1 1 CHAPTER 1 GENERAL INTRODUCTION 1.1 Introduction The research reported in this thesis investigated lateralization of behaviour in feral, domestic (Equus caballus) and Przewalski horses (Equus ferus przewalski) to gain insight into lateralization in horses and to see whether it might have been influenced by domestication and/or handling and management practices. Horses, more so than other domestic animals, have been intensely handled over centuries (Hall, 2005; Levine, 2005). They have been ridden in competitions of dressage, in races and been used as transport and carrier animals (Hall, 2005). Any such activities have been accompanied by intense training and handling by humans. Lateralization in horses is interesting in its own right, especially in the context of studies of other vertebrates. It is also important to see whether any existing lateralization in domestic horses today has little or no link to that in horses that may still be described as ‘wild’ horses (Przewalski) or to horses that have become feral and have been roaming wild for a number of generations. If horses living without human intervention show no lateralization or lateralization contrary to that shown in domestic horses, there may be welfare implications or, indeed, implications for more effective or better training methods in future, as will be explained further in Chapter 2. Lateralization refers to differential processing of information and control of behaviour by the left and right hemispheres of the brain (Hellige, 2001; Andrew and Rogers, 2002; Vallortigara and Rogers, 2005). Such asymmetries can occur at the individual and/or the population level. At the individual level, but not at the population level, the majority of animals in a population or species display preferences but roughly equal numbers of individuals are left and right-biased. In such a case, the population distribution is bimodal or platykurtoic; examples are pawedness in some strains of mice (Collins, 1968) and foreleg preferences in sheep (Versace et al., 2007). Lateralization at the population level means the majority of animals are lateralized in the same direction (a directional bias is present) and the distribution is skewed to the left or right. The most well known example is 90% right handedness in humans for writing (Perelle and Ehrman, 1994). In addition, several species of cockatoos (Callocephalon fimbriatum, Calyptorhynchus banksii, Cacatua galerita) show population biases of 84 to100% in the use of the left foot to manipulate food (Rogers, 1980; Magat and Brown, 2009). General Introduction 2 A similar pattern of lateralization exists in many vertebrate species (reviewed by Rogers, 2002; Andrew and Rogers, 2002). Table 1.1 summarises these lateralized functions and cites the research showing them. Ghirlanda and Vallortigara (2004) used game-theory analysis to show population biases can exist as an evolutionary stable strategy. This model takes into account the existence of a minority of individuals that are lateralized in the direction opposite to that of the majority (i.e. they show reversed lateralization of brain functions). The percentages of the majority vary and can differ within and between species (Vallortigara and Rogers, 2005). According to the model, during predator-prey interactions the frequencies of both majority and minority groups are dependent on probability of escape. If the majority of the herd responds in a similar manner and thus turns to escape in the same direction when confronted by a predator, the group will benefit by staying together (i.e. ‘dilution effect’, Ghirlanda and Vallortigara, 2004). On the other hand, individuals belonging to the minority group (i.e. those that turn in the opposite direction) may benefit by being unpredictable to predators. Ghirlanda et al. (2009) applied the mathematical model from the earlier paper by Ghirlanda and Vallortigara (2004) to predict the strength of population biases based on intra-species interactions. Population biases were shown to be weaker when there is a competitive advantage and stronger when cooperation was essential. It could be said that social hierarchies, although giving a competitive advantage, once formed, serve to maintain cooperation between individuals. Consistent with this, Rogers and Workman (1989) demonstrated a population asymmetry for visual functions in chicks resulted in the formation of more stable hierarchies compared to chicks non-lateralized for visual functions. 