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South African Journal of Animal Science
On-line version ISSN 2221-4062
Print version ISSN 0375-1589
S. Afr. j. anim. sci. vol.52 n.6 Pretoria 2022
http://dx.doi.org/10.4314/sajas.v52i6.10
Pre-rut behavioural changes in farmed red deer with reference to atmospheric conditions
K. TajchmanI, #; P. JaniszewskiII; Z. Steiner-BogdaszewskaIII; F. CeaceroIV
IDepartment of Animal Ethology and Wildlife Management, Faculty of Animal Sciences and Bioeconomy, University of Life Sciences in Lublin, Akademicka 13, 20-950 Lublin, Poland
IIDepartment of Fur-bearing Animal Breeding and Game Management, University of Warmia and Mazury in Olsztyn, Oczapowskiego 2, 10-719 Olsztyn, Poland, janisz@uwm.edu.pl
IIIInstitute of Parasitology of the Polish Academy of Sciences, Research Station in Kosewo Górne, 11-700 Mrqgowo, Poland, kosewopan@kosewopan.pl
IVDepartment of Animal Science and Food Processing, Czech University of Life Sciences Prague, Kamycka 129, 165 00 Praha - Suchodol, Czech Republic, ceacero@ftz.czu.cz
ABSTRACT
Red deer (Cervus elaphus) exhibit specific behaviour during the rutting season, which may have an impact on the safety on cervid farms, both due to aggressive interactions between animals and the safety of people staying there, such as staff and tourists. This issue applies especially to stags whose behaviour changes radically, and the correct interpretation of the observed changes is very important. Therefore, the aim of the study was to analyse the pre-rut behaviour of stags and to show the influence of atmospheric conditions on vocalization and other elements of their behaviour, which facilitate determination of the onset of the rutting season. The observations were conducted in August and September of 2017 and 2018. It was shown that lower temperatures, declines in air humidity, increasing atmospheric pressure, and transition of the moon phase towards the full moon resulted in intensification of the vocalization activity in the red deer in the pre-rutting season, which may accelerate the rutting period in the deer males. The number of vocalizations varied between the years and depended on the mean temperature, air humidity, atmospheric pressure, and moon phase in the pre-rutting and rutting seasons. Through observation of the changing weather conditions, it is possible to predict the time of increased activity of stags and the onset of the rutting period. Predicting the date of mating season in farm breeding, based on daily observations of changes in the behaviour of stags, can be helpful in planning veterinary treatments or selecting the composition of the hinds to be covered by specific stags, which can also contribute to the improvement of their welfare.
Keywords: Cervus elaphus, mating season, vocalization, temperature, rainfall, air pressure
Introduction
Sounds made by animals convey species- and specimen-specific information. Natural selection and evolution have increased the importance of individual signals through ritualization (Rogers & Kaplan, 2002). As in most mammals characterized by sexual dimorphism, the reproductive success of male red deer depends on the competition with other males for access to females (Bartoš, 1986; McComb, 1991). Giving off a full and strong roar by a stag requires good individual quality and appropriate age, which is associated with the development of the vocal apparatus (Fitch & Reby, 2001; Feighny et al., 2006; Riede & Titze, 2008; Frey et al., 2012; Frey & Riede, 2013). During the rutting period, red deer (Cervus elaphus L., 1758) vocalize to get females and to form harems, which is the most important function of male vocalization: to attract females to their territories and discourage competitors from fighting (Garcia et al., 2013). Vocalizations in the rutting period are part of courtship, as they can accelerate ovulation in the hinds (McComb, 1987). Vocalization is used by females to find a mate and contributes to accelerated rutting and may prevent fights and unnecessary energy expenditure in competing males (Clutton-Brock et al., 1979; Reby & McComb, 2003; Reby et al. 2005). It is also worth emphasizing that most hinds conceive at the first ovulation (Guinness et al., 1971); therefore, usually at the onset of the mating season, the stag must be ready to fertilize the largest number of females at the beginning of the rutting season to be successful in transferring genes to the largest number of offspring. As shown by Reby & McComb (2003), stags with the highest number of matings initiated their vocal activity at the onset of the rutting season and continued the vocalization over most of the following days of the rutting period. The females therefore chose the male based on their long-term investment in vocal activity. The pre-rutting period and the effort made by the male at that time are probably more important and exert an impact on the number of fertilized females. Additionally, previous intense efforts, which may be manifested in changes in the stag behaviour, can lead to success in forming a larger harem (Reby & McComb 2003).
