J Ornithol (2015) 156 (Suppl 1):S125–S132 DOI 10.1007/s10336-015-1233-2
REVIEW
Does social complexity link vocal complexity and cooperation? Todd M. Freeberg1,2 • Indrik ¸ is Krams1,3
Received: 1 November 2014 / Revised: 1 May 2015 / Accepted: 6 May 2015 / Published online: 20 May 2015 Ó Dt. Ornithologen-Gesellschaft e.V. 2015
Abstract In some avian species, individuals spend most of their lives in complex social groups. A recent hypothesis argues that social complexity will drive complexity in signaling systems. According to this hypothesis, individuals living in more complex groups (larger and with greater diversity of interactions) require larger and more diverse repertoires of signals, compared to individuals living in groups that are relatively simple in social structure. Social complexity has also been argued to be an important driver of social cognition and cooperation. Although many of these arguments have been based on empirical findings with non-human primates, similar evidence is beginning to emerge from avian studies. Here, we discuss some of this avian evidence, with an emphasis on two model species: Carolina chickadees, Poecile carolinensis (Paridae), and pied flycatchers, Ficedula hypoleuca. In Carolina chickadees, variation in the structure of chicka-dee calls influences behavior of receivers in pro-social and potentially cooperative ways in anti-predator and food detection contexts. In pied flycatchers, breeding individuals were much less likely to travel greater distances to assist in mobbing predators near their conspecific neighbors if those
Communicated by E. Matthysen. & Todd M. Freeberg
[email protected] 1
Department of Psychology, The University of Tennessee, Austin Peay Building 301B, Knoxville, TN 37996, USA
2
Department of Ecology and Evolutionary Biology, The University of Tennessee, Austin Peay Building 301B, Knoxville, TN 37996, USA
3
Institute of Ecology and Earth Sciences, University of Tartu, 51014 Tartu, Estonia
neighbors had failed to assist them in mobbing earlier. More research is needed to determine whether communicative complexity per se makes sophisticated social cognition possible, such as reconciliation and cooperation (and whether the latter might stem from reciprocal altruism or less cognitively demanding processes like conspecific by-product mutualism). Keywords Calling Chickadee Cooperation Flycatcher Signaling Social complexity Zusammenfassung Die Individuen einiger Vogelarten verbringen die meiste Zeit ihres Lebens in komplexen sozialen Gruppen. Eine aktuelle Hypothese argumentiert, dass soziale Komplexita¨t die Komplexita¨t in Signalsystemen beeinflusst. Nach dieser Hypothese sollten Individuen, die in komplexeren Gruppen (gro¨ßer und mit einer gro¨ßeren Vielfalt von Interaktionen) ein gro¨ßeres und vielfa¨ltigeres Repertoire an Signalen aufweisen im Vergleich zu Individuen, die in Gruppen mit relativ einfacher Sozialstruktur leben. Soziale Komplexita¨t wird auch als ein wichtiger Antriebsfaktor fu¨r soziale Kognition und Zusammenarbeit gesehen. Obwohl viele dieser Argumente auf empirischen Ergebnissen von non-humanen Primaten basieren, gibt es Hinweise auf a¨hnliche Aspekte bei Vo¨geln. Hier diskutieren wir einige dieser Belege, mit einem Schwerpunkt auf zwei Modellarten: Carolina chickadees, Poecile carolinensis (Paridae) und Trauerschna¨pper, Ficedula hypoleuca. Bei Carolina chickadees rufen Vera¨nderung in der Struktur des chick-a-dee Rufes Einflu¨sse auf das Verhalten der Empfa¨nger hervor, in prosozialer und potenziell kooperativer Weise, z.B. bei der Reaktion gegenu¨ber Pra¨datoren und im Kontext von Futtererkennung. Bei bru¨tenden Trauerschna¨ppern waren diese viel weniger bereit und na¨herten sich nur auf gro¨ßere
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Distanzen beim Mobbing von Pra¨datoren an, um Nachbarn zu helfen, wenn diese Nachbarn sie zuvor beim Mobbing nicht unterstu¨tzten. Mehr Forschung ist notwendig, um festzustellen, ob kommunikativen Komplexita¨t an sich erst anspruchsvolle soziale Kognition ermo¨glicht, wie Verso¨hnung und Zusammenarbeit (und ob diese mo¨glicherweise von reziprokem Altruismus stammen oder von weniger kognitiv anspruchsvollen Prozessen wie konspezifischen Nebenprodukt-Mutualismus).
