Abstract

The purpose of this review was to investigate the literature on cooperation in members of the family Corvidae, to examine where they excel and where they fall short. Cooperative behavior has been used in the past to investigate cognitive abilities, namely the ability to recognize kin, remembering who they’ve cooperated with in the past, reciprocity, tracking the reputation of others, understanding equity, and low temporal discounting. These abilities were discussed in the context of the literature mentioned in order to tie the research directly to the cognitive abilities of corvids. It was found that while members of this family excel at cooperating in different environments, they tend to have low inhibition control and do not attend to long-term consequences of defection. However, this lack of inhibition control may not suggest cognitive deficits, but simply the impulsive nature of animals in this family.           

  Keywords: Corvidae, cooperation, animal cognition, social behavior

Cooperation in the Family Corvidae

            Cooperation is a widely discussed and rigorously studied topic within the fields of animal behavior and behavioral ecology and was defined briefly by Stephens and Hauser (2004) as joint action for mutual benefit. However, authentic cooperation is difficult for scientists to pin down, as it is difficult to tell when animals truly understand the need to cooperate, as opposed to simply learning they need to complete a task with a conspecific. Because of this, reviews and studies have looked into the requirements for cooperation, particularly cognitive requirements, and have found a few common themes; for animals to cooperate, they need to possess the ability to remember who they’ve cooperated with in the past, engage in reciprocity, track the reputation of others, understand equity, and have low temporal discounting (Bear, Kagan, & Rand, 2017; Esteban, 2013; Stephens & Hauser, 2004). Because of these rigorous cognitive requirements, studying cooperation has often been used to understand the cognitive abilities of animal species, and cooperative behaviors have been shown in some of the most popular “smart” species such as elephants and dolphins (Kuczaj et. al, 2015; Plotkin et. al, 2011).

            There is another group of animals that have recently come into the spotlight on the cognitive stage; the Corvidae family. This group includes crows, jays, ravens, magpies, rooks, and more, and has been studied extensively in recent years to analyze their cognitive abilities, with shocking results. Most studies have found that members of this family are incredible problem solvers with a powerful memory and the ability to make and use tools (Clatyon et. al, 2007; Gould-Beierle, 2000; Hofmann et. al, 2016; St Clair et. al, 2016). However, cooperation across the entire family to assess cognitive abilities has yet to be examined. This review seeks to fill that gap in the literature and use cooperation to assess the cognitive abilities of members of the family Corvidae.

CORVIDAE SOCIAL STRUCTURE

            Corvids are known to exist in flocks and have very complex social structures. For instance, Braun et. al (2012) found that common ravens (Corvus corax) maintain strong social bonds both in captivity and in the wild, and that in the wild, subgroups of two to five individuals are shown to exhibit allo-preening and combined play behaviors. Another study investigated the social intelligence hypothesis in various bird species and found that corvids ranked high in their sociality, and even compared their social complexity to that of primates (Emery et. al, 2007). Because corvids live in these highly complex social environments with related and non-related individuals, it seems likely that cooperation would occur. Thus, the next topic of discussion is naturally when and how corvids cooperate, and when and how they fail to do so.

SUPPORT FOR COOPERATION

Cooperation in the lab

Cooperation tasks, such as the rope-pull task (Plotkin et. al, 2011), and game theory models of cooperation, such as the prisoner’s dilemma (Clements & Stephens, 1995), are commonly used to observe and assess cooperative behavior in a laboratory setting. Many studies have been done using these assays in corvids. For instance, Clements and Stephens (1995) found that when modeling a mutualism environment, wherein mutual cooperation pays best, blue jays (Cyanocitta cristata) readily cooperated with a partner for a food reward. The results of this study displayed that in a highly applicable model of cooperation, the jays were able to understand that in terms of immediate benefit, cooperation would offer the most rewards.

