S28.1: Ecological consequences of social dominance in birds

Department of Biology, University of Oulu, POB 333, FIN-90571 Oulu, Finland, fax 358 8 5531227, e-mail ktkoivul@cc.oulu.fi

Sociality is considered to be a behavioural strategy that, compared to solitary life, reduces mortality risk or improves reproductive success of an individual group member. This is achieved through various mechanisms, that improve individual feeding success, avoidance of predation or reduction of both starvation and predation risks (e.g. Wilson 1975; Bertram 1978; Pulliam & Caraco 1984; Pulliam & Millikan 1982; Inman & Krebs 1987). However, flocking also has its costs. One such cost is competitive pressure arising inevitably from proximity of other individuals (e.g. Wilson 1975; Bertram 1978). When observing bird flocks (e.g. in feeding stations), it is quite easy to recognise that competitive pressure is not equal for all the flock members. In contests over space in feeder some individuals seem to be extremely successful while others seem to lose nearly all interactions. The second phenomenon that the observer soon notices is that contests only rarely escalate to the level of a physical fight. Instead, conflicts are most often solved peacefully, one party voluntarily retreating before actual fighting. It seems that birds are aware of their probability of winning or losing a possible physical conflict and modify their behaviour accordingly. Birds are said to have a ‘dominance system’ (Huntingford & Turner 1987)

In principle, the dominance concept applies to all situations where two or more birds come into competitive contact. However, most often the concept has been used to describe social structure in groups of birds, such as stable colonies, temporary aggregations at communal roosts, breeding colonies, family groups, mating aggregations and non-breeding flocks.

The non-breeding sociality that follows the territoriality and family life of the reproductive season is maybe the most conspicuous pattern in avian social organization. Evolution of sociality of this type and the significance of competitive interactions within winter flocks has been one of the main themes of avian behavioural ecology during the last decades (e.g. Wilson 1975; Bertram 1978; Pulliam & Caraco 1984; Pulliam & Millikan 1982; Inman & Krebs 1987). Because fitness during the non-reproductive phase is comparable to survival chances, starvation and predation risks are the phenomena, and food and shelter are the resources that are considered in most studies of non-breeding flocks and consequences of dominance interactions within them.

In the behavioural literature, the concept of dominance has diverse meanings (e.g. Wilson 1975; Gauthreaux 1978; Bernstein 1981; Kaufmann 1983; Drews 1993). Ornithologists conventionally use the term to describe observed or assumed persistent winnership in ‘agonistic interactions’ (Scott & Fredericson 1951) between flock members, potentially leading to resource monopolisation by the dominant party to the cost of the subordinate party (Drews 1993).

In practice, ecologists most often measure dominance in situations that are contests over some specific resources. Unlike some of us, birds do not fight for fun. Usually ornithologists build the hierarchies by arranging temporarily superabundant food sources in the laboratory or field, where agonistic interactions are expected at high frequency. Alternatively, interactions within free-roaming flocks are observed in natural conditions without predetermined contest situations; food or foraging opportunities can still be suspected to be the usual cause of fights, since birds usually are best observable when foraging. Usually dominance describes relations that are directly measured by observing interactions between individuals, but sometimes dominance refers to sex, age-class or species that dominates another. Further, sometimes dominance is not assessed using observed interactions but inferred from status signal ornaments, for example.

Demonstrations of rank-associated resource access as a consequence of dominance are in danger of circular argumentation. Apparent circularity is obscured by the common implicit interpretation that winnership in specific situations describes an individual’s general competitive ability, and that dominance systems inferred from specific individual encounters have predictive value in contests of other kinds, too. However, it may be best to use dominance to describe the ability of an individual to monopolise resources, and hierarchies as structural concepts describing orders in resource access. Hence, when talking about consequences of dominance we should talk about the ecological patterns and processes that result from resource access asymmetry (see also Wilson 1975, Gauthreaux 1978, Drews 1983).

In this presentation, my aim is to summarize briefly what kinds of rank-associated variation ornithologists have observed in access to the above-mentioned resources. I also summarize whether there might exist balancing costs of dominance (Rohwer & Ewald 1981) and whether differential resource access affects survival or reproductive success. I evaluate the evidence for effects on survival and also mention how rank-dependent resource access during the non-breeding phase could affect reproductive success. If competitive pressure severely constrains resource availability for subordinates and if ultimate fitness consequences exist, birds should be selected to respond flexibly to the social environment in their resource use strategies. This is another level of consequences of dominance that I consider. Finally, a third level of consequences should be observable in traits that determine social status: if ultimate fitness consequences exist, traits ensuring high social status should be strongly selected.

