Behav Ecol Sociobiol (2008) 62:299–307 DOI 10.1007/s00265-007-0417-z

REVIEW

Sibling competition and cooperation in mammals: challenges, developments and prospects Robyn Hudson & Fritz Trillmich

Received: 24 April 2006 / Revised: 2 May 2007 / Accepted: 3 May 2007 / Published online: 31 May 2007 # Springer-Verlag 2007

Abstract Many vertebrates grow up in the company of same or different-age siblings, and relations among them can be expected to significantly influence individual life histories and the development of individual morphological, physiological, and behavioral phenotypes. Although studies in birds still dominate and have stimulated most theoretical considerations, the increasing number of mammalian studies promises to broaden our understanding of this complex field by enabling interesting comparisons with the rather different bird system. It therefore seems timely to bring together recent studies of sibling relations in mammals and to demonstrate what these can offer in the way of fresh insights. In this brief review, intended to accompany a series of papers on a diverse range of mammals, we outline the current state of sibling research in mammals, comparing it to the better studied birds. Most obviously, in mammals, mother and young are in much closer contact during early life than in birds, and siblings can influence each other’s development as well as the mother’s physiology while still in utero. During nursing, mammalian young also encounter a very different feeding Communicated by A. Schulte-Hostedde This contribution represents the introduction to the special issue “Sibling competition and cooperation in mammals”. R. Hudson (*) Instituto de Investigaciones Biomédica, Universidad Nacional Autónoma de México, AP 70228, 04510 Mexico, Federal District, Mexico e-mail: [email protected] F. Trillmich Department of Animal Behavior, University Bielefeld, PO Box 10 01 31, 33501 Bielefeld, Germany e-mail: [email protected]

situation to bird siblings. These contrasts should help stimulate further debate, as well as provide further opportunities to study the relative importance of maternal versus sibling effects on individual development. Finally, we discuss the need to balance studies of sibling competition and conflict with a consideration of the benefits accruing to individuals from sibling presence and the need for long-term studies of the influence of early sibling relations on individual development and life histories. Keywords Sibling conflict . Sibling cooperation . Mammals . Parent–offspring conflict

Introduction Many animals grow up in the company of same or different-age siblings so that relations among them can be expected to form an important part of their developmental environment. More specifically, sibling relations can be expected to play a significant role in shaping individual phenotypes, whether morphological, physiological, or behavioral. In shared developmental environments, competition for limited resources is considered a particularly important mechanism shaping developmental differences among siblings (Mock and Parker 1997). Interest in sibling competition began in earnest with the puzzling observation of obligate siblicide in several taxonomically diverse bird species (Procter 1975; Brown et al. 1977; Gargett 1978; O’Connor 1978; Stinson 1979; Cooper 1980; review in Mock and Parker 1997). Since then, the field has broadened considerably, both in the range of species investigated, including humans, and in the scope of questions asked (Mock and Parker 1997; Sulloway 1996, 2001; Borgerhoff-Mulder 1998; Stockley and Parker

