Wilkinson 2017 Non Kin Cooperation in Bats Review
R Soc Open up Sci. 2021 February; 8(2): 201927.
Non-kin adoption in the common vampire bat
Imran Razik
oneDepartment of Development, Ecology, and Organismal Biological science, The Ohio State University, 318 Due west. 12th Ave, Columbus, OH, USA
2Smithsonian Tropical Research Plant, Balboa, Ancón, Democracy of Panamá
Bridget Chiliad. G. Brown
iDepartment of Evolution, Environmental, and Organismal Biological science, The Ohio Country University, 318 Westward. 12th Ave, Columbus, OH, USA
iiSmithsonian Tropical Research Institute, Balboa, Ancón, Republic of Panamá
Rachel A. Page
2Smithsonian Tropical Research Plant, Balboa, Ancón, Republic of Panamá
Gerald Chiliad. Carter
1Department of Evolution, Environmental, and Organismal Biology, The Ohio State University, 318 W. 12th Ave, Columbus, OH, United states
iiSmithsonian Tropical Research Institute, Balboa, Ancón, Republic of Panamá
Received October 27, 2020; Accepted January 25, 2021.
Abstruse
Individual animals across many unlike species occasionally 'adopt' unrelated, orphaned offspring. Although adoption may be best explained as a by-production of adaptive traits that enhance parental care or promote the development of parental skills, one factor that is possibly important for the likelihood of adoption is the history of cooperative interactions between the mother, adopted offspring and adopter. Using 652 h of behavioural samples collected over four months, nosotros describe patterns of allogrooming and nutrient sharing earlier and afterward an example of non-kin adoption between ii adult female common vampire bats (Desmodus rotundus) that were captured from distant sites (340 km apart) and introduced to one another in captivity. The first female died from an illness 19 days after giving birth. The second female groomed and regurgitated nutrient to the mother more often than any other group member, then groomed, nursed and regurgitated food to the orphaned, female pup. The substantial increase in alloparental care by this female subsequently the female parent'south death was not observed among the 20 other adult females that were present in the colony. Our findings approve previous reports of not-kin adoption in common vampire bats and are consequent with the hypothesis that not-kin adoption can be motivated, in part, by a history of cooperative interactions.
Keywords: adoption, alloparental care, parental intendance, cooperation, vampire bats
1. Introduction
Animals are most likely to care for others' immature (i.eastward. alloparental intendance) in groups where members are related and helpers tin can gain indirect fettle benefits [1,2], equally in about cooperative breeding societies [3,4]. In some cases, alloparental care towards either kin or not-kin could also result in directly fitness benefits for the helper (e.g. group augmentation [five,6]). However, alloparental care tin can besides arise when non-adaptive, misdirected parental care [7–9] is triggered by a combination of rare circumstances, low costs of helping and/or imperfect kin discrimination [1,x].
I extreme class of alloparental intendance is the adoption of orphaned young. Adoption has been reported across 120 mammal species, including marsupials, shrews, primates, rodents, canines, ungulates, elephants, hyraxes, cetaceans and bats [1]. In some cases, individuals adopt kin, through which they might gain indirect fitness benefits [1,11]. In other cases, individuals adopt familiar non-kin (e.thou. chimpanzees: [12]; cercopithecines: [13]; muriquis: [xiv]; phocid seals: [15]), or unfamiliar or seemingly unfamiliar non-kin (east.g. dolphins: [16]; Barbary macaques: [17]; Rhesus macaques: [18]). In humans, the adoption of kin or non-kin children is well described in both traditional and modern industrial societies around the world [xix]. Whether or not adopting non-kin is adaptive remains unclear.
