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The evolution of territoriality in butterflies
Preface
In The descent of man, and selection in relation to sex (1871) Charles Darwin devoted a chapter to butterflies and moths in order to build up a body of facts and cases to support the theory of evolution through sexual selection. He gave plenty of examples of differences in coloration between males and females, and explained this by intersexual selection via female choice, but he also reflected on intrasexual selection through male-male conflicts:
“Although butterflies are such weak and fragile creatures, they are pugnacious, and an Emperor butterfly has been captured with the tips of its wings broken from a conflict with another male.”
-Charles Darwin (1871)
Darwin was not only one of the first to describe male-male contests in butterflies, but was also the first to give a possible explanation for the origin and maintenance of such peculiar behaviour. In fact, Darwin refers to the naturalist Cuthbert Collingwood who described frequent contests between butterfly males in Borneo, on a scientific voyage in 1866-1867. Collingwood (1868) expresses his frustration over the troubles to capture unharmed specimens as he writes:
“Another source of disappointment arose from the fact that not
infrequent, when one thought oneself fortunate in capturing a fine insect, after carefully disentangling it from the net, its wings turned out to be so torn and rubbed as to render it almost useless, except indeed as a decoy. This circumstance is due, I imagine, partly to their frequent battles with one another, in which they whirl round each other with the greatest rapidity, and appear to be incited by the greatest ferocity...”
-Cuthbert Collingwood (1868)
Ever since Darwin‟s and Collingwood‟s time, researchers and naturalists have recorded and studied interactions between males of butterflies. A noticeable part of their behaviour is also that males often are exceptionally faithful to specific patches, which they frequently guard from intruding males via aerial flight disputes, just like the ones described by Collingwood (1868). But despite numerous publications and excellent field studies over decades, there are a number of parts concerning the evolution of territorial behaviour in butterflies that have never been thoroughly investigated. There are also parts of territorial behaviour in butterflies that have received a lot of scientific attention, but that still puzzle researchers today. The aim of this thesis is to investigate the parts of territorial behaviour in butterflies that are still largely unknown, and thereby to shed new light on the questions that despite earlier studies, remain unanswered.
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Territoriality and mating success
Resources are not expected to be randomly distributed in the environment (Parker 1974) and selection will favour animals to search where the resources are concentrated. But what are the resources? In vertebrates the defended resources are sites associated with reproduction or areas that relate to both feeding and reproduction, i.e. a “home range” where both sexes maintain all activities, including reproduction. In insects, a vast majority of the defended resources relates to mating opportunities (Baker 1983). If receptive mates are patchily distributed in the environment it will be favourable to search in areas where the probability of encountering receptive mates is particularly high.
In butterflies, the way mates find each other can be divided into two categories: “perching” and “patrolling” (Scott 1974; Wiklund 2003). Males of patrolling species spend most of their time on the wing and actively search for receptive females. This strategy implies continuous flight, stopping only for feeding or when weather conditions make it difficult to fly. In a patrolling species the male typically detects females while he is flying, whereupon the male approaches the female and courts her. In perching species, the male remains stationary and applies a sit-and-wait tactic, resting at some vantage point, waiting for females to fly by. Here the female is the active and mobile part and if the female flies into the visual field of a perching male, the male will take off from the perching site and investigate the female. The couple will eventually alight whereupon the male starts his courtship ritual. The areas used by males as perching sites are often well defined and may correlate to some resource utilised by females, such as larval host-plants (Baker 1972; Courtney & Parker 1985; Rosenberg & Enquist 1991; Lederhouse et al. 1992) or female food resources (Suzuki 1976; Fischer & Fiedler 2001). However, areas used as perching sites may also lack any obvious correlation to female resources and consist of some topographical or physical structure such as gullies (Cordero & Soberon 1990), elevations and hilltops (Shields 1967; Lederhouse 1982; Alcock 1987) or trees and bushes (Wickman 1985a). Whatever the perching site may be, it is always expected to have a high flow of receptive females passing by.
Males of perching species are often exceptionally faithful to the perching sites and will attempt to exclude other males from the area. Consequently, males of perching species are often defined as territorial. The territories are thought to serve as a rendezvous place where the sexes meet and are expected to be located in areas where the probability to encounter females is particularly high. Consequently, territory residency is assumed to be correlated with high mating success. However, there are few studies that give empirical support for such a prediction (although see Wickman 1985b), and the consensus that territories are used as rendezvous sites is largely based on circumstantial evidence. In paper I we wanted to empirically test the hypothesis that territory residency in butterflies is correlated to high mating success. This would shed new light on the evolution of territoriality in butterflies, since higher mating success for territory owners implies a greater reproductive output and selection for such behaviour.
We used the speckled wood butterfly (Pararge aegeria) as a model species (figure 1a). P.
aegeria is one of the most frequently used species for studies in butterflies. Over the last
decades it has become something of a model species in butterfly research and used in studies on behaviour (e.g. Davies 1978; Wickman & Wiklund 1983; Shreeve 1984, 1986, 1987; Van Dyck et al. 1997a,b; Stutt & Willmer 1998; Kemp & Wiklund 2004; Kemp et al. 2006a,b), life history traits (e.g. Gotthard et al. 1994; Berger et al. 2008; Gotthard & Berger 2010) and climate change effects on the distribution of animals (e.g. Hill et al. 1999). Males of P.
