Dear enemy effect in the Mexican volcano mouse Neotomodon alstoni: Implications of sex in the agonistic behaviour among neighbours

Highlights

• We compared the agonistic behaviour between nearest neighbours and distant neighbours.

• Spatial proximity between neighbours is influenced by the sex and reproductive activity of individuals.

• Females exhibit non-aggressive avoidance among neighbours.

• Males are more aggressive and less tolerant to distant neighbours.

• The volcano mouse exhibits the dear enemy phenomenon.

Abstract

Two opposite phenomena have been found in territorial animals, the “dear enemy’’ and the “nasty neighbour’’, which refer to individuals that show less aggression toward neighbours than toward strangers and vice versa. However, the need to maintain territory should differ for males and females because sexual reproduction is the result of the different adaptive strategies of the sexes. In this study, we explore territorial behaviour in the context of dear-enemy and nasty neighbour effects in the Mexican volcano mouse (Neotomodon alstoni). Patterns of spatial relationships between individuals and the degrees of agonistic behaviour among neighbours were analysed for a period of one year. Results exhibit a greater spatial proximity between male pairs during the non-reproductive period than during the reproductive period, and greater spatial proximity between pairs of females during the reproductive period than during the non-reproductive period. The analysis of agonistic behaviour showed that there is less tolerance for distant neighbours than for nearest neighbours. However, there is a greater frequency of aggression between male pairs than between females, while females appear to exhibit non-aggressive avoidance among individuals. The results support the theory that Mexican volcano mouse exhibits the "dear enemy phenomenon".

Introduction

Territoriality prevents other individuals, including mates, from using acquired limited resources. Therefore, the benefit of having a territory is the increase of resource availability for the individual, family or group (Stamps, 1994; Müller and Manser, 2007). The main suggested disadvantage for resource monopolization is that defence against intruders involves investing time and energy in aggressive territorial contests, and this can increase the risk of injuries (Marden and Waage, 1990; Stamps, 1994). Since aggressive contests are costly, mechanisms may have evolved to adjust defensive actions to the level of threat posed by the intruder should be favoured. It is known, for example, that territory owners may not be equally aggressive toward neighbors and strangers (Temeles, 1994). This is characterised by two contrasting phenomena: 1) the one termed as "dear enemy" (Sensu Fisher, 1954), where territory owners display more aggressive behaviours towards strangers than towards neighbours, and 2) the “nasty neighbour” (Müller and Manser, 2007), where individuals are more aggressive towards their neighbours than towards strangers (Schradin et al., 2010). The dear enemy phenomenon is thought to occur because of the familiarity of neighbouring individuals (the relationship to one another is settled) or because of the lower threat level of neighbours (mate competition) as compared to strangers (mate plus territory competition); the nasty neighbour phenomenon, however, may occur mainly in group-living species in which competing neighbouring groups pose a higher threat for territory owners than itinerant strangers (usually single individuals) with a low capacity for competing for resources against structured territorial groups (Müller and Manser, 2007; Newey et al., 2010).

Additionally, the resources defended in territories may influence the magnitude of the owners’ aggressiveness against neighbours or strangers. For example, in breeding territories greater aggressiveness against strangers than against neighbours or breeding pairs has frequently been observed, while in feeding territories the opposite occurs; that is, the owners’ aggressiveness is shown to be higher towards neighbours than towards strangers (Temeles, 1990, 1994). It is thought that this is because in breeding territories the potential mate and territorial losses to strangers may be higher than potential losses to neighbours; while in feeding territories, an owner's potential losses to neighbours may equal or exceed its potential losses to strangers, as fluctuating food supplies may encourage neighbours to usurp portions of the owners' territories (Temeles, 1990, 1994). In addition, the context might influence defence of territory among neighbours. Some species display seasonal changes in the dear enemy effect, occurring in spring but not in fall, coinciding with seasonal changes in the social environment (Hyman, 2005; Palphramand and White, 2007). It is suggested that the dear enemy effect occurs especially during periods when potential threats to the long-term fitness of territory owners are greatest, such as during the breeding season (Palphramand and White, 2007). Lower aggression during the fall, as compared to summer, may also occur if males are more aggressive during the summer breeding season, when they have to defend both their territory and their paternity, while in the fall they defend only their territory (Hyman, 2005). In some birds, even males displaying the dear enemy effect all year round showed reduced tolerance towards neighbours based on their own mate's fertility status (Moser-Purdy et al., 2017).