Introduction Many animal species have diverse and complex communication systems (Bradbury and Vehrencamp 2011). The social complexity hypothesis for communication argues that species with more complex social groups require greater complexity in their communication compared to solitary species or species with simpler social groups (Freeberg et al. 2012). Social complexity is typically measured in terms of group size or in terms of the diversity of inter-individual relations within groups. Communicative complexity is typically measured in terms of repertoire size or the amount of information (in bits) within the signaling system. Furthermore, there is emerging evidence for cooperative behavior in a wide range of species—where individuals could act in ways that benefit only themselves in many situations, but instead act in ways that also benefit others (Raihani and Bshary 2011). Recent theory argues that social complexity is the key driving force behind both communicative complexity and social processes like cooperation (Krams et al. 2012). Species that are socially complex usually live in stable groups consisting of many members with high fission–fusion dynamics, or networks with diverse connections among individuals (Freeberg et al. 2012). Social complexity is thought to require a greater ability of individuals to produce and recognize a wider range of signals to cope with a higher diversity of social situations. Beyond this, the relationships that result from complex social groups are thought to make possible pro-social behavior like cooperation and reciprocity (Krams et al. 2012). In this review, we describe these arguments in more detail, and briefly review some of the empirical and experimental work that supports these arguments, with an emphasis on two species we have studied with regard to these questions: Carolina chickadees, Poecile carolinensis, that form small stable flocks of unrelated individuals during winter, and territorial pairs of breeding pied flycatchers, Ficedula hypoleuca, that can nest in high densities in which pairs frequently interact with other pairs.
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Social complexity and social cognition We start the discussion with the general idea of cognition in complex social groups. It is generally assumed that sociality evolves when the benefits of living in groups outweigh the costs of living in groups. Although we do not have strong evidence of benefits and costs of sociality for many systems (Silk 2007), it seems clear in some wellstudied systems that this general assumption is valid (Krause and Ruxton 2002; Bourke 2011). Compared to smaller social groups or to solitary life, larger social groups provide a greater ability to detect and defend against predators and competitor groups or species, as well as to detect and exploit important resources like food (Wilson 1975; Krause and Ruxton 2002). To exist successfully in a social group, an individual must be able to perceive and process the behavior of others, and predict their likely subsequent behavior (Brown and Brune 2012). Thus, it is crucial for individuals to be good at processing the cues and signals of other individuals. It is also crucial for individuals to be able to influence the behavior of other individuals through their signaling, to mediate changes in the signaler’s immediate environment that are beneficial to it, and perhaps also to other group members (Lestel and Grundmann 1999; Koops et al. 2014). Thus, sharing of food, coordinating group movement, and joining in an alliance with other individuals to overcome a more dominant rival, to name a few, are key behavior patterns important to many socially complex groups (de Waal and Tyack 2003), often facilitated through communication. An individual in a social group engages in a balancing act between individual- and group-level interests (Krause and Ruxton 2002). If individuals benefit from life in a social group, they generally should act in ways that maintain social group coherence. However, there will be numerous occasions where those same individuals can benefit from more selfish behavior that comes at the expense of other group members, and, therefore, at the expense of maintenance of the social group (Dugatkin 1997). For example, an individual that discovers a food source can signal in ways to attract group members such that those group members and the individual both benefit. However, that individual could also potentially forego signaling, such that it benefits, but its group members do not. Such an individual, and its signaling behavior, might furthermore be influenced by its recent history of interactions with other group members and whether they have acted pro-socially toward the individual. Balancing individual- and grouplevel needs is, thus, thought to be a cognitively demanding problem that individuals in social groups must solve. The first explicit arguments about social complexity selecting for increased cognitive ability addressed the