Vocal activity is an important part of advertising male reproductive potential in red deer (Volodin et al., 2016). It has been shown that older and larger males producing lower-frequency sounds were preferred by females. In this way, hinds ensure their safety during mating and have the prospect of better offspring (Charlton et al., 2007). The mating behaviour of Cervus eíaphus males is rather associated with the defence of their harem (Struhsaker, 1967; Clutton-Brock et al., 1982), i.e., usually mobile groupings in which females are tracked and defended by males. The vocal activity of stags varies depending on the season of the year, time of the day, or age of the animal (Volodin et al., 2016). Additionally, climate change, rising temperatures, changing rainfall, and wind can affect animal activity (Walther et al., 2002; Bowler et al., 2017). It was confirmed in Spain that a decrease in rainfall was associated with a delayed rutting season and decreased rutting intensity, but appeared to favour a higher degree of polygyny and opportunity for sexual selection (Post et al., 1997; Millán et al., 2021). The mating season in red deer has been well described by researchers; however, the time preceding the season, preparation, and behaviour of animals before the rut have been insufficiently explored. It is especially important in farm breeding where deer retain much of the wild characteristics, especially males during rut (Bartoš, 1986). In farmed cervids, it is beneficial for females to get pregnant as soon as possible and at the same time because fawns will be born earlier, which will provide them with better early growth and a proper body weight, which is very important for surviving winter. However, hinds need to have a certain body condition to enter oestrus and the males should be ready for rutting or the following oestrus will take 20 days. Moreover, it is also important in male management that they are replaced once they get exhausted, and to ensure that hinds not pregnant after first cycle will be in the second cycle (Haigh & Hudson, 1993; Mulley, 2007). Predicting the date of the rutting period in farm breeding, based on daily observations of changes in the behaviour of stags, would be of great cognitive and practical importance. Appropriate analysis of behavioural changes by deer breeders can be helpful in determining the date of separating males into separate pastures, planning veterinary treatments or selecting the composition of the hinds to be covered by specific stags, which can also contribute to the improvement of their welfare (Janiszewski et al., 2016; Dziki-Michalska et al., 2021).
Therefore, the aim of the research was to analyse changes in pre-rut behaviour of stags and show the impact of weather conditions on vocalization and other behavioural elements in farmed male red deer that facilitate recognition of the onset of the mating season.
Material and method
Experimental design
The research was carried out at the Research Station of the Institute of Parasitology, Polish Academy of Sciences, Kosewo Górne (Region of Warmia and Mazury; Poland; N: 53o48'; E: 21o23'). In the first year of the study (2017), seven red deer stags aged 2 to 9 years were observed (named: Dziki, 9 years old; Niko, 6 years old; Hubert, 4 years old; Florek and Jasiek, 3 years old; Neo and C12, 2 years old). In the second year (2018), the observations involved the same five stags (except C12 and Jasiek). Stags in both years were kept in summer paddocks in contact with a herd of 40-45 hinds. The breeding system consisted of rotational access to pasture in the paddocks with a density and nutritional scheme recommended by FEDFA (2020) and Mattiello (2009). In 2017, the herd was monitored in terms of mating behaviour. In 2017 and 2018, the frequency and duration of vocalization as well as weather conditions were recorded. At the beginning of the study, the deer were observed for 24 h to establish the time of day with the highest intensity of the vocal activity of the stags. This indicated that the observations should be carried out for one hour in the morning and three hours in the evening. The study was conducted for two months (August, September) in 2017 and 2018 from 05:00 to 06:00 and from 20:00 to 23:00 every other day. A ZOOM H6 sound recorder, a Nikon D70s camera, binoculars, and a Night Vision Scope NV5x60 devices were used to record the sounds produced by the stags and observe their behaviour. The weather conditions were recorded using a thermometer with a hygrometer and weather maps from a nearby meteorological station (Institute of Meteorology and Water Management; Maritime Department; Meteorological station). At the beginning of the study, the herd was accustomed to the presence of the observer. The observations were made at a distance of 2-10 m from the animal group; after 20 min, the animals ignored the presence of the observer. The numbers on the ear tags and diagrams of stags' antlers were used to identify the individual specimens (Fig. 1).
During the observations, all behaviours of the stags were recorded. These included vocalization, i.e., a single roar or few roars per event, being in a male group, stag fights, fighting against vegetation with antlers, chasing the hinds, flehmen response, urinating on the lower abdomen, and other behaviours, which are listed and described in the ethogram (Table 1).
To carry out statistical analyses, the observation period was divided into two terms: pre-rut and early rut. The two periods were delimited by a sudden increase in the number of vocalizations indicating the onset of the rutting period. The most frequent behaviours of the stags (Table 1) were selected for the analysis: vocalization, flehmen response, attempts to fight, staying in a group of males, thrashing the vegetation, and chasing the hinds.
Statistical analysis
The results are expressed as the mean value and standard deviation. The Shapiro-Wilk test was used for the analysis of the distribution of the studied variables. A mixed linear model (GLMmix procedure of SAS software; Statistical Analysis System, 9.4, 2013) was used, in which the following factors were used as constant factors: year, time, and also as regressors: temperature, air humidity, rainfall, atmospheric pressure, wind speed, and moon phase as affecting vocalization. The introduction to the linear model of the day as a random factor and the interaction of the year and time due to the large number of null solutions caused problems with the matrix inversion and, consequently, the singularity of the model.
The Mann-Whitney test were used to compare the vocalizations between the years, and the Student's f-test was used to compare the atmospheric conditions between the years. The simple correlations between the number of vocalizations and other behaviours and the atmospheric conditions were assessed using the r-Pearson correlation coefficient and the Spearman rank correlation coefficient. All relationships were evaluated at the significance level of P <0.05. The statistical analyses were performed using Statistica 9.1 software (StatSoft, Poland).