However, corvids are shown in other studies to go above and beyond simple reward assessments. A study done by Wascher and Bugnyar (2013) found that in two species of corvids (common ravens and carrion crows (Corvus corone)), individuals will not cooperate in situations when they are not receiving equal rewards, or when they recognize that their partner is receiving the same reward but not putting forth as much effort. While this study displays a lack of cooperation, it shows that ravens and crows can understand how much their partner is working, as well as the equity of the rewards they are receiving. This sensitivity to inequity is one of the cognitive requirements of cognition mentioned before, as well as the ability to track the reputation of others (which includes understanding how hard they work).

Lastly, Fraser and Bugnyar (2012) conducted a study looking at reciprocity and agonistic support (defined as a third party intervening in an ongoing conflict to attack one of the conflict participants, thus supporting the other) in common ravens. The researchers found that ravens will engage in long-term reciprocation of agonistic support and were more likely to support relatives and those who preened them. Interestingly, the ravens were not shown to engage in short-term reciprocation, which goes against the common trend in the literature that corvids attend to short-term rewards and reciprocity. The results of this study suggest that ravens check many of the cognitive requirement boxes, including the ability to remember who they’ve cooperated with in the past, the ability to engage in reciprocity, the ability to track the reputation of others, the ability to understand equity, and the ability to limit temporal discounting.

Cooperation in the wild

            While studies conducted in the lab are beneficial because of the high amounts of control a researcher can have over confounding variables, this unnatural environment can also lead to inaccurate understandings of an animal’s true abilities. Thus, it is incredibly beneficial for scientists to also look at behavior in the wild, especially when analyzing cooperation.

            One common cooperative behavior seen in a lot of corvid species is cooperative breeding, wherein individuals will band together to take care of the young of the group, whether they are directly related or not. Baglione et. al (2003) found this behavior in carrion crows, namely in that non-reproducing offspring and immigrant males aid breeding pairs in raising their young. Bosque and Molina (2002) found that cayenne jays (Cyanocorax cayanus) exhibit not only cooperative breeding, but also cooperative nest defending behaviors. Cooperative breeding is a simple yet incredibly common behavior, especially in New World corvids, which contain the most common corvid species such as jays, rooks, ravens, and crows. This behavior allows us to look at kin selection, one of the simplest bases of cooperation, which postulates that individuals care for those related to them in order to increase their direct and indirect fitness. While kin selection may be very basic, it does require various cognitive abilities, including the ability to recognize your kin.

            Outside of kin selection, wild corvid species have also displayed other cooperative behaviors. One study, conducted by Fraser and Bugnyar (2011), found that ravens will reconcile after fights with valuable partners, namely those who the individual will interact with in the future and who they share a valuable relationship with. Before this study, reconciliation had not been shown in avian species, but once again, corvids prove their abilities to understand their relationships with others outside of pair bonds, and how these relationships can help them in the future.

LIMITATIONS OF COOPERATION

            While corvids clearly display several cooperative behaviors that require vast cognitive abilities, some studies show that they often can fall short when it comes to working with others. There is one main shortcoming shown by the research: a lack of patience.

Lack of patience

            As mentioned before, except for a few studies like Fraser and Bugnyar’s (2012), which looked at reciprocity and agonistic support, most of the literature shows a lack of attention to long-term consequences and rewards in the corvid family. For instance, Clements and Stephens (1995) showed that while jays choose to cooperate in a mutualism environment, they do not choose to cooperate when placed in a prisoner’s dilemma environment, wherein the benefits of mutual cooperation are not much better than the benefits of mutual defection. This suggests that they attended more to the short-term rewards than the long-term consequences of defecting, and thus struggle with high temporal discounting. Other studies have shown this lack of cooperation in the absence of immediate benefit (Seed et. al, 2008; Stevens & Stephens, 2004).

Impulsive nature

            However, this lack of attentiveness to long-term consequences could be more related to impulsivity in the Corvidae family than to shortcomings in cognitive abilities. Previous research on corvids’ abilities to delay gratification shows that they struggle with this concept. For instance, Wascher et. al (2012) showed that crows are impulsive in their choice of rewards, even when they know a larger reward will come to them if they wait. So, for corvids to suddenly abandon their impulsive nature in order to cooperate would be abnormal, suggesting that this impulsivity is simply a barrier to cooperation that members of the family must overcome, regardless of their cognitive abilities.