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cohesive and cooperative aspects of sociality (Jolly 1966) and the competitive aspects of sociality (Humphrey 1976). Increased social cognition, as discussed above, requires the ability to behave in a coordinated and potentially cooperative way with one’s group, but also to act competitively when it is to one’s advantage (Gingins et al. 2013). The basic notion about increased social cognition here is that it relates to problem solving abilities in the social domain. Individuals have to deal effectively with—and accurately predict the behavior of—a diversity of other individuals in their environment (Byrne and Whiten 1988). Social cognition relates to a diverse set of mechanisms permitting perception and processing of social stimuli, such as attention, memory, decision-making, recognition of diverse communicative acts, and understanding of third-party relationships. Complex cognitive processing in the social domain, such as third-party relationships and post-aggression reconciliation, is important in anthropoid primates (Cheney and Seyfarth 2007). Recent evidence reveals similar importance in socially complex avian species like parids (Kozlovsky et al. 2014, 2015) and corvids. Ravens, Corvus corax, vocally respond differently to playbacks of group members they have not interacted with for up to 3 years compared to unfamiliar individuals, and their particular vocal response also depends upon the nature of their relationship with that former group member (Boeckle and Bugnyar 2012). Reconciliatory behavior is also commonly seen in ravens among individuals that already have strong social bonds with one another, further suggesting a function for such behavior to repair damaged relationships (Fraser and Bugnyar 2011). Strong social bonds are believed to have adaptive value, and field studies of savannah baboons, Papio cynocephalus, revealed that females with stronger social bonds had higher infant survival rates than females with weaker social bonds (Silk et al. 2003). Such bonds may stem from two social contract-like processes. One process stems from reciprocity or exchange—one individual engages in prosocial behavior to help another at one time, and sometime later that second individual will pay back that behavior by engaging in pro-social behavior to help the first individual (Trivers 1971; Raihani et al. 2012). A recent study with vampire bats, Desmodus rotundus, carefully ruled out kin selection and harassment hypotheses to explain costly food-sharing behavior that is common in this species, finding such blood meal sharing to be due to reciprocity in complex groups specifically among socially-affiliated individuals that regularly groomed one another (Carter and Wilkinson 2013). The second social contract-like process stems from the need for alliances involving multiple individuals. One individual engages in pro-social behavior with another individual to build up a relationship that may be needed in times of future conflict with a third individual
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(Engh et al. 2005; DeScioli and Kurzban 2009). In alliancebased relationships, a first individual values a second individual because that second individual values the first. The importance of relationships between individuals with strong social bonds has been well described in humans and non-human primates (Silk 2002; Dunbar 2012; Seyfarth and Cheney 2012), and recently also in some avian groups like corvids and parrots (Emery et al. 2007). Future research should aim to determine whether individuals needing to contend with such within-group alliances use more elaborate and diverse communication signals than individuals that rarely or never face such within-group alliances. It has long been appreciated that complex phenomena can arise from complex mechanisms and processes, but can also arise from relatively simple mechanisms and processes (Page 2011). Complex behavioral patterns and complex cognitive processes, for example, may stem from relatively simple mechanisms of associative learning processed by relatively simple neural systems (Barrett et al. 2007). Nonetheless, a large and growing body of research is revealing the importance of social complexity to complex cognition in a wide range of species. This complex cognition appears to extend to the question of cooperation. We have tried to introduce these general ideas briefly in this section. We now turn our attention to the potential link between social complexity and signaling.
