BEHAVIORAL BIOLOGY 19, 255--260 (1977), Abstract No. 6198

BRIEF REPORT Cross-Species Fostering" Effects on the Olfactory Preference of Onychomys torridus and Peromyscus leucopus I RICHARD M C C A R T Y 2 AND CHARLES H . S O U T H W I C K

Department of Pathobiology, The Johns Hopkins University School of Hygiene and Public Health, 615 North Wolfe Street, Baltimore, Maryland 21205 Litters of southern grasshopper mice (Onychomys torridus) and white-footed mice (Peromyscus leucopus) were reared by the natural parents or were reciprocally cross-fostered to parents of the opposite species. After weaning, mice were allowed a choice between the soiled beddings of Onychomys and Peromyscus adults of the opposite sex. Compared to controls, cross-fostered mice of botll species displayed decreased preferences for homospecific odors. Cross-fostered Peromyscus males actually switched species preferences to Onychomys odors.

Characteristics of the preweaning environment have been shown to influence the physical and behavioral development of a variety of mammalian species (Dubos, 1969; Newton and Levine, 1968). Parental interactions with the developing young are an important component of this early environment. Previous research with laboratory mice (Mus musculus) has demonstrated parental influences on agonistic behavior (Lagerspetz and Heino, 1970; Southwick, 1968), open-field activity (Denenberg, Hudgens, and Zarrow, 1964; Mugford and Nowell, 1972), adrenocortical response to novel stimuli (Denenberg, Rosenberg, Paschke, and Zarrow, 1969), and social preferences (Denenberg et al., 1964; Quadagno and Banks, 1970). Other studies, however, have reported a lack of parental influences on strain-specific patterns of behavior (Broadhurst, 1961; Collins, 1964). One technique for studying parental influences on the behavior of offspring is the method of cross-fostering young of one strain or species to another shortly after birth. Should the behavior of cross-fostered subjects differ significantly from controls reared by the natural parents, one may assume that such behaviors are influenced by interactions between parent 1 Supported by USPHS Grant MH 23419 awarded to the Johns Hopkins University. We thank Dr. Edwin Gould, Dr. Allyn Kimball, and Dr. Dwain Parrack for helpful comments on the manuscript. 2 Present address: Laboratory of Clinical Science, National Institute of Mental Health, Bethesda, Maryland 20014. 255 Copyright (~ 1977 by Academic Press, Inc. All rights of reproduction in any form reserved.

ISSN 0091-6773

256

McCARTY AND SOUTHWICK

and young (Bols and Wong, 1973; Joffe, 1969). We have examined the effects of cross-species fostering on the development of olfactory preference behaviors in two cricetid rodents, the southern grasshopper mouse (Onychomys torridus) and the white-footed mouse (Peromyscus leu-

copus). All Onychomys and Peromyscus subjects for this study were second and third generation offspring of original wild-trapped breeding stock. A breeding nucleus of eight adult male-female pairs of Onychomys was trapped in the vicinity of Tucson, Arizona and shipped by air to Baltimore. Peromyscus adults were trapped in Baltimore and Harford Counties, Maryland. Adults of both species were permanently pair-mated and housed in clear plastic cages (44 x 22 x 12 cm) with unlimited supplies of food and water. Litters of both species were reared by the natural parents or were cross-fostered to parents of the opposite species. All reciprocal crossfostering of litters of both the Onychomys and Peromyscus litters occurred within 48 hr after birth. Each of the two litters was removed from its home cage with a minimum of disturbance and placed in the nest area with foster parents of the opposite species. The entire procedure required less than 3 min. Control litters were not handled. All mice were weaned at 24-26 days of age and were housed in stainless steel nest boxes (22.5 x 18.5 x 14 cm) that contained a layer of bedding material and free access to food and water. A maximum of one male and one female was selected from litters of each species for tests of olfactory preference behavior at 10-day intervals from 30-100 days of age. The olfactory preference test measured a subject's ability to distinguish between the soiled beddings of Onychomys and Peromyscus adults of the opposite sex. The test apparatus consisted of two identical stainless steel next boxes as described above, each with a hole in the front, 4.5 cm in diameter, that was covered by a sliding plate. For each experimental subject that was weaned, a pair of nest boxes was assigned; one contained an Onychomys adult of the opposite sex and the other aPeromyscus adult of the opposite sex. These adult animals were the source of the soiled bedding material that was used in the preference testing. At the time of testing, the adult animals were removed from the next boxes, the cover platrs were removed, and the boxes were turned to face each other 15 cm apart. Cardboard partitions were then taped to the sides to form a closed neutral area (18.5 x 15 cm). The test subject was placed into the neutral area for a 10-min period, and the following data were recorded: (1) latency (seconds) to leave the neutral area. (2) number of entries into each nest box, and (3) cumulative time (seconds) spent in each nest box. Behavioral measures of each subject were averaged for the eight tests. The patterns of entries into the two nest boxes were combined into a single measure by dividing the number of entries into the next box containing homospecific

