Preorbital Gland Research Articles

Cellular prion protein distribution in the vomeronasal organ, parotid, and scent glands of white-tailed deer and mule deer

ABSTRACT Chronic wasting disease (CWD) is a contagious and fatal transmissible spongiform encephalopathy affecting species of the cervidae family. CWD has an expanding geographic range and complex, poorly understood transmission mechanics. CWD is disproportionately prevalent in wild male mule deer and male white-tailed deer. Sex and species influences on CWD prevalence have been hypothesized to be related to animal behaviours that involve deer facial and body exocrine glands. Understanding CWD transmission potential requires a foundational knowledge of the cellular prion protein (PrPC) in glands associated with cervid behaviours. In this study, we characterized the presence and distribution of PrPC in six integumentary and two non-integumentary tissues of hunter-harvested mule deer (Odocoileus hemionus) and white-tailed deer (O. virginianus). We report that white-tailed deer expressed significantly more PrPC than their mule deer in the parotid, metatarsal, and interdigital glands. Females expressed more PrPC than males in the forehead and preorbital glands. The distribution of PrPC within the integumentary exocrine glands of the face and legs were localized to glandular cells, hair follicles, epidermis, and immune cell infiltrates. All tissues examined expressed sufficient quantities of PrPC to serve as possible sites of prion initial infection, propagation, and shedding.

Seasonal change in frequency of marking with preorbital glands by the Japanese serow (Capricornis crispus)

Seasonal change in frequency of marking with preorbital glands by the Japanese serow (<i>Capricornis crispus</i>)

Seasonal pattern of agonistic and marking behaviour of adult and young pampas deer (Ozotoceros bezoarticus) males

Pampas deer (Ozotoceros bezoarticus) is an endangered species form the southern region of South America. The aim of this study was to describe and compare the seasonal changes in agonistic and marking behaviours in adult and young male pampas deer. The study was conducted in two groups of animals: six adult (4 to 6 years old) and six young (1.5 years old) males. Agonistic and marking behaviours were weekly recorded during 1 year. Both followed a seasonal pattern, closely related to the androgen concentration annual pattern and to the antler cycle. The frequency of both types of behaviours increased before or at the beginning of the rut. In general, the age of the males did not modify greatly the pattern of the agonistic behaviours. Adult males marked more frequently than young males, especially with the preorbital gland—a behaviour also used as a visual signal for other males in other deer species—also with a clear seasonal pattern. Overall, we concluded that pampas deer males have a seasonal pattern of agonistic and marking behaviours closely associated with the reproductive seasonal pattern.

Morphological, Histochemical and Morphometric Studies of the Preorbital Gland of Adult Male and Female Egyptian Native Breeds of Sheep (Ovis aries)

Morphological, Histochemical and Morphometric Studies of the Preorbital Gland of Adult Male and Female Egyptian Native Breeds of Sheep (Ovis aries)

First records of preorbital gland opening in rare wild barasingha (Rucervus duvaucelii) in social contexts may help to explain this phenomenon in cervids

The opening of the preorbital gland in deer serves as a visual communication and has been linked to a wide variety of behavioural situations. As we reported recently, all previous long-term studies on preorbital gland opening were carried out on only one species, whereas case reports on six other rarely studied species have shown associations with different behaviours, thus greatly increasing our overall understanding of the real function of this gland in animal visual communication. Here, we report for the first time preorbital gland opening in the barasingha (Rucervus duvaucelii) in social contexts as observed in a wild population in Kanha National Park, India. We observed this behaviour in two different contexts: agonistic and sexual. Moreover, our record of preorbital gland opening during copulation is the first one amongst cervids. Our findings of preorbital gland opening in both contexts in wild barasingha indicate that the gland was opened only when the individual was highly excited. We suggest that preorbital gland opening may be an important behavioural indicator of an individual involved in a serious intraspecific interaction, and thus a useful tool with which to distinguish between playful and serious behaviours, especially in agonistic and sexual situations.