Non-kin adoption could be explained as a non-adaptive past-product of adaptive traits that enhance parental care or promote the evolution of parental skills. For instance, adoption might ascend as a by-product of traits that evolved to increase interest in conspecific young [1]. In several primate species, females oft appear interested in treatment others' infants and may even try to kidnap infants from other group members, which may be associated with reproductive seasonality or boyhood [13,twenty,21]. Given that determination-making is likewise imperfect and constrained, parents may face a trade-off between the cost of mistakenly providing occasional care to non-offspring and the price of failing to reply to signals of need from true offspring [1,22]. Nevertheless, although adoption may not be adaptive, it can be inherently rewarding to the adopter at the proximate level, equally in the man motivation to adopt unrelated children [nineteen]. The cognitive and neuroendocrine mechanisms that underlie parental care are an inherently interesting discipline, and detailed accounts of adoption in different species can shed light on the shared proximate factors that motivate the decisions of individuals to adopt non-kin young.
1 possible, yet understudied, factor influencing not-kin adoption is the history of cooperative interactions between the mother, offspring and adopter. In non-man primates, some evidence suggests that pre-existing relationships play an important role in an private's conclusion to adopt an orphaned infant [11–13]. If and so, our understanding of not-kin adoption could be improved by tracking cooperative interactions across different relationships through time.
We tracked the allogrooming and food-sharing relationships among 23 woman mutual vampire bats (Desmodus rotundus) before and later one female adopted the orphaned pup of another female bat that was unrelated and previously unfamiliar. The two adult females, named 'BD' and 'Lilith', kickoff met in captivity afterwards being captured from sites 340 km apart. Lilith, the bat that gave birth and died, was near the end of its pregnancy at the start of the study. BD, the bat that became the 'adopter', was previously housed in captivity for another study almost 2 years prior (run across materials and methods). Nosotros observed no evidence that BD was either significant or lactating when offset introduced to Lilith, nor did she prove any signs of pregnancy for the next iv months. Our findings corroborate previous reports of adoption in convict vampire bats [23,24] and provide evidence that adoption may exist motivated, in part, by a history of cooperative interactions.
2. Materials and methods
As part of an ongoing written report on the formation of cooperative relationships, we combined three wild-caught groups of common vampire bats into a single, convict colony at the Smithsonian Tropical Research Plant in Gamboa, Panamá. We primarily captured female bats that appeared fully developed [25,26], which were classified equally 'adults', while younger bats were classified every bit a 'juvenile', if solitary, or 'pup', if attached to the mother. From a cavern at Lake Bayano, Panamá, we captured nine bats, including six adult females, two juvenile males and one juvenile female. From outside a large, hollow tree roost in Tolé, Panamá, we captured seven adult females. From outside another hollow tree roost in La Chorrera, Panamá, we captured eight adult females. These sites were 120–340 km apart and were chosen to ensure that the bats from each site were unrelated and unfamiliar.
To identify bats, nosotros marked individuals with a unique gear up of forearm bands (Porzana and National Tag). On 14 June 2019, groups were simultaneously released into an outdoor flight cage (2.1 × 1.7 × two.three k). On 5 July 2019, we added two more than adult female bats from the capture site in Tolé, Panamá. These 2 bats, BD and BSCS, were banded re-captures from a past study; they were previously captured from the wild roost, studied in captivity from December 2015 to September 2017, then released back into the wild roost (for details see [27,28]).
To mensurate dyadic social interaction rates, we used three infrared surveillance cameras (Foscam NVR Security System) to sample allogrooming and nutrient-sharing interactions amidst the captive bats for 6 h each day from 23 June to 4 August 2019 and from xi Baronial to 14 Oct 2019. Nosotros sampled in i h periods, primarily at 0400, 0500, 0900, 1900, 2000 and 2100 h. On iii of 110 days, we sampled simply 3–4 h, and for 18 days, nosotros sampled at other hours in between. During 640 sampling periods, nosotros recorded all dyadic bouts of allogrooming and oral fissure-licking (possible food sharing) that were at least 5 south in elapsing, noting the thespian and receiver. For allogrooming, we identified the thespian as the individual licking the body of the receiver. For possible food-sharing bouts, the actor was identified every bit the individual regurgitating food to the receiver, which we inferred from rima oris-licking by the recipient while the actor held yet (post-obit [28,29]). To induce food sharing for specific individuals, we individually isolated up to three bats each day and fasted them for 23 h. Each bat was fasted 3–xv times, and bats were mostly fasted in one case every seven days. Bats were weighed before and afterwards fasting. Each night, for 8–12 h, all other bats were provided with cattle claret that was defibrinated with 44 thousand of sodium citrate and 16 g of citric acid per nineteen l container. Cattle blood was either refrigerated for short-term employ or stored frozen, then thawed for later use.