3 forest floor (figure 1b, Davies 1978; Wickman & Wiklund 1983). If a flying object enters the sunspot area, occupied by a P. aegeria male, the resident male immediately takes off and pursues the intruder to investigate what the intruding object might be. If the intruder is a conspecific female, a flight pursuit follows. However, the nature of the flight pursuit is highly dependent on the mating status of the female. If the female is already mated the flight pursuit is ended after just a few seconds, often caused by the female doing a vertical drop into the vegetation. If the female is receptive the flight pursuit will be significantly longer (Bergman, M. unpublished). The female will conduct a rapid flight and the male will follow at a close distance behind. The couple will eventually alight in the vegetation, whereupon the male starts a courtship ritual. But if another male enters the sunspot area, the territory resident will take off and the two will engage in a flight contest (figure 1c), where the winner gets sole ownership of the sunspot and the loser leaves the area and has to search for a new suitable sunspot (Davies 1978; Wickman &Wiklund 1983).
(a) (b)
Figure 1: (a) A male of the speckled wood butterfly (Pararge aegeria) on an oak leaf. (b) A typical habitat for
P. aegeria - a deciduous forest in Ransvik, Kullaberg. (c) Two P. aegeria males in a territorial contest over the
residency of a large sunspot. Photo (a) and (b) by Christer Wiklund. Photo (c) by Martin Bergman. (c)
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There are surely several reasons why studies on mating success in butterflies are few, but it often comes down to the difficulties to observe natural matings in field. Typically females mate very soon after eclosion and a majority of the females in the wild are already mated (Wiklund & Fagerström 1977; Wiklund 2003). Studies on mating success require individual observation of unmated receptive females and, consequently, these studies require the release of laboratory-reared females. Another difficulty with studies of natural mating in butterflies is that in perching species mating does not necessarily occur in the territories (e.g. Bitzer & Shaw 1983; Alcock & Gwynne 1988; Brown & Alcock 1990). When a perching male detects a passing female the male flies up and investigates the passing female. The female response for this is usually a rapid flight, with the male in close association to the female. This can be a way for non-receptive females to avoid male courtship but can also be a way to test the male‟s ability. However, non-receptive females might also respond to the inspecting male by doing a vertical drop into the vegetation (Wiklund pers comm). In some species, such as Polygonia
c-album, Aglais urticae, Inachis io and Vanessa atalanta, the courtship phase is excessively
prolonged; the male follows the female for hours before mating is initiated (Wiklund pers comm). Consequently, matings occur somewhere away from the perching sites and this makes it virtually impossible to locate butterflies in copula. Thirdly, when a female and a male have alighted and copulate they are usually very cryptic and hard to find in nature. For the reasons mentioned above, the experiments here have been in large outdoor cages done using laboratory-reared butterflies (figure 2). The cages have been located at Kronängen, approximately 100 km south of Stockholm in central Sweden. The cages were semi-cylindrical, tunnel shaped and covered with a plastic green tarpaulin (figure 2). In the tarpaulin we had removed one large section (2 x 2 m) and several smaller sections (0.2 x 0.2 m) that created one large sunspot and a mosaic of smaller sunspots on the cage floor, this to create an artificial forest habitat that P. aegeria is naturally flying in (figure 3).
Figure 2: The experimental cages located at Kronängen, approximately 100 km south of Stockholm. Photo by Martin Bergman.
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The results from paper I showed that resident males had a higher mating success than non-resident males; non-residents achieved approximately twice as many matings as non-non-residents (figure 4). Territorial behaviour and defence of large sunspots are favoured through selection and the behaviour is thereby maintained in the population.
Although it was clear that resident males of P. aegeria had a higher reproductive output, it was not clear why. What is the possible mechanism that generates a mating success asymmetry between residents and non-residents? One explanation could be female choice and that females have a preference for male character traits that correlate to residency and the ability to win territorial contests. During the experiments in paper I we recorded rejections of courting males made by females and these data did not support the hypothesis that females
Figure 4: Mating success of resident and non-resident males, respectively, in 127 mating trials during which a female exercised mate choice between a resident male that controlled a 2x2 m sunspot territory and a non-resident male without sunspot territory or with a smaller sunspot. Values are given with a 95% CI.
Figure 3: The cages were covered with a plastic green tarpaulin prepared with holes to create a mosaic of sunspots on the cage floor. Photo by Martin Bergman.
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would have any preference for male character traits associated to residency; residents were rejected as often as non-residents. Another possible mechanism behind the mating success asymmetry could be that females actively search for areas where males can be found, i.e. large sunspots. Neither did we find any indications that this would be the case; females landed as often in small sunspots as in the large sunspot, where the resident male perched. Furthermore, the results also showed that virtually all male-female interactions were initiated by a perched male discovering a female passing by, and 63 % of the matings were preceded by the female being discovered when entering the large sunspot. This pattern could only be explained by female preference for large sunspot or that females are more likely to be discovered and successfully pursued by the male after flying through such sunspot. Since the former explanation did not have any empirical support in paper I, the latter explanation was more likely to hold true and warranted empirical testing.
Perching or patrolling?