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2002; Conley 2004; Mock 2004; Forbes 2005; Drummond 2006). It has also developed into an interdisciplinary enterprise where the interests and expertise of behavioral ecologists, sociobiologists, physiologists, psychobiologists, and developmental psychologists increasingly overlap. Presently, bird studies still dominate and have stimulated most theoretical considerations of the problems arising from parent–offspring interactions and sibling competition (O’Connor 1978; Parker and Macnair 1979; Godfray 1995; Mock et al. 1998; Brilot and Johnstone 2003; Kölliker 2005). The increasing number of studies in mammals, however, promises to broaden our understanding of this complex field by enabling interesting comparisons with the bird system where the laying of an egg finishes the direct physiological interaction between parent and offspring. Mammals represent a very different situation in which mother and young are in much closer contact during early life, and where siblings can influence each other’s development as well as the mother’s physiology while still in utero (O’Gara 1969; vom Saal 1989; Haig 1993). Furthermore, the provision of milk allows a physiologically more direct regulation of supply and demand between a mother and her offspring than is the case for feeding of the young in birds (Collier 1999; Neville 1999). While suckling, mammalian young interact closely with the mother who produces adjusted quantities of nutritionally adapted milk in response to offspring stimulation, often provides immunological support through antibodies contained in the milk (Peri and Rothberg 1986; Adamski and Demmer 2000; Zhou et al. 2000), as well as the thermal brood care that is similarly provided by bird parents. Thus, the very different feeding situation encountered by mammalian compared to bird siblings presents an interesting contrast that should help stimulate further debate on such general questions as the evolution of competitive and begging strategies. In addition, mammalian brood care and the specific influences of lactation offer further access to the study of the relative importance of maternal versus sibling effects on later life history as well as on the development of personality. The overwhelming importance of lactation in mammalian development and thereby the dominating role of the mother has led to a strong focus on the interaction between mothers and their litters as a whole (Rheingold 1963; Krasnegor and Bridges 1990), with little attention given to relations among siblings themselves. Similarly, studies of behavioral ecologists on mammals beginning with Trivers’ seminal paper (1974) have put more emphasis on parent– offspring conflict than on sibling competition (but see Stockley and Parker 2002 for a theoretical treatment). And finally, considering the system as a closed-loop feedback (Alberts and Gubernick 1990; Stern 1996), psychologist have traditionally focused on mother–offspring bonding and the role the mother plays in development so that

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particularly in studies of humans, mother–offspring studies dominate and studies of sibling influences on development are much rarer (but see Sulloway 1996; 2001; BorgerhoffMulder 1998; Conley 2004). Nevertheless, mammalogists have become increasingly interested in sibling interactions to the point that it now seems timely to bring together recent studies and to demonstrate what the field can offer in the way of fresh insights. This exciting development in mammalian research was particularly evident at two recent international meetings, the 2004 meeting of the European Animal Behaviour Societies in Groningen, the Netherlands, and the 2005 International Ethological Congress in Budapest, Hungary. Contributions at these conferences gave rise to the idea to bring together a series of papers demonstrating the wide taxonomic range of current mammalian research in this field (Drake et al. 2007: ungulates; Fey and Trillmich 2007: rodents; Bautista et al. 2007: lagomorphs; Hofer and East 2007, White 2007, Trillmich and Wolf 2007: carnivores). The resulting collection also provides interesting contrasts between species bearing precocial and altricial young as well as between monotocous species bearing one young and polytocous species bearing several young. Furthermore, the series combines examples of field studies and their possibilities for insight into the role of variable environments with studies on both wild and domestic species in captivity, offering the advantages of more controlled environments. The broad comparative approach represented by this series stresses the wide variety among mammals, as among birds, in mechanisms and functions of sibling relations and their interaction with parent–offspring conflict, and provides once more a salutary reminder that there is no "typical" mammal. In this introduction it is our aim to point out areas of investigation where mammals offer additional, even unique, possibilities for research on sibling relations, and to suggest questions that so far have not been addressed broadly. In this way, it is hoped that these considerations, together with the accompanying series of studies, will stimulate further empirical work and theoretical developments in the field.

Mammals: comparisons and contrasts Theory about sibling competition began with Trivers’ (1974) and O’Connor’s (1978) seminal papers and has since given rise to a whole host of sibling competition models, which for reasons of space we can only point to here (Macnair and Parker 1979; Parker and Macnair 1979; Mock and Parker 1997; Wright and Leonard 2002) mostly tailored with birds in mind (for contest competition, see Drummond 2006; scramble competition, Harper 1986; supply and demand models, Hussel 1988; Parker et al.

