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Giant Australian cuttlefish use mutual assessment to resolve male-male contests. 1 Alexandra K ... PDF

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1   Giant Australian cuttlefish use mutual assessment to resolve male-male contests. 2   Alexandra K. Schnell*a, Carolynn L. Smitha, Roger T. Hanlonb, Robert Harcourta 3   a Department of Biological Sciences, Macquarie University, Sydney, NSW, Australia 4   b Program in Sensory Physiology and Behavior, Marine Biological Laboratory, Woods Hole, 5   MA, U.S.A. 6   Received 12 January 2015 7   Initial acceptance 11 February 2015 8   Final acceptance 15 May 2015 9   MS. number: 15-00033R 10   *Correspondence: A. K. Schnell, Macquarie University, Department of Biological Sciences, 11   North Ryde, Sydney, NSW 2109, Australia. 12   E-mail address: [email protected] (A. K. Schnell). 13   14   15   16   17   18   19   20   21 22   Game theory models provide a useful framework for investigating strategies of conflict 23   resolution in animal contests. Model predictions are based on estimates of resource-holding 24   potential (RHP) and vary in their assumptions about how opponents gather information about 25   RHP. Models can be divided into self-assessment strategies (energetic war-of-attrition, E- 26   WOA; cumulative assessment model, CAM) and mutual assessment strategies (sequential 27   assessment model, SAM). We used laboratory-staged contests between male giant Australian 28   cuttlefish, Sepia apama, to evaluate RHP traits and to test game theory models. Mantle length 29   was a key indicator of RHP because it predicted contest outcome, whereby larger individuals 30   were more likely to win a contest. Winners and losers did not match behaviours, ruling out 31   the E-WOA. There was no relationship between contest outcome, duration and escalation 32   rates, arguing against the CAM. Persistence to continue a contest was based on RHP 33   asymmetry, rather than loser and/or winner RHP, providing support for the SAM. Motivation 34   to fight was determined from a male’s latency to resume a contest following the introduction 35   of a female during a contest. The latency to resume a contest was negatively related to the size 36   of the focal male and positively related to the size of their opponent. These results show that 37   competing males are able to gather information concerning RHP asymmetries, providing 38   support for mutual assessment. Furthermore, males showed significant behavioural 39   differences in their responses to relatively larger than to relatively smaller opponents. Using 40   an integrative approach, our study provides a well-substantiated example of mutual 41   assessment. 42   Keywords: contest competition, fighting ability, game theory, resource-holding potential, 43   sequential assessment model, visual signalling 44   45 46   Animals competing over limited resources are likely to incur costs, including increased 47   energy expenditure and risk of predation, injuries or fatal attacks (Maynard Smith, 1974; 48   Maynard Smith & Price, 1973). During contests, animals may gather information from 49   multiple sources to assess the potential costs and benefits of continued conflict, in turn 50   facilitating economic and tactical decision making (Maynard Smith & Parker, 1976; Parker, 51   1974). The decision to withdraw from a contest is usually influenced by the fighting ability of 52   a contestant, termed resource-holding potential (RHP; Maynard Smith, 1974; Parker, 1974; 53   Parker & Stuart, 1976). The information that facilitates these decisions will be dictated by the 54   assessment capabilities of the species (Taylor & Elwood, 2003). 55   Game theoretical approaches serve as an analytical tool for understanding the patterns 56   of behaviour observed in contests across many taxa. Currently, three major game theory 57   models may be applied to animal contests to determine the assessment strategy used for 58   decision making (Table 1). The models can be divided into self-assessment and mutual 59   assessment strategies. The self-assessment models include the energetic war of attrition (E- 60   WOA; Payne & Pagel, 1996; 1997) and the cumulative assessment model (CAM; Payne, 61   1998). These models assume that contestants evaluate their own RHP, but fail to assess their 62   opponent’s RHP. Contestants differ in rates of escalation within phases (i.e. periods defined 63   by behaviours of similar aggressive intensity). The decision point to withdraw is determined 64   by the weaker individual’s threshold for costs. For the E-WOA model, the threshold is based 65   on self-imposed energetic costs. For the CAM, the threshold is determined by combined costs 66   that accumulate as a function of time and energy expenditure, as well as the damage inflicted 67   by the opponent. Mutual assessment is modelled through the sequential assessment model 68   (SAM), which assumes that contestants evaluate their own RHP relative to their opponent’s 69   RHP (Enquist & Leimar, 1983). In this model, contests progress through a series of 70   successive phases, which are thought to provide increasingly accurate information about the 71   RHP asymmetry between contestants. Predictions for these three models are based on 72   estimates of RHP and vary in their assumptions about how opponents gather information 73   about RHP (Table 1). 