J. Anim. Sci. 2005. 83:124-129
© 2005 American Society of Animal Science
ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION |
Preorbital gland opening in red deer (Cervus elaphus) calves: Signal of hunger?1
L. Barto
2,
J. Víchová and
J. Lancingerová
Ethology Group, Research Institute of Animal Production, CZ-104 01 Prague 10-Uh
ín
ves, Czech Republic
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Abstract
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The opening of the preorbital gland in red deer (Cervus elaphus) calves has been hypothesized to be a signal to the mother that her calf is hungry. Closing of the gland should indicate that the calf has received a sufficient amount of milk, and thus the mother should stop the suckling. We tested the hypothesis that the calf signals hunger when its preorbital gland is open and signals satiation when the gland is closed. To test this, the behavior of eight bottle-reared calves was monitored for 6 mo. For each meal during this time period, opening of the preorbital gland was recorded before calves were offered the meal and after they ate. Satiation of the calf was estimated (not begging for more food after the meal = satiated; begging = not satiated). The data set contained 3,116 records of paired measurements of preorbital gland opening (before and after the meal). Calves were satiated after feeding for 90.15% of the meals. The opening of the preorbital gland was associated with feeding and achieving satiety. In most cases (77%), calves opened their preorbital glands before their meal. Eighty-five percent of hungry calves still had preorbital glands open after the meal, whereas preorbital gland opening was decreased (P < 0.03) up to 46.6% in satiated calves. Despite this, we found a large range in individual responses in preorbital gland opening before and after the meal, and also according to whether the calf reached satiety. The heavier calves in this study tended to have their preorbital glands open more frequently than the lighter ones, which may indicate the need for an increased amount of milk intake. There was no clear trend in the frequency of preorbital gland opening with age. In conclusion, preorbital opening is likely to be a signal of calf satiety, as suggested earlier. Nevertheless, preorbital glands were not always open when the calves were hungry and did not vanish during the feeding in all cases.
Key Words: Cervus elaphus • Hunger • Preorbital Gland Opening • Red Deer Calves • Satiety • Signal
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Introduction
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All cervids, with the exception of the moschus, possess preorbital organs, which consist of a glandular region in a pouch adjacent to the nasal 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 that they are used for territorial marking (Gray et al., 1989; Gosling, 1990). This is typical for many ungulates (Mo et al., 1995; Burger et al., 1999a,b) and has also been suggested for some cervids (Schaller, 1967; Müller-Schwarze, 1975; Macnamara and Eldridge, 1987). In addition to its possible role in marking (Clutton-Brock et al., 1982), there seem to be other functions for the preorbital glands in red deer (Cervus elaphus). It has previously been shown that dominant stags open their preorbital glands when they are fighting (Barto
, 1983). Hatlapa (1977) showed that preorbital secretion in red deer has a primary function in establishing mother-offspring bonds. Further, it is believed that the opening of the preorbital gland in red deer calves is a signal to the mother that her calf is hungry. Following this, closing of the gland should signal that the calf has received a sufficient amount of milk, causing the mother to stop suckling (Wölfel, 1976, 1983). The interest in the possible role of the preorbital in signaling mother-calf communication has recently been renewed for practical reasons associated with the worldwide increase in deer farming (Audenaerde, 2002). Therefore, in this study, the hypothesis was tested that the calf signals hunger when its preorbital gland is open and signals satiation when the gland is closed.
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Materials and Methods
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Animals and Handling
This study received approval for animal use and care from the institutional committee.
Preorbital gland opening was observed in eight artificially reared red deer calves (one male, seven females). The calves were collected from a commercial deer farm (Vimperk, Czech Republic) within the first day of their life. They were then weighed, marked by ear tags and numbered collars, and transported to another facility where one person reared and fed them over a period of 6 mo. The calves were imprinted to a foster mother so that they became completely tame. They approached her, vocalized to her, and when being fed, they butted her in the same way they would butt the udder of a nursing hind. A bottle containing milk (1,000 mL of 2% cow milk, 500 mL of 33% cream, six egg yolks, and vitamin C [100 mg of ascorbic acid]; Celaskon, SPOFA, Prague, Czech Republic), prepared after Barto et al. (1991), was offered to the calves four times each day during the first 4 wk, and decreased with the age of the calves to one feeding a day at the end of the bottle rearing, which followed the natural process of weaning at the age of 6 mo. Each calf consumed from 80 to 1,500 mL of milk per feeding according to its age and requirements. The quantity of milk was prepared so that each calf could reach satiety. If it did not, the quantity was either supplemented by milk not consumed by another calf and/or was increased for the next feeding. The calves were kept in an enclosure (500 m2) that provided a shelter and ad libitum access to pasture.
