Avens Publishing Groupt ing Innova t ionsJInviVeterSci MedOpen AccessMay 2021 Volume 9 Issue 1 All rights are reserved by Kolkmeyer CA et al.Behavioural Correlates ofNeutering Male Dogs –aQuestion of Breed?Keywords:Castration; Retriever; Shepherds; Hunting Dogs; Terrier;Personality traits; Panic; AggressionAbstractCastration of dogs is often conducted as a preventive measureagainst diseases and undesirable behaviour. While female dogs arepreferably neutered for medical reasons, owners of male dogs hopefor an improvement in behavior. Although there is a lack of scientificknowledge on this subject, neutering is often conducted to get a moretrainable and less aggressive dog.The aim of this study is to examine castration from an ethologicalperspective and to reveal possible behavioural changes aftercastration related to breed.An online study was conducted consisting of two differentquestionnaires about the dog’s personality. A total of 242 dog ownersparticipated in the study concerning specific behaviour problems (n 130 intact and 112 neutered males). Another 211 owners of males(n 115 intact, 96 neutered) completed the questionnaire aboutpersonality traits (dog sociability, trainability, emotional stability andextraversion) based on Turcsán et al. 2011.Four breed categories were formed following Parker et al. (2017):shepherds, retrievers, terriers, and hunting Dogs. Our study revealsthat intact males are bolder than neutered males. Intact males havelower aggression scores than neutered ones. Castrated males showsignificantly more panic behavior (multinomial logistic Regression, p 0.04).Intact shepherds are bolder than neutered ones (Mann-Whiney-U-Test:p 0.03) and intact terriers are bolder than neutered terriers (MannWhitney-U Test: p 0.04). Intact terriers scored lower for aggressionthan neutered ones. With these results and the data of previousstudies, we question castration to modify behavior, as a measure forreproductive control and as a preventive measure against diseases.IntroductionAt the beginning of industrialization, breeding goals changed frompure specialists, such as hunting and retrieving dogs, to companiondogs, which should rather take on the function of social partners [1].Today, classic working dogs such as the Magyar Vizsla (hunting dog)or the Australian Shepherd (herding dog) are increasingly found inthe home as family members. Today’s requirements for breedersinclude that dogs can adjust to urban living conditions and that theymeet the social needs of humans as family members [32,42].Although the number of dog breeds has increased significantlyover the past century and a half, relatively little empirical researchhas focused on the behavioral characteristics of breeds. However, itis generally accepted that different breeds exhibit different behavioralrepertoires due to selective pressures exerted by humans [5,18,41].Brewer et al. (2002) define a dog breed as a group of individualswithin the C. lupus familiaris subspecies that are very similar on thebasis of a number of characteristics that have been shown to differfrom other groups [6].The more traditional and widely used methods of categorizingbreeds have been promoted by various national and internationalcynological associations, where dog breeds are divided into groupsbased on the type of task dogs must perform. Empirical studiesResearch ArticleAvensPublishingJournalof GroupInvi t ing Innova t ionsVeterinary Science& MedicineKolkmeyer CA1,2*, Schmitz J3 and Gansloßer U2Department of Biology, University of Vechta, Germany2Institut für Zoologie & Evolutionsforschung mit PhyletischemMuseum, Ernst-Haeckel-Haus und Biologiedidaktik, Erbertstr. 1.07743 Jena, Thuringia, Germany3Department of Biology and Biotechnology, Ruhr-UniversitätBochum, Germany1*Address for correspondence:Kolkmeyer CA, Fach Biologie, University of Vechta driverstrasee 22, 49377 Vechta, Germany, Tel: 49 -911790 9360;Email: [email protected]: 1 April, 2021Accepted: 5 May, 2021Published: 10 May, 2021Copyright: 2021 Kolkmeyer CA et al. This is an open access articledistributed under the Creative Commons Attribution License, whichpermits unrestricted use, distribution, and reproduction in any medium,provided the original work is properly cited.examining breed differences in behavior have largely focused on thecategorizations established by the American Kennel Club (AKC) andthe Fédération Cynologique Internationale (FCI) (n 365 breeds, 10breed groups).While the FCI classifies the breeds based on their function andphenotype, there is a more modern approach. A study viewed on thegeographic origin and molecular relations of dog breeds with the aimto investigate how migration, geographical separation and remixingcontributed to the emergence of the dog breeds that exist today [38].They examined the gene sequences of a total of 1,346 dogs from 161breeds. The