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2002; Royle et al. 2004; Kölliker 2005). These models of competition “compete” to a certain extent with models of honest signaling (reviewed in Godfray 1995) in parent– offspring interaction, and it is still far from clear which models best predict offspring behavior under the multitude of circumstances constituting sibling and parent–offspring interaction (Maynard-Smith and Harper 2003). Furthermore, the ecological circumstances favoring different modes of sibling competition are still poorly understood, although models have been suggested for particular cases based on closely related groups (herons, Mock 1985; boobies, Drummond 2001), and a recent review offers an integrated approach to understanding different systems of dominance in vertebrate broods and litters (Drummond 2006). Models treating more specifically the case of interbrood conflict have been developed by Parker (Mock and Parker 1997). Mammals may offer a fresh view on sibling competition and parent–offspring conflict as their interactions differ from those of birds. Siblings in a mammalian litter find themselves in a very different feeding situation from that encountered by birds. Jostling for a position at the teat is largely left to the young, and the mother—usually adopting a specific, largely immobile nursing posture—appears to have little possibility to favor or rebuff a specific offspring during a suckling bout. As milk ejection occurs simultaneously at all teats, the young have to end agonistic interactions to get milk when it becomes available. This may make honest signaling of need before and during feeding less relevant than in bird chicks where the parent feeds from a position that, at least in principle, allows a choice among offspring. Nevertheless, although most of the evidence is anecdotal, a similar situation may exist in carnivores at weaning where there is potential for differential treatment of littermates when parents start to bring food back to the den (Naidenko et al. 2004). A case is also presented by competition among different-age sibs or half sibs, where the mother may rebuff or favor either the younger or older offspring depending on her condition and environmental circumstances (Trillmich and Wolf 2007). A further complication for a general interpretation of mother-young and sibling interaction is presented by the difference in life history between precocial and altricial species. This major life history dichotomy may be reflected in systematic differences in sibling interactions, as precocial young seem to have more options and fewer constraints for coercing parents than less mobile and sensorily limited altricial young. There is presently little information on sibling interactions in precocial birds (but see Kalas 1977; review in Drummond 2006), a lack that may relate to the impression that since precocial birds largely feed themselves (except in specialized feeders like oystercatchers where food continues to be channeled through parents;

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Safriel 1981) they need not compete much for limited parental resources. However, this need not be so, particularly with respect to thermal resources. Small precocial mammals, just as precocial birds, are confronted with high metabolic costs of thermoregulation and small species can reduce these costs by huddling under the parent (Hill 1992). For the parent, it might be cheaper to provide this heat than to let the energy-limited offspring pay themselves. Similarly, proximity to the parent may be of vital importance in the face of predation. In mammals, most precocial species are monotocous and wean before arrival of the next young. However, as mentioned above, even in some of these species successive offspring may compete (Clutton-Brock et al. 1983; Trillmich 1986, 1990; Clutton-Brock 1991; Leippert et al. 2000; Trillmich and Wolf 2007). Furthermore, the precocial caviomorphs, for example the guinea pig, sometimes produce large litters, in which competition for maternal resources like milk and warmth may well play a major role early in life (Fey and Trillmich 2007), and in both birds and mammals, altricial young may compete among themselves for thermally advantageous positions within the litter or brood huddle (Alberts 1978; Webb 1993; Bautista et al. 2007). Lack of a sufficient comparative base, however, precludes broad generalizations at this stage about systematic differences in the mode and outcome of competitive interactions among siblings in altricials and precocials. Monotocous mammals offer an opportunity to look exclusively at interbrood competition without interfering intrabrood conflict. Continuing requests for maternal input by older offspring may interfere strongly with maternal effort directed to the next (potential) offspring (Fuchs 1982; Clutton-Brock et al. 1983; Trillmich 1986; Clutton-Brock 1991; Trillmich and Wolf 2007). In some mammals, including humans, lactation results in temporary suppression of the mother’s fertility (Simpson et al. 1981; CluttonBrock 1991; Banulis and Schlaff 1999; Stevenson 1999), and in kangaroos, in deferred implantation of the waiting embryo (Tyndale-Biscoe and Renfree 1987), thus influencing spacing of reproductive events for the mother and thereby potentially inducing parent–offspring conflict. Understandably, studies have concentrated on the usually more conspicuous, competitive aspect of sibling interactions in broods or litters. However, this seems to be an oversimplification since at the same time that offspring within a nest compete for limited resources they also provide an environment that enables normal development. This is perhaps clearest when considering the thermal requirements of chicks or pups of altricial species, which can only maintain an adequate body temperature if they huddle together (Hull 1973; Hill and Beaver 1982; Hill 1992; Blumberg and Sokoloff 1998; Bautista et al. 2003; Bautista et al. 2007). In these species single offspring