Our analyses of adoption behaviour were motivated past the post-obit events. Four females gave birth while we were collecting behavioural data. One of these females, Lilith, gave nascence on nine August 2019 while existence monitored within a divide ascertainment cage. To sample interactions between Lilith and the newborn pup, we used an infrared camera to record them for an additional 12 one-hr periods between nine and 11 August 2019, resulting in a total of 652 sampling periods. We then returned the mother and pup to the larger group. Three weeks afterward giving birth, Lilith died due to what we doubtable was a gastrointestinal illness. Lilith'south orphaned pup then received all-encompassing allomaternal care from another developed female in the colony, BD, and survived until the end of the experiment on 14 Oct 2019, a span of approximately vii weeks (figure 1 a). Allomaternal care from BD included grooming, regurgitated food sharing and nursing, which we confirmed by manually expressing milk from the nipple on the twenty-four hour period Lilith died.
Evidence of adoption. (a) Notable events relating to the adoption are plotted chronologically from when the mother entered the captive colony to when the study ended. When offset introduced to the captive colony, the female parent was pregnant, and the female that later adopted the orphaned pup was non lactating. (b) The mother and the adopting female reciprocally and increasingly clean-cut each other for approximately eight weeks (dark blue and green lines), while 21 other adult females groomed the mother less (greyness dashed lines) or non at all (not plotted). The vertical dashed line indicates when the female pup was born, while the vertical dotted line indicates when the mother died. After the mother gave nascency, it clean-cut its pup less through time until information technology died due to a suspected gastrointestinal illness. The 'adopter' increasingly groomed the pup following the death of its mother. (c) The adopter increased its rate of food donations to the mother prior to the mother's death and became the mother's top food donor. The adopter also became the peak food donor to the orphaned pup.
To summate hourly rates of dyadic allogrooming and food sharing before and after the female parent'southward death, we summed the full elapsing of dyadic interaction bouts for each sample hour during which each dyad had the opportunity to collaborate. To visualize changes through time, we used local polynomial regression plumbing fixtures (loess method in the R package ggplot2 with a span argument of 0.eight) to plot allogrooming and food-sharing rates between (i) the mother and its pup, (2) all other adult females and the pup and (iii) the mother and all other adult females. To encounter if the increase in BD's helping behaviour was greater than expected past risk, we measured the mean change in allogrooming and food-sharing rates towards the pup before versus after the mother'southward death for all 21 developed females that were present in the colony during both periods (one female died earlier the mother gave birth). We and then calculated the verbal probabilities that BD would have the highest increases by risk (non-parametric test) and nosotros used Grubb'southward test to detect if BD'due south increase in allogrooming and food-sharing towards the pup was an outlier (parametric test). For Grubb'south test, nosotros used log(seconds + one) to increment normality of the allogrooming and food-sharing rates earlier computing the mean change. We conducted all analyses in R version iii.vi.1 [30].
iii. Results
Two unfamiliar and unrelated adult female person mutual vampire bats formed a new allogrooming and food-sharing human relationship. Lilith, the bat that eventually gave nascence, first entered the captive colony on 14 June 2019. BD, the bat that after adopted Lilith's orphaned pup, offset met Lilith on five July 2019. At this time, BD was not noticeably lactating. Directed allogrooming rates between BD and Lilith were like, highly symmetrical, and increased over approximately eight weeks, after which allogrooming rates were relatively stable (figure 1 b). BD became Lilith'southward summit allogrooming partner, while virtually other bats did not groom Lilith much or at all (effigy 1 b). BD was too Lilith'southward top nutrient donor. Based on oral cavity-licking times, nosotros judge that 47% of Lilith'due south total rima oris-licking (begging or receiving food) was directed to BD. Moreover, BD shared nutrient with Lilith during ii trials where Lilith was fasted, equally inferred from oral fissure-licking and a subsequent increase in Lilith's mass.
