ABSTRACT
This study analyses a potential link of certain pathological findings to tail biting and whether tail biting/necrosis occurs in wild boars. Thirteen young wild boars and 17 rearing pigs were pathologically examined and findings compared by Chi2/t-Tests. Sixty-five tails of wild boars were analyzed pathohistologically. Typical pathological findings in wild boars were linked to parasitic infections, which were not seen in rearing pigs. However, significantly more rearing pigs were affected by parameters linked to gut health (P = 0.05) and rhinitis (P = 0.02). Pathological deviations in tails of wild boars were linked to external parasites. Wild boars are not healthier than rearing pigs (or vice versa). However, causes for diseases differ. The gut seems to be challenged in the rearing pigs. This may be explained by a nutritional challenge due to early weaning and might be linked to the development of tail biting. No evidence for tail biting/necrosis in wild boars was found.
Background
Tail biting is a common problem in modern pig husbandry (Schrøder-Petersen & Simonsen, Citation2001; Valros & Heinonen, Citation2015). Although many studies have been carried out, the main conclusion is that the causes are multifactorial (Sonoda et al., Citation2013; Henry et al., Citation2021). One of the factors commonly linked to tail biting outbreaks is the health status (Moinard et al., Citation2003; Grümpel et al., Citation2018; Valros, Citation2022). Some authors have concentrated on the effect of an immune system activation on tail biting (Nordgreen et al., Citation2018; Munsterhjelm et al., Citation2019; Nordgreen et al., Citation2020; Veit et al., Citation2021a,Citationb). Munsterhjelm et al. (Citation2013) as well as Czycholl et al. (Citation2023) analyzed health parameters in tail biters and bitten pigs obtained by pathological examinations, coming to the general conclusion that most of the pigs (including the controls) had signs of a generalized activation of the immune system. In both studies, the animals were all from farms on which tail biting occurred. So the relevant question is: Which of the findings in the health parameters collected in those studies can be rated as normal in growing pigs and which of those findings may be linked to the occurrence of tail biting? To answer this question, one needs a population of pigs in which tail biting does not occur. However, as the problem of tail biting is still not fully understood and cannot be securely controlled, it basically occurs worldwide on all pig farms (D’Eath et al., Citation2018; Edwards & Valros, Citation2021). For evaluation of normal behavior, in farm animal ethology, one often chooses to compare the behavioral repertoire to the wild form (Stolba & Wood-Gush, Citation1989; Jensen, Citation2017).
In general, up to now, only few scientific studies about the general health status of wild boars (López-Olvera et al., Citation2006; Meier & Ryser, Citation2018) or feral pigs (Dzięciołowski & Clarke, Citation1990; Gipson et al., Citation1999) exist. Instead, studies have rather concentrated on the occurrence of specific diseases and pathogens as well as associated risk assessments (Al Dahouk et al., Citation2005; de Mendoza et al., Citation2006; Ruiz-Fons et al., Citation2008; Roic et al., Citation2012; Cano-Manuel et al., Citation2014; Meier & Ryser, Citation2018; Cilia et al., Citation2020). Thus, there is a lack of information about the general health status of wild boars. Moreover, it remains unclear what health findings associated to a general activation of the immune system can be rated as normal, i.e. without clinical relevance.
Apart from the health findings, also the adrenal glands may be of specific interest regarding the evaluation of stress (which again is strongly linked to tail biting (e.g. Sonoda et al., Citation2013; Valros & Heinonen, Citation2015; Henry et al., Citation2021)). The hypothesis is that more stress leads to an increase of the adrenal gland weight as the adrenal gland is the terminal organ in the stress cascade and when more stress hormones are being produced, the weight increase is a sign of this adaptation process (Bento et al., Citation2016; Herbach et al., Citation2016; Rauw & Raya, Citation2017; Berger et al., Citation2019). This hypothesis was recently confirmed for pigs by Witt et al. (Citation2023). Analyzing and comparing the adrenal gland weight may thus help in determining and comparing the stress level of wild boars and rearing pigs.
With regard to tail biting, some authors have discussed if pathological changes of the tail may possibly also occur in wild boars (Camerlink & Ursinus, Citation2020). To the authors’ knowledge, except for anecdotal reports, there is no scientific evidence for this. To provide scientific evidence, this study further focused in detail on pathological findings in the tails of wild boars.
Therefore, in the present study, we looked in detail at the health status of wild boars obtained by pathological examinations with the aim to provide an overview of the health status of wild boars and to compare the health findings to those of domestic pigs. Special emphasis was paid to health parameters that might play a causative role in the development of the behavioral disorder tail biting (for example, parameters related to the gut health or respiratory infection as pointed out amongst others by Munsterhjelm et al., Citation2013 and Czycholl et al., Citation2023). We chose young wild boars for comparison, as tail biting in pigs with undocked tails often occurs during the rearing phase (Veit et al., Citation2016). Especially at this young age, signs for an activation of the immune system may well occur without having a clinical relevance, as the immune system has to be challenged to develop (Rook, Citation2009; Stiemsma et al., Citation2015).
Summing up, this study focusses on three research aims: (1) Information gain on the general health status of young wild boars. (2) Compare the health status of wild boars to rearing pigs. This is specifically carried out with regard to the question as to which findings concerning the health status point towards a general activation of the immune system without clinical relevance and in contrast, which findings concerning the health status may be of specific relevance with regard to the pathogenesis of tail biting. (3) Provide a description of pathological findings in the tails of wild boars to answer the question, whether tail biting and/or tail necrosis also occurs in wild boars.