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quickly cool and may die directly from hypothermia or indirectly by no longer being able to stimulate further parental care (Stern 1996). Indeed, the thermoregulatory importance of brood- or littermates, particularly in early life, might also help explain why parents so often undergo the costs of producing doomed, supernumery young (reviewed in Mock and Forbes 1995). Additionally, sufficient stimulation of parents, be it via sucking in mammals or begging in birds, is vital for maintaining parental care and such stimulation can sometimes be achieved only by a group of siblings. Notable in this respect are the tricks cuckoo chicks have been proposed to play after eliminating the host brood; to maintain parental effort in feeding the single chick, the parasite simulates the begging sounds of an entire brood (Kilner et al. 1999). Cowbirds apparently follow the alternative strategy of allowing host chicks to survive to keep parental feeding rate sufficiently high to allow normal development and growth of the parasitic chick (Kilner 2003). Similar effects also occur in utero. Embryos may have to send strong signals to allow implantation and to maintain a pregnancy, and several fetuses may jointly create a sufficient signal in multiple pregnancies (Haig 1993). This applies particularly if mothers tend to abort small litters as in pigs (Polge et al. 1966), and continues when several offspring are needed to maintain maternal care later in life as shown for bears (Tait 1980; Dahle and Swenson 2003). An interesting variation is provided by egrets, which will abandon unprofitably small broods early in a breeding season in favor of a larger brood later on. Later in the breeding season, however, parents support small broods, as it is either a small brood or none at all (Mock and Parker 1986). Interesting here is that this may provide a check on the siblicidal behavior of the nestlings—if they kill a sib early in the season it may result in parents abandoning them. Such cases of sibling “cooperation” can perhaps be classified as byproduct mutualism (Dugatkin 2002) as benefits accrue to all members of the sibship (see also Bautista et al. 2007). Mechanisms Behavioral mechanisms of sibling competition have been studied in considerable detail in a variety of species (Mock and Parker 1997; Drummond 2006), but the physiological processes associated with such competition have only recently received attention (Fey and Trillmich 2007). Behavioral Behavioral mechanisms of sibling competition range from spectacular aggressive interactions, sometimes leading to siblicide, through various milder agonistic interactions, to

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scramble competition not involving overt aggression but which nevertheless can have indirect lethal consequences (Drummond et al. 2000; Bautista et al. 2005; Drummond 2006). In some cases these behaviors resemble territoriality, for example, where kittens, piglets and young hyraxes defend specific teats (Ewer 1959; Fraser and Jones 1975; Hoeck 1977; Drake et al. 2007), as well as possible negotiation among siblings in the absence of parents (Roulin et al. 2000). These struggles generally run their course without obvious interference by parents (but see Johnstone 1996; Lougheed and Anderson 1999; Naidenko et al. 2004; White 2007; Trillmich and Wolf 2007). One difference between birds and mammals in the way offspring interact with their parents is begging. Whether an individual attempts to make itself more obvious to a parent by giving visual and acoustic displays as in altricial bird chicks, or in attempting to approach a teat may make a big difference in the options of the parent to influence distribution of food among squabbling offspring (White 2007; Trillmich and Wolf 2007). A bird parent approaching the nest can in principle choose from which side to approach and who to feed a given morsel of food. In contrast, a mammalian mother such as a mouse, rabbit or guinea pig standing over a litter, or a cat or sow lying down to nurse has little possibility to influence sibling interactions (but see Trillmich and Wolf 2007). Thus, at least in relation to suckling, begging in mammals seems to be a group effort that induces the mother to take up the nursing posture rather than an individual attempt to obtain food directly—except for the cases of monotocous mammals where begging may even take the form of tantrums as in individual primate young (Simpson et al. 1981; Gomendio 1991; Hrdy 1999). Once the mother adopts an appropriate posture, sibling competition can run its course largely without maternal interference. It is then only at a stage when pups are fed solid food—as in canids—that actual begging behavior similar to that observed in birds is seen. Thus, food supply by mammalian mothers is largely regulated in a manner corresponding to the “restaurant hypothesis” (Algers 1993; Jensen et al. 1998) whereby the intensity and duration of suckling by the young will determine milk yield through a positive feedback on maternal physiology. Nevertheless, it remains unclear in what way short- and long-term need can be communicated by a litter in such a system if no obvious begging signals are available (Laurien-Kehnen and Trillmich 2003). Here mammalian young may have to depend on the feedback system provided by the mother’s lactational physiology to achieve their ends. However, it is not clear to what extent mammalian species in general correspond in their lactational physiology to the better studied primate (human), lagomorph (rabbit), rodent (rat) and ungulate pattern of milk flow