74   Mutual assessment is assumed to be a more efficient strategy than self-assessment 75   because animals can minimize costly and futile persistence by gathering information about 76   relative RHP (Enquist & Leimar, 1983). However, studies on a wide range of animal contests 77   that have shown mutual assessment (e.g. Englund & Olsson, 1990; Junior & Peixoto, 2013; 78   Kemp, Alcock, & Allen, 2006; Pratt, McLain, & Lathrop, 2003) have recently been called 79   into question (Briffa & Elwood, 2009; Elwood & Arnott, 2012; Taylor & Elwood, 2003). 80   Taylor and Elwood (2003) contended that such studies may have actually presented artefacts 81   of alternative mechanisms. For example, a negative association between contest duration and 82   RHP asymmetry, which is thought to be indicative of the SAM (i.e. mutual assessment), 83   could also arise if the weaker contestant accrued costs faster than its opponent (i.e. self- 84   assessment, E-WOA). Taylor and Elwood (2003) recommended a statistical framework to 85   distinguish between mutual and self-assessment strategies. This framework has been 86   implemented in many studies, revealing that self-assessment is more prevalent than 87   previously thought (e.g. Brandt & Swallow, 2009; Prenter, Elwood, & Taylor, 2006; Stuart- 88   Fox, 2006). However, distinguishing between assessment strategies remains a challenge, and 89   consequently several recent studies report inconclusive results (e.g. Batista, Zubizarreta, 90   Perrone, & Silva, 2012; Egge, Brandt, & Swallow, 2011; Jennings, Gammell, Carlin, & 91   Hayden, 2004; Kelly, 2006). 92   Recently, there has been renewed debate about whether mutual assessment is more 93   cognitively complex than self-assessment because of its apparent requirement for comparative 94   decision making (Elwood & Arnott, 2012; Elwood & Arnott, 2013; Fawcett & Mowles, 95   2013). Elwood and Arnott (2012) and Fawcett and Mowles (2013) argued that mutual 96   assessment could entail cognitively simple threshold decision making. They noted that the 97   original SAM model (i.e. mutual assessment) does not require an explicit comparison of RHP; 98   rather, information about RHP is directly transmitted as a relative measure (i.e. as error-prone 99   estimates of relative fighting ability). Moreover, Elwood and Arnott (2012) argued that many 100   studies provide insufficient evidence of individuals comparatively assessing RHP, and that 101   many claims of comparison of body size, claw size or dewlap size still need to be 102   substantiated. One experimental approach to substantiate such claims involves assessing the 103   motivational state of an animal in a contest by using a novel stimulus that causes a contestant 104   to temporarily cease fighting (see Arnott & Elwood, 2009a; Elwood, Wood, Gallagher, & 105   Dick, 1998). The latency to resume the contest provides a measure of the individual’s 106   motivation to fight (see Table 1 for predictions). Another approach is to test the ability of a 107   contestant to assess relative values (e.g. body size or claw size) in the context of aggression 108   (see e.g. dogs, Canis familiaris, Taylor, Reby, & McComb, 2010). Testing such capabilities 109   during a contest may validate claims of mutual assessment. 110   This study investigated the assessment strategy used to resolve conflict in male giant 111   Australian cuttlefish, Sepia apama. These cuttlefish engage in dynamic signalling during 112   agonistic contests, similar to other species in which game theory models have been tested 113   (e.g. hermit crabs, Briffa & Elwood, 2001; chameleons, Stuart-Fox, 2006; wasps, Tibbetts, 114   Mettler, & Levy, 2010). Contests typically occur in the presence of females during their 115   reproductive season (austral winter months: May–August). However, even in the absence of 116   females, males engage in contests in both field (Hanlon, 1999) and laboratory settings 117   (Schnell, 2014). The fighting tactics of males are influenced by body size, which varies 118   widely at maturity. Small males tend to reduce direct aggression by being surreptitious or 119   through deceptive signalling (i.e. female mimicry; Hanlon, Naud, Shaw, & Havenhand, 120   2005). Large males regularly engage in agonistic contests, which are typically mediated 121   through visual displays but can escalate to physical pushing and grappling (Hall & Hanlon, 122   2002). Variation in body size and its effect on agonistic behaviours suggest that this species 123   has evolved the ability to assess the size of its opponents and alter its behaviour accordingly. 124   However, the assessment strategy used during these contests has not been tested. The 125   application of game theory models to cuttlefish contests may be an effective tool for 126   determining patterns of fighting behaviour (i.e. self-assessment or mutual assessment 127   strategy) in this particular system. 