J. Anim Sci. 2007. 85:494-496. doi:10.2527/jas.2006-446
© 2007 American Society of Animal Science
Technical note: Preorbital gland opening in red deer (Cervus elaphus) calves as an indicator of stress1
J. Barto
ová-Víchová2,
L. Barto and
L. 
vecová
Ethology Group, Research Institute of Animal Production, POB 1, CZ-104 01 Praha 10, Uh
ín
ves, Czech Republic
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Abstract
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The opening of the preorbital gland of red deer (Cervus elaphus) calves has been previously associated with feeding and satiety. However, it has been suggested to be most likely affected by some other factor or factors, possibly by excitement of the calf. If so, a calf should open its preorbital gland while being exposed to any stressful procedure. The hypothesis was tested that the preorbital gland is closed in a relaxed calf, whereas it is opened in a stressed calf. Preorbital opening was observed in 41 newborn red deer farm calves during a regular daily routine consisting of a search for newborn calves, their inspection, weighing, and painful marking with an ear tag. The openness of the preorbital gland (preorbital gland closed or opened) was recorded just before manipulation of a lying calf (i.e., in a calm calf) and then during the manipulation (i.e., in a distressed calf). Before manipulation, in all but 3 calves (7.3%, all of which were males), the preorbital gland was closed. All calves observed (100%) opened their preorbital gland during their manipulation, at least by the time the ear was punctured by the ear tag. The proportion of individuals with an open gland was lower (P < 0.001) before than during manipulation (7.3 vs. 100%, respectively). Hence, openness of the preorbital gland in newborn red deer calves was associated with a stressful manipulation by the humans, which suggests that it may be a simple and easily recognized indicator of calf stress.
Key Words: Cervus elaphus • excitement • preorbital gland opening • red deer calf • stress
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INTRODUCTION
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All cervids possess preorbital organs, which consist of a glandular region in a pouch adjacent to the nasal (medial) corner of the eye (Schaffer, 1940
; Müller-Using and Schloeth, 1967). There is no clear evidence of a role across species for this preorbital gland (Gray et al., 1989). The most frequently reported role of preorbital secretions is in territorial marking (Gray et al., 1989; Gosling, 1990). In addition to its possible role in marking (Clutton-Brock et al., 1982), other functions may exist for the preorbital glands in red deer (Cervus elaphus).
Dominant stags open their preorbitals when they are fighting (Barto, 1983). Hatlapa (1977) showed that pre-orbital secretion in red deer has a primary function in establishing mother-offspring bonds. Further, opening of the preorbital gland in red deer calves has been reported to be a signal to the mother that her calf is hungry (Wölfel, 1976, 1983), but no data were proposed to prove this presumption. Therefore, in a previous study, using bottle-reared red deer calves, we tested the hypothesis that the calf signals hunger when its preorbital gland is open and signals satiation when the gland is closed (Barto et al., 2005). Opening of the preorbital gland was associated with feeding and achieving satiety. Nevertheless, the preorbital glands were not open always when the calves were hungry and did not, in all cases, vanish during feeding. From these results, we concluded that the preorbital opening was most likely also affected by other factor or factors, possibly by excitement of the calf (Barto et al., 2005).
In this study, we hypothesized that a calf would open its preorbital gland while being exposed to a stressful procedure, such that the preorbital gland would be closed in a relaxed calf and open in a stressed calf. If so, the preorbital opening could be a simple and easily recognized indicator of calf stress for producers.
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MATERIALS AND METHODS
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This study received approval for animal use and care from the institutional committee.
Forty-one newborn red deer calves (21 males, 20 females) born within 2 consecutive seasons (18 and 23 calves, respectively, in 2004 and 2005) were observed at the experimental farm of the Research Institute of Animal Production at Podlesko (Prague, Czech Republic). Calves were born by a group of hinds in grassy enclosure from May 20 to June 1, 2004, and May 17 to June 27, 2005. Hinds were accustomed to human presence and daily routine, but they were not tame.
Our hypothesis was tested during a regular daily procedure, which consisted of a search for newborn calves, their inspection, weighing, and marking with an ear tag. Every morning during the calving season, newborn calves hidden on the ground were sought out by caretakers (ranging from 2 to 4 people) walking through the enclosure. Upon discovery, calves were subjected to manipulations that are part of routine practice on the experimental deer farm (i.e., no stress was induced in calves beyond the routine practice). Each calf, which had already dried off, was weighed with a hanging scale, marked using a color collar and an ear tag, and had its sex determined. All calves were handled in this same order. It was our presumption that such a manipulation frightened the calves, in particular the painful moment when the ear was punctured by the ear tag. To avoid any additional stress on the newborns, no control hormone concentration levels were assessed. After each calf was manipulated, it was placed back to the ground. Each calf was manipulated just once to reduce a risk of possible disruption of mother-offspring bond. In fact, no cases of desertion by any of the mothers occurred as a result of handling interference. All calves were manipulated within their first 48 h after birth.
The openness of the preorbital gland (preorbital gland closed or opened) was assessed and recorded in 2 periods: 1) just before manipulation of a lying calf (i.e., in a calm calf) and 2) during the manipulation (i.e., in a distressed calf). The preorbital gland was considered as "open" when the back of the gland (a white spot) was visible (Figure 1) and was considered "closed" when no slit could be distinguished (Figure 2). As more than half of the calves ran away as soon as they were released, it was not possible to measure the time it took for the gland to close after manipulating the calf.
Data were analyzed using SAS (SAS Inst. Inc., Cary, NC). As zero counts of closed preorbitals occurred during manipulation, McNemar’s test for matched-pair data (McNemar, 1947; Stokes et al., 2000) could not be used to calculate differences between openness of the preorbital glands before compared with during manipulation. Instead, differences were tested using a 
2 test for equal proportions (PROC FREQ).