Social complexity and communicative complexity Why do we observe such incredible diversity in communicative complexity when we compare different species? What factors select for communicative complexity? Several hypotheses have been raised over the years to explain communicative complexity, including those having to do with sexual selection and those having to do with the diversity of predator types faced by a species (Oller and Griebel 2004, 2008). A recent hypothesis explaining communicative complexity is the social complexity hypothesis for communication (Freeberg et al. 2012). According to this hypothesis, species or populations forming complex social groups require more complex signaling systems than species or populations forming simpler groups. In a comparative study of a large number of species of non-human primates, the typical social group size was strongly positively associated with the size of the vocal repertoire, even after controlling for phylogeny (McComb and Semple 2005). As another example, marmot and squirrel (Sciurid) species that form groups with more social roles have more distinct alarm calls in their vocal repertoires, relative to species that form groups with fewer social roles (Blumstein and Armitage 1997; Pollard and
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Blumstein 2012). In the findings emerging from recent studies on this question, despite the diversity of measures used by researchers, increased social complexity is associated with increased communicative complexity—possibly to communicate a wider variety of distinct messages to conspecifics (Freeberg et al. 2012). Much of the research assessing potential links between social complexity and communicative complexity has been comparative. One study assessed the question using different flocks of the same species—Carolina chickadees, Poecile carolinensis (Freeberg 2006). The study had two parts, and tested the effect of flock size on the complexity of the key vocal signal used by birds in social interactions—the chick-a-dee call. The first part was an observational field study, in which flock sizes of chickadees were recorded and were classified in terms of whether the number of individuals present at the time of recording was large (three or more: Carolina chickadee flocks are frequently made up of four individuals) or small (one or two individuals). The set of chick-a-dee calls for each flock was coded for note composition, and the uncertainty of note composition (bits of information related to the diversity of notes being used in the calls) was determined (Freeberg 2006). Chickadees from larger groups had greater uncertainty in their chick-a-dee calls (that is, greater complexity of note usage and note orderings) than chickadees from smaller groups. The second part of the study was experimental, in that captive aviary flocks were generated to have two, four, or six individuals in each. Chickadees placed into larger flocks had greater complexity in their chick-a-dee calls than did chickadees placed into smaller flocks. This study, thus, provided the first experimental evidence in support of the social complexity hypothesis for communication. Although it is a relatively recent hypothesis, evidence from diverse taxonomic groups and from different signaling systems is emerging to support the social complexity hypothesis for communication (Freeberg et al. 2012). More complex social groups do seem to drive communicative systems with a greater diversity of signals. What might be the significance of that greater diversity of signals? In other words, what might be the function of the diversity and variation seen in signaling systems of species with complex social groups? We turn to some possible answers to these questions in the next two sections, where we review experimental studies we have conducted.
Communication and finding food Coordination at the group level is important in many socially complex groups for many reasons, including obtaining and defending important resources like food and
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territory. Such coordination may stem from cooperation and altruism (although, as we mentioned above, simpler mechanisms could also give rise to such behavioral patterns; see Barrett et al. 2007). Processes such as cooperation and altruism are generally thought to be more likely in complex social groups under standard evolutionary models, such as kin selection, byproduct mutualism, reciprocity, and game theory (Bshary and Bergmueller 2008). Frequently in social groups, a single individual might discover a food resource. In such situations, individuals of many species have been shown to produce vocal signals that can increase the likelihood of group members coming into the area of the signaler (Elgar 1986; Roush and Snowdon 1999). Recruitment of group members to the location of a food source can bring many potential benefits to the signaler, including increased vigilance against predators, but it may also serve a cooperative function among socially bonded individuals (Mahurin and Freeberg 2009). In some species, this vocal behavior in the context of newly-found food may relate to the complexity of social relationships within a group. For example, recent studies with chimpanzees, Pan troglodytes, played back approach calls of group members to individuals that had recently discovered food, and the food-finders were more likely to produce food calls when the approach calls were from group members with which they shared frequent affiliation interactions, compared to approach calls from more socially distant group members (Schel et al. 2013). This means that, at least in some socially complex species, individuals have some voluntary control over their signaling, and may communicate selectively in cooperative ways with group