Pre-orbital gland opening during aggressive interactions in rusa deer (Rusa timorensis)

The opening of the preorbital gland in cervids has a visual meaning and is frequently associated with agonistic and/or stress related situations. Apart from in red deer, this behaviour has scarcely been studied and the range of situations when it may occur remains unclear. In this study we report the unusual case of preorbital gland opening in rusa deer, Rusa timorensis, associated to direct aggressive agonistic interaction (biting/kicking) between two adult hinds. This case observed in Tierpark Berlin (Germany) is the first one ever recorded in female–female interactions in cervids. Preorbital gland opening was also studied in 116 social interactions in Plzeň Zoo (Czech Republic). Preorbital gland opening by the dominant adult male was twice observed with relation to alert behaviour, which is also rare. In order to contextualise our observations we summarise the current knowledge about the behaviour associated with preorbital gland opening in R. timorensis and in cervids in general.

Secretion marking with preorbital glands in goitered gazelle,Gazellasubgutturosa(Artiodactyla: Bovidae)

Scent marking is a widespread component of mammal communication and important in the maintenance of territories as a form of status signal advertising territorial ownership, and potential source of information on the quality and competitive ability of the signaller. Marking behaviour with preorbital glands is a common research topic for tropical antelopes, while such behaviour in goitered gazelles, until now, has been poorly understood. We investigated this behaviour in goitered gazelles and found that adult males marked with their preorbital glands all year round, but especially intensively during the rut and most often while patrolling their territories and chasing females; rarely did they mark during territorial conflicts. Adult males preferred to mark the most conspicuous eatable shrubs that reached close to the height of the male. With a few minor exceptions, goitered gazelle performed marking behaviours in a manner similar to other antelope species, and overall did not show any distinctive differences. Preorbital marking behaviour as an essential part of social organization demonstrated its conservatism, but environmental factors also had their impacts, which led to considerable quantitative seasonal fluctuations in marking behaviour.

Preorbital Carcinoma in Two Kirk's Dik-diks (Madoqua kirkii)

Two Kirk's dik-diks suffered from chronic, unilateral, therapy-resistant enlargement of the preorbital gland. Computed tomographic imaging revealed a homogenous preorbital mass destroying the adjacent maxillary bone in one animal. Squamous cell carcinoma was diagnosed microscopically in both cases. Immunohistochemically, the neoplastic cells uniformly expressed cytokeratin (CK) 5/6 and CK14. Additionally, tumour cells were strongly labelled for p53 suggesting a possible role of this tumour suppressor gene in tumorigenesis. Chronic obstruction of the preorbital gland due to excessive accumulation of secretory products is considered as a likely cause of glandular and periglandular inflammation with subsequent malignant transformation.

Pre-orbital gland opening: Part of sucking behavior in red deer (Cervus elaphus) calves1

Opening of the pre-orbital gland in red deer (Cervus elaphus) was previously found to be associated with feeding and negatively associated with achieving satiety in bottle-reared red deer calves. We speculated that this acted as a signal from a calf to the mother that it was hungry. Thus, we focused on a possible association between the pre-orbital gland opening and the sucking behavior in red deer calves. We recorded 63 sucking attempts and 150 sucking bouts within a stable social group of 24 farmed red deer females with 19 calves ages 16 to 90 d. The probability of the pre-orbital gland opening or remaining open during a sucking bout rapidly decreased with the on-going sucking phase (P < 0.001), and it was less after than during a sucking attempt (P < 0.03). The proportion of open pre-orbital glands at the end of sucking depended on whether the nursing female (27.85%) or the calf (0%, P < 0.01) terminated the sucking bout. The open pre-orbital gland of the calf after the sucking bout significantly predicted a subsequent sucking attempt (P < 0.001). The probability of open pre-orbital gland was not significantly affected by the age of the calf, sex or birth weight, or age of the nursing female. In conclusion, our study provides evidence that the opening of the pre-orbital gland is one of the general patterns of calf sucking behavior, specifically that it reflects the level of satisfying calf needs.