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regulation (Fraser 1980; Mena et al. 1990; Cameron 1998; Collier 1999; Neville 1999). Genetic In contrast to birds, there is no evidence so far of obligate siblicide in any mammal, at least postnatally. In pronghorn antelope, however, it is reported to occur prenatally (O’Gara 1969), and Forbes (2005) has also argued that humans meet the statistical definition for parental obligate brood reduction in twin pregnancies, although whether this is a result of sibling competition remains unclear. Consistent with theory, this may relate to the ability of mammalian mothers, via lactation, to provide a steadier flow of nutriments to their young (Dall and Boyd 2002) than is often the case in birds (Dall and Boyd 2004), thereby bridging nutritional bottlenecks, which might otherwise oblige littermates to kill sibs to ensure their own survival. Nevertheless, if mothers are unable to maintain a sufficient milk supply, competition among littermates may result in facultative siblicide (Hofer and East 2007; Trillmich and Wolf 2007). The genetics of parent–offspring and sibling interactions become highly complex in any case as siblings form a selective environment for each other as well as for their parent(s) and parents through brood care obviously represent an important component of the offspring’s environment (Mousseau and Fox 1998). Thus, there is selection going on among all of these players and coadaptation via linkage disequilibrium is to be expected in the long run (Kölliker 2005). Physiological Best documented are hormonal mechanisms. Notable is the deposition by mother birds of varying quantities of hormones, for example testosterone, in eggs (Schwabl 1993), the effects of which on development and sibling interactions are currently being keenly investigated (Groothuis et al. 2005). Similar effects have also been shown in mammals where the interaction between mother and offspring occurs in utero usually for a much longer period and may influence offspring phenotype quite strongly (Kaiser and Sachser 1998; 2001). Further, mammalian offspring are known to influence each others’ development in utero via the differential production of steroid hormones, best known being the masculinization of females by adjacent male embryos (vom Saal 1989; Zielinski et al. 1992). In all these cases, however, it is an open question whether the phenotypic changes observed are adaptive for the mother, for the offspring, for both or for neither. Although there is much speculation, hard data are lacking for mammals as well as for birds (see discussion in Groothuis et al. 2005).

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Sequential siblings or half siblings may also influence each others’ development. This is most obvious in marsupials where a young present in the pouch may delay the development of further offspring in utero by stimulating the production of prolactin, resulting in delayed implantation of the embryo in waiting (Tyndale-Biscoe and Renfree 1987; and Fuchs 1982; Eisen and Saxton 1984 for a similar phenomenon in rodents). However, in many other mammals, including humans, that produce overlapping litters or overlapping single young, negative effects on pre- and postnatal growth and survival of offspring associated with competition for the mother’s resources are also well known (reviewed in Hausfater and Hrdy 1984; Martínez-Gómez et al. 2004; see also Trillmich and Wolf 2007). Furthermore, mammals born in larger litters are generally smaller than those from smaller litters and grow more slowly since mothers do not seem to compensate fully with increased milk yield for the increased demands of a larger litter (Drummond et al. 2000; Laurien-Kehnen and Trillmich 2003). This implies slower development and sometimes catch-up growth after independence from maternal milk. Given that such catch-up growth is suspected to have negative long-term influences on health and fertility (Metcalfe and Monaghan 2001; Mangle and Munch 2005), it is unclear how growing up in a larger litter will influence life history. In this context, the physiology-life history nexus described by Ricklefs and Wikelski (2002) is important, as is the ‘thrifty phenotype’ hypothesis (reviewed in Bateson et al. 2004), which proposes that young growing up under nutritionally limited conditions may be better adapted metabolically to nutritional hardship in the future than those developing without such constraints. Given these considerations, it is surprising that so little investigation has been directed to the effects of litter or brood size and the concomitant competition among siblings on the stress-associated physiological state of the individuals (but see Naguib et al. 2004; Blas et al. 2005; Fey and Trillmich 2007) and the possible short- and long-term consequences on the immune system, metabolic rate, development of temperament (or personality traits), and later survival and fertility. Whether such stressors are necessarily negative or may imply beneficial levels of activation remains to be seen. Perspectives Increasing information on sibling relations in mammals and the possibilities this offers for comparison with the betterstudied birds raises many unresolved questions and promising research topics, and among them are the following. –