On 9 Baronial 2019, Lilith gave birth to a female pup (figure one, vertical dashed line). In the following weeks, BD extended its cooperative behaviour from Lilith to Lilith'due south pup. As Lilith groomed and shared food with its pup less through fourth dimension, BD'due south rates of allogrooming and nutrient sharing with Lilith's pup increased (effigy one). During this time, observations from video footage suggested that BD began to nurse the pup, which seemed to increase gradually. Past contrast, other colony members rarely groomed or shared food with Lilith's pup (figures1 and ii).
Increases in rates of allogrooming and food sharing from 21 adult females to the orphaned pup earlier and later on the mother'south expiry. The 'adopter' increased its allogrooming and food-sharing rates to the pup more than whatsoever other female. The allogrooming and food-sharing rates are shown for 21 bats, but virtually of the slopes are not visible because many of the rates are zero both before and afterwards the mother's death.
After giving birth, Lilith fell ill. During the calendar week of Lilith's death, nosotros observed that Lilith spent 96 min oral cavity-licking seven adult females, including BD. This corporeality of begging is a dramatic increment from the week prior, during which fourth dimension Lilith spent just 2 min rima oris-licking two developed females, again including BD. Lilith was the potential donor for only 13 min of recorded mouth-licking interactions with all other adult females while she was alive (figure one c).
On 28 August 2019, Lilith died due to what we suspect was a gastrointestinal affliction (figure i, vertical dotted line). On this mean solar day, we observed that BD was lactating and providing milk to the pup. Afterwards this day, BD increased its rate of allogrooming the pup by 47 seconds per hour (s h−one) and food sharing with the pup by 15 southward h−1 (figure two), which was greater than the 20 other bats (non-parametric rank test p = 0.048 for both allogrooming and food sharing; parametric outlier test, allogrooming: Grand = 3.0, p = 0.007, food sharing: G = four.0, p < 0.0001). BD became the pup's highest ranked groomer and food donor, but BD was not the elevation groomer or food donor for whatever of the seven other juvenile bats in the colony. BD groomed the pup an boilerplate of 52 s h−1 but clean-cut other juveniles merely 0 to 4 s h−1. BD fed the pup an average of 13 s h−1 simply fed other juveniles 0 to one s h−1. BD was however nursing the pup when we finished observations on 14 October 2019.
Amidst all bats, BD was not exceptionally cooperative. Overall, BD ranked fifth for having the highest allogrooming and food-sharing rates towards other adult females. Besides Lilith and her pup, BD was also the top groomer for only one other bat (some other bat from the same wild roost) and was not the top donor for whatever other bat. Moreover, BD's behaviour to other adult females changed afterward Lilith's death. Before Lilith'due south death, BD ranked tertiary and eighth for highest allogrooming and food-sharing rates to other adult females (excluding Lilith). Afterward Lilith's decease, BD'south rank decreased to ninth and 12th for highest allogrooming and food-sharing rates.
4. Discussion
We observed the consummate social history leading upwardly to a case of non-kin adoption between unrelated common vampire bats. In captivity, a mother gave birth then died after several weeks. During this time, some other previously unfamiliar and unrelated female person responded to changes in demand of both the mother and the pup (figure 1). After the female parent's death, the female increased the charge per unit at which it allogroomed and regurgitated food to the orphaned pup. Nosotros also noticed that this female was providing the pup with milk. This increase in helping behaviour was uniquely directed to the pup (in comparison to other juveniles or adults in the colony), and no other female helped the orphaned pup to most the same extent (figure 2).