The ways to locate mates vary greatly between species, but there are also examples of animals where the mate locating strategy varies within species (Krebs & Davies 1993; Andersson 1994). In species where the competition between males is strong and the ability to acquire matings is limited, males that lose contests with dominant opponents have to adopt a suboptimal strategy to acquire matings. Among insects subordinate males often adopt the role of a satellite in the vicinity of a dominant male and acquire matings by intercepting females on their way to a territory owner (Otte 1972; Cade 1980; Alcock 2005).
In butterflies, a perching mate locating strategy is often combined with territorial behaviour and defence of the perching site. When suitable territories are in short supply, males will frequently fail to gain a territory and these males are often described to adopt a patrolling mate locating behaviour, as an alternative mate locating strategy (Davies 1978; Shreeve 1987; Van Dyck et al. 1997a; Fischer & Fiedler 2001). However, it has not been clear whether males that have lost a territorial contest, adopt a patrolling strategy in the sense of Scott (1974), and become as mobile as a patrolling species and spend virtually all of their time on the wing in long continuous flights, in search for females. It could also be that males that have lost a territorial contest continue to search for a suitable territory and after losing a number of contests, settle in a suboptimal territory.
Several studies have observed both perching and patrolling behaviour in the same population of P. aegeria (see Davies 1978; Owen et al. 1986; Shreeve 1987; Jones and Lace 1992;Van Dyck et al. 1997b; Jones et al. 1998; Stutt and Willmer 1998; Van Dyck & Matthysen 1998; Merckx & Van Dyck 2005). However, the classification of P. aegeria males as patrollers is often based on snapshots of male behaviour, with short observations of males in field. In paper II we wanted to thoroughly study the mate locating behaviour in P. aegeria males and test the hypothesis that males adopt both a perching and a patrolling mate locating strategy. Since this requires long continuous observations we performed controlled experiments in large outdoor cages. This allowed us to follow individual butterflies for longer periods. By studying the behaviour of the same individual both before and after contests we could test if non-resident males, i.e. loser of territorial contests, abandon a perching mate locating strategy and instead adopt a patrolling strategy if suitable territories are in short supply.
The results from paper II showed that all males adopt a perching strategy when suitable territories are present. When a male was alone in the experimental cage, which contained only one large sunspot, the male spent approximately 90 % of the time perching in the large sunspot. Although resident males took off and performed shorter scouting flights, they were
7 locally stationary and spent virtually all their time in the same large sunspot, on the lookout for females. To study what happens when there are more males than suitable territories we introduced two males into the experimental cage and studied the behaviour of residents and non-residents respectively. Upon introduction, the two males engaged in a territorial contest over the sunspot territory. The winner became resident in the large sunspot and the male that lost the contest became non-resident. The non-resident increased the proportion time spent flying during a 20 minute period after the interaction (figure 5). From spending only 10 % of the time in flight when territories are available, non-residents increased their activity to spend approximately 60 % of their time in flight, immediately after a contest. However, after 20 minutes the non-resident gradually adopted a stationary and perching behaviour again (figure 5), but instead of perching in the large sunspot the non-resident alighted in a small sunspot. Forty minutes after the contest the resident and non-resident invested the same amount of time in flight activity, but with a vast difference in perching sites, while the resident perched in the large sunspot the non-resident perched in a small sunspot.
Figure 5: Time spent in flight by prospective residents and nonresidents, during the first 60 min period when only single males were present in the cage, and by residents and nonresidents during the last 60 min when two males were present in the cage simultaneously. Each bar indicates the mean ± SE for a 10 min interval.
From the results in paper II we can conclude that male P. aegeria invariably adopt a perching mate locating strategy when suitable sunspot territories are available. When territories are in short supply, males that fail to occupy large sunspots spend a short time in extended flight in search for another suitable sunspot. If there are no suitable territory sunspots available, the male eventually returns to a perching strategy, but instead of a preferred large sunspot he alights in a smaller, suboptimal sunspot, making the best of a bad job. Previous descriptions of male P. aegeria adopting a patrolling strategy are most likely
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based on too short observations and are thereby misleading. It is probable that earlier studies have recorded the behaviour of males in the exodus flight, which follows a male‟s failure to take over a sunspot territory from another male. Paper II underlines the importance of long continuous observations to fully understand the mate locating behaviour in butterflies.
Vision
Paper I showed that resident males had a higher mating success than non-resident males. Furthermore, from paper II we could conclude that non-resident males did not adopt a patrolling mate locating strategy, but utilized smaller sunspots as perching sites when larger sunspots were in short supply. The results from these two studies indicate that sunspot size correlates with reproductive success; perching in a large sunspot generates a higher reproductive output than perching in a small sunspot. The reason for this may be that large sunspots, but not small ones, represent suitable rendezvous sites for the sexes to meet. However, this implies that females prefer large sunspots rather than small sunspots and have a behavioral preference for locating and visiting large sunspots. But data on female dispersal from paper I did not support this hypothesis, females landed as often in large sunspots as in small sunspots. The mechanism resulting in a mating success asymmetry may also be that larger sunspots facilitate visual detection and flight pursuit of females passing by. In paper III we aimed to test the visual ability of perching males. But first we conducted a field study to confirm that our observations from the cage experiments, that male P. aegeria preferred large sunspots over smaller sunspots as perching sites, is also true in their natural habitat. To assess the characteristics of defended sunspots, we identified and measured sunspots that were used as perching sites by male P. aegeria, in the deciduous forest of Ransvik in southern Sweden. The characteristics of these sunspots were contrasted to sunspots that were not used as perching sites in the same area. The measurements showed that sunspots used as perching sites were significantly larger than sunspots not utilized by males. So now the question was: does a large sunspot enhance the ability to visually detect and pursue a passing object?