Pre-orbital gland opening in farmed red deer (Cervus elaphus) during stressful handling1

Stressful manipulation by humans has been previously shown to result in opening the pre-orbital gland of the newborn red deer. We hypothesized that exposure of red deer to stressful handling would result in opening the pre-orbital gland. Further, we tested the potential factors associated with pre-orbital opening, including season, sex, age and struggling behavior. Pre-orbital gland status was observed in 76 red deer (48 males, 28 females) during 281 handling events with the animal isolated and fixed in a mechanical restraint cradle (crush) within 3 consecutive years. The deer age ranged from 1 to 5 yr in males, and from 1 to 11 yr in females at the beginning of observations. The proportion of handling events with an open gland was considerably greater during than before handling (27.76 vs. 0%, respectively, P < 0.001). The deer that struggled or stiffened revealed 2-fold greater incidence of pre-orbital opening (P < 0.01), regardless of sex. Thus, pre-orbital opening seemed to accompany the behaviors that have been found to be related to acute stress. The probability that the animal opens its pre-orbitals during handling sharply increased at the beginning of the rut (mating season, P < 0.01). Deer that threatened the handler (10% out of 215 observations) opened their pre-orbitals 30 times more often than nonthreatening ones. These effects indicate that other motivations are likely involved in the opening of pre-orbitals, in addition to the perception of a stressful event. Incidence of pre-orbital opening decreased with age in both sexes (P < 0.05) across 3 consecutive yr of observations, which suggests habituation to repeated handling. Sex of the animal did not influence the probability of pre-orbital opening. We found significant variability in pre-orbital opening across the individuals (P < 0.001). In conclusion, we confirmed an association between opening of the pre-orbital gland and stressful handling in sub-adult and adult red deer, although repeated human handling did not elicit such incidence of pre-orbital opening as found in newborn red deer calves. Our results support multifactorial origins of pre-orbital opening and prompt the necessity of further research to distinguish between different motivations that might have been involved in opening of pre-orbitals.

Histomorphology of preorbital gland in territorial and non-territorial male blackbuck Antelope cervicapra, a critically endangered species

The preorbital gland is a specialized dermal gland of antelopes which plays an important role in territorial marking behavior and pheromonal communication. To our knowledge, there is little information available on the role of preorbital gland marks in Indian antelopes (blackbucks). Males are seen averting the gland during behavioural display and territorial marking but the functional aspect of this gland has not been examined. Hence, the aim of this study was to describe the histomorphology of the preorbital gland in territorial and non-territorial male blackbucks to determine its morphology and secretory function. The results showed that the preorbital gland is composed of modified sebaceous and apocrine glands. The apocrine gland is lined by simple cuboidal epithelial cells; the serous parts of the secretory products are often seen in the apical portions of the cells. The myoepithelial cells contain actin filaments lying on the basal membranes of the apocrine gland. There are some considerable histological changes in the presence of the sebaceous and apocrine glands in territorial males in comparison to non-territorial males. The following histological changes associated with occurrence of the sebaceous and apocrine glands have been observed in territorial and non-territorial male blackbucks: (1) increase of size of sebaceous and apocrine glands and (2) increase in density of sebaceous and apocrine glands in territorial males compared to non-territorial males. It is suggested that the higher development (i.e., size) and density of sebaceous and apocrine glands in territorial males could depend on hormone production (i.e., testosterone). Based on the histological observation and the role of sebaceous and apocrine glands in the preorbital gland supported by literature, it is possible to conclude that both territorial and non-territorial blackbuck males may produce pheromonal substances through preorbital gland (secretion) for olfactory communication.

Diurnal variation in preorbital gland scent marking behaviour of captive male Indian Blackbuck (Antelope cervicapra L.) and its territorial significance