Materials and methods
To reach the formulated research aims, we subjected 13 carcasses of young wild boars killed during routine hunting practice to a thorough pathological examination and compared the respective findings to those of 17 clinically healthy rearing pigs. Moreover, we analyzed 53 additional tails of wild boars pathologically. Those tails were also collected by hunters during routine hunting practices.
Animals and data collection
A call was made to German hunting organizations as well as directly to local hunters, informing them about this project. They were asked to donate young wild boars that they did not want to process further for food production for scientific purpose. In the time period from November 2020 to November 2022, altogether 13 wild boars were collected in this way. In November 2022, another call was made to hunters, but also veterinary inspection offices (that in some communes in Germany collect the tails of wild boars for a specific premium being paid to hunters in the bounds of the combat of African Swine Fever) that specifically tails of wild boars were needed for research purposes. In this way, 53 tails could be collected until end of December 2022.
The rearing pigs were standard cross breds and originated from one conventional farm in Northern Germany, where they were kept according to the national standards. Males were not castrated and tails were undocked. The rearing pigs had been killed for another purpose in another study between June 2019 and March 2021 (approval by national animal research authority: V241 – 10950/2017 (44-4/17)). The rearing pigs all came from one conventional farm in Northern Germany. The piglets were housed in mixed gender groups with an average space allowance of 0.4 m2 per animal. Mash feed was provided ad libitum with an animal to feeding place ratio of 2:1. The drinking system consisted of nipples and bowls, the floor was fully slatted and no bedding material was offered. Plastic sticks, plastic balls, hard wooden sticks and long straw were provided as enrichment material.
Pathological examinations
The 13 wild boar and 17 rearing piglet carcasses were subjected to the same pathological examinations (complete necropsy, including pathohistological examinations of all organ systems) which was carried out according to the standard protocol of the Department of Pathology of the University of Veterinary Medicine Hannover, Foundation. For the pathological examinations, all pigs were placed on the back. In short, this protocol starts with the survey of the preliminary report and the survey of the signalement (animal species, sex, age, color, specific signs, weight). After an assessment of the outside body (condition of the carcass, nutritional status, skin and fur condition, body orifices, mucous membranes), the subcutaneous tissue and muscles are evaluated. All joints are cut open and evaluated as well as the sternum, femur and spine. Along with the spine, also the discs are observed. Moreover, the blood/blood clotting is noted. Thereafter, the inner body is inspected, separated into peritoneal and pelvic cavity as well as the chest cavity. All organs are evaluated regarding their position and appearance as well as larger blood and lymph vessels, lymphatic tissue and large nerve cords. The adrenal glands were carefully dissected from surrounding tissue, measured with a ruler for height, length, width and weighed. The mouth, pharynx and throat are also inspected. All sinuses are cut open and the conches are examined as well as the eyes, in which also the intraocular pressure was measured and the auditory canal along with the bulla tympanica. The brains were extracted in situ for further analysis of the brain structures. Of all organ systems and associated lymph nodes, samples were taken for further pathohistological examinations using standard stains and procedures. A detailed description of the protocol can be found online (Sektionsbericht, Citation2022). Moreover, further information on the variables collected by the use of this protocol can be found in Czycholl et al. (Citation2023).
In the present study, only those variables that were observed in at least one pig are presented and compared between the two groups. Therewith, altogether, 61 variables linked to the health status are analyzed. An overview of the 61 observed variables along with a short description and the measurement scale (numerical or binomial) is provided in . Binomial means that the presence of this finding was coded as 1, the absence as 0. The additional 53 tails were analyzed macroscopically and histologically, again according to the standard protocol of the Department of Pathology of the University of Veterinary Medicine Hannover, Foundation and all findings taken into consideration.
Table 1. Variables of the pathological examination found in wild boars (13) and rearing pigs (17) and P-values of the comparison between the two groups by Chi2 and t-Tests, respectively.
Statistics
All statistical analyses were carried out using SAS® 9.4 (SAS Institute, Cary Inc.). For the comparison of the health status of wild boars and rearing pigs, each of the 61 variables were compared using t-tests and Chi2-tests. In the case of numerical variables (body weight, adrenal gland weight, relative adrenal gland weight), it was first tested that the test assumptions (normal distribution, variance homogeneity) were met by using the procedure PROC UNIVARIATE in SAS. Thereafter, unpaired two-sided t-tests comparing the group of wild boars to the group of rearing pigs were carried out using the procedure PROC TTEST for variables on numerical scale (which were all normally distributed). All other variables were binomial, whereby 0 presented the absence and 1 presented the presence of the respective parameter. Hence, the frequency of affected wild boars in comparison to the frequency of affected rearing pigs was compared by means of a 2 × 2 table, using the procedure PROC FREQ. The general assumptions for the Chi2 test (comparison of categorical variables, independent observations, mutually exclusive cells in the contingency table, sufficient number of observations) were met.