The observations of preorbital gland opening started on May 30 (the day when the first five calves were placed into the enclosure) and lasted until December 14, when the calves were "weaned" and placed into a herd of calves that were naturally weaned by their mothers. Preorbital opening was recorded during two periods: just before the meal was offered and just after the meal was eaten. The preorbital gland was considered "open" when the back of the gland (a white spot) was visible, and it was considered "closed" when no slit could be distinguished. After the meal, the satiation of the calf was estimated (not begging for more food by vocalizing toward the foster mother, butting or licking her, or attempting to get the bottle after the meal = satiated; begging = not satiated).
Statistical Analyses
All data were analyzed using SAS software (Version 9.1; SAS Inst., Inc., Cary, NC). The differences in preorbital opening before and after a meal were tested using McNemar’s 
2 test for matched-pair data (McNemar, 1947), calculated according to Stokes et al. (2000). To assess the effect of satiety on preorbital opening, we applied an analysis of categorical repeated measurements based on the generalized estimating equation approach (Liang and Zeger, 1986) using the GENMOD procedure. The GENMOD procedure was designed to model the probability of opening the preorbital gland. To account for the repeated measures on the same individuals across the period of observation, the analysis was performed with the individual calf in the REPEATED statement. The explanatory variables were the classes "satiety of the calf" (yes or no; not begging for more food after the meal, "satiety of the calf" = yes; begging, ’satiety of the calf’ = no) and the continuous variable "age of the calf" (in days). Both explanatory variables and interaction term were tested, but are not reported unless they were statistically significant (P < 0.05). Individual differences in preorbital gland opening among the calves were tested by a modified model of the logistic regression (PROC GENMOD), with the effect of the calf as an explanatory variable. The other explanatory variables were the same classes as in previous model: "satiety of the calf" and "age of the calf." A record of preorbital opening was omitted when any of the variables required for the analysis was missing.
The relationship between preorbital gland opening and the birth weight of the calves was tested using the Cochran-Armitage trend test (Agresti, 1990; Stokes et al., 2000).
To see whether there was any individual pattern in preorbital gland opening after the meal, a Spearman correlation was applied between the percentage of pre-orbital glands open after the meal when the calf was satiated and when it was not satiated.
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Results
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During the 196 d of observations, 3,967 meals were offered to the calves. After the removal of incomplete records (i.e., records for which the feeding person did not recognize whether the preorbital glands were open or closed, whether the calf was satiated after the meal, etc.), the data set had 3,116 records of paired measurements of preorbital opening (before and after the meal) for which all required variables were observed. The calves were satiated after feeding for 90.15% of the meals.
The McNemar test revealed significant differences between the percentages of preorbital glands opened before vs. after the meal (2(1) = 519.38; P < 0.001). The gland was mostly open before the meal (77.02%); however, after the meal, the percentage of preorbital opening decreased to 50.45% (Figure 1).
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Figure 1. Proportion of preorbital gland opening of the red deer calves before and after a meal. A greater proportion (P = 0.001) of preorbital gland opening occurred before a meal than after a meal. Significance was computed by MacNemar’s matched pair data test (n = 3,116).
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To assess the effect of satiety on preorbital gland opening of the calves after the meal, the data set was analysed using a logistic regression model. The resultant model only contained the effect of the "satiety of the calf" (2(1) = 5.14; P < 0.03). The odds ratio of 6.66 estimated for the "satiety of the calf" indicates that the odds of the satiated calves of having their preorbital glands open was 6.66 times the odds of the unsatiated calves (confidence limits 3.40 to 13.05).
We found large individual variability among the calves in the frequency of preorbital opening (Figure 2). The final logistic regression model contained the statistically significant effects of the "identity of the calf" (2(7)= 29.84; P = 0.001), the "satiety of the calf" (2(1) = 68.18; P < 0.001) and the third term interaction of the "identity of the calf" x "satiety of the calf" x "the age of the calf" (2(15) = 307.46; P < 0.001). Figure 3 (top) shows the individual differences in the predicted value of preorbital gland opening before the meal plotted against the age of the calf. The predicted probability of preorbital gland opening was further plotted against the age when the calf was not satiated (Figure 3, middle) and when it was satiated after its meal (Figure 3, bottom).