Results
Inter-year differences
During the observations in the pre-rutting period, the average air temperature was 15.61 oC, i.e., almost five degrees higher than in the mating season; similar to the average air humidity. The average precipitation rate was substantially higher in the pre-rutting period than during the mating season. The average atmospheric pressure and wind force were similar in both observation periods (Table 2).
The comparison of the observations carried out in 2017 and 2018 demonstrated that the air temperature fluctuated largely in the first year of the study. A marked decrease was observed at the beginning of September, which resulted in the acceleration and increase in the frequency of vocalization by almost two days. In mid-September 2017, the air temperature decreased again, which also contributed to intensification of the roaring activity of the stags (Fig. 2).
The number of vocalizations in 2017 and 2018 was compared with reference to the weather conditions in the pre-rutting period. The vocalization emitted by the stags and the average length of a single roar in the pre-rutting period did not differ substantially between the years (Table 3). However, there were substantial differences between 2017 and 2018 in the sum of single vocalizations, the number of morning and evening vocalizations at 20:00-21:00 and 22:00-23:00, and the sum of evening vocalizations during the early rutting season (P <0.05) (Table 3).
The pre-rutting period differed between 2017 and 2018 in terms of the mean temperature (lower mean temperature recorded in 2017), air humidity in the evening, atmospheric pressure, and wind speed (P <0.05). The mean temperature, atmospheric pressure, and wind force were lower in 2017, and only air humidity in the evening hours was higher than in 2018 (Table 4).
The early mating season differed between 2017 and 2018 in terms of the mean temperature, morning temperature, average humidity, the amount of rainfall, atmospheric pressure, wind strength, and precipitation (P <0.05). The mean temperature, morning temperature, average humidity, and rainfall were higher in 2017, and only the values of atmospheric pressure, wind force, and precipitation were lower than in 2018 (Table 4).
Pre-rutting and rutting period differences
The mean number of vocalizations was almost thirty times higher in the mating season than during the pre-rutting period. In both periods, the stags vocalized more often in the evening than in the morning. Moreover, single roars were almost 1.5 times longer during the rutting season than in the pre-rutting period (Table 2). The number of stag vocalizations was compared with reference to the weather conditions prevailing in the pre-rutting period and during the mating season (Table 5, 6, 7). The influence of the year, temperature, air humidity, atmospheric pressure, and moon phase were evident on the vocalization of farmed deer (P <0.05, Table 5).
The mean number of vocalizations in the morning and evening hours was correlated with the mean temperature at the time of observation (P <0.05) in the pre-rutting period. Moreover, the sum of deer vocalizations increased with a decline in air temperature (P <0.05). A negative correlation was found between the mean temperature and the number of vocalizations between 05:00 and 06:00, between 20:00 and 21:00, and between 21:00 and 22:00 (P <0.05). The sum of evening vocalizations increased with the decrease in the average temperature and at 20:00-21:00 and 21:00-22:00 in the pre-rutting period (P <0.05). There was also a negative correlation of the average air humidity with the sum of vocalizations and the number of sounds produced in the evening (P <0.05). Furthermore, the average air humidity had an impact on the average length of a single vocalization in the pre-rutting period (P <0.05). The average air humidity in the evening had an impact on the number of vocalizations at 20:00-21:00 and 21:00-22:00 and on the average length of a single vocalization of the animals in the pre-rutting period (P <0.05). The mean atmospheric pressure had a positive effect on the number of vocalizations at 20:00-21:00 and 21:00-22:00 in the pre-rutting period (P <0.05). The moon phase exerted a positive effect on the number of vocalizations in the morning and evening hours, the sum of sounds produced in the evening, and the average length of single roars produced by the stags in the pre-rutting period (P <0.05). The precipitation sum and average wind force did not have an impact on the number of sounds produced by the stags in the pre-rutting period (Table 6).
During the mating season, the number of deer vocalizations exhibited a negative correlation with the mean atmospheric pressure in the morning and evening hours (P <0.05). In turn, the phase of the moon had a positive effect on the sum of sounds emitted by the stags and on the number of deer vocalizations at 05:00-06:00 and 21:00 and 22:00 (P <0.05). The number of deer vocalizations during the rutting season was not correlated with the ambient temperature, air humidity, rainfall sum, and wind strength (P< 0.05) (Table 7).
Characterization of pre-rutting and early rutting behaviour
During the observation in the pre-rutting period, behaviours such as mating stag-doe, driving out the opponent, driving out hinds, chasing the hinds, detachment of velvet from the antlers with the help of vegetation, fighting against vegetation with antlers, flehmen response, urinating on the lower abdomen, being in a male group, stag fights, and a single roar or few roars per event were recorded (Table 1). The most frequently repeated behaviour was a single roar or few roars per event (55.5%). Flehmen response (11.3%), thrashing the vegetation with antlers (11.2%), and stag fights (9.3%) were quite frequently repeated as well. The rare types of behaviour included urinating on the lower abdomen (2%), taking a hind from another stag's group (4%), mating stag-doe (which was recorded on the last day of the observations) (0.3%), and driving out younger males (0.2%) (Table 1). The hinds were not chased until the beginning of September, and this behaviour was observed more frequently as the rut approached. Except for vocalizations, these behaviours were shown by the stags more often in the morning than in the evening. The relationship between the most common behaviours and weather conditions was assessed. It was shown that flehmen response, attempted fights, staying in a group, thrashing the vegetation, or chasing of the hinds by the stags did not depend on the weather conditions. Only the chasing of the hinds was negatively correlated with the mean evening temperature (P <0.05) (Table 8).