Results
General findings in wild boars
All findings are presented in . Thirteen wild boar carcasses were made available by different hunters in Northern Germany. For the analysis of the tails of these boars, only twelve tails were available, as from one wild boar carcass, the hunter had cut the tail to hand it in to the official authorities in order to get paid a specific premium. Moreover, only 24 adrenal glands could be analyzed, as two could not be found due to internal lesions caused by the shot. Of the 13 wild boars, five were males and eight were females. The lightest wild boar weighed 3.74 kg, the heaviest 19.60 kg (average weight: 8.94 (± 5.20) kg). One wild boar had a deviation in the skin condition, namely a 11 × 5 × 2 cm large hematoma with oedema at the right axilla. In one wild boar, sarcocysts were observed, this wild boar was also diagnosed to have an inflammation in the skeletal musculature. Another wild boar had an inflammation of the N. ischiadicus. In four of the tails, histologically, an eosinophilic dermatitis was found, however, no other changes in the tails were observed. Eight animals presented with eosinophilic pneumonia. All of these and three additional animals (i.e. altogether eleven) had nematodes in their lungs. Other findings in the chest cavity were alveolar histiocytosis, hyperaemia, oedema, emphysema of and hemosiderosis in the lung, hyperplasia and purulent inflammation of different lymphoid tissue, myocarditis and inflammation of the thymus. Findings in the peritoneal cavity were serous effusion, lymphohistiocytic inflammation of the diaphragm and hyperaemia, lymphohistiocytic inflammation as well as milk spots in the liver. Moreover, in three wild boars, a hyperplasia and in one of those also a hyperaemia of the spleen was found. Nematodes were commonly seen in the gut (eight wild boars) and of these eight animals, three also had a gut inflammation. Five wild boars were diagnosed to have a gastritis and in one wild boar, crypt abscesses were found in the colon associated lymphoid tissue. In the evaluation of the oral cavity, pharynx and throat, rhinitis and in the tonsils hyperplasia, purulent inflammations and crypt abscesses were detected. One wild boar had a tongue inflammation as well as nematodes in the tongue. Two wild boars had nematodes in the trachea, of which one also had a tracheitis.
Comparison between findings in wild boars and rearing pigs
In the following, statistically significant differences between wild boars and rearing pigs are stated in more detail. All findings of both groups are shown in along with the P-values obtained from the statistical comparisons. Wild boars were on average lighter than the rearing pig groups (8.94 (±5.20) kg vs. 17.82 (± 6.91) kg (P = 0.0009). Three wild boars, but none of the rearing pigs, were found to be in a thin nutritional status (P = 0.03). The adrenal gland weights in total were lighter in wild boars (right: 1.02 (± 0.32) g vs. 1.33 (± 0.29) g, P = 0.007); left: 1.04 (± 0.31) g vs. 1.39 (± 0.32) g, P = 0.01), however, when corrected for body weight, the relative adrenal gland weight was significantly higher in the wild boars (right: 0.16 (± 0.13) vs. 0.07 (± 0.01), P = 0.01; left: 0.08 (± 0.02), P = 0.0003). While none of the wild boars had scratches on the skin, this was a common finding in rearing pigs (twelve of 17 affected, P = <0.0001). Parasites and findings linked to parasites were only observed in wild boars, whereas statistically significant differences were found for the parameters: (1) lung: nematodes: eleven of 13 (P < 0.0001), (2) liver: milkspots: five of 13 (P = 0.005), (3) gut: nematodes eight of 13 (P = 0.0002). While none of the wild boars had a hyperplasia of the colon associated lymphoid tissue, this was seen in four of 17 rearing pigs (P = 0.05). Likewise, only one of 13 wild boars, but seven of 17 rearing pigs had crypt abscesses in the colon associated lymphoid tissue. In the mesenteric lymph nodes, however, three of 13 wild boars, but none of the rearing pigs had an eosinophilic inflammation (P = 0.03). Rhinitis was less often diagnosed in wild boars (four of 13) compared to rearing pigs (13 of 17, P = 0.01). In the gut, crypt abscesses were not seen in wild boars, but in five of 17 rearing pigs (P = 0.03).
Pathological examination of tails of wild boars
In the histological examination of 53 additional tails of wild boars, in 45 tails, a mild, focal, perivascular, eosinophilic dermatitis was found. In two of those tails, in fact, sections of mites were found. Two other tails had additionally a focal purulent ulcerative dermatitis. In the 13 wild boars, in which the total carcass was examined, four tails with mild, focal, eosinophilic dermatitis were observed in the histologic examination. No other pathological findings were made in the tails. In comparison, findings in the 17 rearing pigs included, in addition to moderate, lymphohistiocytic, confluent dermatitis (n = 2) especially ulcerative forms of dermatitis (n = 6). Furthermore, crusts (n = 4), blood (n = 4), necrosis (n = 5), intralesional bacteria (n = 1) and osteomyelitis (n = 1) were observed in the tails of 17 clinically healthy rearing pigs.
Discussion
General findings in wild boars
Wild boars were specifically affected by different parasitic burdens. Organ systems that were particularly affected included the lung, the gut and the liver. Moreover, less often, signs for parasitic infections were found in the heart in the form of single protozoan intracellular cysts, in the diaphragm and skeletal musculature in the form of sarcocysts, in the tongue and in the trachea (nematodes). Probably, the fact that three of the wild boars were in thin (but not emaciated) body condition can be explained by the parasitological findings, as these three individuals were also affected by nematodes in lung, trachea and gut and one of them of sarcocysts in heart, skeletal musculature and diaphragm and another one of nematodes in the tongue. This hypothesis is supported by the findings of López-Olvera et al. (Citation2006), whereas Dzięciołowski and Clarke (Citation1990) did not find evidence for a clear connection between parasitic burden and nutritional status. Other possible explanations are that one of the animals in thin body condition was a male that had already left the group and might have been challenged by finding new feed sources and other resources without the group. The other two were very young females that were shot in winter, a season where a higher challenge for young animals may be present due to feed availability and outdoor climate. This explanation would fit to the observations concerning seasonal influences of body condition by Dzięciołowski and Clarke (Citation1990). On the tails of the twelve carcasses in which tails were present, signs for external parasites were sometimes observed in the form of a mild, often focal eosinophilic dermatitis. Some of the detected health issues can further be linked to traumatic injuries (e.g. skin alterations and the atrophy of the N. ischiadicus). Additionally, there were findings that can be interpreted as a general activation of the immune system (e.g. the findings in the different lymphoid tissues). Some of the findings can be interpreted as agonal changes (hyperaemia of the lung, liver and spleen, oedema and emphysema of the lung). Generally, these findings are comparable to other studies detecting presumably parasitic infections in feral pig or wild boar populations with the according inflammation responses in the respective tissues (Gipson et al., Citation1999; López-Olvera et al., Citation2006). Although many of the indicators of the general activation of the immune system are most probably also linked to the parasitic infections, in general, these signs of activation of the immune system (in particular, hyperplasia of the spleen and lymphoid tissue as well as signs of inflammation in lymphoid tissues) may also be linked to the general development of the immune system in wild boars, as it is fact that the immune system needs to be challenged to develop (Rook, Citation2009; Stiemsma et al., Citation2015).