The probability of orphaned pups beingness adopted in vampire bats remains unknown. Uwe Schmidt [23] suspected that adoption was non an unusual behaviour in vampire bats based on an unreported number of cases where newly caught pups, whose wild-defenseless mothers died during transportation to the laboratory, were subsequently adopted by unfamiliar females in his captive colony. In each case, these adopting females began to lactate, as nosotros observed here. In the same colony, captive-built-in pups that lost their mothers were likewise adopted by other females [24]. In one documented case, a pup of unreported sex lost its mother at 17 days of historic period, and an adult female then clean-cut, nursed and shared food with this pup, but it did not survive. In another example, a juvenile male person lost its mother at 79 days of historic period, and a female person in the colony so began to share food with and nurse the orphaned male. This female person was not lactating earlier her interactions with the orphaned pup; its previous pup was built-in 2 years prior and had died 16 months before the adoption. Past tracking the weight of the juvenile male person for one year, the authors plant that the juvenile was dependent on the adopting female for milk and regurgitated food until an age of about 300 days [24]. Other group members, including males and unfamiliar females, occasionally shared food with the juvenile male [24]. Based on these observations, it was suggested that female vampire bats form stable social groups with communal care of immature [24], but subsequently studies in the field and laboratory provide evidence confronting communal offspring care, instead suggesting that cooperative behaviour occurs within individually differentiated relationships, rather than as group-level investments made indiscriminately to any grouping member [25,29,31–33].
Adoption is non commonly reported among other bats. In one documented case, a female bottom short-nosed fruit bat (Cynopterus brachyotis) adopted its orphaned grandson in captivity after losing a premature pup of nearly the same age [34]. Less extreme forms of alloparental care, such equally allonursing and pup-guarding, are more frequently observed in some other bat species (reviewed by [35,36]).
Information technology is important to annotation that the few observed cases of adoption in vampire bats all occurred in captivity. During more than 400 h of field ascertainment, Wilkinson [25,31,32,37] observed allogrooming of vampire bat pups, just he never observed allonursing. Adoption would be hard to observe in wild colonies because orphaned pups are uncommon. In our captive colony, information technology is also interesting to note that some other female, BSCS, noticeably increased its allogrooming rate to the pup afterward the mother's death (effigy 2). Both BD and BSCS had previously lived in captivity for virtually two years during another study [27,28]. We therefore speculate that both captivity and decease of the mother might increase the probability of adoption in vampire bats. Still, the overall probability of adoption is hard to approximate because observations of orphaned pups are rare.
There are several reasons why common vampire bats might present an interesting comparative case for hereafter studies on the biological mechanisms behind adoption and maternal intendance behaviour. First, unlike well-nigh bats, female vampire bats ofttimes lack reproductive seasonality and can reproduce year-round, such that a female which adopts an unrelated pup volition presumably reduce its own reproductive success, even if it recently lost a pup. 2d, unlike most cooperative convenance mammals, an orphaned vampire bat pup is unlikely to be closely related to a random female in its colony because colonies take a low mean kinship, effectually r = 0.08 [31,38], and a unmarried immigrating female bat would exist likely to be unrelated to others encountered in the colony, which is the context simulated in our study. Third, relative to other bats, alloparental intendance poses an extreme energetic and opportunity cost. Female vampire bats give birth to a single pup after a gestation period of five to seven months [26,39], and a new mother will carry its pup for one to two months, during which time the weight of the pup volition at to the lowest degree double. After iv to five months, pups volition have grown fourfold in mass and will begin to fly and feed on claret [26]. Weaning does not occur until approximately 9 months of age [26,xl]. By dissimilarity, weaning in other bat species in the same family typically occurs after merely ane to three months [41–43]. Finally, reciprocal nutrient-sharing behaviour among non-kin adults is probable to exist based on the co-option of cooperative traits that originated for maternal care [28,30]. The aforementioned co-option of traits and expansion of cooperative behaviour from kin to non-kin may also help to explain not-kin adoption.
Our observation of non-kin adoption in vampire bats is similar in some respects to cases in chimpanzees [eleven,12]. Hobaiter et al. [11] suggested that chimpanzees may adopt an unrelated orphan if they previously experienced positive social interactions with that orphan prior to the mother's death. If so, and then social interactions between adopter and adopted orphan may also be facilitated past a shut social or affiliative human relationship betwixt the adopter and the biological parent. However, it is unknown if or how not-kin adoption based on previous social experience might affect lifetime fettle for both adopters and adoptees. Adoptive parents can experience energetic and opportunity costs from adoption that volition vary across species, individuals and environments [1,13]. The survival of offspring would announced more likely after being adopted [one], but this is not always evident, especially among populations with high mortality [1,12,thirteen].