CONCLUSION

            All in all, past research has shown that corvids possess many of the cognitive requirements for cooperation, including conspecific recognition, reciprocity, and an understanding of equity (Baglione et. al, 2003; Bosque & Molina, 2002; Clements & Stephens, 1995; Fraser & Bugnyar, 2012; Fraser & Bugnyar, 2011; Wascher & Bugnyar, 2013), and these findings exist both in lab settings and in the wild. However, they also showed a lack of inhibition control and high levels of temporal discounting in many corvid species (Clements & Stephens, 1995; Seed et. al, 2008; Stevens & Stephens, 2004). Despite these shortcomings, corvids show incredible levels of cooperation, suggesting high cognitive abilities, which falls in line with previous research done on their cognitive abilities outside of cooperation (Clatyon et. al, 2007; Gould-Beierle, 2000; Hofmann et. al, 2016; St Clair et. al, 2016). This review suggests many possible avenues of research, including looking into other examples of cooperation in corvids to expand the wealth of literature, or comparing the cognitive abilities of corvids and other non-human animals (or even humans themselves).

References

Baglione, V., Canestrari, D., Marcos, J.M., & Ekman, J. (2003). Kin selection in cooperative alliances of carrion crows. Science, 300(5627), 1947-1949. doi: 10.1126/science.1082429

Bear, A., Kagan, A., & Rand, D. G. (2017). Co-evolution of cooperation and cognition: the impact of imperfect deliberation and context-sensitive intuition. Proceedings. Biological Sciences, 284(1851). https://doi.org/10.1098/rspb.2016.2326

Bosque, C., & Molina, C. (2002). Communal breeding and nest defense behavior of the cayenne jay (Cyanocorax cayanus). Journal of Field Ornithology, 73(4), 360-362. http://dx.doi.org/10.1648/0273-8570-73.4.360

Braun, A., Walsdorff, T., Fraser, O., & Bugnyar, T. (2012). Socialized sub-groups in a temporary stable raven flock? Journal of Ornithology, 153, 97–104. http://dx.doi.org/10.1007/s10336-011-0810-2

Clayton, N.S., & Emery, N.J. (2007). Social cognition by food-caching corvids. The western scrub-jay as a natural psychologist. Philosophical Transactions of the Royal Society B: Biological Sciences, 362(1480), 507–522. http://dx.doi.org/10.1098/rstb.2006.1992

Clements, K.C., & Stephens, D.W. (1995). Testing models of non-kin cooperation: mutualism and the prisoner’s dilemma. Animal Behavior, 50, 527-535. http://dx.doi.org/10.1006/anbe.1995.0267

Emery, N. J., Seed, A. M., von Bayern, A. M. P., & Clayton, N. S. (2007). Cognitive adaptations of social bonding in birds. Philosophical Transactions of the Royal Society B: Biological Sciences, 362, 489-505. https://doi.org/10.1098/rstb.2006.1991

Fraser, O.N., & Bugnyar, T. (2012). Reciprocity of agonistic support in ravens. Animal Behaviour, 83, 171–177. https://doi.org/10.1016/j.anbehav.2011.10.023

Fraser, O. N., & Bugnyar, T. (2011). Ravens reconcile after aggressive conflicts with valuable partners. PLoS ONE, 6(3), 1-9. http://dx.doi.org/10.1371/journal.pone.0018118

Freidin, E. (2013). A critical review of the hypothesis that cognitive requirements constraint animal reciprocity. Revista Argentina de Ciencias Del Comportamiento, 74(2). Retrieved from https://search.ebscohost.com/login.aspx?direct=true&AuthType=ip,shib&db=edsdoj&AN=edsdoj.7ee1526acf1b47c98df6e309cb393fc9&site=eds-live&scope=site