Comparison between findings in wild boars and rearing pigs
In contrast to the frequent findings linked to parasitic infections in wild boars, none were observed in rearing pigs. These differences between the groups were of statistical significance and are linked to the high hygiene status and the use of anthelminthics in modern pig husbandry (Nansen & Roepstorff, Citation1999; Madec, Citation2005) and is a common finding also when comparing indoor to outdoor systems or systems with rather poor hygiene (Davies, Citation2011). Significantly more inflammations and proliferations of different lymph nodes were found in wild boars, which can probably be linked to the occurrence of nematodes in the lungs. However, despite the frequent findings of nematodes in the gut, colon associated lymphoid tissue as well as the gut itself (crypt abscesses) where more often affected in rearing pigs. This can possibly be explained by nutritional challenges by the weaning process, which supports the findings of Czycholl et al. (Citation2023) who also detected signs of nutritional challenges specifically pronounced in tail biters. Weaning in wild boars and semi-naturally kept pigs is usually a gradual process over several months (Newberry & Wood-Gush, Citation1985; Jensen & Recén, Citation1989; Veit et al., Citation2016), while pigs used in this study were weaned at an age of 28 days (according to the standard procedure on conventional farms in Germany), which can be seen as a quite abrupt and stressful event in the life of pigs (Veit et al., Citation2016). It is well known that rearing pigs may be affected by diarrhoea and enteritis (post-weaning diarrhoea), which has led to multiple standard treatments in pig husbandry, which are discussed very controversially for different reasons and partly forbidden by politics (Diana et al., Citation2017; Rhouma et al., Citation2017; Eriksen et al., Citation2021). The fact that the wild boars in this study, including also two older wild boars that were most probably already weaned as they were without a group, did not show these pathological changes demonstrates that these findings should not be regarded as normal and are caused by husbandry practices. Likewise, while none of the wild boars was observed to have scratches on the skin, this was a typical finding in the rearing pigs. Again, such scratches are a common finding in rearing pigs (Stukenborg et al., Citation2012; Desire et al., Citation2016) as they are usually mixed in a new group after rearing and thus, rank fights occur frequently in the first few days (Stukenborg et al., Citation2011; Büttner et al., Citation2015). Fights for rank order in young wild boars are uncommon as the animals are familiar with each other as no mixing of groups usually occurs (Meynhardt, Citation1984; Jensen & Recén (Citation1989); Stolba & Wood-Gush, Citation1989). Again, this finding highlights that one should be cautious in simply getting used to this finding as it is so frequent as it cannot be regarded as normal. Solutions such as gradual weaning (van Nieuwamerongen et al., Citation2017), group housing suckling systems, in which the piglets from different litters become habituated to each other before rearing (Bohnenkamp et al., Citation2013; Grimberg-Henrici et al., Citation2019) or family pens (Stolba & Wood-Gush, Citation1984) may be more species-appropriate. Although wild boars were not unaffected, significantly more rearing pigs were diagnosed to have a rhinitis. Rhinitis is usually caused by bacterial or viral infections and has been described as typical infection disease of the upper airways in domestic as well as in wild pigs (Fritze, Citation1983; Rutter & Luther, Citation1984; Lutz, Citation1988; Chanter et al., Citation1989). There are hints for a higher prominence in pig husbandry than in the wild (Lutz, Citation1988), which may be due to a higher infection pressure in husbandry and potentially an easier and faster disease spread among the pigs (Lutz, Citation1988; Drew, Citation2011; Andres & Davies, Citation2015; Salines et al., Citation2020). Moreover, Hamilton et al. (Citation1996) and Hamilton et al. (Citation1999) proved the connection of rhinitis occurrence to air quality (ammonia level, dust) in pig husbandry, which also contributed to the explanation that rhinitis was more often found in rearing pigs than wild boars. Lastly, none of the carcasses of the wild boars showed signs of tail necrosis while five of the rearing pigs were affected. However, also the rearing pigs affected by tail necrosis did not show signs of a generalized necrosis syndrome, as described by Reiner et al. (Citation2021) in addition to the tails in the pathological examination.