The frequency and intensity of the behaviours exhibited by the stags varied, depending on their age. The highest activity was observed in the case of 'Dziki', who was the oldest stag in the herd, whereas 'C12', one of the youngest animals, was the least active. 'Dziki' vocalized most often and the average length of the roar produced by this stag was 1.7 seconds. An exception was 'Hubert' (4 years old), whose activity was more intense than the average value. There was a positive correlation between the age of the animals and their activity. The intensity of the analysed behaviours increased with the age of the stags.
Discussion
It is assumed that the rutting period in the study area begins in mid-September and lasts until mid-October. However, the mating season depends largely on climatic conditions (Coulson et al., 2003). The weather affected the pre-rut behaviour. However, once the animals enter the rut, the weather is not important but there is a year effect: in the year with "autumn-like" pre-rut (lower temperature), the vocalizing behaviour is more intense. The number of vocalizations in 2017 and 2018 was compared and it was shown that there were two large decreases in the temperature in September in the first year of observations, which resulted in acceleration of vocalization by two days, but the average temperature during the early rutting period in 2017 was higher than in 2018. Similar results were also reported in a deer population in Scotland, where there was a 10-day shift in the onset of the rutting season caused by global warming over a 30-year period (Coulson et al., 2003). There is a general tendency for deer to start the mating season earlier than in the past. The rutting season in Europe begins earlier in the western than in the eastern parts, which is usually explained by the continental climate of the eastern part of the continent. Through comparison of the reproductive phenology of deer in France and Norway, Loe et al. (2005) concluded that the temperature and the associated spring vegetation development were crucial for the timing and synchronization of the rutting period (Langvatn et al., 2004; Pettorelli et al., 2005; Macháček et al., 2014; Paoli et al., 2018).
Male vocalization is usually most pronounced when females reach their oestrus peak and lasts 4-5 weeks (Clutton-Brock & Albon, 1979). During the rut, day and night general activity of the stags is intensified as well (Kamler et al., 2008; Pépin et al., 2009). Similar observations were recorded in farmed deer, and the behaviour in the analysed animals was consistent with the Bützler (1974) ethogram; moreover, the behaviour related to chasing the hinds was observed only during the early rutting season.
At the beginning of the rutting season, the most intensified activity is usually exhibited by young stags at ~5 y (Pépin, 2001); however, it declines with the duration of the period or is inconsistent, which is confirmed by the present observations of farmed deer. Younger, free-living males tend to be more mobile but they move in areas where older males are present (Smith-Flueck & Flueck, 2006). Interestingly, the animal with the lowest activity was the youngest in the herd and had distorted antlers limiting the vision in his right eye. In the pre-rutting period, the stag was increasingly being pushed away from the herd. Consequently, at the end of the observation period, the stag stayed alone and did not show any typical pre-rutting behaviour. In their research, Topiński (1974); Clutton-Brock et al. (1982); Bartoš & Bahbouh (2006); Bartoš et al. (2007); Janiszewski et al. (2008); and Veiberg et al. (2004) showed that, at the peak of the rutting season, the male's breeding status was influenced by the body weight and antler size. Therefore, the size and shape of antlers is the main condition for achieving dominance in the herd. The condition of antlers depends on the health status of stags, which is reflected in the length of vocalization. It has been shown that males with poor health status produce shorter roars and their mating season is shorter too. Importantly, the extension of the rutting period may induce the occurrence of repeated oestrus in females (Volodin et al., 2016). The possibility of predicting such phenomena is extremely important in deer farming practice.
Previous analyses showed that middle-aged males (8 years old) started to vocalize earlier (Yoccoz et al., 2002), as in the studies of the red deer in the Isle of Rum, Scotland (Clutton-Brock et al., 1982) and reindeer (Rangifer tarandus) (Espmark, 1964). In the study of the farmed deer, the 9-year-old stag (Dziki) showed the most intense and earliest vocal activity, and the average length of its single roar was quite long, although the size and condition of the antlers were similar to those of three other younger males (Niko, Jasiek, Neo). Therefore, it can be concluded that the experience and behaviour displayed before the rutting period is more important. In their longer-lasting influence on females, they contribute to faster ovulation and greater success in fertilization and, consequently, transmission of their genes (Reby & McComb, 2003).
The activity of the farmed deer was manifested mainly by the increased frequency of vocalization, especially during the mating season. Observations reported by Volodina et al. (2006) showed that stags vocalized most often between 05:00 and 06:00 and between 20:00 and 23:00 Additionally, the peak vocal activity of deer in Russia was recorded at 08:00-09:00 in Tver and at 07:0009:00 and 16:00-18:00 in Kostroma (Volodin et al., 2016). In the Alpine deer population in Italy, the deer vocalized mainly at night and early in the morning, with a peak at 05:00-07:00 (Bocci et al., 2013). In turn, the stags in the population from the Isle of Rum population vocalized mainly during the day (Clutton-Brock & Albon, 1979), likewise farmed stags in France (Pepin et al., 2001). Many results confirm that deer exhibit the highest overall activity at sunrise and sunset (Feighny et al., 2006; Pépin et al., 2009), which was also observed in the case of the farmed deer in Poland.