128   The central aim of our study was to determine the fighting strategy used by giant 129   Australian cuttlefish during male–male contests. First, we assessed the male traits that may be 130   associated with RHP. Second, we used specific predictions of the three major game theory 131   models (E-WOA, CAM, and SAM; see Table 1 for predictions) to determine whether the 132   decision to withdraw from a contest was based on the absolute RHP of the loser (self- 133   assessment) or on the RHP of the loser relative to the winner (mutual assessment). Third, the 134   contestant’s assessment of RHP was substantiated by measures of motivation and aggression. 135   136   <H1>METHODS 137   <H2>Study species, collection and husbandry 138   Thirty-four male and four female adult giant Australian cuttlefish were caught via scuba in 139   coastal areas of Sydney, Australia (34°50’S, 151°22’E) between April and May 2012. They 140   were transported (< 50 min) to the aquarium facility at Cronulla Fisheries Research Centre in 141   a custom-made transport tank (9.0 x 8.0 cm and 8.0 cm high, maximum capacity = 3 142   subjects). Water in the transport tank was oxygenated and maintained at a natural ambient sea 143   temperature (15–17 °C). Sex was determined by coloration and the dimorphic state of the 144   fourth arm. Subjects were housed individually in open-air tanks that received a constant flow 145   (approximately 10 litres/min) of filtered ambient sea water. Cuttlefish were fed a mixed diet 146   of food items including live Australian ghost shrimp, Trypaea australiensis, and thawed 147   frozen prawn, squid or pilchard every evening. 148   <H2>Male traits 149   We measured mantle length and dimorphic arm length (ventral-most pair; Fig. 1) to the 150   nearest 0.1 mm and weighed cuttlefish to the nearest 1 g using a Precisa electronic balance 151   (30000D IP65 Wedderburn scales TYP 480-9580, Switzerland). We also measured ‘passing 152   cloud’ behaviour which is a chromatic signal typically expressed by males during the lateral 153   display (Fig. 1b). It involves the expansion and contraction of chromatophores to produce the 154   appearance of light and dark bands flowing unidirectionally over the mantle. The number of 155   clouds and speed of travel are relatively consistent; however, the expression of this behaviour 156   varies in intensity. To measure changes in intensity, we recorded the duration and the contrast 157   of the bands. There was no variation in the duration of bands; however, the contrast of bands 158   changed throughout the agonistic interactions. We therefore measured the intensity using 159   contrast differences between light and dark bands. Contrast differences are likely to be 160   visually conspicuous because the visual systems of cuttlefish are sensitive to polarized light 161   (Mäthger, Shashar, & Hanlon, 2009; Shashar, Rutledge, & Cronin, 1996). We calculated the 162   brightness of the bands on the mantle of each male displaying passing cloud. This was 163   measured on a laptop (Apple Macintosh, OS X 10.9.2) broadcasting the video recordings and 164   using Apple Macintosh Digital Color Meter. We recorded the RGB values at 10 random 165   locations on both light and dark bands. Brightness values were calculated from RGB values (0 166   = black and 255 = white) using the luminance formula from Poynton (2003): 167   Y = 0.2126 × R + 0.7152 × G + 0.0722 × B 168   The means of each set of brightness values was then used to approximate contrast differences 169   between the bands. Correlations of all four male attributes (mantle length, arm length, mass 170   and passing cloud intensity) were then determined using Pearson correlation coefficients (see 171   Appendix Table A1). 172   <H2>Male contests 173   Laboratory-staged contests were carried out in June and July 2012. Twenty-two males that 174   varied in size (mean mantle length = 415.1 mm; range 295–509 mm; mean body weight = 175   6348 g; range 4015–9324 g) were used. We used a repeated measures design, in which each 176   male was assigned to (1) a size-symmetric opponent (within 7% of mantle length of each 177   other) and (2) a size-asymmetric opponent (at least 20% mantle length difference). Subjects 178   were assigned a random sequence of the treatments (i.e. size-symmetric and size-asymmetric) 179   to control for order effects. Trials were staged 4 weeks apart to minimize experience effects, 180   since different agonistic experiences can sometimes affect the outcome of a contest (i.e. 181   winner–loser effect; Hsu & Wolf, 1999). 182   The contest arena was a circular 5000-litre (height 12.0 cm, diameter 23.4 cm; 2.38 m2 183   per cuttlefish) tank divided in half. A clear partition was fixed in place to physically isolate 184   subjects and prevent injury during the contests. An opaque partition slid loosely next to the 185   clear partition to visually isolate subjects during the first phase of the tests. Water was able to 186   flow between both compartments to facilitate chemical exchange between the male subjects. 187   A high-definition video camera (SONY HDR-SR11E) fitted with a wide-angle lens (Raynox 188   HD-5050PRO 0.5 x) was placed directly over the test arena to record (MTS format 1920 × 189   1080 lines) behavioural responses. 