Potentially, competitive inequality and its consequences can show up whenever resources are not evenly distributed, and in fact, superior resource access of dominants has been witnessed for diverse resources.

Dominants have been shown to have prior access to preferred feeding habitats, which may be food rich patches (Slotow & Paxinos 1997) or patches containing high-quality food (Langen & Rabenold 1994). Even if all group members in principle have equal access to patches, dominants can interfere in the feeding success of subordinates (e.g. Krebs et al. 1972; Baker et al. 1981; Millikan et al. 1985; Pöysä 1988; Enoksson 1988; Richner 1989; Piper 1990; Keys & Rothstein 1991, Langen & Rabenold 1994). This has been observed using several currencies, such as time or food intake rate. At an extreme, despotism of dominants over food may become a form of kleptoparasitism (Rohwer & Ewald 1981; Lahti et al. 1998), a well-documented pattern e.g. interspecific contests in Larids. This form of exploitation has received surprisingly little attention although kleptoparasitism may be common whenever social birds consume high-value food items after extensive handling or a delay.

Another large set of studies describing resource monopolisation by dominants are those showing that both in space and time dominants monopolise the safest parts of the environment. In studies of habitat use, dominants displaced subordinates to sites where predation pressure was suspected to be high (Ekman & Askenmo 1984; Schneider 1984; Ekman 1987; Hogstad 1988b; Lens & Dhondt 1992; Piper 1990; Koivula et al. 1994). For example, finches feeding in open habitats prefer to feed near forest edges or bushes, possibly because their antipredatory behaviour includes use of vegetation as physical cover (e.g. Lima et al.1987). Dominants used the patches nearest the edges while subordinates were forced to use more open sites (e.g. Schneider 1984; Lima et al. 1987).

Maybe the most coherent set of studies of rank-dependent habitat and predation risk are of boreal tits. Dominant Willow Tits Parus montanus feed in the upper parts of the canopy and monopolise space near trunks, while subordinates use lower and outer parts of trees (Ekman & Askenmno 1984; Hogstad 1988a). Upper and inner parts are considered to provide the best protection against the most serious predator, the Pygmy Owl Glaucidium passerinum, a sit-and-wait ambush predator that makes short and descending strikes (Ekman 1986). In fact subordinate tits are overrepresented among Pygmy Owl prey remnants (Ekman 1986). Despite using outer tree parts, subordinate tits also leave the forest edges to feed in the openings more often than do dominants (Koivula et al.1994). Association between microhabitat segregation and competitive ability is clear, because after removal of dominants subordinates readily switch to use the upper and inner parts of the canopy and reduce their use of forest openings (Ekman & Askenmo 1984; Koivula et al. 1994). Interestingly, when the main predator changes, the habitat segregation pattern also changes. In a population of Willow Tits in Latvia, Krams (in litt.) observed that in contrast to northern conspecifics, dominant tits monopolised the lower parts of the canopy in young coniferous forests, and after removal of dominants, subordinates abandoned tree tops. Here the Sparrowhawk Accipiter nisus is the most abundant predator, and it follows edges of vegetation, making surprise attacks on birds outside cover. Hence, tree tops in dense and young forest stands can be considered dangerous for its prey (Krams in litt.).

Sometimes dominants do not take full advantage of their superior resource access but seemingly let the subordinates exploit the resources freely (Popp 1987; Senar et al. 1989; Ekman 1990). If family groups are involved, this is understandable since indirect fitness benefits can be achieved by aiding kin (e.g. Kortchal et al. 1993); but if non-kin groups are involved, such apparent restraint could reflect unstable dominance or that dominants for some other selfish reason temporarily abandon despotic behaviour.

Unstable dominance may result from fluctuations in underlying asymmetries (see Maynard Smith & Parker 1976). Value of the resources may vary temporarily or spatially, affecting individuals willingness to absorb the costs of fighting (Maynard Smith & Parker 1976). For example, in American Goldfinches Carduelis tristis and in Dark-eyed Juncos Junco hyemalis dominance may be reversed when motivation of subordinates increases, for example through food-deprivation (Popp 1987; Cristol 1992). In some species dominance is site dependent and switches in rank reflect site-dependent resource value asymmetries (e.g. Piper & Wiley 1989).