The weight of adrenal glands was included in this study, as it might be an indicator of chronic stress (Czycholl et al., Citation2023; Witt et al., Citation2023) and we wanted to draw a conclusion about the stress level of wild boars in comparison to rearing pigs. While the total adrenal gland weight was significantly higher for rearing pigs, the relative adrenal gland weight, i.e. the adrenal gland weight corrected for body weight (as the organ’s weight depends on body weight as shown e.g. by Bento et al. (Citation2016) and Herbach et al. (Citation2016)), was significantly higher in wild boars. This could, on the one hand, mean that the wild boars perceived more stress than the rearing pigs. However, it is well known that the domestication process had significant influences on the stress susceptibility of the domesticated species, i.e. changes in stress hormone release, receptor density and gene expression as well as morphological changes to gland tissue occurred by selection for animals being less prone to stress (Trut et al., Citation2009; Humayun et al., Citation2012). Hence, this finding can most probably be explained by the fact that a wild species was compared to a domesticated species. Likewise, the significantly lighter body weight of wild boars can be explained by the domestication process (Trut et al., Citation2009; Rauw & Raya, Citation2017).
Pathological examination of tails of wild boars
In the pathohistological examination of the additional 53 tails of wild boars, in 45 tails, signs of mild, focal, perivascular, lymphohistiocytic and / or eosinophilic dermatitis were detected, which are most probably linked to external parasites such as ticks, mosquitos or mites. In fact, in two of the pathohistological sections, sections of mites were visible, supporting this hypothesis and probable causation. Affection by mites in wild boars and feral pigs has been described by other authors (Haas et al., Citation2015; Sannö et al., Citation2021; Valldeperes et al., Citation2021), whereby the prevalence in the German population remains, up to the authors’ knowledge, unknown. In two other tails, in addition, a focal purulent ulcerative dermatitis was found, whereby the most probable causation is traumatic injury with secondary bacterial infection. No signs of tail biting or tail necrosis were observed. Hence, in the present study, which is to the authors’ knowledge the first one to publish results on a larger sample of tails of wild boars analyzed scientifically, no signs of tail biting or tail necrosis were observed, supporting the general hypothesis that tail biting is a true behavioral disorder, thus only occurs in the domesticated species (Taylor et al., Citation2010) and is linked to modern indoor pig production systems, although also observed with lower prevalence in outdoor pig production and semi-naturally kept pigs (Sonoda et al., Citation2013).
Limitations of the study
The study is based on a low sample size, as it proved difficult to obtain carcasses from young wild boars. Hence, the presented data should be understood as a descriptive statistic approach and statistical differences obtained should be interpreted with caution. Moreover, it could not be controlled for the age of the wild boars obtained and the age could only be roughly estimated. Hence, differences could also be due to age differences or simply differences with regard to the comparison of wild and domesticated form (e.g. concerning maturity of the immune system). Hence, this study provides first insights and points at directions, but results cannot be simply generalized.
Conclusion
The aims of the study were to: (1) Describe the general health status of young wild boars, (2) Compare the health status of wild boars to rearing pigs with regard to the question, which findings concerning an activation of the immune system may be of relevance with regard to tail biting; (3) Describe pathological findings in the tail of wild boars with regard to typical findings linked to tail biting. Overall, it can be concluded that wild boars are not in general healthier than rearing pigs (or vice versa), however, the causes for the diseases differ and are in wild boars especially linked to parasitic burden. In wild boars as well as in rearing pigs, a general activation of the immune system can be observed. Interestingly, despite nematodes only present in the gut of wild boars, the gut seems to be specifically challenged in the rearing pigs which may possibly be explained by a nutritional and the general systemic challenge due to early weaning. Finally, there is no scientifically proven evidence for tail necrosis or tail biting in the wild boar population.
Ethics approval
The wild boars were killed during routine hunting practices, which was intensified also to very young wild boars, which are not always used for food production, due to the combat of African Swine Fever in Germany. All rearing pigs were farmed animals kept according to the standards in Germany. They were part of a larger control group in another study and thus killed for another purpose, for which the national animal research authority gave approval (V241 – 10950/2017 (44-4/17)).
Author contributions
IC designed and conceived the study; IC, JK, WB were responsible for the project administration; IC acquainted funding; IC, CP, WB collected the data; IC, KB analyzed and interpreted the data; CP, WB, JK provided resources; IC wrote the original manuscript; KB, CP reviewed and edited the manuscript. All authors have read and agreed to the submitted version of the manuscript.
Acknowledgements
The authors wish to acknowledge support of the QS research fund in a former project which allowed creation of the present study, as well as all hunters that donated carcasses or tails.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Data availability statement
All data is available from the corresponding author upon reasonable request.
Additional information
Funding
References
- Al Dahouk, S., Nöckler, K., Tomaso, H., Splettstoesser, W. D., Jungersen, G., Riber, U., Petry, T., Hoffmann, D., Scholz, H. C., Hensel, A. & Neubauer, H. (2005). Seroprevalence of brucellosis, tularemia, and yersiniosis in wild boars (Sus scrofa) from north-eastern Germany. Journal of Veterinary Medicine, Series B, 52(10), 444–455.
- Andres, V. M. & Davies, R. H. (2015). Biosecurity measures to control Salmonella and other infectious agents in pig farms: A review. Comprehensive Reviews in Food Science and Food Safety, 14(4), 317–335.
- Bento, P. L., Center, S. A., Randolph, J. F., Yeager, A. E. & Bicalho, R. C. (2016). Associations between sex, body weight, age, and ultrasonographically determined adrenal gland thickness in dogs with non-adrenal gland illness. Journal of the American Veterinary Medical Association, 248(6), 652–660.
- Berger, I., Werdermann, M., Bornstein, S. R. & Steenblock, C. (2019). The adrenal gland in stress – adaptation on a cellular level. The Journal of Steroid Biochemistry and Molecular Biology, 190, 198–206.