In the pre-rutting period, the average length of a single roar produced by the stags was 1.67 s, which was similar to the results reported by Feighny et al. (2006) when analysing hinds from the Rocky Mountains (Canada), and over twice as long as the vocalization of red deer hinds or calves living in Spain during the rutting period (Volodina et al., 2006). The average length of a single roar in the early rutting period in the study on the farmed deer was 2.47 s. This value was higher than that reported by Feighny et al. (2006) and lower than in the study of farmed deer breeding conducted by Volodina et al. (2006) and similar to the value measured in wild stags. As shown by Frey et al. (2012), the duration of the roars of Iberian deer during fights was shorter, i.e., on average 1.90 s, and ranged between 0.83 and 3.86 s. In turn, in their study of Manchurian deer, Volodin et al. (2013) recorded a longer mean vocalization time of 3.07 ± 0.52 s. The frequency of vocalization of the farmed stags in the pre-rutting period was low, i.e., 5.45. During the early mating season, it increased to 173.26 s; nevertheless, it was lower than the value recorded in the deer from Tver but higher than the activity of the animals in Kostroma (central Russia) (Volodin et al., 2016). The differences may have been related to the different density and structure of the herd, as already demonstrated in many studies (Clutton-Brock & Albon, 1979; Bowyer and Kitchen, 1987; Clutton-Brock et al., 1997; Yoccoz et al., 2002), which was nevertheless similar to the conditions in Kostroma and in free-living animals (Clutton-Brock & Albon, 1979).
As mentioned in the Introduction, weather conditions may affect the mating season in red deer. The study carried out by Prebanic and Ugarkovic (2015) showed no correlation between the activity of deer and air temperatures in the pre-rutting period. In contrast, the present study of the farmed deer showed a relationship between the air temperature and vocalization in the pre-rutting period, whereas no such relationship was observed during the early mating season. Moreover, the average air temperature and atmospheric pressure influenced the sum of activities of the farmed stags in the morning hours, and the average temperature in the evening induced behaviour consisting of chasing of the hinds by the males. Douhard et al. (2013) showed a negative relationship between the temperature and the roaring count index, which can be explained by a reduction in animal activity accompanying a rise in the temperature. Similarly, the results presented by Volodin et al. (2013; 2015) revealed a negative relationship between the number of roars and air temperature in Siberian and Far Eastern deer.
Interestingly, wind force has not been shown to influence vocalization or other deer behaviour, even though the wind affects sound dispersion, as well as the overall behaviour of many species (Ruzicka & Conover, 2011). Moreover, weather conditions, especially wind that have an impact on odour i.e., scents suspended in the air and odour plumes, should affect stag behaviour because it is the smell that indicates that the female is ready for copulation (Müller-Schwarze, 1971).
The moon phase also increased the frequency of vocalization in the farmed stags, not only during the rutting season (as shown by Prebanić & Ugarković, 2015), but also in the pre-rutting period. The lower air temperatures in the pre-rutting period and the transition towards the full moon increased the activity of the farmed deer in Poland. In contrast, Woodside (2010) showed that the moon phases, especially the full and new moon phases, have an inconsiderable effect on the activity and range of movement in Cervidae. The results reported by Bocci et al. (2013) indicate that the frequency of vocalization in red deer decreases with increasing humidity. A similar observation was recorded in the farmed deer in Poland in the described research.
Conclusion
In conclusion, lower temperatures, lower air humidity, increasing atmospheric pressure, and transition towards the full moon phase contribute to an increase in the vocal activity of deer in the pre-rutting period, which may accelerate the onset of the rutting period in males. The number of vocalizations varied in 2017 and 2018, and depended on the average temperature, air humidity, atmospheric pressure, and moon phase in the pre-rutting period and during the rutting season. Thus, by observing the changing weather conditions, it is possible to predict the time of increased activity of stags and the onset of rutting. Probably due to the experience gained with age, the older stags made greater investments in vocal activity earlier than the younger ones. Prediction of the mating behaviour of males has a huge impact on acceleration or repeatability of ovulation in hinds, which is particularly valuable information for deer breeders and wildlife managers.
Authors' Contributions
KT (ORCID 0000-0003-4725-9020) participated in designing the study, wrote the manuscript, was involved in drafting and revising the manuscript for intellectual content, carried out data analysis and interpretation, and was involved in the preparation and revision of the manuscript and supervision of the manuscript. PJ (ORCID 0000-0003-4654-7805) participated in designing the study. ZSB (ORCID 0000-0001-6645-6172) contributed to the acquisition, analysis, and interpretation of data. FC (ORCID 0000-0001-9014-147X) was involved in the preparation and revision of the manuscript. All authors reviewed and approved the manuscript before it was submitted for publication.
Conflict of Interest
The authors declare that they have no conflict of interest.