Alternatively, it is suggested that when foregoing despotic monopolisation of resources dominants somehow benefit from the presence of subordinates. For example, by being submissive dominants can ensure that subordinates survive or remain in the flock. This may allow dominants to enjoy important flock benefits such as advantages of many eyes in food finding or predator scanning (Senar et al. 1989). Subordinate flock members can also be valuable as potential mates. In fact, some species groups consist of mated pairs (Paulus 1983; Hepp & Hair 1984; Smith 1984; Ekman 1990; Thompson & Baldassare 1992) and dominant males are suggested act as subordinates in favor of their subordinate mates (Hepp & Hair 1984; Ekman 1990)

Ekman (1990) proposed that Willow Tit alpha males not only let the medium-ranked females take the best parts of the resources, but also protect them against interference by other males that outrank the females (see also Hogstad 1992, Lens & Dhondt 1993; Koivula et al. 1994). Because of protection, females that are usually mates of alpha males use protected feeding sites more than predicted from their rank (Ekman 1990; Koivula et al. 1994), they are not subject to aggression as often as predicted from their rank (Ekman 1990) and enjoy equal nutrition with the subordinate males despite their lower rank (Hogstad 1992). Unselfishness of dominant Willow Tit males is also manifest in their tendency to expose themselves during predator attacks by giving alarm calls more frequently than other social categories (Alatalo & Helle 1990).

Ekman (1990) suggested that the protective and submissive dominant male gets his investment back in the form of improved reproductive success in the next breeding season. In the event his female mate perishes, getting a replacement mate would otherwise be unlikely because of a prevailing male-biased sex-ratio (Ekman et al. 1981; Ekman 1990). Behaving submissively and protectively can be costly, but costs may be even higher if the male has no mate when breeding season starts.

Rohwer & Ewald (1981) suggested that dominance could involve costs that outweigh the advantage of resource access priority, resulting in equal net pay-offs for subordinate and dominant strategies. One such cost could be the repeated agonistic encounters especially in unstable dominance systems. Costs of fighting include for example increased risk of injury and time and energy loss (Rohwer & Ewald 1981). Also in stable dominance systems dominants have been shown to keep a higher metabolic rate and thus consume more energy than subordinates (Roskaft et al. 1986; Hogstad 1987b; Bryant & Newton 1994). This difference, however, exists only during active periods, and dominants do not necessarily suffer higher nighttime energy consumption (Reinertsen & Hogstad 1994). Bryant and Newton (1994) concluded that despite dominant Dippers Cinlus cinclus having higher metabolic rates than subordinates, the cost was small when compared with daily energy expenditure. Their view was that metabolic costs are unlikely to have a significant impact on energy balance or survival in Dippers.

One option for potential subordinates faced by extremely high costs of low status is to abandon local group life and seek conditions where the social environment is not so hostile. This may have several kind of consequences, for example in group dynamics and space use patterns (Ekman 1988; 1989) or even in latitudinal distribution of migratory birds (Gauthreaux 1982). This set of ecological phenomena is not, however, considered here in detail but instead, I concentrate on situation where flocking is for some reason the alternative chosen by subordinates, and examine the adaptations the birds use to cope with the competitive pressure caused by dominants.

It is possible that despite the dominants’ despotism, subordinates still can get a reasonable share of resources (e.g. Millikan et al. 1985, Richner 1989). For example, Millikan et al. (1985) concluded that despite the significant interference in foraging by dominant finches, subordinates were still capable of meeting their daily energy needs. In principle, subordinates can do this by increasing foraging effort at the expense of other duties such as predator avoidance. For example, subordinate Great Tits Parus major use less time for scanning for predators than do the dominants (Krams in litt.). Other possibility is that subordinates escape the interference by using risky microhabitats. That birds by this behaviour respond to restricted foraging opportunities is shown, for example, in feeding experiments of Hogstad (1988c), who found in Willow Tit that extra food increased vigilance time and also induced shift to utilisation of less risky microhabitats.

In addition to choosing to use unsafe habitats, subordinates can also choose to forage at times when dominants for some reason do not forage. Predation risk may vary also in time as well as in space. For diurnal birds predation pressure can be assumed highest during dawn and dusk because both diurnal and nocturnal predators are active in dawn and dusk and senses of day-active birds may be poorly adapted to dimness (Martin 1994; Lahti 1998). Lahti et al. (1997) found that dominant tits began their daily activities later and started roosting earlier than subordinates (Lahti et al. 1997). They also claimed that by extending ‘working days’ subordinates took more predation risk than dominants and thereby compensated for reduced access to food. This interpretation was strengthened by experiments where extra food induced shortening of daily activity in Willow Tits (Lahti et al. 1997). Similarly, Dark-eyed Juncos responded to experimental food-deprivation in the evening by starting their daily activity earlier the following morning (Lima 1988).