To experimentally test the male visual system we used an apparatus (figure 6) that allowed us to present a model butterfly to a perching male and that permitted us to control the pathway and speed of the model, making the presentations highly repeatable. This kind of method was used in some earlier, now classical papers, which investigated the visual abilities of perching male butterflies (Magnus 1958; Tinbergen et al. 1972; Douwes 1975). These studies demonstrated that the stimulus required eliciting an approach by a perching male does not have to be very specific. Indeed, numerous field observation have described how perching males in a variety of species respond to all kinds of flying objects, including heterospecific butterflies (e.g. Davies 1978; Lederhouse 1982; Shreeve 1984; Alcock 1985; Alcock & O‟Neill 1986; Alcock & Gwynne 1988; Rutowski 1992), other insects (Davies 1978; Lederhouse 1982; Alcock & O‟Neill 1986; Alcock & Gwynne 1988; Rutowski 1992; Van Dyck et al. 1997b), birds passing by (Meyer 1879; Proctor 1976; Lederhouse 1982; Bitzer & Shaw 1983; Alcock & O‟Neill 1986) and pieces of wood thrown over the head of the perching male (Alcock & Gwynne 1988; Kemp et al. 2006b). The experimental apparatus was mounted so that the butterfly model travelled in three different trajectories when it passed the perching male. The trajectories were selected so that the butterfly model was illuminated for 2 meters or 1 meter when passing the male, or not illuminated at all, passing just outside the sunspot. We also recorded the position of the perching male in the sunspot, to estimate the distance to the passing model.
9 The results from paper III showed that perching males are more successful in pursuing and intercepting a passing model when the model is flown through the sunspot. The males were also more efficient in pursuing and intercepting the model when the model was flown for a longer distance through the sunspot (figure 7). These results are based on experiments with an artificial butterfly model in a large cage, and so it might be relevant to address the issue of how this applies to a natural situation. In our experimental setup we varied the trajectory of the model and thereby the distance that the model was illuminated by the sun when it passed the perching male. In nature the time that a passing female is sunlit is likely to increase with the size of the sunspot used as perching site by a male. At a certain distance, when a female is passing a male that perches in a small sunspot, the probability that the female will be sunlit at all is small, and consequently the probability of a successful detection and pursuit by the male is low. If the sunspot is larger, the female will be sunlit for a longer time and the pursuit and interception of the female will be more successful.
Figure 7: The mean ± SE level of male response to the flying model when flown just outside, or 1 or 2 m through a sunspot in which a focal male was perched; the response levels were: (0) no response, (1) male takes off from the ground but does not pursue the flying model, (2) male takes off and pursues the flying model, and (3) male takes off, pursues and completes flight pursuit of the flying model
Figure 6: Schematic diagram of the model presentation apparatus as viewed from the side. In the trials the male would be sitting on the ground while the butterfly model passing by. The trajectory of the model was adjusted so that the model was sunlit for 1 meter or 2 meters when passing the perching male, or not sunlit at all, passing the perching male in the shade, just outside the sunspot.
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Another possible reason why males perch in large sunspots may be that the ability to detect and pursue a moving object is enhanced if the object is seen against the blue sky. It has been suggested that perching male butterflies should choose their perching sites to optimize the chance of visually detecting females against the blue sky (Rutowski 2000, 2003). During the experiments in paper III we estimated if the perching male was able to view the butterfly model against the blue sky as a background, behind the 2 x 2 meter hole made in the tarpaulin covering the roof. The data showed no effect of the background the model was seen against; males detected the model equally often when the model was seen against the blue sky as when it was seen against the tarpaulin cage roof.
From paper III we can conclude that male P. aegeria adopt territories in sunspots larger the average sunspot in nature and they do this because a large sunspot improves the ability to pursue and intercept receptive females passing by. This explains the mechanism that underlies the mating success asymmetry between residents and non-residents (paper I). Furthermore, this also implies that there is a variation in territory quality in nature, which correlates to the size of the sunspot.
Contest settlement in butterflies
Conflict over resources is a widespread phenomenon among animals and a prominent component of animal mating systems (reviewed in Huntingford & Turner 1987). The understanding of the evolution of animal conflict is now vast. But still some groups of animals continue confusing researchers, because of the difficulties to predict outcome of fights. Butterflies is such a group.
An essential part of animal conflict theory is that conflicts are solved due to an asymmetry in fighting ability, or resource-holding potential (RHP, Parker 1974). The individual that possesses the greatest RHP is expected to win a conflict with another individual. RHP is often strongly correlated to physical or morphological traits and nature is full of beautiful examples of traits meant to increase the fighting ability. Large body size, horns and antlers are all the result of selection for fighting ability and skills to acquire matings. However, not all animals that compete for mating opportunities via male-male conflicts show obvious morphological adaptations. In territorial butterfly species, males compete over mating opportunities by engaging in aerial flight contests, but seem to lack any obvious physical adaptations for fighting. What decides RHP in butterflies has been in researchers‟ focus over the last decades (reviewed in Kemp & Wiklund 2001).