References
Bartoš, L., 1986. Dominance and aggression in various sized groups of red deer stags. Aggressive Behave. 12, 175-182. https://doi.org/10.1002/1098-2337(1986)12:3<175::AID-AB2480120304>3.0.CO;2-Z [ Links ]
Bartoš, L. & Bahbouh, R., 2006. Antler size and fluctuating asymmetry in red deer (Cervus elaphus) stags and probability of becoming a harem holder in rut. Biol. J. Linn. Soc. 87(1), 59-68. https://doi.org/10.1111095-8312.2006.00555.x [ Links ]
Bartoš, L., Bahbouh, R. & Vach, M., 2007. Repeatability of size and fluctuating asymmetry of antler characteristics in red deer (Cervus elaphus) during ontogeny. Biol. J. Linn. Soc. 91, 215-226. https://doi.org/10.1111095-8312.2007.00789.x [ Links ]
Bocci, A., Telford, M. & Laiolo, P., 2013. Determinants of the acoustic behaviour of red deer during breeding in a wild alpine population, and implications for species survey. Ethol Ecol Evol 25(1), 52-69. https://www.tandfonline.com/doi/abs/10.1080/03949370.2012.705331 [ Links ]
Bowler, D.E., Hof, C., Haase, P., Kröncke, I., Schweiger, O., Adrian, R., et al. 2017. Cross-realm assessment of climate change impacts on species' abundance trends. Nat. Ecol. Evol. 1(3), 1-7. https://doi.org/10.1038/s41559-016-0067 PMID: 28812743 [ Links ]
Bowyer, R.T. & Kitchen, D.W., 1987. Sex and age-class differences in vocalizations of Roosevelt elk during rut. Am. Midl. Nat. 118(2), 225-235. [ Links ]
Bützler, W., 1974. Aggressive and reproductive behaviour, social rank hierarchy and activity rhythms in the Red deer (Cervus elaphus L.). Fortschritte der Verhaltensforschung 16, 80. [ Links ]
Charlton, B.D., Reby, D. & McComb, K., 2007. Female red deer prefer the roars of larger males. Biol. Lett. 3.(4), 382-385. https://doi.org/10.1098/rsbl.2007.0244 [ Links ]
Clutton-Brock, T.H. & Albon, S.D., 1979. The roaring of red deer and the evolution of honest advertising. Behaviour 69(3-4), 145-170. https://doi.org/10.1163/156853979X00449 [ Links ]
Clutton-Brock, T. H., Albon, S.D., Gibson, R.M. & Guinness, F.E., 1979. The logical stag: Adaptive aspects of fighting in red deer (Cervus elaphus L.). Anim. Behav. 27, 211-225. [ Links ]
Clutton-Brock, T.H., Albon, S.D. & Guinness, F.E. 1982. Parental investment in mate and female offspring in polygynous mammals. Nature 289, 487-489. [ Links ]
Clutton-Brock, T.H., Rose, K.E. & Guinness, F.E., 1997. Density-related changes in sexual selection in red deer. Proc. Royal Soc. B 264(1387) 1509-1516. DOI: 10.1098/rspb.1997.0209 [ Links ]
Coulson, T., Kruuk, L.E.B., Tavecchia, G., Pemberton, J.M. & Clutton-Brock, T.H., 2003. Selection of neonatal traits in red deer. Evolution 57, 2879-2892. DOI: 10.1111/j.0014-3820.2003.tb01528.x [ Links ]
Douhard, M., Bonenfant, C., Gaillard, J.-M., Hamann, J.-L. & Jacques, M.G., 2013. Roaring counts are not suitable for the monitoring of red deer, Cervus elaphus, population abundance. Wildlife Biol. 19(1), 94-101. DOI:10.15298/rusjtheriol.15.2.03 [ Links ]
Dziki-Michalska, K., Tajchman, K., Kowalik, S. & Bogdaszewski, M., 2021. The relationship between plasma cortisol level and the body weight and antler size in farmed fallow deer. S. Afr. J. Anim. Sci. 51(3), 355- 361. DOI: 10.4314/sajas.v51i3.9 [ Links ]
Espmark, Y., 1964. Rutting behaviour in reindeer (Rangifer tarandus L.). Anim. Behav. 12, 159-163. DOI: 10.1016/0003-3472(64)90117-4 [ Links ]
FEDFA, 2020. Federation of European Deer Farmers Associations https://www.fedfa.com/ (accessed 12 Dec 2020). [ Links ]
Feighny, J.A.,Williamson, K.E. & Clarke, J.A., 2006. North American elk bugle vocalizations: Male and female bugle call structure and context. J. Mammal. 87, 1072-1077. https://doi.org/10.1644/06-MAMM-A-079R2.1 [ Links ]
Fitch, W.T. & Reby, D., 2001. The descended larynx is not uniquely human. Proc. Royal Soc. B P ROY SOC B- BIOL SCI 268, 1669-1675. DOI: 10.1098/rspb.2001.1704 [ Links ]
Frey, R., Volodin, I., Volodina, E., Carranza, J. & Torres-Porras, J., 2012. Vocal anatomy, tongue protrusion behaviour, and the acoustics of rutting roars in free-ranging Iberian red deer stags (Cervus elaphus hispanicus). J. Anat. 220, 271-292. DOI:10.1111/j.1469-7580.2011.01467.x [ Links ]