dogs came from all parts of the world, with the exception ofAntarctica, and all had very different breeding histories. The resultingbreed groups were summarized as clades and the researchers wereable to identify 23 clades in total. In this study four breed clades areexamined: “shepherds”, “retrievers”, “terriers” and “hunting Dogs”.Within these breed clades, differences in social behavior betweenneutered and non-neutered males are to be analyzed.The topic of neutering dogs is always controversial [39,40,43,21,46]and almost all dog owners are confronted with this question at somepoint. Despite new scientific findings on various health side effectsof castration, this surgical procedure is still the method of choicefor reproductive control, to remove undesirable behavior and as apreventive measure against some diseases like e.g. testicular cancer inmales or pyometra in females [35].Behavioral reasons relate to problem behavior such as urinemarking or, from the point of view of dog owners, inappropriateaggressive behavior. A large-scale Questionnaire study” by Niepel(2007; n 1010) in Germany showed that the reasons vary dependingon the dog’s gender. According to the study of Niepel male dogs areneutered to 74% for behavioral and only 21% for medical reasons.The study by Mertens & Unshelm (1997) also in Germany revealedsimilar results [31]. As a reason for castration in males, 69% statedbehavioral problems and only 24% stated medical causes.A very important hormone in connection with consequencesof castration is cortisol. It is dependent on some neurotransmittersCitation: Kolkmeyer CA, Schmitz J, Gansloßer U. Behavioural Correlates of Neutering Male Dogs –a Question of Breed?. J Veter Sci Med. 2021;9(1): 6

Citation: Kolkmeyer CA, Schmitz J, Gansloßer U. Behavioural Correlates of Neutering Male Dogs –a Question of Breed?. J Veter Sci Med. 2021;9(1): 6ISSN: 2325-4645(serotonin and oxytocin) and also on the sex hormones. Serotonin,oxytocin and sex hormones (such as testosterone and estrogen) act asimportant antagonists of cortisol. Accordingly, they have a cortisolsuppressing effect and can reduce anxiety [16].So neutering a dog because of defensive food aggression,territorial or leash aggression - generally all forms of aggression basedon insecurity or self-protection - can even worsen this inappropriatebehavior [8].The main aims of our study are (1) to find out, if neutered andintact dogs of different breeds show differences in the personality traitsof extraversion, dog sociability, emotional stability and trainability(based on Turcsán et al. 2011) and (2) to analyse differences in stressindicating behavior or panic and fear between intact and neuteredmales of the respective breeds.Materials and MethodsDog owners completed the online questionnaires between Apriland December 2020. Questionnaires were distributed to friends,family, social media, dog schools and breeders. All dogs live with theirowners in a family association. For determination of breed we reliedon the owners’ assignment without checking them e.g. by means ofpictures, pedigree excerpts etc. Both dogs kept exclusively as familydogs and also dogs that are led for hunting were included. The dogbreeds were categorized according to Parker et al., (2017) into thefollowing breed categories see (Table 1)Case StudiesIn the first part of the questionnaire, the demographic data ofowners (age, gender) and dogs (age, gender, breed and neuteringstatus) were asked. The following questions were about theenvironment and the daily routine of the dogs. In addition, theproblems in living together with the dog and any previous diseaseswere included. In this work, questions regarding breed, gender andcastration status were used for analysis and were evaluated usingMicrosoft Excel (version 2016). The exact breeds of the participatingdogs can be found in the appendix.behavior and a more peaceful communication with conspecifics.Emotional StabilityIs related to the dog’s behavior in stressful situations. Low scoresindicate anxious and stressful behaviour ( neuroticism). High scoresindicate a calm and emotional stable dog.Trainability opennessLow scores in this trait indicate a less playful and inventivecharacter. Dogs with low scores are considered less open andinquisitive.Statistical AnalysesThe statistical evaluation and some graphical representation of theresults were carried out in SPSS software (by IBM, version 27). The datawere tested for normal distribution using the Kolmogorov-Smirnowtest [22]. Since all data are not normally distributed, non-parametrictests were used for the analysis. Independent data, e.g. comparisonsof intact and castrated males were calculated using the MannWhitney U test [30], comparisons with k-samples, e.g. comparisonsof personality traits between breed categories examined by theKruskal-Wallis H test ( H test) [25]. In