seasonal variation in the dimension of scent-marking gland of three desert rodents and its possible...

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Proc. Indian Acad. Sci. (Anirn. Sci.), Vol. 92. Numher 4 July 1983. pp. 299-304 © Printed in India. Seasonal variation in the dimension of scent-marking gland of three desert rodents and its possible relationship with their reproductive performance SAROJ KUMARl and lSHWAR PRAKASH* *Coordinating and Monitoring Centre for Rodent Research and Training. Central Arid Zone Research Institute. Jodhpur 342 003, India MS received 13 December 1982; revised 2 May 1983 Abstract. The two gerbils, Tatera indica and Meriones hurrianae, and the metad, Rattus meltada pallidior exhibit significant monthly variations in the dimension (maximum length X maximum breadth) of the ventral scent marking gland. Peaks in gland size occur late in winter and monsoon which generally correspond to the maximum breeding activity of these rodents during the year. However. the monthly averages of gland area and incidence of pregnancy in the three species do not follow the same trend. It is difficult, therefore. to conclude if the scent-marking behaviour and the breeding performance of the rodents are inter-related. Keywords. Scent marking gland; breeding season; olfactory communication; Tatera indica; Meriores hurrianae; Rattus meltada I. Introduction Scent-marking by rodents through cutaneous glands has been anributed to a number of functions pertaining to olfactory communication among them. Whether odour of the exudation of ventral scent marking gland plays an important role in the reproductive activity of mammals is not clear. However, it has been found that the frequency of scent-marking in the female desert gerbil, Meriones hurrianae enhances significantly (P<O.Ol) during pro-oestrus and oestrus as compared to that when the females are in dioestrus (Kumari and Prakash 1981) and scent-marking appears to have a function of advertising the ready-to-mate state offemales. Similar observations have been recorded in the female Indian gerbil, Tatera indica which possess the mid- ventral marking gland (Prakash and Idris 1982). In certain other mammals also, it is reported that the gland activity and marking behaviour increase considerably during breeding season (Eibl-Eibesfeldt 1953; Erlinge 1968; Mykytowycz 1966; Stoddart 1972; Townsend 1953). Contrary to this, evidence is available that scent glands are active throughout the year, irrespective of breeding season among other mammals (Pearson 1946; Sokolov and Skurat 1966). An attempt to examine the relationship between the gland size and reproductive activity of three field rodents inhabiting the desert region was made and the results are presented in this paper. 2; Methods Field rodents, T. i. indica. M. hurrianae (Gerbillinae) and the' soft-furred field-rat or the metad, Rattus meltada pallidior (Murinae) were collected from desert grasslands during 1979. 1980 and 198 r. The body weight of the freshly captured animals, their 299

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Proc. Indian Acad. Sci. (Anirn. Sci.), Vol. 92. Numher 4 July 1983. pp. 299-304© Printed in India.

Seasonal variation in the dimension of scent-marking gland of threedesert rodents and its possible relationship with their reproductiveperformance

SAROJ KUMARl and lSHWAR PRAKASH**Coordinating and Monitoring Centre for Rodent Research and Training.

Central Arid Zone Research Institute. Jodhpur 342 003, India

MS received 13 December 1982; revised 2 May 1983

Abstract. The two gerbils, Tatera indica and Meriones hurrianae, and the metad, Rattusmeltada pallidior exhibit significant monthly variations in the dimension (maximumlength X maximum breadth) of the ventral scent marking gland. Peaks in gland sizeoccur latein winter and monsoon which generally correspond to the maximum breeding activity of theserodents during the year. However. the monthly averages of gland area and incidence ofpregnancy in the three species do not follow the same trend. It is difficult, therefore. toconclude if the scent-marking behaviour and the breeding performance of the rodents areinter-related.