members with which they are more closely bonded. In some contexts, coordination in obtaining food seems more appropriately labeled collaboration. Collaboration with a partner to manipulate an apparatus with tools to obtain food, including the transfer of correct role-specific tools, has been demonstrated in chimpanzees (Melis and Tomasello 2013). Collaboration in a food-related task has also been experimentally demonstrated in spotted hyenas, Crocuta crocuta. The animals coordinated (temporally and spatially) in an experimental rope-pulling task to obtain food, and did so with little or no explicit training (Drea & Carter 2009). Similar findings were obtained while studying rooks, Corvus frugilegus, in a joint string-pulling task to obtain food; rook pair performance in the task was better the more socially tolerant the two individuals were with one another (Seed et al. 2008). Although these studies did not explicitly assess the signals and cues individuals used in interacting with one another to collaborate on these tasks, communication was clearly necessary for these tasks to be accomplished. There should be a need for communicative sensitivity to changes in social context, and an individual should quickly
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Fig. 1 a Carolina chickadees produce more ‘D’ notes in their chick-a-dee calls when they first detect food and before a flockmate arrives, compared to their calls after a flockmate arrives. b Playback of calls containing a large number of ‘D’ notes are more effective at recruiting chickadee receivers, compared to playbacks of calls containing a small number of ‘D’ notes. Data are presented as means (filled circles) and 95 % confidence intervals (whiskers). Data adapted from Mahurin and Freeberg (2009)
be able to adjust its signaling in light of those changes, for example, by changing signal type or the structuring/ ordering of particular signals used. This ability to adjust signals quickly has long been documented in avian species (e.g., Catchpole and Slater 2008), and recent evidence from playback experiments reveals a similar ability in Mexican free-tailed bats, Tadarida brasiliensis (Bohn et al. 2013). A field study involving individually-color marked Carolina chickadees tested whether individuals modified the note composition of their chick-a-dee calls when they first detected food, in a way to aid in recruiting flock mates. The first bird to arrive at a feeding station stocked with highly preferred seed produced significantly more ‘D’ notes in its calls before a flock mate arrived, compared to its calls produced after the flock mate arrived (Fig. 1a; Mahurin and Freeberg 2009). Playbacks of calls with a large number of ‘D’ notes were more effective at recruiting chickadee receivers to take seed from a feeding station near the playback speaker, compared to playbacks of calls with a small number of ‘D’ notes (Fig. 1b; Mahurin and Freeberg 2009). This study did not rule out the possibility that the sheer number of ‘D’ notes being played back, rather than the ‘D’ note composition of the calls, was the key factor explaining the shorter recruitment times for the ‘many D’ note playbacks (see Wilson and Mennill 2011). However, the study revealed that signalers can rapidly change the note composition of their chick-a-dee calls in the context of newlydiscovered food, and these changes to the calls of signalers can benefit receivers in the signaler’s flock. Individuals of a socially complex species, therefore, vary their vocal signals in ways that benefit group members in a context involving food. Whether they can do this in a different context is where we turn next.
Communication and anti-predatory behavior There is considerable evidence in social groups of alarm calling in response to the immediate threat of a dangerous predator and of mobbing-related calling in response to the presence of a dangerous predator that is not an immediate threat (Templeton et al. 2005; Micheletta et al. 2012). Additionally, recent evidence reveals that individuals call in strategic ways that communicate danger to group or family members, depending upon the type of threat or the perceptual experience of the potential audience. For example, Japanese great tits, Parus minor, produce distinct calls when avian predators are detected compared to when snake predators are detected, and playbacks of these calls to soon-to-fledge nestlings produce adaptive nest-fleeing behavior to snake predator calls but not to avian predator calls (Suzuki 2011, 2014). Siberian jays, Perisoreus infaustus, typically call when they detect a dangerous hawk predator, but they produce largely distinct calls to hawks that are flying, attacking in flight, or perched (Griesser and Ekman 2004; Griesser 2008). In both these cases, receivers of the particular vocal variant of alarm call being produced by the signalers are able to benefit from the signaler’s calling. In the case of Siberian jays, this behavior has real survival benefits for receivers, who are often genetically related to the signaler (Griesser 2013). Furthermore, heterospecifics (often members of mixed-species flocks with the signaler) can exploit and benefit from the call variation of signalers in these predator contexts (Templeton and Greene 2007; Randler and Vollmer 2013). In considering social complexity, researchers typically assess group size—larger groups are generally more complex than smaller groups (McComb and Semple 2005;
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Fig. 2 Pied flycatcher pair responses to predator stimuli presented near a neighboring pair’s nest box in the contexts of the neighboring pair’s distance (close *25 m; far *75 m) and whether the neighboring pair had earlier helped them mob a predator (cooperated) or had not helped them mob (defected). Each column of data is based upon data from 12 to 14 experimental pairs. Data adapted from Krama et al. (2012)