In addition to dawn and dusk, periods when a predator is visible or has just appeared can be considered to represent high-risk segments of the potential activity time. Some studies show that these periods are avoided by dominants, while subordinates seem to be less selective (De Laet 1985; Hegner 1985; Hogstad 1988b; Koivula et al. 1995). For example, Zanette & Ratcliffe (1994) observed that subordinate and middle-ranked Black-capped Chickadees Parus atricapillus that froze and hid after appearance of predator were the first to break cover while dominants hid longer. Waite & Grubb (1987) observed that Tufted Titmouse Parus bicolor subordinates were also the first to break the freeze. Waite & Grubb (1987), however, concluded that by this strategy subdominants gained only marginal foraging advantage. Also when Koivula et al. (1995b) presented predator models to captive tits, subordinates were the first to abandon hiding but only when their level of satiation was lower than that of dominants. This supports the possibility that early breaking of a freeze really functions to compensate for limited food access.

As when assuming higher predation risk to compensate for starvation risk, subordinates who are forced into unsafe microhabitats can decrease predation risk by investing more in antipredatory activities at the expense of foraging effort. In some species, subordinates dedicate more time to scanning their surroundings (Ekman 1987; Waite 1987), although this may reflect subordinates’ greater need to scan for dominant companions to avoid their aggression (Waite 1987).

Restricted access to food is most likely to cause reduced survival among subordinates during periods of limited food supply, exceptionally high energy needs, or when foraging is prevented by some accidental event. Because of such situations, birds store energy in their tissues, in their digestive tracts or as external hoards. Reserves are usually kept below the physiological maxima, implying that carrying them involves significant costs, such as decreased ability to escape predators or increased exposure to predation when acquiring reserves (review in Witter & Cuthill 1993). Provided that birds optimise their reserve levels by balancing the costs and benefits of fat load, fatness levels should increase with reduced food supply or increasing uncertainty over feeding conditions (McNamara & Houston 1990; Houston & McNamara 1993). The positive association between increasing uncertainty and reserve levels is supported by variety of observational, experimental and comparative studies (e.g. Ekman & Hake 1990; Witter et al. 1995; Rogers 1987).

In bird flocks existence of potential competitors may promote extra uncertainty in feeding conditions, and experimental evidence from starlings shows that reserve levels are higher when housed in contact each other instead of solitarily (Witter & Swaddle 1995). In dominance-structured flocks subdominants can be faced with higher uncertainty in feeding conditions than dominants. Therefore, if food resources do no limit the resource acquisition, subordinates are expected to carry more reserves than dominants (Clark & Ekman 1994). During the last years this idea has got wide support (Ekman & Lilliendahl 1993; Witter & Swaddle 1995; Gosler 1996; Hake 1996; Krams in litt.), although some studies have found the opposite, subordinates being heavier and carrying more reserves (Fretwell 1969; Piper & Wiley 1990; Lundberg 1985; Senar et al. 1992; Koivula et al. 1995b; Verhulst & Hogstad 1996). The difference between dominance classes can be more than marginal. For example, dominant white-throated sparrows are estimated to survive 50% longer than subordinates because of their higher fatness levels (Piper & Wiley 1990).

These results indicate that for some species and in some environments reserves are constrained by resource availability while in some instances they are not. Alternatively, variable fattening patterns may imply that strategic decisions with respect to social environment depend on other dimensions of the environment. Verhulst & Hogstad (1996) suggested that when rank-dependent predation pressure while foraging is high compared to rank-dependent acquisition rates, the optimal level of reserves is higher among dominants than among subordinates. The possibility of variable rank-dependent responses show up nicely in experiments of Ekman and Lilliendahl (1993) and Verhulst & Hogstad (1996). Using the same species and similar experimental design, these two works got opposite results. Both removed dominant birds from stable and small-sized tit flocks. Ekman & Lilliendahl (1993) observed body-mass decline among remaining subordinates, while Verhulst & Hogstad (1996) observed that removal of dominants was followed by increasing body masses among subordinates.