- Bohnenkamp, A.-L., Traulsen, I., Meyer, C., Müller, K. & Krieter, J. (2013). Comparison of growth performance and agonistic interaction in weaned piglets of different weight classes from farrowing systems with group or single housing. Animal, 7(2), 309–315.
- Büttner, K., Scheffler, K., Czycholl, I. & Krieter, J. (2015). Network characteristics and development of social structure of agonistic behaviour in pigs across three repeated rehousing and mixing events. Applied Animal Behaviour Science, 168, 24–30.
- Camerlink, I. & Ursinus, W. W. (2020). Tail postures and tail motion in pigs: A review. Applied Animal Behaviour Science, 230, 105079.
- Cano-Manuel, F. J., López-Olvera, J., Fandos, P., Soriguer, R. C., Pérez, J. M. & Granados, J. E. (2014). Long-term monitoring of 10 selected pathogens in wild boar (Sus scrofa) in Sierra Nevada National Park, southern Spain. Veterinary Microbiology, 174(1-2), 148–154.
- Chanter, N., Magyar, T. & Rutter, J. M. (1989). Interactions between Bordetella bronchiseptica and toxigenic Pasteurella multocida in atrophic rhinitis of pigs. Research in Veterinary Science, 47(1), 48–53.
- Cilia, G., Bertelloni, F., Piredda, I., Ponti, M. N., Turchi, B., Cantile, C., Parisi, F., Pinzauti, P., Armani, A., Palmas, B. & Noworol, M. (2020). Presence of pathogenic Leptospira spp. in the reproductive system and fetuses of wild boars (Sus scrofa) in Italy. PLOS Neglected Tropical Diseases, 14(12), e0008982.
- Czycholl, I., Büttner, K., Becker, D., Schwennen, C., Baumgärtner, W., Otten, W., Wendt, M., Puff, C. & Krieter, J. (2023). Are biters sick? Health status of tail biters in comparison to control pigs. Porcine Health Management, 9(1), 1–18.
- Davies, P. R. (2011). Intensive swine production and pork safety. Foodborne Pathogens and Disease, 8(2), 189–201.
- D’Eath, R. B., Jack, M., Futro, A., Talbot, D., Zhu, Q., Barclay, D. & Baxter, E. M. (2018). Automatic early warning of tail biting in pigs: 3D cameras can detect lowered tail posture before an outbreak. PLoS One, 13(4), e0194524.
- de Mendoza, J. H., Parra, A., Tato, A., Alonso, J. M., Rey, J. M., Peña, J., García-Sánchez, A., Larrasa, J., Teixidó, J., Manzano, G. & Cerrato, R. (2006). Bovine tuberculosis in wild boar (Sus scrofa), red deer (Cervus elaphus) and cattle (Bos taurus) in a Mediterranean ecosystem (1992–2004). Preventive Veterinary Medicine, 74(2-3), 239–247.
- Desire, S., Turner, S. P., D’Eath, R. B., Doeschl-Wilson, A. B., Lewis, C. R. G. & Roehe, R. (2016). Prediction of reduction in aggressive behaviour of growing pigs using skin lesion traits as selection criteria. Animal, 10(8), 1243–1253.
- Diana, A., Manzanilla, E. G., Calderón Díaz, J. A., Leonard, F. C. & Boyle, L. A. (2017). Do weaner pigs need in-feed antibiotics to ensure good health and welfare? PLoS One, 12(10), e0185622.
- Drew, T. W. (2011). The emergence and evolution of swine viral diseases: To what extend have husbandry systems and global trade contributed to their distribution and diversity? Revue Scientifique et Technique de l'OIE, 30(1), 95–106.
- Dzięciołowski, R. M. & Clarke, C. M. H. (1990). Physical condition and ectoparasite infestation of feral pigs in New Zealand. Acta Theriologica, 35(3-4), 299–309.
- Edwards, S. & Valros, A. (2021). Understanding and preventing tail biting in pigs. In Sandra Edwards (Ed.), Understanding the behaviour and improving the welfare of pigs (Cambridge, UK: Burleigh Dodds Science Publishing), pp. 361–400.
- Eriksen, EØ, Kudirkiene, E., Christensen, A. E., Agerlin, M. V., Weber, N. R., Nødtvedt, A., Nielsen, J. P., Hartmann, K. T., Skade, L., Larsen, L. E. & Pankoke, K. (2021). Post-weaning diarrhea in pigs weaned without medicinal zinc: Risk factors, pathogen dynamics, and association to growth rate. Porcine Health Management, 7(1), 1–19.
- Fritze, U. (1983). Rhinitis atrophicans beim europäischen Wildschwein (Sus scrofa scrofa L. 1758) nach natürlicher und experimenteller Infektion. Dissertation. Tierärztliche Hochschule.
- Gipson, P. S., Veatch, J. K., Matlack, R. S. & Jones, D. P. (1999). Health status of a recently discovered population of feral swine in Kansas. Journal of Wildlife Diseases, 35(3), 624–627.
- Grimberg-Henrici, C. G. E., Büttner, K., Lohmeier, R. Y., Burfeind, O. & Krieter, J. (2019). The effect of group-housing with free-farrowing pens on reproductive traits and the behaviour of low-risk and high-risk crushing sows. Applied Animal Behaviour Science, 211, 33–40.
- Grümpel, A., Krieter, J., Veit, C. & Dippel, S. (2018). Factors influencing the risk for tail lesions in weaner pigs (Sus scrofa). Livestock Science, 216, 219–226.