Theoretical models suggests that conflicts can be settled due to the convention “resident wins, intruder retreats” (Maynard Smith & Parker 1976; Maynard Smith 1982), where the resident and intruder roles per se are used as arbitrary cues for a quick settlement of a contest, the so- called uncorrelated-asymmetry hypothesis (cf. Kemp & Wiklund 2001). Intuitively, this would of course be applicable to contest settlement in the seemingly weaponless group butterflies. Thus, in the 70s Nick Davies (1978) conducted a now classical field study where he tested the uncorrelated-asymmetry hypothesis by using males of the speckled wood butterfly (Pararge aegeria). He found that resident males always won contests with intruder males and interpreted the results as empirical support for the uncorrelated-asymmetry hypothesis. A few years after Davies‟ study, Wickman & Wiklund (1983) conducted another field study with P. aegeria as a model. In clear contradiction to Davies‟ (1978) results and in clear contradiction to the uncorrelated-asymmetry hypothesis, they observed several occasions when an original owner regained the ownership of the territory after a few minutes‟ absence. This kind of take-over of territories, where the resident is defeated by an intruder,
11 has later been confirmed in P. aegeria (Kemp & Wiklund 2004) and recorded in other butterfly species (Hernándes & Benson 1998; Kemp 2000). Kemp and Wiklund (2004) argued that Davies‟ results were most likely explained by the experimental procedure used by Davies (1978), where the individuals in the “intruder-role” were treated in a way that negatively affected their motivational level to engage in a territorial fight. Even though studies have shown that resident males do not always win contests with intruders (Wickman & Wiklund 1983; Kemp & Wiklund 2004), there is a clear consensus that residents generally are more likely to win contests (Kemp & Wiklund 2001).
Shortly after Davies (1978) published his study, it was challenged by Austad et al. (1979). They argued that the resident males could actually be better able persist in a contest because they achieve a higher body temperature when perching in a sunspot. This hypothesis was later empirically tested in P. aegeria by Stutt and Willmer (1998) and they concluded that individuals that were warmer could fly for a longer period and were therefore more likely to win a contest. However, this hypothesis was later tested and ruled out by Kemp and Wiklund (2004), since they found no differences in body temperature between residents and non-residents. Kemp & Wiklund (2004) argued that Stutt and Willmer (1998) in resemblance with Davies (1978) had handled their animals during the experiment in a way that affected their motivation to fight in a negative way.
Several of the possible hypotheses for contest settlement in butterflies have been empirically tested and often also rejected. But the most common, and perhaps the most intuitive, mechanism for contest settlement is still that an asymmetry in morphology/physiology decides who will win a contest. Several physical traits have been tested in butterflies but without any real consensus in how morphology/physiology affects contest outcome. For instance, in some species there is a positive correlation between body size and contest outcome, where larger males are more successful in territorial contests (Rosenberg & Enquist 1991; Martínez-Lendech et al. 2007; Peixoto & Benson 2008) while in other species the smaller males are the more successful ones (Hernándes & Benson 1998). However, there are also several species where body size does not affect contest outcome (Lederhouse 1982; Kemp 2000, 2005; Takeuchi 2006a,b; Paper I). Age has also been shown to influence the outcome of territorial contests, with older males having higher contest persistence in some species (Kemp 2002a, 2005) while younger males have an advantage in other species (Kemp 2003, 2005). Yet in some other species age has no or little effect on contest resolution (Kemp
et al. 2006a; Takeuchi 2006b; Paper I). The effect of fat reserves on contest outcome has also
been investigated but without any clear connection to contest settlement and individual RHP (Kemp 2002b, 2005; Takeuchi 2006b; Martínez-Lendech et al. 2007). Neither does wing morphology seem to be of importance for contest outcome in butterflies (Kemp 2002b; Kemp
et al. 2006b).
In paper IV we wanted to investigate a previously untested mechanism of contest settlement in butterflies. Motivational asymmetries are known to influence outcome in animal contests but has received surprisingly little attention in butterfly contest research. Theory suggests that residents will win frequently because they stand to gain a higher pay off if they are successful, due to the time and energy invested in establishing and defending the resource (cf. the ‟dear enemy‟ phenomenon, Temeles 1994). Residents might also win more frequently due to an information asymmetry, where the resident is better informed about the quality of the resource than the intruder. The resident then places a greater subjective value on the contested area and is prepared to fight harder for the resource than the intruder is (Enquist & Leimar 1987). Kemp & Wiklund (2001) argued that the latter might be potentially relevant in butterflies.
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Resident males could conceivably assess the value of the contested area if there are reliable indicators of the potential rate of encountering receptive females. Such indicators could be the encounter frequencies of females or conspecific males (Kemp and Wiklund 2001).