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RESULTS
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The data set contained 41 records of paired measurements of preorbital gland opening (before and during manipulation) recorded in newborn calves. Before manipulation in all but 3 calves (7.3%, all of which were males), the preorbital gland was closed when calves were lying on the ground. All observed calves (100%) opened their preorbital gland during their manipulation, at least by the time when the ear was painfully punctured by the ear tag.
The proportion of individuals with an open gland was considerably lower (P < 0.001) before than during manipulation (7.3 vs. 100%, respectively). Thirty-eight calves (92.7%) behaved along with the advanced hypothesis (P < 0.001), such that calves with a closed preorbital gland reacted to the stressful event uniformly by opening it. All 3 calves with initially opened preorbital glands kept it open during manipulation.
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DISCUSSION
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Openness of the preorbital gland in newborn red deer calves was found to reflect a stressful manipulation of the calf. All calves opened their preorbital glands during manipulation. In 3 of the 41 calves, the preorbital gland was open also before manipulation. It is likely that preorbital opening in these calves was caused by the approaching humans. In 2 cases, a calf would stand up and run away when the observers tried to touch it or when they were passing along near the lying calf. However, these calves were easily recaptured and manipulated when lying down again or next day.
We observed individual differences in latency of preorbital opening among calves. Some calves opened their preorbital glands when being touched by observers only, whereas others failed to open the gland until the ear was punctured. An open preorbital gland in the lying calves when approached by humans might reflect increased excitability of these calves.
In spite of large individual variability in its latency, opening of the preorbital gland occurred invariably in association with handling newborn calves by humans. Preorbital secretions play a role in olfactory communication in many ungulate species, at least in scent marking of adult males (Wyatt, 2003). Recent research has shown that in hider ungulate species, females cannot discriminate calls from their own and from nonfilial calves, whereas calves are able to distinguish their mothers’ calls from those of other females (Torriani et al. 2006). This might highlight the importance for the females of the olfactory component of the mother-offspring recognition process, as suggested previously by Hatlapa (1977). Nevertheless, it is unlikely that preorbital gland opening in newborn calves might be a signal of a distressed calf to the mother, either behavioral or olfactory, because mothers of hider ungulate species spent much of their time too far from their calves to receive such signal in the first days after giving birth.
As preorbital opening occurs in different situations associated with arousal, we presume it is likely to be a side effect of general excitement, both positive and negative, of an organism, as proposed in our previous study (Barto et al., 2005). Similar to other behavior, such as male-male mounting (Barto and Hole
ková, 2006), preorbital opening may not necessarily be associated just with stress but also with interest, forthcoming feeding, or sexual arousal. Thus, in the context of feeding, closing of the preorbital glands may reflect calming of the calf during suckling rather than some sort of physiological reaction to satiety as previously suggested (Wölfel, 1976, 1983). Nevertheless, this does not mean that a specific function of the gland opening does not exist in other situations, such as when attacking others (Barto, 1983), roaring during the rut (Volkman et al., 1978), scent marking by adult males (Burger, 2005), establishing mother-calf bonds (Hatlapa, 1977), etc. Further investigation is needed to determine what other specific functions the preorbital glands may serve.
The interest in the role of the preorbital opening in mother-calf communication has recently been renewed for practical reasons associated with the worldwide increase of deer farming (Audenaerde, 2002). Our results suggest that, for practical purposes, the preorbital opening may be a simple and easily recognized indicator of calf stress.
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Footnotes
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1 We thank Petr Janovsk
and Vratislav Káda for excellent field assistance and Trevor DeVries for his kind help with preparing the English manuscript. We are grateful for the constructive comments of the 3 anonymous reviewers. The project was supported by the Ministry of Agriculture of the Czech Republic (MZe 0002701402). 
2 Corresponding author: bartosova.jitka{at}vuzv.cz
Received for publication July 7, 2006.
Accepted for publication September 24, 2006.
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LITERATURE CITED
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Audenaerde, P. M. F. 2002. European view on the deer farming industry of the world. Pages 73–76 in Proc. 2002 NADeFA Annu. Conf. World Deer Farming Congr. III. J. B. Wood, ed. NADeFA, Austin, TX.
Barto, L. 1983. Some observations on the relationships between pre-orbital gland opening and social interactions in red deer. Aggress. Behav. 9:59–67.
Barto, L., and J. Holeková. 2006. Exuberant ungulates: Male-male mounting in three species of deer. Pages 154–171 in Homosexual Behaviour in Animals: An Evolutionary Perspective. P. L. Vasey and V. Sommer, ed. Cambridge Univ. Press, UK.
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Volkman, N. J., K. F. Zemanek, and D. Müller-Schwarze. 1978. Antorbital and forehead secretions of black-tailed deer (Odocoileus-hemionus-columbianus) their role in age-class recognition. Anim. Behav. 26:1098–1106.[CrossRef]
Wölfel, H. 1976. Vorläufiger Bericht über einige neue Beobachtungen zur muterlosen Aufzucht des Rothirsches (Cervus elaphus). Z. d. Köln. ZOO 19:16–19.
Wölfel, H. 1983. Zur Jugendentwicklung, Mutter-Kind-Bindung und Feindvermeidung beim Rothirsch (Cervus elaphus) II. Ztschr. Jagdwissensch. 29:197–213.
Wyatt, T. D. 2003. Pheromones and Animal Behaviour: Communication by Smell and Taste. Cambridge Univ. Press, UK.
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Abstract
INTRODUCTION
