) and 74 visible (400-700 nm) light range (Horch et al. 2002; Jordão et al. 2007), they are expected to 75 see UV cues and to show a dichromatic colour discrimination (Jacobs 2018). Behavioural bioRxiv preprint doi: https://doi.org/10.1101/2021.02.06.430085; this version posted March 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 4 76 experiments, conducted on banana fiddler crabs (Austruca mjoebergi), suggest that colour (UV 77 light included), but not brightness, is important for conspecific reckoning and mate choice 78 (Detto et al. 2006; Detto 2007; Detto and Backwell 2009; Dyson et al. 2020). 79 The adaptive value of UV light reflection in fiddler crabs, however, is still poorly 80 understood and might be attributed to different ecological interactions. For instance, Detto and 81 Backwell (2009) hypothesize that, if UV reflection enhances male conspicuity, increasing their 82 detectability by female fiddler crabs, the trait should have been fixed in the population. On one 83 hand, the argument of Detto and Backwell (2009) seems to follow Fisher’s runaway selection 84 hypothesis (see Henshaw and Jones 2020), according to which a secondary sexual trait 85 expressed in one sex should become correlated with a preference for the trait in the other sex. 86 On the other hand, UV reflection could also be understood as a handicap that attracts the 87 attention of predators and warrants signal honesty about individual quality to reproductive 88 partners (Zahavi 1975). Bright colourations (which also include UV reflection) has been 89 pointed out as honest indicators of low parasite loads (Hamilton and Zuk 1982) or, in a more 90 general sense, good genes (Andersson et al. 1998). Yet, these possibilities remain to be tested 91 in fiddler crabs. 92 Another explanation is that ultraviolet reflection could also result from a trade-off 93 between the advantages of intraspecific conspicuous signalling and the disadvantages of 94 predator attraction (Hemmi et al. 2006; Cummings et al. 2008). Fish subjected to these 95 conditions have been reported to develop UV light reflection, which could yield a private 96 communication channel (i.e., wherein a species produces a signal that is detected by 97 conspecifics but not predators; see Cummings et al. 2003). In fiddler crabs’ list of predators, 98 we usually find many bird species, which detect UV light very well, such as plovers (Ribeiro 99 et al. 2003) and terns (Land 1999). bioRxiv preprint doi: https://doi.org/10.1101/2021.02.06.430085; this version posted March 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 5 100 Recently, a taxonomic review of family Ocypodidae Rafinesque, 1815 (Crustacea: 101 Brachyura) divided fiddler crabs’ former taxon (i.e., Uca) in 11 different genera (Shih et al. 102 2016). The endemic genera from the Americas (Leptuca, Minuca, Petruca and Uca) now 103 encompass 57 species, approximately 55% of fiddler crabs’ current species. Among all 104 104 fiddler crab species, only four (Afruca tangeri, Austruca mjoebergi, Tubuca signata and 105 Tubuca capricornis), from Europe/Africa and Australia, already had the utility of their claw 106 colouration examined (Cummings et al. 2008; Detto et al. 2006; Detto 2007; Detto and 107 Backwell 2009; Dyson et al. 2020). More surprisingly, Leptuca, fiddler crabs’ most heavily 108 studied taxon (Nabout et al. 2010), and the richest genus in Ocypodidae family, enclosing 109 almost one third of all fiddler crab species (i.e., 30 species according to Shih et al. 2016), has 110 not yet been explored with respect to the ecological pressures shaping its claw colouration. 111 Hence, at first, we test two competing hypotheses regarding the functional significance 112 of fiddler crabs’ enlarged claw colour, using Leptuca leptodactyla as an experimental model.