To investigate the motivational asymmetry hypothesis we staged contests between males of P.
aegeria in the large outdoor cages at Kronängen. After the dominance relationship was
settled, with one male being the resident and the other male the non-resident, we removed the resident male from the cage. The non-resident male was now allowed to either interact with a female for 30 minutes, or spent 30 minutes alone in the cage. When we reintroduced the resident male, after a 30 minute absence, we found that the non-resident males that had interacted with a female for 30 minutes were now more motivated to persist in a territorial contest and more likely to defeat the original resident, reverse the contest outcome, and now become dominant (figure 8). By introducing females into the sunspot territory we manipulated the value of the resource and affected the motivational level in the males to a level that allowed them to defeat their previous superior opponent
When we removed the initial resident from the large sunspot the non-resident claimed the sunspot territory within minutes. However, there was some interesting variation in the length of time it took before the initial non-resident perched in the large sunspot. We found that in the female encounter group, males that were particularly fast in taking over the vacant sunspot territory were also more likely to later reverse the contest outcome. This might reflect a variation in intrinsic motivation and we contend that this intrinsic motivation is reflected in the eagerness to take over vacant territories.
In the experiments in paper IV not all trials in the female encounter group resulted in a reversed contest outcome. This implies that other asymmetries, in addition to the female-encounter-based motivation asymmetry tested here, influence contest outcome in butterflies. Since there are no strong effects of asymmetry in intrinsic fighting ability based on morphological/physiological factors, and since both males were naïve with no contest experience, we contend that an intrinsic motivation state can have a profound influence on contest outcome. In the trials where the contest outcome was not reversed, it is likely that the asymmetry in intrinsic motivation was simply too big, and a 30 minute interaction with a
Figure 8: The outcome of contests between males of P. aegeria during the second contest period when the original winner had been reintroduced, and after the original losers had either interacted with a female during 30 min (female encounter group) or been alone for 30 min (control group); „reversal‟ (open bars) denotes that the male that lost the contest during the first contest period reversed the outcome and won the contest against the original winner in the second contest period, and „no reversal‟ (filled bars) denotes that the same male won in both contest periods.
13 female was not enough to manipulate the motivation to the extent that it reached a reversal in contest outcome (figure 9).
Figure 9: A model of male‟s motivation to persist in territorial contests. Each male has a given level of intrinsic motivation. But the level of motivation can also be affected by extrinsic factors, such as encounters with females, and become higher or lower than the intrinsic motivational level. (a) When the trial ended in a reversed contest outcome the non-resident‟s motivation was manipulated to be higher than the resident‟s intrinsic level of motivation. (b) When the trial ended with the same outcome the asymmetry of intrinsic motivation was too big.
The results in paper IV are the first study to empirically show that motivational asymmetries are an important component in contest settlement in butterflies. The role of motivation is a new and interesting approach in the extended and puzzling research field of butterfly contests and we contend that motivational asymmetries may be a key factor in other systems.
Female behavior
Mate locating behavior of males is very much dependent of the distribution of receptive females. A mating system is really the interaction of male behavior and female behavior (Wickman & Rutowski 1999). This is especially true in perching species, where the females are the mobile part and the males remain stationary. Consequently, the areas utilized as perching sites are ultimately decided by the dispersal of females. Although several authors have stressed the importance of female behavior when studying mate locating behavior in males (e.g. Rutowski 1991; Rutowski et al.1996; Wickman & Rutowski 1999, Kemp 2001; Wiklund 2003), there are relatively few studies of female behavior in relation to male territoriality. The reasons for this may be several, but one is the fact that most females in the wild are already mated and studies of the behavior of receptive females require the release of laboratory-reared animals.
Although there is a lack of empirical studies on female behavior, earlier publications have indicated that females have sophisticated adaptations to optimize their reproductive success. Researchers have observed and investigated courtship solicitation behavior, where virgin females and females in need of a fresh spermatophore, actively pursue males or behave in a highly conspicuous way (e.g. Rutowski 1980; Rutowski et al. 1981; Wiklund 1982; Wickman 1986, 1992; Wickman & Jansson 1997; Hiroki & Obara 1998; Daniels 2007). The theory of sexual selection suggests that females are expected to behave in a way so as to minimize time spent unmated, in order to maximize time for ovipositing. In paper V we wanted to test the
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hypothesis that virgin and mated females behave differently, with the prediction that virgin females behave in a more conspicuous way, as a way to acquire matings. Furthermore, since the adult life of a butterfly is highly time-limited, age is expected to have an effect on mate locating behavior in females. As the cost of being choosy increases with increasing age, older females are expected to be less choosy and more willing to mate. Therefore, in paper V we also tested the effect of age, with the prediction that older females would behave more conspicuously than young females. We conducted experiments in the cages at Kronängen where we studied female behavior for 20 minutes in young and old, mated and virgin females. The results from paper V showed that females behave in a way that is consistent with the idea that females are selected to minimize time spent unmated; older virgin females are more active and spend more time in flight, and make more individual flights than mated and young virgin females, and so behave more conspicuously (figure 10).
But we also wanted to test what possible consequences a higher activity can have. The prediction and the intuitive result would of course be that the increased activity of older virgin females leads to a faster detection and mating by a male. To empirically test this we introduced a male into the experimental cage and after he settled in the large sunspot we introduced a female and recorded the time it took until the male detected her. As predicted, males discovered virgin females faster than mated females (figure 11).