1.2 Hemispheric specialisation Substantial research into lateralization has led to establishing some general principles of function. Generally, it is said that the right hemisphere is involved in attending to global and spatial geometric cues, detection of novelty, viewing of conspecifics, rapid species-typical responses in emergency situations and the expression of intense emotions (reviews, Rogers, 2002; Rogers and Andrew, 2002; MacNeilage et al., 2009). The left hemisphere is involved in attending to object-specific and local cues, object discrimination, routine learned behaviour patterns and responses that require inhibition of an immediate response while a decision is made (review, Rogers and Andrew, 2002). Table 1.1 Summary of the main functions found to be lateralized in vertebrates. Left Hemisphere Right Hemisphere References Approach Withdrawal humans, Davidson 1992, 1995; Davidson et al. 1985, 1990, 2000; dogs, Quaranta et al. 2007; Australian magpies, Koboroff et al. 2008 Considered Rapid responses fish, Miklosi et al. 1998; Miklosi and Andrew 1999; Bisazza and deSanti 2003; toads, Robins and Rogers 2004 responses Object specific cues/ Geometric cues/ humans, Hellige 2001; Volberg and Hübner 2006; Hübner and Studer 2009; chicks, Tommasi et al. 2000, 2003; Local characteristics Global characteristics Tommasi and Vallortigara 2004; Chiandetti et al. 2005; Chiesa et al. 2006; pigeons, Yamazaki et al. 2007 Reactivity/fear chicks, Andrew et al. 1982; Dharmaretnam and Rogers 2005; hens, Evans et al. 1993; fish, Cantalupo et al. 1995; toads, Lippolis et al. 2002; dunnarts, Lippolis et al. 2005; Australian magpies, Hoffman et al. 2006; lizards, Bonati et al. 2010; domestic horses, Larose et al. 2006; Austin and Rogers 2007; dogs, Siniscalchi et al. 2008; Novelty chicks, Vallortigara and Andrew 1991, Andrew and Dharmaretnam, 1991; Vallortigara et al. 1999a, 2001; toads, Introduction General Robins and Rogers 2006a; cows, Robins and Phillips 2009; dogs, Siniscalchi et al. 2010; magpies, Koboroff et al. 2008; domestic horses, Basile et al. 2009a Categorisation of stimuli chicks, Rogers and Anson 1979; Mench and Andrew 1986; Dharmaretnam and Rogers 2005; humans, Marsolek 1995, 1999; Zwaan and Yaxley 2004; Marsolek and Burgund 2008; pigeons, Güntürkün and Kesch 1987; Yamazaki et al. 2007; quails, Valenti et al. 2003; zebra finch, Alonso 1998; cows, Robins and Phillips 2009 Processing vocalisations rhesus monkeys, Hauser and Andersson 1994; sea lions, Boye et al. 2005; dogs, Siniscalchi et al. 2008; of conspecifics mangabeys, Basile et al. 2009b; domestic horses, Basile et al. 2009a Viewing of conspecifics chicks, Vallortigara and Andrew 1994; fish, Bisazza et al. 1999; Deng and Rogers 2002; tadpoles, Bisazza et al. 2002; Sovrano et al. 2001; dolphins Sakai et al. 2006; sheep, Peirce et al. 2000, 2001; da Costa et al. 2004; Versace et al. 2007 Copulation stilts, Ventolini et al. 2005; chicks, Rogers 1982; sparrows, Nyland et al. 2003; newts, Green 1997 Aggression rats, Denenberg 1981; chicks, Howard et al.,1980; Zappia and Rogers 1983; Rogers et al. 1985; Vallortigara et al. 1998, 2001; lizards, Deckel 1995; Hews and Worthington 2001; Hews et al. 2004; Gelada baboons, Casperd and Dunbar 1996; toads, Robins et al. 1998; frogs, Robins and Rogers 2006b 3 Routine chicks, Rogers and Anson 1979; Mench and Andrew 1986; Dharmaretnam and Rogers 2005; pigeons, Güntürkün behaviour and Hoferichter 1985; Güntürkün and Kesch 1987; zebra finch, Alonso 1998; quails, Valenti et al. 2003 Emergency chicks, Andrew et al. 1982; Dharmaretnam and Rogers 2005; primates, Hatta and Koike, 1991; hens, Evans et al. behaviour 1993; fish, Cantalupo et al. 1995; toads, Lippolis et al. 2002; dunnarts, Lippolis et al. 2005; Australian magpies, Hoffman et al. 2006; domestic horses, Larose et al. (2006), Austin and Rogers 2007; lizards, Bonati et al. 2010 General Introduction 4 The suite of right-hemisphere functions includes a superior ability to process global cues (humans, Volberg and Hübner 2006; Hübner and Studer 2009; chicks, Tommasi and Vallortigara, 2004), as used in spatial ability (chicks, Tommasi et al., 2003; humans, Hellige 2001), attending to novelty (toads, Robins and Rogers, 2006a) and in vigilance (humans, Warm et al., 2009; magpies, Koboroff et al., 2008). All of these functions play a role in detecting and attending to potential threats. According MacNeilage et al. (2009), early in the evolution of vertebrates the right hemisphere controlled responses to unexpected, potentially dangerous stimuli. Later, such responses may have become accompanied by high arousal and intense emotions, such as fear, which are also controlled by the right hemisphere. As MacNeilage (1998, 2007) has pointed out, the right hemisphere is used in functions related to survival risk (MacNeilage, 1998) and the left hemisphere is used in behaviour involving routine motor actions (MacNeilage, 2007). The right hemisphere processes variance, hence attending to novelty, which makes it good at responding to potential threats by predators or conspecific rivals