Keywords. Scent marking gland; breeding season; olfactory communication; Tatera indica;Meriores hurrianae; Rattus meltada

I. Introduction

Scent-marking by rodents through cutaneous glands has been anributed to a numberof functions pertaining to olfactory communication among them. Whether odour ofthe exudation of ventral scent marking gland plays an important role in thereproductive activity of mammals is not clear. However, it has been found that thefrequency of scent-marking in the female desert gerbil, Meriones hurrianae enhancessignificantly (P<O.Ol) during pro-oestrus and oestrus as compared to that when thefemales are in dioestrus (Kumari and Prakash 1981) and scent-marking appears tohave a function of advertising the ready-to-mate state offemales. Similar observationshave been recorded in the female Indian gerbil, Tatera indica which possess the mid­ventral marking gland (Prakash and Idris 1982). In certain other mammals also, it isreported that the gland activity and marking behaviour increase considerably duringbreeding season (Eibl-Eibesfeldt 1953; Erlinge 1968; Mykytowycz 1966; Stoddart1972; Townsend 1953). Contrary to this, evidence is available that scent glands areactive throughout the year, irrespective of breeding season among other mammals(Pearson 1946; Sokolov and Skurat 1966). An attempt to examine the relationshipbetween the gland size and reproductive activity of three field rodents inhabiting thedesert region was made and the results are presented in this paper.

2; Methods

Field rodents, T. i. indica. M. hurrianae (Gerbillinae) and the' soft-furred field-rat orthe metad, Rattus meltada pallidior (Murinae) were collected from desert grasslandsduring 1979. 1980 and 198r. The body weight of the freshly captured animals, their

299

300 Saro) Kumari and Ishwar Prakash

gland size (maximum length X maximum breadth) and reproductive status wererecorded for every freshly-eaptured rodent. The testes weight were determined on asemi-micro balance with an accuracy of 0.001 g. Statistical methods followed fordetermining correlation coefficient and analysis of variance are after Snedecor andCochran (1967).

3. Results

The ventral scent-marking gland is present in both the sexes of M. hurrianae, in themales of T. indica and R. m. pal/idior. It also occurs in a few females of T. indica.

The gland area of male T. indica between months fluctuate significantly as evidencedby the analysis of variance (F11.38 = 11.48, P< 0.01). The mean monthly gland areaexhibits three peaks, during February, April and September, and is the lowest duringNovember and December (figure I). When the data are pooled on a seasonal basis, it is

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Ficure 1. Monthly fluctuations in the dimensions of scent marking gland of male T. indicaand percent incidence of pregnancy.

Table I. Seasonal variations in the area of scent marking gland and incidence of pregnancyin T. indica and R. m. pallidior.

T. indica R. m. pallidior

Season Average gland % pregnant Average gland % pregnantarea of male (mm") females area of male (mm2

) females

Winter 67.9 29.3 157.3 59.7(Dec-Feb)

Summer 64.0 24.7 195.2 61.3(March-June)

Monsoon 58.3 38.6 160.6 61.1<July-Sept)

Post-monsoon 46.4 24.0 190.0 63.6(Oct-Nov)

Seasonal variation in scent-mark ing gland of"desert rodents 30I

evidenced that the gland area in male rodents is maximum during winter and graduallydeclines till post-monsoon (table I).

A comparison of mean monthly gland area of male T. indica and the incidence ofpregnancy (Jain 1970) indicates quite an inverse relationship between the two. Whenthe gland size is largest in April (figure I). the pregnancy rate is fairly low and when thelatter is maximum during June-August period. the gland area of male T. indica shows adownward trend. Similarly. when the gland area is minimum during November thefrequency of pregnant females is high (38%). Similarly in September. when the glandarea shows a peak. the incidence of pregnancy is lowest (9%). Surprisingly the seasonaldata indicate a slight similarity in the fluctuation trend between the two (table I).

Mean monthly gland area of the desert gerbil. M. hurrianae ranges in males from80.8 to 160 mm2 and among females from 35 to 104 mm". Analysis of varianceindicates that the differences between months (F l1 .149 = 3.75. P< 0.05). between sexes

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bF1aure 2. Monthly fluctuations in the dimensions of scent marking gland of male and femaleM. hurrianae and percent incidence of pregnancy.

Table 2. Seasonal variations in the area of scent marking gland and incidence of pregnancyin M. hurrianae.