Frey, R. & Riede, T., 2013. The anatomy of vocal divergence in North American elk and European red deer. J. Morphol. 274, 307-319. https://doi.org/10.1002/jmor.20092 [ Links ]
Garcia, M., Charlton, B.D., Wyman, M.T., Fitch, W.T. & Reby, D., 2013. Do red deer stags (Cervus elaphus) use roar fundamental frequency (F0) to assess rivals? PLoS ONE 8(12): e83946. DOI:10.1371/journal.pone.0083946 [ Links ]
Guinness, F., Lincoln, G.A. & Short, R.V., 1971. The reproductive cycle of the female red deer, Cervus elaphus L. J Reprod Fertil 27, 427-438. DOI: 10.1530/jrf.0.0270427 [ Links ]
Haigh, J.C. &Hudson, R.J., 1993. Farming wapiti and red deer. St. Louis: Mosby 369 p. [ Links ]
Janiszewski, P., Dmuchowski, B., Gugolek, A. & Zelobowski, R., 2008. Body weight characteristics of farm-raised fallow deer (Dama dama L.) over the winter period. J. Cent. Eur. Agric. 9(2), 337-342. [ Links ]
Janiszewski, P., Bogdaszewski, M., Murawska D. & Tajchman, K., 2016. Welfare of farmed deer: Practical aspects. Pol. J. Natur. Sc. 31(3), 345-361. [ Links ]
Kamler, J.F., Jedrzejewski, W. & Jedrzejewska, B., 2008. Home ranges of red deer in a European old-growth forest. Am. Midl. Nat. 159, 75-82. DOI:10.1674/0003-0031(2008)159[75:HRORDI]2.0.CO;2 [ Links ]
Langvatn, R., Mysterud, A., Stenseth, N.C. & Yoccoz, N.G., 2004. Timing and synchrony of ovulation in red deer constrained by short northern summers. Am. Nat. 163(5), 763-772. https://doi.org/10.1086/383594 PMID:15122493 [ Links ]
Loe, L.E., Bonenfant, C., Mysterud, A., Gaillard, J.M., Langvatn, R., Klein, F., Calenge, C., Ergon, T., Pettorelli, N. & Stenseth, N.C., 2005. Climate predictability and breeding phenology in red deer: Timing and synchrony of rutting and calving in Norway and France. J Anim Ecol 74, 579-588. https://doi.org/10.111365-2656.2005.00987.x [ Links ]
Macháček, A., Dvořák, S., Ježek, M. & Zahradník, D., 2014. Impact of interspecific relation between native red deer (Cervus elaphus) and introduced sika deer (Cervus nippon) on their rutting season in the Doupovské hory Mts. J. For. Sci. 60(7), 272-280. https://doi.org/10.17221/47/2014-JFS [ Links ]
Mattiello, S., 2009. Welfare issues of modern deer farming. Ital. J. of Anim. Sci. 8, 205-217. DOI: https://doi.org/10.4081/ijas.2009.s1.205 [ Links ]
McComb, C., 1987. Roaring by red deer stags advances the date of oestrus in hinds. Nature 330, 648-649. [ Links ]
McComb, C., 1991. Female choice for high roaring rates in red deer, Cervus elaphus. Anim. Behav. 41, 79-88. [ Links ]
Millán, M.F., Carranza, J., Pérez-González, J., Valencia, J., Torres-Porras, J., Seoane, J.M. et al. 2021. Rainfall decrease and red deer rutting behaviour: Weaker and delayed rutting activity though higher opportunity for sexual selection. PLoS ONE 16(1): e0244802. DOI: https://doi.org/10.1371/journal.pone.0244802 [ Links ]
Mulley, RC., 2007. Reproductive management of fallow deer. In: Current Therapy in Large Animal Theriogenology. 2nd ed. St. Louis: Sunders Elsevier 952-965. DOI:10.1016/B978-072169323-1.50132-X [ Links ]
Müller-Schwarze, D., 1971. Pheromones in black-tailed deer (Odocoileus hemionus columbianus). Animal Behaviour 19(1): 143-153. https://doi.org/10.1016/S0003-3472(71 )80149-5 [ Links ]
Paoli, A., Weladji, R.B., Holand, 0. & Kumpula, J., 2018. Winter and spring climatic conditions influence timing and synchrony of calving in reindeer. PloS ONE. 13(4): e0195603. https://doi.org/10.1371/journal.pone.0195603 PMID: 29694410 [ Links ]
Pépin, D., Cargnelutti, B., Gonzalez, G. & Joachim, J., 2001. Diurnal and seasonal variations of roaring activity of farmed red deer stags. Appl. Anim. Behav. Sci. 74(3), 233-239. DOI:10.1016/S0168-1591(01)00172-1 [ Links ]
Pépin, D., Morellat, N. & Goulard, M., 2009. Seasonal and daily walking activity patterns of free-ranging adult red deer (Cervus elaphus) at the individual level. Eur. J. Wildl. Res. 55, 479-486. DOI: 10.1007/s10344-009-0267-2 [ Links ]
Pettorelli, N., Mysterud, A., Yoccoz, N.G., Langvatn, R. & Stenseth, N.C., 2005. Importance of climatological downscaling and plant phenology for red deer in heterogeneous landscapes. Proc. Royal Soc. B. 272(1579), 2357-2364. https://doi.org/10.1098/rspb.2005.3218 PMID: 16243701 [ Links ]