190   To acclimate subjects to the apparatus, individuals were placed in the test arena for 191   three 65 min periods over 3 consecutive days. During acclimation sessions the subjects were 192   tested separately, so that males did not come into visual contact or chemical exposure with 193   one another until the experimental phase. Subjects were placed gently into one of the two 194   compartments in the test arena. Following a 5 min period, the opaque partition was removed 195   by sliding it out of the water. After 60 min subjects were recaptured and transferred back to 196   their home tank. After each acclimation session, the test arena was drained, cleaned and 197   refilled using fresh filtered sea water to ensure subjects were not responding to any chemical 198   cues left in the water from previous test subjects. By the third acclimation session subjects 199   exhibited no signs of disturbance, such as inking or jetting, from the transfer procedure. The 200   experimental trials followed the same procedure used in the acclimation sessions. Subjects 201   typically engaged in more than one contest during the 60 min staged experimental trials and 202   therefore the repeated measures design was unbalanced. We observed 75 contests in 21 203   experimental trials (mean number of contests = 3.43; range 1–7); one trial without mutual 204   displaying between contestants was excluded. 205   <H2>Probing motivational state in response to a female stimulus 206   The motivational state experiments were carried out in June 2012. Twelve males that varied 207   in size (mean mantle length = 411.76 mm; range 350–464 mm; mean body weight = 5113 g; 208   range 4278–6324 g) and had not participated in any previous experiments were used. We used 209   a repeated measures design, in which each test male was assigned a size-asymmetric opponent 210   (at least 20% mantle length difference) and tested twice using the same opponent. Probing 211   motivational state is typically tested using a startle stimulus (see Arnott & Elwood, 2009a; 212   Elwood et al., 1998). However, initial pilot observations revealed that male subjects did not 213   respond to small startle stimuli whereas larger startle stimuli caused focal males to ink, 214   making it impossible to record the behaviour of the test subjects. We used a female to distract 215   the focal male instead. This consistently caused the focal male to cease fighting and inspect 216   the female before resuming the contest. The test arena was the same as the contest arena 217   except it was divided into three compartments that did not allow chemical exchange. The 218   edges of the clear Perspex partition were sealed with a silicon sealant. Two compartments 219   were equal in size and the third compartment was smaller. Test males were placed in the 220   equal-sized compartments and a female was placed in the smaller compartment. Following a 221   30 min acclimation period the opaque partition between the males’ compartments was 222   removed. One minute after the onset of display by both male cuttlefish, the opaque partition 223   to the female compartment was removed on one side only, so that one male contestant (i.e. the 224   focal male) could see the female. The female compartment in the test arena was designed so 225   that when only one opaque partition was removed her presence was undetected by the male 226   opponent (i.e. stimulus male). The specific timing of introducing the female was chosen 227   following initial laboratory-staged contest experiments, and selected to give sufficient periods 228   of display and escalation. Following each interaction, the subjects were returned to their home 229   tanks and 48 h later the original pairs were retested in the same manner, but with the 230   previously nondistracted stimulus male now being designated as the focal male and exposed 231   to the female. Four females of similar size (mean mantle length = 299.71 mm; range 293–304; 232   mean body weight = 3266.34 g; range 3104–3326) were used as a stimulus to reduce 233   pseudoreplication. Males had not encountered the females prior to this experiment. 234   <H2>Decision making in response to aggressive rivals with variable RHP 235   The decision-making experiments were carried out in July 2012. Eight medium-sized males 236   (mean mantle length = 415.88 mm; range 390–431 mm; mean body weight = 5424 g; range 237   4515–5834 g) that were used in the laboratory-staged contest experiments were subsequently 238   used as focal subjects. A repeated measures design was used, in which each focal male was 239   assigned a smaller live-male stimulus (mantle length approximately < 20%) and a larger live- 240   male stimulus (mantle length approximately > 20%). Focal males were assigned a random 241   sequence of the treatments (i.e. small and large) to control for order effects. Focal males were

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Alexandra K. Schnell*a, Carolynn L. Smitha, Roger T. Hanlonb, Robert Harcourta. 2 *Correspondence: A. K. Schnell, Macquarie University, Department of Biological Sciences,. 10. North Ryde, Sydney . assessment) or on the RHP of the loser relative to the winner (mutual assessment). Third, the. 133.
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