Individuals of different sexes could perceive neighbours as a different type of threat; therefore, each sex could exhibit one of the two contrasting phenomena of territorial defence (dear enemy or nasty neighbour). The level of threat to the owners’ territory could be sex-dependent, as sexual reproduction is the result of the different adaptive strategies of the sexes, including different interests in the defence of resources that can be seen in their territorial defence. Males of many mammal species do not invest in their offspring via direct parental care, so their fitness is closely tied to the number of litters sired (Trivers, 1972), territorial defence being mainly focused on maintaining access to females and preventing access to reproductive competitors (Ostfeld, 1985). Usually, in mammals and other groups (e.g., arctic ground squirrel, Lacey and Wieczorek, 2001; collared lizard, Baird et al., 2001; white-bellied antbird, Fedy and Stutchbury, 2005), the males show higher aggressive behaviour in defending their territories than do females, especially when females are sexually receptive. Thus, resident males are highly aggressive towards male but not female intruders (Mus musculus, Palanza et al., 1996; Rhabdomys pumilio, Schradin, 2004). The dear enemy effect in male mammals has been demonstrated in several species, including Gerbillus dasyurus (Gromov et al., 2001), Mycrotus oeconomus (Rosell et al., 2008), Mesocricetus brandti (delBarco-Trillo et al., 2009), and the subterranean rodent Ctenomys talarum (Zenuto, 2010). Meanwhile, the nasty neighbour phenomenon has been found in male R. pumilio mice, where neighbours are the most important competitors for paternity, 28 % of offspring are sired by neighbouring males and only 7 % by strangers (Schradin et al., 2010).

Female mammals, however, use their competitive ability to acquire energy and nutrients in order to increase fecundity and the survival of the young, since female fitness is more dependent on food acquisition and the protection of the young (Trivers, 1972). Therefore, female territorial defence is expected to be mainly directed towards providing exclusive food access (Ostfeld, 1985) or protecting vulnerable offspring from potential risks, such as infanticides from conspecifics (Wolff and Peterson, 1998). Territorial females show more aggression and lower tolerance towards intruders (males or females) regardless of relatedness and familiarity, especially during pregnancy, lactation, and during the period when they are establishing colonies (Palanza et al., 1996, 2005). This low tolerance of females resembles to that of birds, where females respond more aggressively towards neighbours than towards non-neighbours during the courtship and chick rearing stages, which is the opposite of the dear enemy phenomenon (Circus cyaneus, Temeles, 1989, 1990; Anthornis melanura, Brunton et al., 2008). Additionally, in some mammals, a different tolerance towards neighbours between males and females has been observed. In Mus spicilegus, males respond less aggressively towards their immediate neighbours than towards more distant ones, while females tend to be more aggressive towards their immediate neighbours (Simeonovska-Nikolova, 2012).

In this study, we have explored territorial behaviour in the context of the dear enemy and the nasty neighbour effects in the Mexican volcano mouse (Neotomodon alstoni). This rodent is found in forests dominated by pines, firs, and oaks with an understory of bunch grasses (Davis and Follansbee, 1945). Little is known about the social structure of the Mexican volcano mouse. However, in lab experiments, this species exhibits a dominance hierarchy with intensive aggressiveness among individuals of the same sex, especially among males after mating (Granados, 1994; Granados et al., 1996). In addition, both sexes of this species exhibit parental care of litters and invest a similar amount of time in nest maintenance and vigilance (Granados, 1994; Granados et al., 1996; Luis et al., 2004). The evidence of parental care and reduced aggression levels observed in monogamous systems, suggests that some individuals may show the existence of a reproductive monogamy system, at least temporarily (Luis et al., 2004). In field conditions, spatial use studies have shown that the activity area of males is larger than that of females and it overlaps with the activity area of several (up to four) females (Canela-Rojo and Sánchez- Cordero, 1984; Rojas-Martínez et al., 2012). Findings on space use suggest that it is a social species that forms small related groups with a polygamous mating system (Rojas-Martínez et al., 2012), and that they could defend females to mating against other males. In addition, the size of activity area for both sexes is influenced positively by the reproductive activity, being more evident in males than females (Canela-Rojo and Sánchez- Cordero, 1984). Neotomodon alstoni presents a low overlap between activity areas (61 % among males, 47.3 % among females; Canela-Rojo and Sánchez- Cordero, 1984). The highest overlapping values of the area of activity in both sexes are reached during the spring (60.5 %), while during the summer is 20.7 %, and it disappears during the autumn and winter (Canela-Rojo and Sánchez- Cordero, 1984). These findings suggest that the defence of resources should differ between the sexes, which could be more related to the defence of the territory by males, with the objective of monopolizing reproductive couples. On the other hand, females would present the defence of the food resource, in order to ensure a successful breeding.

Since males of volcano mouse overlap their activity areas with that of several females, meanwhile females have low overlap with other females, and that activity areas of males and females is modified by the reproductive activity, allows to hypothesize that whether males and females differ in spatial organization then they will differ in territorial defence. We expect males to show agonistic behaviour against other males, especially against distant neighbours during the reproductive period, if they defend females against other unknown males, or conversely if they defend females against familiar males. Likewise, we expect females to display agonistic behaviour against other females, regardless the neighbour proximity. This may be true if they defend their food resources from unknown or, females can be expected to display agonistic behaviour against unknown neighbours (males and females), if they defend their litters from unrelated individuals, especially during the reproductive period. Thus, this study was directed to explore 1) whether spatial proximity between nearest residency sites of individuals is affected by the sex of the neighbours, and 2) whether males and females respond differently to distant or near neighbours (dear enemy or nasty neighbour effects), and in relation with the sex of the neighbours, in a wild population of Mexican volcano mice, during a reproductive and non-reproductive period.