257

RODENT OLFACTORY PREFERENCE

odors by the number of entries into the next box containing heterospecific odors. Olfactory preference was calculated by dividing the cumulative time spent in the homospecific nest box by the total time spent in both nest boxes and converting the result to percentage scores. At the end of each test, the subject was returned to its home cage. Fresh bedding was placed in each of the nest boxes, the cover plates were replaced, and the resident mice were returned. For each succeeding test, the experimental subject was presented with a choice between the same two nest boxes, each containing a 10-day accumulation of soiled bedding. The positions of the nest boxes was randomly varied to eliminate the effects of spatial cues on nest box preference. Table 1 presents a summary of the measures of olfactory preference for control and cross-fostered Onychomys and Peromyscus males and females averaged over the eight tests. Onychomys males and females reared by the natural parents displayed a significant preference for nest boxes that contained soiled bedding of Onychomys adults of the opposite sex (P < 0.05). In contrast, Onychomys males and females reared by TABLE 1 M e a n Olfactory Preference B e h a v i o r s (-+ SEM) of Control and C r o s s - f o s t e r e d Onychomys torridus and Peromyscus leucopus Males and F e m a l e s a Variable

Control male

Crossfostered male

Control female

Crossfostered female

10

10

10

10

12.0 _+ 2.3

19.0 _+ 5.3

10.7 --- 2.8

7.3 -+ 1.6

1.2 __. 0.1

1.1 -+ 0.1

1.2 --- 0.1

1 . 0 -+ 0.1

Onychomys Sample size L a t e n c y to leave neutral a r e a (sec) H o m o s p e c i f i c nest b o x preference Preference for odors (%)

Onychomys 60.3 -

2.4 c

47.6 -+ 3.3

64.1 --- 3.3 c

48.2 -+ 2.8

Peromyscus Sample size L a t e n c y to leave neutral area (sec) Homospecific nest b o x preference Preference for odors (%)

10

8

10

7

26.0 -4- 10.0

12.7 _+ 3.0

52.3 --- 8.1 a

9.9 -4- 1.9

2.0 _+ 0.4 b

0.5 -4- 0.1

2.1 --- 0.3 b

1.1 -+0.2

74.1 -+ 4.5 a

27.4 -+ 5.1

71.0 -+ 4.2 a

46.8 -+ 7.7

Peromyscus

a E a c h subject was t e s t e d at 10-day intervals from 30-100 days of age. b p < 0.05. e p < 0.01. a p < 0.001 (two-tailed t-test).

258

McCARTY

AND

SOUTItWICK

Peromyscus foster parents showed a decreased preference for homospecific odors (P < 0.01) that was consistent over each of the eight tests (Fig. 1). Foster-reared subjects did not differ from controls in the latency to leave the neutral area or in the pattern of entries into the two nest boxes that contained the test odors (P > 0.05). Peromyscus males and females preferred the soiled bedding of the species that provided parental care (Fig. 2). Those subjects reared by the natural parents spent more time in and entered more frequently nest boxes that contained Peromyscus odors while cross-fostered subjects spent more time in and entered more frequently nest boxes that contained Onychomys odors. Foster-reared Peromyscus females had a decreased mean latency to leave the neutral area when compared to controls (Table 1). Previous research has suggested that young mammals tend to develop social preferences for stimuli associated with the species that provides parental care (Cairns and Johnson, 1965; Denenberg et al., 1964; Fox, 1969; Mason and Kenney, 1974). In addition, female rodents are thought to be more sensitive than males to species-typical odors to which they are exposed during the preweaning period (Mainardi, Marsan, and Pasquali, 1965; Quadagno and Banks, 1970). Our results, however, demonstrate an

?O60- _

Males ~

5( uJ

z e,, ul

u.

4¢ .._/;

o.

7(]-

z ~

6(]-

P~

i

511 .

oL/3'0 FIG. 1. M e a n o l f a c t o r y p r e f e r e n c e torridus m a l e s a n d f e m a l e s .

•

.

i

i

i

male-female

.

I o

I

I

i

cross-foster

.

,'o ' ,''

DAYOFAGE scores

of control

and cross-fostered

Onychomys

259

RODENT OLFACTORY PREFERENCE Males

100 -

5O I.IJ

o

z

C¢ LU IJ. I.¢J

,.--h"

r,/ D...

o cross-foster

• male-female

Females

100

-

z