Figure 10: The percentage of time spent flying by females of the speckled wood butterfly,
Pararge aegeria, during a 20 min
trial. Values are given as mean ± 95% confidence intervals.
15
Figure 11: The difference between mated and virgin females in the probability of being detected by a male. If the female remained undetected for 1800 s (30 min) the trial was ended.
If females in a territorial species adjust their behavior to minimize time spent unmated they would be expected to search for areas where males can be found. In P. aegeria this would mean a female preference to visit large sunspots. The results in paper V did not support this prediction; virgin females did not alight more often than mated females in large sunspots. Hence, females adjust their behavior only by an increased activity, but with the clear consequence of a fast encounter with a male. From paper V it also stands clear that a vast majority of male-female interactions are initiated by a female being detected and pursued by a male perching in a large sunspot. This confirms the results from paper I, that residency increases the probability of encountering a female. The results also confirm that the main strategy for males to acquire matings is to perch (cf. paper II), since 90 % if the interactions were initiated by a female being detected by a perching male.
The study in paper V is novel, since it demonstrates how females adjust their behavior in accordance to both mating status and age, as a strategy to encounter mates. This study also stresses the importance of the distribution and behavior of receptive females to fully understand the mating system of a species.
16
Conclusions
Males are expected to search for females where they are likely to be found. Females of P.
aegeria fly in open forest habitats and visits sunspots on the forest floor for thermoregulatory
reasons. The predictability of female behavior encourages males to search in sunspots. Indeed, males are found in sunspots on the forest floor, on the lookout for females visiting the sunspot (paper I-V). However, males are only found in sunspots above a certain size as they only perch in sunspots larger than the average sunspot on the forest floor (paper III). This behavior is maintained by a mating success advantage, where using large sunspots instead of small sunspots as perching areas generates a higher reproductive output (paper I). The mating success asymmetry is not explained by female choice or by a female preference for large sunspots per se (paper I, IV), but rather the large sunspot facilitates visual performance of perching males and improves flight pursuit and interception of females (paper III). Territorial contests between P. aegeria males are not settled due to an obvious morphological/physiological asymmetry (paper I), as is common in many other animals. Rather, variation in resource value and motivational asymmetries are important for settling contests (paper V). Males of P. aegeria use a perching mate locating strategy. The perching/patrolling dichotomy ultimately relates to how matings are initiated. Even though it is most likely that some matings are initiated by a flying male detecting a female in flight, or even that a flying male detects a resting female, there is no doubt that a vast majority of male-female interactions (paper IV) and matings (paper I) are initiated by a perching male detecting and intercepting a flying female. In addition, the fact that both resident males and males that recently have lost a contest spend approximately 90 % of their time perching (paper II), strongly indicates that this is the main way for finding females.
A keystone in the evolution of territoriality in butterflies is a predictable distribution of receptive females. If the distribution of females is predictable, and the choice of perching site affects mating success, selection will favor exclusion of other males from the area and territoriality is likely to evolve. The quality of the perching site/territory is determined by the physical features of the site, how it affects a male‟s ability to visually detect and pursue receptive females. Since mate location in butterflies is almost exclusively based upon vision, physical features of territories that facilitate visual detection of females should correlate with territory quality in most perching species. But the quality of the perching site is also highly affected by the rate of butterflies that enter the territory. The inflow of other butterflies clearly affects the male‟s subjective assessment of the territory and creates an information asymmetry between a resident and an intruder, and often the resident puts a higher subjective value on the territory, based on his female encounter experiences. The physically based territory quality, in the case of P. aegeria, the size of a sunspot, may also have an influence on the subjective assessment and valuation of a territory and only further studies can evaluate how physical traits of a territory affect mate motivation to persist in territorial contests. Female-induced motivation is, however, not the only mechanism for contest settlement in butterflies, and a physical territory quality induced motivation might be a part of the explanation. An individual intrinsic motivational level might also be an important part in understanding contests in butterflies. How variation of this intrinsic motivation is shaped and why it exists is an attractive field for future research on territoriality in butterflies.
17
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22
Territorialitet hos dagfjärilar
Hos flera av Sveriges dagfjärilsarter är hanarna territoriella och etablerar revir på bestämda utkiksplatser. Dessa ställen används som mötesplatser för honor och hanar, och de skyddas från inkräktare genom intensiva reviruppgörelser där hanarna utmanar varandra i flygdueller. Kunskapen om hur detta beteende har uppkommit och hur det bibehålls har länge varit bristfällig. Likaså har kännedomen om hur revirstrider avgörs och vilka egenskaper som utmärker en vinnare i fjärilsvärlden under lång tid varit knaper. Här presenteras aktuell forskning om territoriellt beteende, parningsframgång och revirstrider hos fjärilar. Studierna är utförda med kvickgräsfjäril Pararge aegeria som modellart.