M. hurrianae

Season Average gland area (mm") % pregnant

male female females

Winter 118.1 59.3 16.8(Dec-Feb)

Summer 105.4 54.7 16.0(March-June)

Monsoon 140.2 38.9 18.6(July-Sept)

Post-monsoon 91.4 70.4 23.3(Oct-Nov)

302 Saro] Kumari and Ishwar Prakash

(F1.149= 105.93, P< 0.001) and interactions between month and sexes (F11 149 = 6.29,P< 0.00 I) are significant. The gland size of male and female desert gerbil followsalmost a similar trend from January to June, both showing a peak in February.Thereafter, the gland size in females declines up to October, showing a peak again inNovember. However, in male animals, from June onwards, till September the glandsize increases steeply, thereafter it falls and corresponds with the maximum breedingepoch of females (figure 2). However, the receding gland area in females during thisperiod is rather perplexing. The analysis of data on season-wise basis reflects thisdifference more clearly (table 2); whereas the gland area is maximum in male desertgerbils, it is minimum in females during monsoon when their breeding activity issustained at a higher level (Kaul and Ramaswami 1968).

The mean monthly gland area in male R. m. pallidior exhibits peaks in March-April,July and November and is low in May-June, August, and September (figure 3). Thevariations between the months are significant (F,o .82 = 8.992, P<O.OI). The trend ofmonthly variations in gland area is almost reverse to that of frequency of pregnancy(figure 3). During October the incidence of pregnancy is maximum (Rana and Prakash1982) but the gland area is fairly low. At 47% pregnancey rate (September) the glandarea is low, whereas when the gland area is highest (March, April), the pregnancy rateis 58.7 and 62.2% respectively. In February and May when pregnancy frequency is 66.6

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Fleure 3. Monthly fluctuations in the dimensions of scent marking gland of male R. m.pa/lidior and percent incidence of pregnancy.

Table 3. Relationship between gland area and testicular weight.

Species

T. indica

M. hurrianae

R. m. pa/lidior

Mean ± S.E.Gland area (mm")

60.33 ± 4.23

138.33± 12.26

200.45 ± 12.03

Mean ± S.E. Pairedtestes weight (mg)

1.59± 0.15

0.33 ± 0.03

0.51 ± 0.09

Correlationcoefficience (r)

+ 0.3776**

+ 0.3313**

+ 0.4250··

** Level of significance P< 0.01

Seasonal variation in scent-marking gland of desert rodents 303

the gland area is very low, 142rnrn" and 136mm" (figure 3) respectively. The seasonalaverages indicate that the proportion of the pregnant females varies very little all theyear round but the gland area shows two clear peaks (table 1), one during summer andthe other during post-monsoon. Such apparent variations in gland area of male metadswere not expected when the incidence of pregnancy did not show significantfluctuations.

On an overall basis, however, the gland area and paired testes weights aresignificantly (P< 0.01) correlated (table3).

4. Discussion

The two gerbils and the metad exhibit significant(P< 0.01) monthly fluctuation in thegland area. This fluctuation trend is more or less similar in the three species withrespect to the observed peaks which occur late during winter and monsoon. Thesepeaks also correspond generally t o the breeding activity of these rodents which ismaximum during these seasons. The overall correlation would suggest that during themaximum breeding period of the rodents, atleast the male glands are larger indicatingthe increase in the secretory activity of the scent-marking gland and its enhanced role inolfactory perception. Such generally increased scent-marking activity during thebreeding season and comparative quiescence during the non-breeding season has alsobeen reported in the wild rabbit, hare (Mykytowycz 1966), in 'kangaroo rat (Quay1953) and Mongolian gerbil (Mitchell 1967).

The above conjecture is not quite supported if the monthly averages of gland areaand incidence of pregnancy in the three species studied are compared. During anumber of months when the gland area is maximum the incidence of pregnancy isverylow and vice-versa (figures I to 3). The seasonal variations in the two do not quitefollow the same trend except that for male M. hurrianae. Another quite importantevidence brought out is that the fluctuation in the gland area of male and female M.hurrianae follows entirely different paths; it is maximum in males during monsoonwhen it is minimum in females (table 2).