Scent marking is a common behaviour among mammals, which involves the deposition of a pheromone, intended to elicit a response from conspecifics. The present study is aimed to establish the diurnal profile of the distribution of scent marking behaviour and its influence of the marker. The frequency of preorbital gland scent marking behaviour was observed in territorial and non-territorial male Indian blackbucks on 72 days, over a period of 18 weeks, starting data collection at 06.00 and continuing until the end of the photophase at about 16.00. An ANOVA with post hoc (DMRT) test was assessed to compare the frequency of preorbital gland scent marking at six 2-hour intervals using pooled data for territorial and non-territorial males. The result showed that the preorbital gland scent marking behaviour occurred significantly (P < 0.001) more often between 10:00–12:00 hrs and 16:00–18:00 hrs. It suggests that scent-marking behaviour in Indian blackbuck has a preferential incidence at a particular time, and this might have occurred in association with feeding hours. Moreover, an ANOVA with a post hoc comparison (DMRT) test revealed that the frequency of scent marking is significant (P < 0.001) when territorial males are compared to non-territorial males. We conclude that territorial male preorbital gland scent marking has the following proposed functions: (i) marking related to use for defense of the home range or territorial region may serve as a permanent threat signal and (ii) marking related to suppressing daily activities in non-territorial males (i.e. feeding, aggression, mating, scent marking, and territorial patrolling activities etc.), and involves maintenance of hierarchy and the avoidance of physical combat.

Synthesis and Antimicrobial Activity of Long-Chain 3,4-Epoxy-2-alkanones

3,4-Epoxy-2-dodecanone, a major component in the preorbital gland of the African grey duiker (Sylvicapra grimmia), showed antimicrobial activity in preliminary tests. The C11 to C17 homologues of this compound were prepared and their activity against several pathogenic dermal bacteria and fungi was tested. 3,4-Epoxy-2-dodecanone and 3,4-epoxy-2-tridecanone inhibited the growth of Trichophyton mentagrophytes at 25 μg/mL. Moderate inhibition of the growth of the bacteria Propionibacterium acnes and the lipophilic yeast, Pityrosporum ovale, was seen for several of the homologues.

Technical note: Preorbital gland opening in red deer (Cervus elaphus) calves as an indicator of stress1

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.

Preorbital gland opening in red deer (Cervus elaphus) calves: Signal of hunger?1

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.

Straight and branched-chain fatty acids in preorbital glands of sika deer, Cervus nippon.

Using GC-MS analysis, 11 major volatile compounds were found in the preorbital gland secretion from a female sika deer, Cervus nippon. These compounds are the C14 through C18 straight-chain fatty acids, (ZZ)-9,12-octadecadienoic acid, 12-methyltridecanoic acid, 13-methyltetradecanoic acid, 14-methylpentadecanoic acid, 14-methylhexadecanoic acid, and 15-methylhexadecanoic acid. The five branched-chain acids make up over 29% of the volatiles in the gland. This is the first time branched-chain carboxylic acids have been reported from ungulate preorbital glands.

The effect of neighbouring klipspringer on the scent–marking behaviour of a group of klipspringer in the Kruger National Park

Both the male and the female klipspringer scent-mark their ranges. A pair of pre-orbital glands below the eyes produces the scent. The secretion is a sticky, substance that is deposited on a suitable twig. Klipspringer scent marks were surveyed in a specific klipspringer range in the Kruger National Park with the use of a strip transect method. The results showed that klipspringer in the Kruger National Park scent-mark more frequently on the boundaries of their ranges and also more on those sides where there is another resident klipspringer group.

Chemical communication in Eurasian deer (Cervidae): do individual odours also code for attributes?