the second case, if statisticalsignificance was recognized, an adapted post-hoc test was carried outafter the Kruskal-Wallis-test. This test includes a comparison of theindividual groups including a Bonferroni correction to adjust thelevel of significance (Dunn-Bonferroni test). In general, the level ofsignificance was set at α 0.05. The nominal data of the case studieswere statistically analyzed using a multinominal logistic regression totest the differences in dog behavior on a multivariable level.ResultsBUDAPEST QuestionnairesFigure 1 shows the differences between the intact and castratedbreed clades and between the intact and castrated dogs in thepersonality traits. Significant differences could be calculated for bothBUDAPEST QuestionnaireThe questionnaire from Turcsán et al. (2011) provides informationon the four personality traits extraversion, dog sociability, emotionalstability and trainability. The questionnaire contains a total of 24questions that are answered by a 3-point scale. The answers in thefour categories were evaluated by forming scores. The results of thequestionnaire were analyzed by using Microsoft Excel (version 2016)and SPSS software (by IBM, version 27). The following personalitytraits (based on Turcsán et al. 2011) were analysed:Boldness Extraversion(we prefer the last term to avoid confusion with the behavioralsupertrait as in the shy-bold-system): Low scores indicate an anxiousand insecure character. High scores indicate an open-minded,extrovert character.Dog SociabilityLow scores indicate a high tendency for bullying or fightingbehavior towards conspecifics. High scores indicate non-suspiciousJ Veter Sci Med 9(1): 6 (2021)Figure 1: Boxplot of the respective breed categories shepherds (n 36 intactand n 27 neutered), retrievers (n 35 intact and n 15 neutered), terriers(n 26 intact and n 37 neutered) and hunting Dogs (n 18 intact and 17 neutered), separated into intact and neutered males. A) extraversion, B)sociability, C) emotional stability, D) trainability. * p 0.05, ** p 0.01, *** p 0.001 (Mann-Whitney U test).Page - 2

Citation: Kolkmeyer CA, Schmitz J, Gansloßer U. Behavioural Correlates of Neutering Male Dogs –a Question of Breed?. J Veter Sci Med. 2021;9(1): 6ISSN: 2325-4645Table 1: The number and categorization of the dog breeds into clades based on the genetic study by Parker et al. 2017.Hunting DogsDalmatianGerman Shorthaired PointerGerman Wirehaired PointerGreat MünsterländerIrish setterViszlaWeimaranerTerriersn (casestudies)n (Budapestquestionnaire)Shepherdsn (casestudies)n (Budapestquestionnaire)53Australian Shepherd42341Bearded Collie11Border collie1310Collie213Irish Wolfhound112Italian Greyhound1122Shetland Sheepdog (Sheltie)2n (Budapestquestionnaire)Retrieversn (CaseStudies)2217028n (CaseStudies)Airedale Terriern (Budapestquestionnaire)1Flat Coated Retriever64Border Terrier23Golden Retriever1412Cairn Terrier44Golden x Labrador Retriever11Irish Terrier1Labrador Retriever4631Jack Russell Terrier3732Norfolk Terrier22Parsons Russell Terrier1516West Highland White Terrier33Yorkshire Terrier21Noca Sotica Duck Tolling Retrieverthe shepherds (U-Test: p 0.03) and the terriers (U Test: p 0.04).The intact shepherds show higher scores for extraversion (Mdn 6,SD 1.2) than the castrated shepherds (Mdn 5, SD 2). The dataalso reveal that the intact terriers have higher extraversion values (Mdn 6, SD 1.3) than neutered ones (Mdn 5, SD 1.6). Nosignificant differences could be found for the personality traits ofsociability (B), emotional stability (C) and trainability (D) (U-test: p 0.05).Using the questionnaire about the dog’s personality, differencesin extraversion could be determined. Although no major differencesbetween the breed categories of retrievers and hunting dogs could befound, there were significant differences between the shepherds andthe terriers. The intact shepherds differ from the neutered shepherdsand likewise the intact terriers differ from the neutered terriers. Intactmales have higher values in extraversion and are therefore consideredto be more open-minded and less fearful than neutered dogs.Case StudiesThis agrees with the results of Hakanen et al. (2020) that intactmales are less anxious than neutered males [14]. Kaufmann et al.