Freeberg et al. 2012). There are, however, other metrics of social complexity. Earlier we mentioned measures like social network complexity—the diversity of connections among individuals in a group. Another metric of social complexity involves territory size. In territorial species, for example, individuals possessing smaller and generally nonoverlapping territories are thought to be in a more socially complex setting in comparison with individuals possessing larger territories (Freeberg et al. 2012). Assuming similar movement rates, individuals possessing smaller territories will be experiencing neighboring conspecifics (as well as their signals and cues) at higher rates than individuals possessing larger territories. In effect, such small territories generate a richer social network of interacting individuals. As such, the social complexity hypothesis for communication predicts that species exhibiting smaller territories should have greater communicative complexity than species exhibiting larger territories (Freeberg et al. 2012). Although no comparative data exist to address the question (to our knowledge), might we expect to see cooperative behavior in species with small territories? A recent study tested this possibility with pied flycatchers, Ficedula hypoleuca, a species in which breeding pairs can nest closely with one another, and where individual signals can easily transmit across neighboring territories. Researchers presented predator stimuli near next boxes and then recorded whether neighboring territorial pairs came to assist in
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mobbing at another pair’s nest box (Fig. 2; Krama et al. 2012). When nest boxes were close together (roughly 25 m apart), a flycatcher pair aided in mobbing the predator model at a neighbor pair’s nest box whether that neighbor pair had earlier helped them mob or not. This suggests that mobbing behavior ‘in aid’ of a neighbor in these contexts, when a potential predator is close to one’s own nesting site, may be best understood as by-product mutualism—engaging in a behavior that appears to help another but that likely is self-beneficial. However, when nest boxes were farther apart (roughly 75 m apart), a flycatcher pair aided in mobbing the predator model at a neighbor pair’s nest box only if that neighbor pair had earlier helped them mob at their nest box (Krama et al. 2012). In experimental situations where the neighbor pair had been captured by the researchers and could not aid in mobbing at a pair’s nest box, the pair later was much less likely to travel the greater distance to help mob at the neighbor pair’s nest box. Thus, in these more distant nest box pairings, byproduct mutualism cannot explain the results—reciprocity seems the strongest mechanism to explain the findings.
Conclusions and future directions We have briefly reviewed a large, and growing, volume of literature related to social complexity, communicative complexity, and cooperation. Socially complex groups (including many primate and avian species) are predicted to be communicatively complex. Furthermore, such groups are predicted to exhibit complex cognitive processing ability in the social domain, including altruism and cooperation. For species that are highly vocal, an important potential means of cooperating is via calling behavior, and we have reviewed some of the work in bird species (primarily corvids and parids) that reveals how variation in vocal behavior by a signaler can benefit receivers—often members of the signaler’s flock. If this is true, then, increased vocal complexity that is driven by social complexity might facilitate complex social cognitive abilities such as cooperation. Alternatively, perhaps pro-social behavioral processes such as cooperation are simply part of the fabric of social complexity—one aspect of the rich nature of interactions and relationships within groups where individuals are socially bonded with one another. If so, cooperative behavior might be much more widespread in non-human animal groups than has been generally thought, and may be one of the features of social complexity that drive communicative complexity. Clearly we are at the beginning stages of being able to answer these questions, but the evidence that is emerging indicates this to be an exciting and important arena for future research. Our main goal here has been to try to make linkages
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between two lines of research inquiry that have rarely interconnected—tests of relationships between social complexity and communication on the one hand, and tests of relationships between social complexity and cognitive processes on the other hand. We hope that we have done these exciting topics justice in this brief review, and that we have raised many questions for fellow researchers. Finally, we hope that these ideas and questions will spur further research into potential links between social complexity, communicative complexity, and cooperation in avian species. Acknowledgments We thank the organizers of the IOC for accepting our proposal for a symposium on this topic, and are grateful to the presenters for their wonderful research presentations in the symposium. IK acknowledges the support of a Fulbright Research Award to work at the University of Tennessee during the writing of this manuscript. We thank David Book, Sheri Browning, Brittany Coppinger, Elizabeth Hobson, Amiyaal Ilany, Arik Kershenbaum, Steven Kyle, and two anonymous reviewers for helpful comments on earlier drafts of this manuscript. We thank Dr. Christoph Randler for the German translation of our abstract.
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