Att på ett effektivt sätt finna en partner är av största vikt för en dagfjäril. Med en livslängd som fullvuxen fjäril på en till två veckor är tiden knapp. Hos dagfjärilar kan man identifiera två huvudsakliga sätt på vilka hanarna finner honor. De kan antingen använda sig av en
patrullerande eller en stationär strategi (Scott 1974). Patrullerande hanar spenderar största
delen av sitt liv flygande och rör sig över stora områden i sin jakt på honor. En stationär hane tillbringar istället största delen av sin tid med att sitta och vänta på att en hona ska flyga förbi. Om hanen väljer en stationär eller patrullerande strategi är ofta artspecifikt. Dessutom väljer närbesläktade arter ofta samma strategi. Alla svenska arter i familjen vitfjärilar (Pieridae) är patrullerare, medan alla svenska arter i underfamiljen vinterpraktfjärilar (Nymphalinae) är stationära. En stationär hane rör sig över ett begränsat område, och även om kortare inspektionsrundor är vanliga återkommer han ofta till sin utkiksplats och fortsätter sitt spanande efter honor. Skulle en annan hane närma sig en utkiksplats som redan är upptagen flyger den sittande hanen upp, och de två inlåter sig i en revirstrid i luften. Vinnaren får tillgång till utkiksplatsen, medan förloraren tvingas lämna området och söka vidare efter en annan lämplig utkiksplats.
På vilka platser det är fördelaktigt för en hane att söka efter honor bestäms av honornas beteende. Stationära hanar etablerar utkiksplatser där sannolikheten att träffa på honor är särskilt hög. Det kan vara i nära anslutning till någon resurs som används av honan, t.ex. nektarväxter där hon söker föda eller värdväxter där hon lägger sina ägg. Skogslevande fjärilar behöver ofta uppsöka solfläckar för att värma sig, och för hanarna kan det därför vara fördelaktigt att söka efter honor där.
Även om man länge antagit att de stationära hanarnas utkiksposter fungerar som mötesplatser för könen, och att en bra utsiktsplats därför ökar innehavarens parningsframgång, har det empiriska stödet för denna hypotes länge varit svagt. Det finns flera tänkbara anledningar till detta, men en del av problemet är troligen de begränsningar som är förknippade med fältstudier. Fjärilshonor parar sig kort efter att de kläcks ur puppan, vilket betyder att de flesta honor man ser i fält redan är parade. Studier av parningar och parningsframgång kräver därför att man använder uppfödda fjärilar, där man kan garantera att honorna är oparade. Ytterligare en svårighet med att studera parningar hos just stationära arter är att de inte nödvändigtvis sker inom territoriets gränser. När en hona kommer inom en stationär hanes synfält flyger hanen upp. Därpå följer en mer eller mindre utdragen flygjakt, där honan flyger iväg med hanen tätt efter. När de två sedan landar och parar sig, ofta en bit därifrån, är paret vanligtvis mycket väl kamouflerat och svårt att upptäcka.
23 Av dessa anledningar genomförde vi beteendestudier under kontrollerade förhållanden i stora utomhusburar med kvickgräsfjäril (Pararge aegeria, figur 1) som modellart. Burarna (4 x 8 x 15 m) täcktes av en pressning med ett stort hål (2 x 2 m) och flera mindre hål (0,2 x 0,2 m). Syftet med hålen var att skapa ett artificiellt skogslandskap med en stor solfläck och en mosaik av mindre solfläckar på burarnas gräsbeklädda botten. Vi placerade även ut ett antal julgranar av plast för att ännu mer efterlikna en skogsmiljö. Hanar av kvickgräsfjäril etablerar revir i stora solfläckar som bildas när solens ljus tränger igenom trädskiktet. Där sitter de sedan och spanar efter honor som flyger förbi (figur 2).
Genom att låta två hanar göra upp om herraväldet över den enda stora solfläcken och sedan introducera en hona i experimentburarna kunde vi konstatera att de hanar som vunnit strider med andra hanar och innehade en stor solfläck fick majoriteten av parningarna (figur 3; Bergman m.fl. 2007). Därmed kunde vi empiriskt styrka den sedan länge förmodade men sällan testade hypotesen att utkiksplatser försvaras av hanarna för att de fungerar som mötesplatser för könen. En hög parningsframgång för de hanar som framgångsrikt lyckats försvara en solfläck gör att dessa hanars egenskaper blir bättre representerade i kommande generationer, och därmed bibehålls det territoriella beteendet i populationen.
Det stod nu klart att de hanar som utnyttjar stora solfläckar som utkiksplatser, och som framgångsrikt försvarar dem mot andra hanar, har hög parningsframgång. Däremot var det fortfarande inte helt klarlagt vad som orsakar dessa skillnader i parningsframgång. Man kan
Figur 1: Hane av kvickgräsfjäril (Pararge aegeria) sittande
på ett eklöv. Foto: Christer Wiklund.
Figur 2: Hane av kvickgräsfjäril (Pararge aegeria) sittande
i en solfläck på spaning efter förbiflygande honor. Notera även de slitna vingarna. Foto: Martin Bergman.
Figur 3: I ett experiment introducerades en
hona i en bur där två hanar var närvarande; en dominant hane som kontrollerade ett revir i en stor solfläck, och en hane utan tillgång till revir. I 65 % av de totalt 127 fallen parade sig honan med hanen i den stora solfläcken, och endast i 35 % av fallen fick den revirlöse hanen parningen. Punkterna indikerar sannolikheten att få en parning för en hane med respektive utan
revir. Värdena är givna med ett
konfidensintervall på 95 %.