Are there systematic differences in the competitive strategies used and their outcome between well-armed

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young able to inflict serious injury (hyenas, seals, pigs, this special issue) and less well-armed young (rabbits, guinea pigs, this special issue)? Here, we expect evolutionarily stable strategy modeling to provide theoretical guidance as to when we might expect armed young to evolve and how we might expect armament to influence the form and outcome of sibling conflicts. Why do we sometimes observe maternal intervention (Naidenko et al. 2004; White 2007; Trillmich and Wolf 2007, and in humans) as originally predicted by the model of O’Connor (1978) and not in other cases? What are the circumstances—environmental and social— or life-history strategies that make such interference likely? Why does such behavior apparently not exist among birds where parents act as passive bystanders (but see Lougheed and Anderson 1999 for blue-footed boobies)? To what extent might parent–offspring interests be congruent given the potential for parental retaliation by curbing investment if siblicidal offspring make the brood less valuable to parents (Forbes 1993)? What are the benefits of having (same or different age) siblings? Despite the obvious potential for kin selection among siblings sharing a common nursery this aspect has been somewhat neglected in the literature in favor of the consideration of costly competitive and outright aggressive interactions (but see Kilner 2003; Bautista et al. 2003). However, from prenatal effects such as the need to have siblings to produce strong enough signals to maintain a pregnancy, to postnatal thermoregulatory efficiency or joint stimulation of parental feeding efforts, through to the benefits of sibling presence in later reproductive life, for example, by the formation of reproductively supportive matrilines or coalitions for hunting and territorial defense (Cheney and Seyfarth 1983; Caro and Collins 1987; Gilbert et al. 1991; Colmenares 1992; Gomper and Wayne 1996; Hrdy 1999), positive effects of sibling presence may be just as important and widespread as the effects of competition. In this regard, there is a need for long-term studies of the effect of sibling relations extending well beyond the period of parental dependence. Related to the above, is being bigger and more dominant necessarily better in life history terms or might siblings who occupied socially different nursery niches be equally successful in later reproductive life (see Drummond et al. 2003 for a possible example in blue-footed boobies), possibly by pursuing different behavioral and physiological strategies (for example, Bateson et al. 2004)? There is a need for the analysis of sibling effects not only among same-age individuals (twins, littermates), but also between successive litters or individual young of the same mother (interbrood conflicts). In this

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situation, the potential for conflict between mother and offspring seems most obvious and may help to provide examples of real conflict about fitness outcomes between mother and offspring (questioned, for example by Mock and Forbes 1992) in the sense of the original formulation of Trivers (1974). And finally, in relation to our own species, the effort to describe, classify, and explain individual differences in personality (temperament) is one of the principal interests of human psychology. Traditionally, the contribution of the early social environment to this complex process has focused on the role of parent– (particularly mother–) child relations, the work of Sigmund Freud being one (in-) famous example. However, interest among psychologists in the role of sibling relations is growing in recognition of the fact that in the large families typical of many societies and presumably of our evolutionary past, contact among siblings is at least as intense as that between parents and their children (Sulloway 1996; 2001; Conley 2004).

Acknowledgements We would like to thank Tatiana Czeschlick who enthusiastically took up the idea of producing this special issue and helped it along from the time of its conception, through gestation and to the final version. A. Schulte-Hostedde put a tremendous amount of work into editing this special issue and helped in many ways to see the manuscripts through the sometimes erratic process in a friendly and efficient manner. Robyn Hudson and Fritz Trillmich contributed equally and have been arranged in alphabetical order.

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