Adoption can exist explained completely, or in function, as a by-product of normal parental care. For instance, if parental behaviours are triggered by a common set of neuroendocrine mechanisms or stimuli (eastward.g. [44]), then the same traits that lead to adaptive behaviour nether typical circumstances could also cause non-adaptive adoptions under the rare circumstance of an orphaned infant in dire need. Moreover, the generally atypical circumstances associated with captive conditions may sufficiently increase the likelihood of non-kin adoption, which may not occur ofttimes or at all in the wild. Some authors have suggested ways in which non-kin adoption might be adaptive for the adopter, including reciprocity [13,45], 'match-making' between biological and adopted young to grade uniform mating pairs [46], or kinship deceit, by which adopters exploit kin-recognition heuristics and deceive adopted young into a false perception of kinship, thereby causing these young to afterwards help at the nest [47]. Most, if not all, adaptive explanations predict that non-kin adoption of orphaned infants should exist biased towards the philopatric sex, simply this design has non been conspicuously shown [11–13]. In the case of vampire bats, information technology is likewise hard to explain why a female would invest in an disproportionate helping relationship with an baby over a potentially reciprocal human relationship with an developed female [48], merely these arguments exercise non eliminate the possibility that adopters may eventually receive social benefits from adopted individuals.
5. Conclusion
Observations of not-kin pup adoption in captive common vampire bats are consequent with the hypothesis that non-kin adoption is a by-product of proximate cognitive and neuroendocrine mechanisms that are crucial for parental care and triggered by unusual circumstances. Our observations also suggest that adoption is influenced by the history of cooperative interactions between female parent, offspring and adopter, although more evidence is needed to examination this hypothesis. The probability of non-kin adoption in vampire bats and whether it affects the fitness of adopters remains unclear, especially exterior of convict conditions, but we can brand 2 testable predictions. If not-kin adoption in vampire bats is adaptive, nosotros predict that female pups should be adopted more than often than male person pups considering females are philopatric. If female vampire bats are more motivated to help the offspring of more closely bonded partners, and then vampire bat pups should be biased towards inheriting the cooperative relationships of their mothers, i.e. social inheritance of network ties [49].
Supplementary Material
Acknowledgments
We thank the Smithsonian Tropical Research Institute for providing logistical support and the following individuals who helped with vampire bat care and/or aspects of data collection: D. Aparicio, Yard. Cohen, 50. Dück, D. Girbino, East. Kline, C. Marroquin, S. Ripperger and S. Stockmaier. Nosotros besides thank Thousand. J. West-Eberhard for initial conversations on this topic; J. K. Augustine, S. N. Gershman, I. M. Hamilton and the graduate students of The Ohio State Academy's EEOB Animal Beliefs grouping for their useful suggestions during manuscript preparation, equally well equally the 4 bearding reviewers for their insightful comments during the review process.
Ethics
This work was canonical by the Smithsonian Tropical Research Plant Beast Care and Use Committee (#2015-0501-2022) and the Panamanian Ministry of the Environment (#Sexual activity/A-67-2019).
Authors' contributions
I.R. and Thousand.G.C. conceived and designed the experiments. I.R., B.K.1000.B. and Thou.G.C. performed the experiments and nerveless the data. I.R. and Grand.G.C. analysed the data and prepared figures. G.G.C. and R.A.P. coordinated the study and provided critical resources. I.R. and G.G.C. drafted the initial manuscript, and all authors revised it critically for intellectual content.
Competing interests
The authors declare that they have no competing interests.
Funding
I.R. was supported by a short-term fellowship from the Smithsonian Tropical Research Plant, a student research grant from the Brute Behavior Guild and a graduate enrichment fellowship from The Ohio State University. B.One thousand.Grand.B. was supported by a student research grant from Sigma Eleven and a Critical Departure for Women Professional person Development Grant from The Ohio State University.
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