Gould-Beierle, K. (2000). A comparison of four corvid species in a working and reference memory task using a radial maze. Journal of Comparative Psychology, 114(4), 347–356. https://doi.org/10.1037/0735-7036.114.4.347

Hofmann, M.M., Cheke, L.G., & Clayton, N.S. (2016). Western scrub-jays (Aphelocoma californica) solve multiple-string problems by the spatial relation of string and reward. Animal Cognition, 19(6), 1103–1114. Retrieved from https://search.ebscohost.com/login.aspx?direct=true&AuthType=ip,shib&db=mnh&AN=27470204&site=eds-live&scope=site

Kuczaj, S.A., II, Winship, K.A., & Eskelinen, H.C. (2015). Can bottlenose dolphins (Tursiops truncatus) cooperate when solving a novel task? Animal Cognition, 18(2), 543–550. https://doi.org/10.1007/s10071-014-0822-4

Plotkin, J.M., Lair, R., Suphachoksahakun, W., & de Waal, F.B.M. (2011). Elephants know when they need a helping trunk in a cooperative task. PNAS, 108(12), 5116-5121. https://doi.org/10.1073/pnas.1101765108

Seed, A. M., Clayton, N. S., & Emery, N. J. (2008). Cooperative problem solving in rooks (Corvus frugilegus). Proceedings: Biological Sciences, 275(1641), 1421-1429. http://dx.doi.org/10.1098/rspb.2008.0111

Stephens, J.R., & Hauser, M.D. (2004). Why be nice? Psychological constraints on the evolution of cooperation. Trends in Cognitive Sciences, 8(2), 60-65. doi:10.1016/j.tics.2003.12.003

St Clair, J.J.H., Klump, B.C., Wal, J.E.M., Sugasawa, S., & Rutz, C. (2016). Strong between-site variation in New Caledonian crows’ use of hook-tool-making materials. Biological Journal of the Linnean Society, 118(2), 226–232. https://doi.org/10.1111/bij.12757

Stevens, J. R., & Stephens, D. W. (2004). The economic basis of cooperation: tradeoffs between selfishness and generosity. Behavioral Ecology, 15(2), 255-261. https://doi.org/10.1093/beheco/arh006

Wascher, C. A. F., & Bugnyar, T. (2013). Behavioral responses to inequity in reward distribution and working effort in crows and ravens. PLoS ONE, 8(2), 1–9. http://dx.doi.org/10.1371/journal.pone.0056885

Wascher, C.A.F., Dufour, V., & Bugnyar, T. (2012). Carrion crows cannot overcome a delay of gratification in a quantitative exchange task. Frontiers in Comparative Psychology, 3(118), 1-6. https://doi.org/10.3389/fpsyg.2012.00118

Male Bean Beetles (Callosobruchus maculatus) Show a Preference for Virgin Females

McKeon, E. J., Dyer, Z., Umana, J., and Levin, I. I.

Agnes Scott College

Abstract

The male bias for choosing virgin mates has been shown in many different invertebrate species, and has many consequences for male fitness. The current study sought to explore male mate choice in Callosobruchus macalatus and to provide more evidence for the virgin mate bias. We hypothesized that male bean beetles prefer virgin mates, and we predicted that if we presented virgin male simultaneously with the choice between a virgin and a non-virgin female to mate with, the male would chose the virgin female. Our results supported a significant bias for virgin females in open field mate trials, X²_{(1, N = 20)} = 19.80, p < 0.0001, and showed an 8:1 bias for virgin:mated females. These findings also provide many options for future research in the field.

Discussion

Our hypothesis that male bean beetles prefer virgin mates was highly supported (p < .0001), and we found that there was no influence of female size on male choice latency (p = .607). Another group of researchers in our lab investigating the effects of female and male size on mate choice and copulation success found no significant effects of female size on male choice. Therefore, we can reasonably assume that mate choice in bean beetles is at least strongly influenced by female mating status, and is in line with previous studies investigating this bias in other animal species (Baruffaldi & Costa, 2014; Burris & Dam, 2015; McNamara, Jones, & Elgar, 2004).