Another perplexing phenomenon observed is that when all the three species followthe same trend as far as the reproductive performance is concerned the fluctuations inthe gland area differ between the species. Ifthere was any definite relationship betweenthe gland area and breeding activity, the variations in the former are expected to followalmost a similar trend. In a number of other mammals such as Siberian hamster(Vorontosov and Gurtovoi 1959), black-tailed deer (Muller-Schwarze 1971),kangaroo rat (Quay 1953) Mongolian gerbil (Mitchell 1967), white rat (Stanely andPowell 1941) and several artiodactyles (Von-Schumacher 1936; Moy 1969) thesecretory activity of the marking glands is reported to be consistent throughout theyear irrespective of the breeding seasons.

The results of the above studies and those of the present one provide ratherinconclusive evidence about the relationship between the reproductive performanceand the dimensions of the ventral scent marking gland of rodents.

Acknowledgement

The authors are thankful to Shri S P Malhotra for facilities and encouragement.

304 Saroj Kumari and Ishwar Prakash

References

Eibl-Eibesfeldt I 1953 Zur Ethologie des hamsters (Cricetus cricetus); Z. Tierpsychol. 10204-254Erlinge S 1968 Territoriality of the Otter, Lutra lutra L., Gikos 1981-98Jain A P 1970 Body weight, sex ratio, age structure and some species of reproduction in the Indian gerbil,

Tatera indica indica Hardwicke, in the Raiasthan Desert. India; Mammalia 34 415-432Kaul 0 K and Ramaswami L S 1968Reproduction in the Indian Desert Gerbil, MerioneshurrianaeJerden;

Acta. Zool. 50 233-248Kumari S and Prakash I 1981 Scent marking behaviour of Merioneshurrianaeduring oestrus; Anim. Behav.

29 1269-1271Mitchell 0 G 1967 The supposed role of the gerbil ventral gland in reproduction; J. Mammal. 48 142Moy R F 1969 A study of five skin glands of the pronghorn (Antilocapra americana) M.Sc. Thesis,

University Montana, MissoulaMuller-Schwarze 0 1971 Pheromones in black-tailed deer (Odocotleus hemionus columbianus); Anim.

Behav. 19 141-152Mykytowycz R 1966 Observation on odoriferous and other glands in the Australian wild rabbit, O.

cuniculus and hare Lepus europaeus;a. Anal gland. CSIRO Wildl. Res. 11 11-29;b. Inguinal glands;CSI RO Wild\. Res. 11 49-64; c. Harder's Lacrymal and sub mandibular glands: CSIRO Wildl. Res. II

65-90Pearson 0 P 1946 Scent glands of a short tailed shrew; Anat. Rec. 9461 5-629Prakash I and Idris M 1982Scent marking by the female Indian gerbil Tatera indica from two distinct desert

habitat during oestrus; Indian J Exp. Bioi. 20915-916Quay W B 1953 Seasonal and sexual difference in the dorsal skin gland of the kangaroo rat (Dipodomys);

J. Mammal. 34 1-14Rana B 0 and Prakash I 1982 Reproduction biology of the soft-furred field rat Rattus meltada pallidior.

J. Bombay Nat. Hist, Soc. (in press)Snedecor G Wand Cochran W G 1967 Statistical methods (Ames, Iowa State: University Press)Sokolov Wand Skurat L 1966 A specific mid ventral gland in gerbils; Nature (London) 211 544-545Stanely A J and Powell R A 1941Studies on the preputial gland of the white rat; Proc. Louisiana. Acad. Sci.

523-29Stoddart D M 1972The lateral scent organs of Arvicola terrestris (Rodentia: Microtinae); J. Zool. (London)

166 49-54Townsend J E 1953 Beaver ecology in western Montana with special reference to movements; J. Mammal.

34 459-479Vorontosov N Nand Gurtovoi N N 1959 Structure of the mid abdominal gland of the true hamster

(Cricetini, Cricetinae, Rodentia, Mammalia); Dokl. Acad. Sci. U.S.S.R. (Bioi. Sci.) 125 385-388Von-Schumacher S 1936 Oas stirnorgun des Rehbockes (Capreolus capreolus capreolus L.) ein bisher

unbekanntes Dufforgan; Z. Mikrosk. Anat. Forsch. 39215-230