The above examples indicate that subordinates can to some extent flexibly take account of the social environment in their behaviour. At the level of individual decision-making subordinates may well minimise the joint risks of starvation and predation, but it is still possible that total risk of mortality is higher or that reproductive success is lower among subordinates than among dominants.

That subordinates do worse in terms of survival is nowadays a fixed part of textbook knowledge in behavioural ecology. This statement rests on large number of studies providing empirical support (Fretwell 1969; Baker & Fox 1978; Kikkawa 1980; Ekman et al. 1981; Smith 1984; 1994; Arcese & Smith 1985; Desrochers et al. 1988; Hogstad 1988c; 1989b; Koivula & Orell 1988; Piper & Wiley 1990; Ekman 1990; Lahti et al. 1998b; but see Bryant & Newton 1997). There is, however, a large imbalance between the generality accorded to survival effect and the quality and quantity of supporting evidence. Although the number of studies is large, the number of species in which the effect has been found is much smaller. Surprisingly, in most studies researchers have not controlled for even the most obvious confounding factors such as sex and age, although these correlates of rank are also well-recognised correlates of survival. Associations such as age, experience, sex and dispersal habits might well contribute importantly to the correlations between rank and survival. When most obvious interdependent factors have been controlled, a survival effect has still appeared in some species (e.g. Desrochers et al. 1988; Ekman 1990), but has not shown up in other taxa (Bryant & Newton 1997) or has been restricted to certain sex or demographic groups (Koivula et al. 1996). It is obvious that the dearth of proper evidence is a result of logistical difficulties: unless you are working with a highly sedentary species, simultaneous measures of social status and survival are nearly impossible. Even in sedentary species control of confounding factors and especially the effect of emigration is difficult. Hence, there is a clear need for further studies before one can make strong generalisations over the survival effects of dominance.

If studies describing association between rank and survival are few, reports on rank-dependent reproductive success are even more scarce. Here logistical problems surely have made it difficult to obtain data, but of course it may also be that non-breeding social status actually is a poor predictor of reproductive success as observed in some species (Koivula et al. 1996). Absence of dominance effect could be because contacts between flock members are no longer important when the birds prepare to breed. For example, it is possible that flocks break up relatively early in the non-breeding season. In fact, demonstrations of better reproductive success by dominants come from bird species forming permanent groups, where continuous interference by dominants is possible (e.g. Lambrecht 1986).

There are several possibilities for how non-breeding dominance might affect reproduction. In flocks where birds are in continuous contact which each other, they can acquire information on each other, which at least potentially enables non-random mating through female choice if dominants are preferred mates. In fact, there is some evidence that dominants are more likely to mate (Møller 1988; Brodsky et al. 1988; Komers & Dhindsa 1989; Orell et al. 1994) or mate earlier than subordinates (Møller 1988). Territory quality or some other factor associated with breeding resource quality or quantity is another possible route to better mating or breeding success of dominants. Some important resources for breeding may be acquired during the social phase and dominants may take the best parts of them (Arcese & Smith 1985; Møller 1988; but see Lemel 1989). For example, dominants may acquire a territory more easily or dominant males monopolising good quality territories may be more likely to become paired, as Arcese and Smith (1985) observed in Song Sparrows Melospiza melodia. In juvenile Black-capped Chickadees, high ranking birds gained more breeding territories than the low-ranking ones, who were forced to disperse and face poor breeding opportunities when the breeding season approached (Smith 1994). Still, Komers & Dhindsa (1989) showed that dominants may be preferred mates even without any concurrent variation in breeding resources (see also Brodsky et al. 1988).

Although evidence for fitness consequences of dominance is not very strong, significance of dominance in shaping ecological phenomena deserves attention not only among avian behavioural ecologists but also among ornithologists in other fields of ecology. At least in species in which survival effects have been witnessed, dominance may be a strong selective force shaping traits that are connected to determinants of dominance status. For example, if prior occupancy tends to correlate with dominance (Nilsson & Smith 1988; Koivula et al. 1993), traits such as timing of breeding, length of fledgling phase or timing of migration can be strongly selected (Nilsson & Smith 1988; Cristol et al. 1990). If resource holding power determines status and it is in turn determined by body size or condition, dominance can modify growth strategies or the optimal solution in the trade-off between offspring quality and quantity (Røskaft 1983). If mating status secures high status (Paulus 1983, Lovvorn 1989; Thompson & Baldassare 1992) or if resource access is dependent on mate's competitive ability (Ekman 1990) evolutionary consequences in mating behaviour can be predicted.

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