(2017) also found out on the basis of questionnaire and video analysesthat intact males are more likely to perform social behavior thancastrated males [21]. The latter often appeared to be more stressedand nervous and consequently stayed more out of the social situation.One explanation for this lies in the abovementioned elimination ofthe stress-relieving sex hormones and the associated increase of thestress hormone cortisol [16].There are noticeably high scores for stress and insecurity in allfour breed categories in comparison to the other behavior problemssee (Figure 2).Aggressive behavior occurred in all breed classes, with theexception of the hunting dogs, more frequently in the castrated thanthe intact males.Panic was recorded among shepherds, hunting dogs and retrieversonly among neutered dogs. The differences for the castration statusare statistically significant for the trait panic (multinomial logisticregression, p 0.04). When the effect sizes are considered individually,it is noticeable that the significant value is mainly due to differences incastration status and not due to differences in breed.No significant differences could be found for the stress/uncertainty axis, although the shepherds run upwards here and theretrievers comparatively have low values (Figure 2).DiscussionPossible explanations for the results can be found in the evaluationof the dog owners as well as in the current research on castration andmodern dog breeds.J Veter Sci Med 9(1): 6 (2021)Figure 2: Results of the case studies. Comparison of behavioral problemsbetween neutered (n 112) and Intact (n 130) male dogs (n 242 dogs) relatedto the breeds: shepherds (n 36 intact and 26 neutered), hunting Dogs (n 26 intact and 21 neutered), retrievers (n 41 intact and 26 neutered), terriers(n 27 intact, 39 neutered).Page - 3

Citation: Kolkmeyer CA, Schmitz J, Gansloßer U. Behavioural Correlates of Neutering Male Dogs –a Question of Breed?. J Veter Sci Med. 2021;9(1): 6ISSN: 2325-4645Why the clades of the shepherds and the terriers show significantdifferences in extraversion can only be speculated at this point.Terriers were bred for independent work such as finding rats andkilling prey. They are considered as fearless and impulsive [24]. Thehigher values of extraversion in non castrated males could thereforebe the result of typical breeding effects.Turcsàn et al. (2011) found that terriers received high scores forextraversion and differ significantly from other breeds [44]. Whileherding dogs (such as Australian Shepherd or Border Collie) couldbe classified as low calm, high trainable, low sociable and low bold,(i.e. introverted in the five factor terminology) hunting dog breeds(such as Irish Setters or Pointer) and retrievers (such as Golden orLabrador Retrievers) turned out to be low calm, medium trainable,high sociable and high bold. These data partly coincide with ourresults. The retrievers had the higher scores for sociability and thehunting dogs were high bold here too. The latter, however, did notturn out to be highly sociable, but achieved lower scores. It mustbe noted that some representatives of the clade hunting dogs (e.g.German Wirehaired Pointer or Vizsla) can also be found in Turcsánet al (2011) in cluster 2 (low sociable), which in turn corresponds toour results.The Australian Shepherd was the most frequent breed withinthis study in the clade of the shepherds. The Australian Shepherdis considered (if kept correctly!) as a balanced, rarely contentiousand active herding dog, who is very eager to work [24]. The highextraversion of the Australian Shepherds can also be seen here as thebreeding result of a highly motivated working breed [42].The overall low panic and aggression scores for retrievers andhunting dogs are one of the reasons that both Golden and LabradorRetrievers are among the most popular assistance dog breeds [3].Hunting dogs are selected to pay more attention to their environmentstill remaining calm or obedient. In this study, the hunting dogsconsisted mainly of Weimaraners, which are considered spirited andsometimes impetuous hunting dogs with a reliable pointing. They arehighly vigilant and are therefore not suitable for beginners or peoplewho tend to be a bit casual [24].The higher values for aggressive behavior in the neutered dogscoincide with the results from Kaufmann et al. (2017). Here theresearchers also found by means of questionnaire and video analysesthat neutered males are more likely to aggression than intact males,which in turn supports the assumption that aggressive behaviorcannot be influenced positively by castration per se (Niepel, 2007)[21,35].Regarding aggression control, it should also not be disregardedthat only types of aggression can be influenced by castration that aredependent on sex hormones.So from a behavioral point of view, it is controversial to whatextent neutering affects social or especially aggressive behavior sincedogs may become more aggressive due to the lack of sex hormones[17]. Feddersen-Petersen (2008) writes that aggressive behavior canalso indicate a disturbed organism-environment relationship [10].Nelson et al. 1997, Huntingford & TurnerJ Veter Sci Med 9(1): 6 (2021)Above all, the different types of aggression must be taken intoaccount.For example, there is also serotonin-dependent aggressivebehavior. If the serotonin level is too low, aggressive behavior can befavored. Conversely, however, high serotonin levels can also lead