- Haas, C., Rossi, S., Meier, R. & Ryser-Degiorgis, M. P. (2015). Evaluation of a commercial ELISA for the detection of antibodies to Sarcoptes scabiei in wild boar (Sus scrofa). Journal of Wildlife Diseases, 51(3), 729–733.
- Hamilton, T. D., Roe, J. M., Hayes, C. M., Jones, P., Pearson, G. R. & Webster, A. J. F. (1999). Contributory and exacerbating roles of gaseous ammonia and organic dust in the etiology of atrophic rhinitis. Clinical Diagnostic Laboratory Immunology, 6(2), 199–203.
- Hamilton, T. D., Roe, J. M. & Webster, A. J. (1996). Synergistic role of gaseous ammonia in etiology of Pasteurella multocida-induced atrophic rhinitis in swine. Journal of Clinical Microbiology, 34(9), 2185–2190.
- Henry, M., Jansen, H., del Rocio Amezcua, M., O’Sullivan, T. L., Niel, L., Shoveller, A. K. & Friendship, R. M. (2021). Tail-biting in pigs: A scoping review. Animals, 11(7), 2002.
- Herbach, N., Wiele, K., Konietschke, U. & Hermanns, W. (2016). Pathologic alterations of canine and feline adrenal glands. The Journal of Pathology, 6(03), 140.
- Humayun, K. A. K. M., Aoyama, M. & Sugita, S. (2012). Morphological and histological studies on the adrenal gland of the chicken (Gallus domesticus). The Journal of Poultry Science, 49(1), 39–45.
- Jensen, P. (2017). The Ethology of Domestic Animals: An Introductory Text: Cabi (Oxfordshire, UK: CABI Publishing).
- Jensen, P. & Recén, B. (1989). When to wean — observations from free-ranging domestic pigs. Applied Animal Behaviour Science, 23(1-2), 49–60.
- López-Olvera, J. R., Höfle, U., Vicente, J., Fernández-de-Mera, I. & Gortázar, C. (2006). Effects of parasitic helminths and ivermectin treatment on clinical parameters in the European wild boar (Sus scrofa). Parasitology Research, 98(6), 582–587.
- Lutz, W. (1988). Verbiegungen des Gesichtsschädels beim Wildschwein (Sus scrofa scrofa L.) als mögliche Folge einer Rhinitis atrophicans. Zeitschrift für Jagdwissenschaften, 34(2), 125–131.
- Madec, F. (2005). The role of animal hygiene and health management in pig production. Proceedings of the XIIth International Congress, International Society for Animal Hygiene (ISAH).
- Meier, R. K. & Ryser, M. P. (2018). Wild boar and infectious diseases: Evaluation of the current risk to human and domestic animal health in Switzerland: A review. Schweizer Archiv fuer Tierheilkunde, 160(7-8), 443–460.
- Meynhardt, H. (1984). Schwarzwildreport: Mein Leben unter Wildschweinen (Kiel: Neumann Verlag).
- Moinard, C., Mendl, M., Nicol, C. J. & Green, L. E. (2003). A case control study of on-farm risk factors for tail biting in pigs. Applied Animal Behaviour Science, 81(4), 333–355.
- Munsterhjelm, C., Nordgreen, J., Aae, F., Heinonen, M., Valros, A. & Janczak, A. M. (2019). Sick and grumpy: Changes in social behaviour after a controlled immune stimulation in group-housed gilts. Physiology & Behavior, 198, 76–83.
- Munsterhjelm, C., Simola, O., Keeling, L., Valros, A. & Heinonen, M. (2013). Health parameters in tail biters and bitten pigs in a case–control study. Animal, 7(5), 814–821.
- Nansen, P. & Roepstorff, A. (1999). Parasitic helminths of the pig: Factors influencing transmission and infection levels. International Journal for Parasitology, 29(6), 877–891.
- Newberry, R. C. & Wood-Gush, D. G. M. (1985). The suckling behaviour of domestic pigs in a semi-natural environment. Behaviour, 95(1-2), 11–25.
- Nordgreen, J., Edwards, S. A., Boyle, L. A., Bolhuis, J. E., Veit, C., Sayyari, A., Marin, D. E., Dimitrov, I., Janczak, A. M. & Valros, A. (2020). A proposed role for pro-inflammatory cytokines in damaging behavior in pigs. Frontiers in Veterinary Science, 7, 646.
- Nordgreen, J., Munsterhjelm, C., Aae, F., Popova, A., Boysen, P., Ranheim, B., Heinonen, M., Raszplewicz, J., Piepponen, P., Lervik, A. & Valros, A. (2018). The effect of lipopolysaccharide (LPS) on inflammatory markers in blood and brain and on behavior in individually-housed pigs. Physiology & Behavior, 195, 98–111.
- Rauw, W. M. & Raya, L. G. (2017). Effects of stress on growth and development: From domestication to factory farming. In Colin G. Scanes & Rodney A. Hill (Eds.), Biology of Domestic Animals (Boca Raton, FL: CRC Press), pp. 241–265.
- Reiner, G., Kuehling, J., Loewenstein, F., Lechner, M. & Becker, S. (2021). Swine inflammation and necrosis syndrome (SINS). Animals, 11(6), 1670.
- Rhouma, M., Fairbrother, J. M., Beaudry, F. & Letellier, A. (2017). Post weaning diarrhea in pigs: Risk factors and non-colistin-based control strategies. Acta Veterinaria Scandinavica, 59(1), 1–19.
- Roic, B., Jemersic, L., Terzic, S., Keros, T., Balatinec, J. & Florijancic, T. (2012). Prevalence of antibodies to selected viral pathogens in wild boars (Sus scrofa) in Croatia in 2005–06 and 2009–10. Journal of Wildlife Diseases, 48(1), 131–137.