Post, E., Stenseth, N.C., Langvatn, R. & Fromentin, J.M., 1997. Global climate change and phenotypic variation among red deer cohorts. Proc. Royal Soc. B. 264(1386), 1317-1324. https://doi.org/10.1098/rspb.1997.0182 PMID: 9332016 [ Links ]
Prebanić, I. & Ugarković, D., 2015. Analysis of seasonal activities of red deer (Cervus elaphus L.) in relation to the mating season, lunar phases and air temperature. Russ. J. Ecol. 46(4), 393-395. DOI:10.1134/S1067413615040153 [ Links ]
Reby, D. & McComb, K., 2003. Anatomical constraints generate honesty: Acoustic cues to age and weight in the roars of red deer stags. Anim. Behav. 65, 519-530. https://doi.org/10.1006/anbe.2003.2078 [ Links ]
Reby, D., McComb, K., Cargnelutti, B., Darwin,C.J., Fitch, W.T. & Clutton-Brock, T.H., 2005. Red deer stags use formants as assessment cues during intra-sexual agonistic interactions. Proc. Royal Soc. B 272(1566), 941947. https://doi.org/10.1098/rspb.2004.2954 [ Links ]
Riede, T. & Titze, I.R., 2008. Vocal fold elasticity of the Rocky Mountain elk (Cervus elaphus nelsoni)-producing high fundamental frequency vocalization with a very long vocal fold. J. Exp. Biol. 211, 2144-2154. DOI: 10.1242/jeb.017004. [ Links ]
Rogers, L.J. & Kaplan, G., 2002. Songs, Roars, and Rituals: Communication in Birds, Mammals, and Other Animals. Publisher: Harvard University Press, London, UK, pp. 224. [ Links ]
Ruzicka, B. & Conover, M.R., 2011. Influence of wind and humidity on foraging behaviour of olfactory mesopredators. Can Field Nat 125(2). DOI:10.22621/cfn.v125i2.1196 [ Links ]
Smith-Flueck, J.M. & Flueck, W., 2006. Defense of territories by rutting red deer stags, Cervus elaphus, in Patagonia, Argentina, In: Advances in Deer Biology: Deer in a Changing World, Bartoš, L., Dusšek, A., Kotrba, R., Batosšova-Víchová, J., eds. Publisher: Research Institute of Animal Production, Praha, Czech Republic, p.174-178. [ Links ]
Struhsaker, TT., 1967. Auditory communication among vervet monkeys (Cercopithecus aethiops) In: Social Communication Among Primates. Altmann S.A., ed. Publisher: Chicago: University of Chicago Press, USA, pp. 281 -324. [ Links ]
Topiński, P., 1974. The role of antlers in establishment of the red deer herd hierarchy. Acta Theriol. 19(32), 509-514. [ Links ]
Woodside, G.J., 2010. Rocky Mountain elk (Cervus elaphus nelsoni) behaviour and movement in relation to lunar phases. Masters Thesis. Corvallis, OR: Oregon State Univ. Press. [ Links ]
Veiberg, V., Loe, L.E., Mysterud, A., Langvatn, R. & Stenseth, N.C., 2004. Social rank, feeding and winter weight loss in red deer: Any evidence of interference competition? Oecologia 138(1), 135-142. https://www.jstor.org/stable/40005390 [ Links ]
Volodin, I.A., Sibiryakova, O.V. & Volodina, E.V., 2016. Sex and age-class differences in calls of Siberian wapiti Cervus elaphus sibiricus. Mamm. Biol. 81(1), 10-20. DOI:10.1016/j.mambio.2015.09.002 [ Links ]
Volodin, I.A., Volodina, E.V., Frey, R. & Maymanakova, I.L., 2013. Vocal activity and acoustic structure of the rutting calls of Siberian wapiti (Cervus elaphus sibiricus) and their imitation with a hunting luring instrument. Russ. J. Theriol. 12, 99-106. DOI:10.15298/rusjtheriol.12.2.06 [ Links ]
Volodin, I.A., Matrosova, V.A., Volodina, E.V., Garcia, A.J., Gallego, L., Márquez, R. et al. 2015. Sex and age-class differences in calls of Iberian red deer during the rut: Reversed sex dimorphism of pitch and contrasting roars from farmed and wild stags. Acta Ethol. 18(1), 19-29. DOI 10.1007/s10211-013-0179-8 [ Links ]
Volodina, E.V., Volodin, I.A., Isaeva, I.V. & Unclk, C., 2006. biphonation may function to enhance individual recognition in the dhole, Cuon alpinus. Ethology 112, 815-825. DOI: 10.1111/j.1439-0310.2006.01231 .x [ Links ]
Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C. et al. 2002. Ecological responses to recent climate change. Nature. 416(6879), 389-395. https://doi.org/10.1038/416389a PMID:11919621 [ Links ]
Yoccoz, N.G., Mysterud, A., Langvatn, R. & Stenseth, N.C., 2002. Age- and density-dependent reproductive effort in male red deer. Proc. Royal Soc. B 269(1500), 1523-1528. DOI:10.1098/rspb.2002.2047 [ Links ]
Submitted 30 June 2022
Accepted 28 September 2022
Published 28 February 2023
# Correspondence: katarzyna.tajchman@up.lublin.pl