toaggression. The dog breeds Cocker Spaniel and Golden Retriever inparticular can have a certain genetic defect, which disrupts the buildup and breakdown of serotonin. As a result, these dogs are prone toaggressive attacks [20].In partner protection, jealousy behavior and in pair bonding, it isalso not the sex hormones that play a role, but two other hormones:oxytocin and vasopressin [29,2]. The latter evokes the aggressivebehaviors occurring in partner protection and in jealousness.Oxytocin is important above all for a positive, social bonding witha conspecific. In order for developing a bond, however, vasopressinmust be produced as a preliminary stage before oxytocin production.Accordingly, in general terms, every bond also includes a certaindegree of jealousy. Consequently, partner protection and jealousbehavior cannot be eliminated by castration, as Bielsky & Young(2004) were able to show in mice and rats.In addition to the hormone-related behaviors, there are alsosome that are influenced by transmitters. Aggressive behavior thatoccurs in the course of self-defense is controlled, for example, bynorepinephrine. This catecholamine, also known as the fightinghormone, is preferred in a stressful situation when it comes toprotecting or defending yourself. The norepinephrine acts primarilyin a self-rewarding learning effect, which means that successfulcourses of action are learned and saved (an example would be thelearned leash aggression). Again, even with this type of aggressivebehavior, castration is not very promising, as there is no connectionbetween the sex hormones and self-defense [1,34]. In our study,aggressive behavior also occurs among neuters and there were nosignificant differences, i.e. neutering does not seem to have a positiveeffect on aggressive behavior. This is an important aspect consideringaggression as a common reason for castration.The increased panic with more neutered animals again providesan indication of the behavioral consequences of neutering, whichwas also found by Zink et al. (2014) in castrated Vizslas [45]. Ourresults show only significance for the castration status, not for thebreeds, which could be an indication that panic behavior occursmore frequently in neutered males regardless of the breed. If thestress hormone cortisol is included again, as already described inthe introduction, it becomes clear that anxiety-related aggressionsare controlled by cortisol and that testosterone as an inhibitor is nolonger present as a result of castration [16].Serpell & Hsu (2005) and also Kubinyi et al. (2009) as well asStarling et al. (2013) showed that the neutered males and femaleswere the most insecure dogs in comparison to the intact ones. Inaddition, the neutered dogs of both sexes were also the less sociabledogs [41,26,42].In Müllers study (2017), the representatives of the shepherdsclade showed fewer distance-keeping signals than the retriever clade.The herding dogs seem to be generally more open-minded and opentowards conspecifics, so that they are often assessed by their dogPage - 4

Citation: Kolkmeyer CA, Schmitz J, Gansloßer U. Behavioural Correlates of Neutering Male Dogs –a Question of Breed?. J Veter Sci Med. 2021;9(1): 6ISSN: 2325-4645owners as more excitable. This less developed distancing tendencycan possibly due to the breeding effects of shepherds for herding work[33].However, the results regarding the terriers were surprising. Theseare considered fearless energetic and proactive dogs with low selfprotective behavior and a high tendency to react with aggressionwhen threatened [24]. The fact that the terriers do not distinguishthemselves significantly from the other breed categories in anyemotional characteristic was therefore an unexpected result.Beside the genetic and morphological aspects, the experiencesand handling of the dog certainly play a major role in how castrationaffects a dog, because each animal tends to coping strategies [9,10].Likewise, when it comes to castration, placebo effect should always betaken into account [47], which is based on a certain expectation of dogowners to improve or remove specific behaviors through castrationOur results once again show the importance of individual-basedinformed decision-making processes regarding this ever-presenttopic.Archaeological Science 36: 473-490.14.Hakanen E, Mikkola S, Salonen M, Puurunen J, Sulkama S, et al. (2020)Active and social life is associated with lower non-social fearfulness in petdogs. 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The topic of neutering dogs is always controversial [39,40,43,21,46] and almost all dog owners are confronted with this question at some point. Despite new scientific findings on various health side effects of castration, this surgical procedure is still the method of choice for reproductive control, to remove undesirable behavior and as a .