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Figure 2. Proportion of opened or closed preorbital glands before a meal, after a meal when the calf was not satiated and after the meal when the calf was satiated for individual calves. Each bar represents results for one calf and n = 521, 332, 234, 445, 368, 403, 400, and 413 observations per calf (from left to right, respectively).
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Figure 3. Predicted probability (computed by logistic regression) of preorbital gland opening plotted according to age of the calf before the meal (top panel), after the meal when the calf was not satiated (middle panel), and after the meal when the calf was satiated (bottom panel). Individual calves were characterized by the same style of the curve in the top, middle, and bottom panels.
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A significant trend was found in the frequency of preorbital opening according to the birth weight of the calves (Cochran-Armitage trend test: Z = –24.60; P < 0.001). The probability of the preorbital glands being open increased (from 19.93 to 83.45%) with increasing birth weight of the calves (Figure 4). There was a high Spearman correlation between the percentage of preorbital glands open after the meal when the calf was satiated and when it was not satiated (rs = 0.83; n = 8; P = 0.01).
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Figure 4. Proportion of preorbital glands open (black bars) and closed (hatched bars) in calves according to their birth weight and significance of the Cochran-Armitage trend test. Each bar represents results for one calf and n = 445, 234, 521, 332, 403, 368, 400, and 413 observations per calf (from left to right, respectively).
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Discussion
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The opening of the preorbital gland in bottle-fed red deer calves was found to be associated with feeding and the attainment of satiety. In most cases, calves opened their preorbital gland before their meal. Those calves that were hungry after their meal had their preorbital gland still open after the meal, whereas preorbital gland opening was found to be decreased in satiated calves. This was highly evident during the critical period of the age of the calves up to d 30, when the calves were fully dependent on milk (Barto et al., 2001). Therefore, we can conclude that preorbital opening is likely to be a signal of calf satiety as recommended by Wölfel (1976, 1983). Nevertheless, the preorbital gland was not always open when the calves were hungry or willing to get milk, and it did not vanish in all cases during the feeding.
A large range was found in individual response in preorbital gland opening both before and after the meal, and also according to whether the calf reached satiety by eating. A high correlation between the percentage of preorbital glands open after the meal when the calf was satiated and when it was not satiated suggests a high general individual predisposition for opening its preorbital glands. A good example is the calf shown by a solid line on Figure 3
, who tended to have its preorbital glands opened regardless of whether it was before or after the meal and whether it achieved satiety. This may reflect some sort of agitation for the dam’s attention, perhaps due to frustration from the social stress of living in a group of calves. Unfortunately, we do not have data to assess this. The heavier calves in this study tended to have their preorbital glands open more frequently than the lighter calves, which may suggest the need for a larger amount of milk. There was no clear trend in the frequency of preorbital gland opening with age. Even though the period of the full dependency on milk finished at the age of approximately 30 d (Barto et al., 2001), the calves in the present study kept opening their preorbital glands for a long time afterwards. This may indicate some role of preorbital glands opening in social contact with the surrogate mother and/or an expression of the emotional stage of the calf dealing with its individual strategy to get milk.
The preorbital gland signal of calf satiety was most likely also affected by some other factor or factors. One good candidate for this could be excitement. It has been reported that the preorbital glands of fighting males are open (Barto, 1983) and are also commonly open in rutting stags. Despite this, it is not yet clear whether the open preorbital gland serves as a visual or an olfactory signal.
In conclusion, preorbital gland opening was not always present when the calves were hungry and did not always close during feeding. This suggests that for practical purposes, preorbital gland opening should be accepted with caution as a reliable indicator of calf satiety as recommended by Wölfel (1976, 1983).
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Footnotes
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1 The authors thank T. DeVries for his kind help with preparing the English manuscript. The project was supported by the Grant Agency of the Czech Republic (GA 524/02/0711) and a grant from the Ministry of Agriculture of the Czech Republic (MZe 0002701402). 
2 Correspondence: POB 10 (phone: +420-267-009-657; fax: +420-267-710-779; e-mail: bartos{at}vuzv.cz).
Received for publication August 31, 2004.
Accepted for publication October 13, 2004.
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Abstract
Introduction
