Startle durations reveal visual assessment abilities during contests between convict cichlids

Abstract

In animal contests, the widespread ability of contestants to assess their opponents’ resource holding potential (RHP) relative to their own, termed mutual assessment, has recently been questioned. It is possible that each contestant may only have information about its own abilities or state, incurring costs up to a particular threshold then giving up, termed self-assessment. We used a technique that provides a measure of fight motivation to discriminate between different assessment models during aggressive encounters between male convict cichlids, Amatitlania nigrofasciata. A novel stimulus was applied to cause a startle response in one contestant of an aggressively interacting, size mis-matched pair, whereby the animal temporarily stops fighting. The time taken to resume the contest has been verified to provide a measure of the motivation to fight, from which it is possible to infer if any visual information concerning opponent asymmetries has been gathered. The data showed support for two differing types of assessment. There was some support for self-assessment, with startle duration being negatively related to own size, and, in a later trial series some support for an opponent only assessment strategy, with startle duration being positively related to opponent size. These results are consistent with individuals learning to use visual information about opponents when deprived of other sensory cues. Evidence within a trial supporting visual mutual assessment was lacking and possible reasons for this are discussed.

Introduction

Fighting is costly (e.g. Glass and Huntingford, 1988, Kelly and Godin, 2001, Briffa and Elwood, 2004) and selection is expected to favour gathering information to enable appropriate tactical decisions (Parker, 1974, Maynard Smith and Parker, 1976, Parker and Rubenstein, 1981, Arnott and Elwood, 2009a). For example, if both contestants assess their opponent's fighting ability, termed resource holding potential (RHP), relative to their own, then the one with the lower RHP could terminate the contest and thus reduce time, energy and risk of injury from engaging in a contest that it would inevitably lose. This idea of ‘mutual assessment’ is central to the ‘sequential assessment’ (SAM) model (Enquist and Leimar, 1983, Enquist et al., 1990) and the asymmetric war of attrition (AWOA) model of animal conflict (Maynard Smith and Parker, 1976, Parker and Rubenstein, 1981, Hammerstein and Parker, 1982). However, contestants may fail to gather information about the opponent because of high costs of doing so and/or lack of sensory or cognitive ability (Taylor and Elwood, 2003, Elias et al., 2008). In this scenario, competitors may only have information about their own ability or state, persisting in the contest to a threshold of costs, in accord with their own RHP coupled with the estimated value of the resource (Arnott and Elwood, 2007, Arnott and Elwood, 2008), such that weaker rivals tend to reach their limits first and give up. This ‘pure self-assessment’ strategy (Arnott and Elwood, 2009a) is a feature of the ‘war of attrition without assessment’ model (WOA-WA, Mesterton-Gibbons et al., 1996) and the ‘energetic war of attrition’ (E-WOA, Payne and Pagel, 1996, Payne and Pagel, 1997).

The perceived superiority of mutual assessment, because of lower potential costs, together with the frequent finding of a negative relationship between RHP difference and contest duration (e.g. Austad, 1983, Englund and Olsson, 1990, Enquist et al., 1990, Hack, 1997, Pratt et al., 2003), led authors to conclude that this strategy was typical in animal contests. However, Taylor and Elwood (2003) noted that analyses used in many studies could not distinguish between mutual and self-assessment, and that the prevalence of mutual assessment was overstated. These authors suggested a statistical framework to discriminate between mutual and self-assessment, involving an examination of the relationship between winner size (RHP) and fight duration (cost), rather than relying on composite measures of size (RHP) difference between contestants. A number of recent studies have taken such an approach and indicate that self-assessment may be much more common than previously supposed (e.g. Bridge et al., 2000, Taylor et al., 2001, Morrell et al., 2005, Prenter et al., 2006, Stuart-Fox, 2006, Brandt and Swallow, 2009; reviewed by Arnott and Elwood, 2009a). However, discriminating between assessment strategies is still problematic, with a number of recent studies providing conflicting and inconclusive results (e.g. Jennings et al., 2004, Kelly, 2006). As such, the central aim of the present study was to employ an alternative technique to test for visual assessment in animal contests.

Information gathering about opponent asymmetries should alter motivation (Parker and Stuart, 1976) and this is inferred by variation in costs that animals are prepared to pay, in terms of contest duration (e.g. Thornhill, 1984), vigour of particular activities (Briffa et al., 1998), injury (Austad, 1983), or physiological change, such as lactate accumulation or glucose depletion (e.g. Briffa and Elwood, 2001a, Briffa and Elwood, 2002, Briffa and Elwood, 2004, Prenter et al., 2006) but these measures have limitations (Arnott and Elwood, 2009b).

Another approach is to probe the motivational state of the animal directly by the use of a novel startling stimulus that causes an animal to temporarily break off from the fight. The time taken to resume the contest allows a measure of the motivation to fight, i.e. the longer the startle response shown by an animal, the less motivated it is to fight (Elwood et al., 1998, Arnott and Elwood, 2009b). A major advantage of this probe is that it can be applied at any time in the contest and is not limited to the eventual loser. The technique has recently been validated to provide a measure of fight motivation during aggressive interactions between pairs of male convict cichlid fish, Amatitlania nigrofasciata (Arnott and Elwood, 2009b), with the duration of the startle response showing clear negative correlations with the escalated aggressive activities of frontal displaying and biting. Here we test specifically for visual assessment of opponents in that species.

With mutual assessment, the prediction is that motivation of a contestant should be dependent on the size (a measure of RHP) of the opponent, as well as its own size. However, with self-assessment the prediction is that motivation to fight should depend only on own size, because no information about the opponent is gathered (Fig. 1). Thus, the use of the startle response has the potential to clearly distinguish mutual from self-assessment (Arnott and Elwood, 2009a).

A further prediction of mutual assessment, in the sequential assessment model, is that information about the opponent is relatively poor and unreliable at the start of an interaction, becoming increasingly accurate as the contest progresses (Enquist and Leimar, 1983, Enquist et al., 1990). To test this we subject the fish to two startles, one at an early stage and one at a later stage of the interaction. If mutual assessment occurs we predict that the startle response will be more influenced by the opponent in the second test than in the first. In a second attempt to test the above prediction of the sequential assessment model we used each pair twice. In the first interaction one fish was the focal startled fish and the other the stimulus fish. In the second interaction, staged the following day, the roles were reversed. If information about opponents is gathered and remembered we predict there will be more evidence of mutual assessment in contestants tested as the focal fish on the second day compared to those tested as the focal on the first day of pairing.

Our technique required fish to be in separate tanks, displaying through glass. This restricts the fish to visual information because the tactile cues produced by pushing water at the opponent (tail beating), biting and mouth-wrestling are removed, as are any potential olfactory cues. Thus we predicted that with repeated experience with different opponents the ability to use just visual cues would be improved and there would be a shift to increasing ability to use visual information about the opponent over a sequence of tests. Therefore, we use each fish three times, on each occasion facing a different opponent, to ask if visual opponent assessment improves with practice.