Our study did have a few weaknesses, including our small sample size (N=20) and the lack of knowledge about the actual mechanism(s) males use to identify female mating status, although McNamara, Jones, and Elgar (2004) suggest olfaction plays a key role in this process in a similar species, the Hide Beetle (Dermestes maculatus). However, the latter weakness is in itself a strength in that it identifies a possible avenue of research in the area of male mate choice. 

Our findings also support the idea that male mate choice is a crucial aspect in increasing paternity and lowering sperm competition in polygamous species, as seen in other past studies (Archer & Elgar, 1999; Gromko & Pyle, 1978). This bias for virgin females makes sense in this context, as males who mate with virgin females are not faced with automatic sperm competition as males who mate with virgin females do. Virgin females are also often younger, which possibly could be related to an increase in fecundity. Conversely, if a male encounters an older virgin, she likely either has valuable characteristics that have allowed her to maintain this virginity into her old age, or she might live in an area with a low concentration of competing males, which could also decrease the chances of sperm competition. Either way, having a bias for virgin females is a effective, and evidently common, method males can use to assure paternity and direct fitness. Further research could be done to see if this bias exists in other species, such as avians or mammals.

References

Šešlija, D., Marečko, I., & Tucić, N. (2008). Sexual selection and senescence: do seed beetle males ( Acanthoscelides obtectus, Bruchidae, Coleoptera) shape the longevity of their mates? Journal of Zoological Systematics & Evolutionary Research, 46(4), 323–330. https://doi.org/10.1111/j.1439-0469.2008.00469.x

Baruffaldi, L., & Costa, F. G. (2014). Male reproductive decision is constrained by sex pheromones produced by females. Behaviour, 151(4), 465–477. https://doi.org/10.1163/1568539X-00003136

Gromko, M. H., & Pyle, D. W., (1978). Sperm Competition, Male Fitness, and Repeated Mating by Female Drosophila melanogaster. Evolution, 32(3), 588. https://doi.org/10.2307/2407724

Martinossi‐Allibert, I., Savković, U., Đorđević, M., Arnqvist, G., Stojković, B., & Berger, D. (2018). The consequences of sexual selection in well‐adapted and maladapted populations of bean beetles. Evolution, 72(3), 518-530. https://doi.org/10.1111/evo.13412

Sakurai, G., & Kasuya, E. (2008). Different female mating rates in different populations do not reflect the benefits the females gain from polyandry in the adzuki bean beetle. Journal of Ethology, 26(1), 93. https://doi.org/10.1007/s10164-007-0036-1

Johnstone, R. A., Reynolds, J. D., & Deutsch, J. C. (1995). Mutual mate choice and sex differences in choosiness. Evolution, 50(4), 1382-1391. https://doi.org/10.1111/j.1558-5646.1996.tb03912.x

Archer, M. S., & Elgar, M. A. (1999). Female preference for multiple partners: sperm competition in the hide beetle, Dermestes maculatus (DeGeer). Animal Behavior, 58(3), 669-675. https://doi.org/10.1006/anbe.1999.1172

Bonduriansky, R. (2001). The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biological Reviews, 76(3), 305-339. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/11569787

Burris, Z. P., & Dam, H. G. (2015). Female mating status affects mating and male mate-choice in the copepod genus Acartia. Journal of Plankton Research, 37(1), 183–196. https://doi.org/10.1093/plankt/fbu090

Crudington, H. S., & Siva-Jothy, M. T. (2000). Genital damage, kicking and early death. Nature, 407, 855–856. https://doi.org/10.1038/35038154

Johnstone, R. A., Reynolds, J. D. and Deutsch, J. C. (1996). Mutual Mate Choice And Sex Differences In Choosiness. Evolution, 50, 1382-1391. https://doi.org/10.1111/j.1558-5646.1996.tb03912.x