AbstractEvidence for signal coding for attributes such as age, sex or population of origin, was sought in odour profiles derived from natural secretions of the preorbital gland of red deer Cervus elaphus (n= 26), sika deer C. nippon (15), Chinese muntjac Muntiacus reevesi (23) and Chinese water deer Hydropotes inermis (53); from metatarsal secretions from red deer (n= 35), sika (30), fallow (193) and roe deer Capreolus capreolus (26); and from roe deer interdigital glands (n= 48). Volatiles were eluted from sample materials at body temperature, to restrict analysis to those elements which would occur within the natural odour profile; the different volatile elements were then separated by gas chromatography. Initial results of these analyses were strongly suggestive of some level of signal‐coding for attributes of the signaller. Few secretions (species × gland) contained many volatiles which differed significantly between deer from different populations of origin and, except in the muntjac preorbital and sika deer metatarsal secretions, separation of populations was generally rather poor in formal discriminant function analyses (DFA). However, where no constraint is imposed on the number of volatiles allowed to enter the analysis, secretions from at least one gland accurately discriminated between the sexes in the original sample for most species; separation of sexes was only ineffective for Chinese water deer and fallow deer. Discrimination between deer of different age‐classes was similarly effective in the original sample for red deer preorbital and roe deer metatarsal secretions and fair for preobital secretions of Chinese water deer; unbalanced age‐structure of samples did not permit analysis for muntjac or sika deer. Sometimes the actual predictive power of discrimination was poor; it is notable that this was characteristically associated with small sample sizes and the evidence indicates that scent secretions from most species sampled here offer the potential for coding for at least the sex and age of the signaller. Although chromatographic analysis of odours from some glands reveals consistent differences between odour profiles characteristic of sex, age or population, this does not imply that the signal is deliberately coding for such information, or that the deer use the information available. It is possible that differences in the composition of secretions in relation to age or sex of the signaller, for example, is coincidental or of secondary significance.

Individual signatures in scent gland secretions of Eurasian deer

AbstractEvidence for individuality of odour profile, coding for individual identity, was sought in scent profiles derived from natural secretions of the preorbital gland of red deer Cervus elaphus (n= 26), sika deer C. nippon (15), fallow deer Dama dama (50), Chinese muntjac Muntiacus reevesi (23) and Chinese water deer Hydropotes inermis (53); from metatarsal secretions from red deer (n= 35), sika (30), fallow (193) and roe deer Capreolus capreolus (26), and from roe deer interdigital glands (n= 48). Volatiles were eluted from sample materials at body temperature, to restrict analysis to those elements that would occur within the natural odour signal; the different volatile elements were then separated by gas chromatography. For each species considered, secretions from at least one scent gland were individually distinct and sufficiently complex to code for identity. Within our samples no two individuals produced identical odour profiles; yet in analysis of metatarsal gland secretions of individual fallow deer sampled in successive years, odour signatures of individuals remained consistent over time. The wider potential for individual coding was assessed through calculation of the number of different possible combinations of all volatiles recovered in any species×gland system. Every secretion considered seems to have the potential to provide individually characteristic signals (with the exception of secretions from the fallow deer preorbital gland, which notably contained no odour information under any analytical system). Complexity of signals differed markedly between species as did the gland‐type responsible for production of the most complex or distinctive signal. No simple evolutionary patterns are apparent to account for this variation and we suggest that the form of gland selected for production of a signal carrying information about individual identity is a function of habitat type and sociality.

Individual signatures in scent gland secretions of Eurasian deer

Evidence for individuality of odour profile, coding for individual identity, was sought in scent profiles derived from natural secretions of the preorbital gland of red deer Cervus elaphus (n= 26), sika deer C. nippon (15), fallow deer Dama dama (50), Chinese muntjac Muntiacus reevesi (23) and Chinese water deer Hydropotes inermis (53); from metatarsal secretions from red deer (n= 35), sika (30), fallow (193) and roe deer Capreolus capreolus (26), and from roe deer interdigital glands (n= 48). Volatiles were eluted from sample materials at body temperature, to restrict analysis to those elements that would occur within the natural odour signal; the different volatile elements were then separated by gas chromatography. For each species considered, secretions from at least one scent gland were individually distinct and sufficiently complex to code for identity. Within our samples no two individuals produced identical odour profiles; yet in analysis of metatarsal gland secretions of individual fallow deer sampled in successive years, odour signatures of individuals remained consistent over time. The wider potential for individual coding was assessed through calculation of the number of different possible combinations of all volatiles recovered in any species×gland system. Every secretion considered seems to have the potential to provide individually characteristic signals (with the exception of secretions from the fallow deer preorbital gland, which notably contained no odour information under any analytical system). Complexity of signals differed markedly between species as did the gland-type responsible for production of the most complex or distinctive signal. No simple evolutionary patterns are apparent to account for this variation and we suggest that the form of gland selected for production of a signal carrying information about individual identity is a function of habitat type and sociality.