- Rook, G. (2009). Review series on helminths, immune modulation and the hygiene hypothesis: The broader implications of the hygiene hypothesis. Immunology, 126(1), 3–11.
- Ruiz-Fons, F., Segalés, J. & Gortázar, C. (2008). A review of viral diseases of the European wild boar: Effects of population dynamics and reservoir rôle. The Veterinary Journal, 176(2), 158–169.
- Rutter, J. M. & Luther, P. D. (1984). Cell culture assay for toxigenic Pasteurella multocida from atrophic rhinitis of pigs. Veterinary Record, 114(16), 393–396.
- Salines, M., Rose, N. & Andraud, M. (2020). Tackling hepatitis E virus spread and persistence on farrow-to-finish pig farms: Insights from a stochastic individual-based multi-pathogen model. Epidemics, 30, 100369.
- Sannö, A., Ander, M., Ågren, E. & Troell, K. (2021). Sarcoptic mange in the wild boar, Sus scrofa, in Sweden. Current Research in Parasitology & Vector-Borne Diseases, 1, 100060.
- Schrøder-Petersen, D. L. & Simonsen, H. B. (2001). Tail biting in pigs. The Veterinary Journal, 162(3), 196–210.
- Sektionsbericht (2022). Anleitung zur Anfertigung eines Sektionsberichtes. Institut für Pathologie, Stiftung Tierärztliche Hochschule Hannover, Hannover, Germany, April 2022. Accessed 25 November 2023, available at: https://www.tiho-hannover.de/fileadmin/20_Pathologie/Anleitung-Sektionsbericht_12.04.2022.pdf.
- Sonoda, L. T., Fels, M., Oczak, M., Vranken, E., Ismayilova, G., Guarino, M., Viazzi, S., Bahr, C., Berckmans, D. & Hartung, J. (2013). Tail biting in pigs—causes and management intervention strategies to reduce the behavioural disorder. A review. Berliner Munchener Tierarztliche Wochenschrift, 126(3-4), 104–112.
- Stiemsma, L. T., Reynolds, L. A., Turvey, S. E. & Finlay, B. B. (2015). The hygiene hypothesis: Current perspectives and future therapies. ImmunoTargets and Therapy, 4, 143.
- Stolba, A. & Wood-Gush, D. G. M. (1984). The identification of behavioural key features and their incorporation into a housing design for pigs. Annales de recherches veterinaires, 15(2), 287–302.
- Stolba, A. & Wood-Gush, D. G. M. (1989). The behaviour of pigs in a semi-natural environment. Animal Sciences, 48(2), 419–425.
- Stukenborg, A., Traulsen, I., Puppe, B., Presuhn, U. & Krieter, J. (2011). Agonistic behaviour after mixing in pigs under commercial farm conditions. Applied Animal Behaviour Science, 129(1), 28–35.
- Stukenborg, A., Traulsen, I., Stamer, E., Puppe, B. & Krieter, J. (2012). The use of a lesion score as an indicator for agonistic behaviour in pigs. Archives Animal Breeding, 55(2), 163–170.
- Taylor, N. R., Main, D. C. J., Mendl, M. & Edwards, S. A. (2010). Tail-biting: A new perspective. The Veterinary Journal, 186(2), 137–147.
- Trut, L., Oskina, L. & Kharlamova, A. (2009). Animal evolution during domestication: The domesticated fox as a model. Bioessays, 31(3), 349–360.
- Valldeperes, M., Moroni, B., Rossi, L., López-Olvera, J. R., Velarde, A., Molinar, R. M., Mentaberre, G., Serrano, E., Angelone, S., Lavín, S. & Granados, J. E. (2021). First report of interspecific transmission of sarcoptic mange from Iberian ibex to wild boar. Parasites & Vectors, 14, 1–13.
- Valros, A. (2022). The tale of the Finnish pig tail–how to manage non-docked pigs? Animal, 16, 100353.
- Valros, A. & Heinonen, M. (2015). Save the pig tail. Porcine Health Management, 1(1), 1–7.
- van Nieuwamerongen, S. E., Soede, N. M., van der Peet-Schwering, C. M. C., Kemp, B. & Bolhuis, J. E. (2017). Gradual weaning during an extended lactation period improves performance and behavior of pigs raised in a multi-suckling system. Applied Animal Behaviour Science, 194, 24–35.
- Veit, C., Foister, S., Valros, A., Munsterhjelm, C., Sandercock, D. A., Janczak, A. M., Ranheim, B. & Nordgreen, J. (2021a). The use of social network analysis to describe the effect of immune activation on group dynamics in pigs. Animal, 15(9), 100332.
- Veit, C., grosse Beilage, E. & Krieter, J. (2016). Review of the behavioural disorder tail biting in pigs. Der Praktische Tierarzt, 97(3), 232–241.
- Veit, C., Janczak, A. M., Ranheim, B., Vas, J., Valros, A., Sandercock, D. A., Piepponen, P., Dulgheriu, D. & Nordgreen, J. (2021b). The effect of LPS and ketoprofen on cytokines, brain monoamines, and social behavior in group-housed pigs. Frontiers in Veterinary Science, 7, 617634.
- Witt, J., Krugmann, K., Wilder, T., Krieter, J., Bussemas, R., Witten, S. & Czycholl, I. (2023). Nebennieren als potentieller Tierwohlindikator bei Schweinen. Züchtungskunde, 95(4), 241–254.