McNamara, K. B., Jones, T. M., & Elgar, M. A. (2004). Female Reproductive Status and Mate Choice in the Hide Beetle, Dermestes maculatus. Journal of Insect Behavior, 17(3), 337–352. https://doi.org/10.1023/B:JOIR.0000031535.00373.b1

In order to determine ways to increase horse health, three studies were created to analyze importance of socialization in overall horse health. The first proposal, a correlational study, correlated horse health, using the Equine Guelph Horse Health Check scale, and socialization using a Pearson’s r test to determine whether or not socialization was a factor in horse health. Once a significant correlation was found, an observational study was set up to see if quality of socialization in a domesticated herd could be increased. The amount of hay was increased during this two-phase observational study, and observers recorded instances of fighting behavior and tested their relationship using a Chi-squared test. Because some horses are required to be isolated for medical or social reasons, a third, experimental study was created wherein a dependent samples t-test was conducted to analyze the relationship between comforting behaviors, or lack thereof, from humans and stereotypic behavior. The results of the studies may provide insight on how to increase the physical and mental health of isolated and non-isolated horses.

Keywords: horses, socialization, animal behavior, veterinary medicine, equine health

Increasing Physical and Mental Health of Horses (Equus caballus) Through Socialization

Even though horses are one of the few animals that humans have domesticated for means other than consumption, not much research has been done on them and their social lives. What little research that has been done has revealed fascinating aspects of this creature’s life. For instance, Wathan, Waller, and McComb (2015) were able to study equine facial expressions and put together a manual called EquiFACS (Equine Facial Action Coding System). The researchers studied the movements of eyelid muscles, nasal muscles, ear muscles, and lower cheek muscles, and were able to describe seventeen different facial expressions in horses, ten of which are shared with humans. Other research has found that horses are social learners. Krueger, Farmer, and Heinze (2016) found that socially low-ranking and younger horses learned how to operate a feeding mechanism from their superiors, even though earlier research had suggested that horses were not social learners. What these earlier researchers failed to consider, according to Krueger et al. (2016), was that horses will only learn from those higher on the social ladder than themselves. Therefore, an older, high-ranked horse will not learn from a younger horse at the bottom of the social ladder. Horses are also very adept at recognizing others’ social status compared to their own, both in captivity (Krueger & Heinze, 2007), and in the wild (Cameron, Linklater, Stafford, & Minot, 2002). To further the importance of equine social structure Andrieu, Henry, Hausberger, and Thierry (2015) completed a study where they found that horses of a low social rank may gently influence group movements towards a source of food they have been previously informed of, they will not directly lead their group.

Not surprisingly, there are many sources of socialization issues in horses such as orphan syndrome, physical limitations such as blindness or lameness, and excessive stall confinement, all of which lead to either not being able to or not being allowed to socialize with the herd (Marcella, 2006). One of the symptoms of poor socialization, as discussed by Dezfouli, Tavanaeimanesh, Naghadeh, Bokaei, and Corley (2013) is stereotypic behavior. Stereotypic behavior is defined as repeated coping behaviors such as weaving, cribbing, chewing, pacing, and wind sucking. Horses have often been shown to exhibit these sorts of behaviors to cope with a poor environment or a lack of socialization.

What’s even more fascinating is that horses are shown to experience cross-species social learning. Schuetz, Farmer, and Krueger (2016) found that horses that watched a human complete a small series of steps to obtain food performed significantly better than those who did not have the steps demonstrated to them. Schuetz et al. (2016) also found that horses who struggled with the steps often approached the experimenters, which they deemed to be comfort-seeking behavior. There have also been studies conducted to analyze the ways humans can make horses happier and healthier through their behavior. For instance, Rozempolska-Rucinska, Trojan, Kosik, Prochniak, and Gorecka-Bruzda (2013) did a review of various studies where they found that “natural horsemanship training” (NHT), which is a training method that strives to develop a rapport with the horse, use methods derived from the observation of wild horses, and reject abusive training methods like whipping and fear conditioning. The study found that NHT led to higher rates of horse happiness, comfort, understanding, and willingness to work with humans in the future (Rozempolska-Rucinska, Trojan, Kosik, Prochniak, & Gorecka-Bruzda, 2013). Likewise, Graham and McManus (2016) found that an increasing number of people in the horse-racing industry are dropping use of the whip due to increased mental instability in their horses.

In fact, more and more people are beginning to understand how important a trainer’s disposition and methods are in maintaining overall horse mental health. Kydd, Padalino, Henshall, and McGreevy (2017) found that when introducing horses to round pen work, the more experienced a trainer was, the less “bad” behaviors a horse exhibited, the faster they learned to work in the round pen, and the more comfortable they were with the trainer. But training is not the only way horse owners can increase their horse’s comfort and mental health. According to Harrison and Von Geldern (2017), allowing the horse to play on its own and playing with it directly can increase mental health and social skills in a herd. Thus, humans play an incredibly important role in the health of their horses, and the literature raises the question: what other ways can we increase a horse’s health and wellbeing.

The purpose of these studies is to investigate three topics; whether horses benefit from being in large social groups, whether these large social groups can be made more socially healthy, and how humans can influence health of horses who cannot be in a large social group.

References

Andrieu, J., Henry, S., Hausberger, M., & Thierry, B. (2015). Informed horses are influential in group movements, but they may avoid leading. Animal Cognition, 19, 451-458. doi: 10.1007/s10071-015-0945-2.

Cameron, E. Z., Linklater, W. L., Stafford, K. J., & Minot, E. O. (2002). Social grouping and maternal behavior in feral horses (Equus caballus): The influence of males on maternal protectiveness. Behavioral Ecology and Sociobiology, 53, 92-101. doi: 10.1007/s00265-002-0556-1.

Dezfouli, M. M., Tavanaeimanesh, H., Naghadeh, B. D., Bokaei, S., & Corley, K. (2013). Factors associated with stereotypic behavior in Iranian stabled horses. Comparative Clinical Pathology, 23, 1651-1657. doi: 10.1007/s00580-013-1840-3.

Graham, R., & McManus, P. (2016). Changing human-animal relationships in sport: An analysis of the UK and Australian horse racing whips debate. Animals, 6, 1-17. doi: 10.3390/ani6050032.

Harrison, J., & Von Geldern, J. (2017). To play or not to play? Horse and Rider, 56, 91-95.

Krueger, K., Farmer, K., & Heinze, J. (2013). The effects of age, rank, and neophobia on social learning in horses. Animal Cognition, 17, 645-655. doi: 10.1007/s10071-013-0696-x.

Krueger, K., & Heinze, J. (2007). Horse sense: Social status of horses (Equus caballus) affects their likelihood of copying other horses’ behavior. Animal Cognition, 11, 431-439. doi: 10.1007/s10071-007-0133-0.

Kydd, E., Padalino, B., Henshall, C., & McGreevy, P. (2017). An analysis of equine round pen training videos posted online: Differences between amateur and professional trainers. PLOS ONE, 12, 1-12. doi: 10.1371/journal.pone.0184851.

Marcella, K. L. (2006, May). Poor socialization can stem from a variety of circumstances. DVM: The Newsmagazine of Veterinary Medicine, 2-5.

Rozempolska-Rucinska, I., Trojan, M., Kosik, E., Prochniak, T., & Gorecka-Bruzda, A. (2013). How “natural “training methods can affect equine mental state? A critical approach – a review. Animal Science Papers and Reports, 31, 185-194.

Schuetz, A., Farmer, K., & Krueger, K. (2016). Social learning across species: Horses (Equus caballus) learn from humans by observation. Animal Cognition, 20, 567-573. doi: 10.1007/s10071-016-1060-8.

Wathan, J., Burrows, A. M., Waller, B. M., & McComb, K. (2015). Equifacs: The equine facial action coding system. PLoS ONE, 10, 1-35. doi: 10.1371/journal.pone.0131738.