Biochemical Systematics and Ecology, Vol. 9, No. 4, pp. 351-354, 1981. 0305-1978/81/040351-04 $02.00/0" Printed in Great Britain. © 1981 Pergamon Press Ltd.

Olfaction and Parental Behavior in Ring Doves

JEFFREY COHEN* Institute of Animal Behavior, Rutgers - The State University, 101 Warren Street, Newark, NJ 07102, USA

Key Word Index - Streptopelia risoria; Ayes; ring dove; parental behavior; olfaction in birds.

Abstract- In the ring dove, several sensory cues emanating from the squab (young) have been shown to be important in maintaining parental care. However, no information exists on the role of olfaction in parental behavior. In the experiments described, the body odor of squabs was artificially altered by application of a fruit-scented substance to its back. This resulted in high mortality of treated squabs by day 7 post-hatching. The body weights of the fruit-scented squabs that died were lower than those of living controls, suggesting that some change in parental feeding had occurred. Behavioral observations also indicated qualitative differences in parental care towards fruit-scented vs control young. Toxicity was ruled out as a cause of squab death since subcutaneous injection of the fruit substance to squabs led to 100% squab survival High squab mortality following fruit-scent treatment could be prevented by bilateral olfactory nerve cuts in the parents. Taken together, these data suggest that olfactory cues may play a role in parental care in ring doves, and add support to the notion that olfactory cues can influence avian behavior.

Introduction Olfactory cues influence a wide variety of behavior in vertebrates [1]. In birds, the role of olfaction generally has been considered minimal in view of their comparatively small olfactory bulbs [2]. However, a small, yet growing literature has indicated that olfaction in birds may be involved in homing [3], food seeking [4], aggression [5], and sexual behavior [6]. We report here observations suggesting the role of olfactory cues in the maintenance of parental behavior in the ring dove (Streptopel/a risoria). Changing the body odor of the young (squabs) shortly after hatching results in their high mortality. This is apparently caused by parental aggression and a decline in parental feeding.

A fertile pair of ring doves typically produce a a clutch of two eggs which the male and female take turns incubating until hatching (14-15 days); they then brood until the squabs are old enough to leave the nest (about 8-10 days). At the time of hatching, the squab is naked; its eyes are closed and it shows poor motor coordination. This con- dition of helplessness continues for the first 6-8 days in the nest during which the squabs are completely dependent on the parents for nourish- ment (feeding) and thermoregulation (incubation) [7]. Parents feed squabs by regurgitating a substance called "crop milk", the sloughed-off epithelial lining of the crop sac which develops

"Present address: The Rockefeller University, New York, NY 10021, USA.

under the influence of prolactin stimulation. Sensory inputs from squabs such as tactile and visual cues have been found important in maintaining both crop sac development and parental care [8, 9]. Auditory cues are also important in the normal rearing of the young [10]. However, the question as to whether olfactory cues are involved in successful breeding of ring doves has never been studied. During their early period as nestlings, the squabs and their excre- tions have a distinct aroma which dissipates as soon as they are old enough to beg for food (about 9-10 days of age). These observations prompted us to explore the possibility that olfactory cues influence parental behavior.

Results We first determined whether application of a fruit- scented substance to the back of hatchlings affected their survival and the behavior of the parents towards them. On the fourth day post- hatching we found many of the squabs in both the fruit-scented and "alone" (no scent; thermal protection only) groups had died (Fig. 1). This trend continued to day 7; less than a third of the fruit-scented squabs, and none of the "alone" squabs survived. Fewer odor-painted than oil- painted squabs survived on days 6 (P< 0.05) and 7 (P< 0.01, Kolomogirnov-Schmirnoff test, two- tailed). Since oil-painted squabs were raised normally, it appeared that neither squab handling

(Received 30 September 1980: received for publicadon 9 April 1981 )

351

352 JEFFREY COHEN

I00 -- ~o ~ga z eo

Q_ 4O . . . . . . O,L \ -%

09 2 0 ~ ~ " -~ALONE (N-f4) ' ~

I 2 3 4 5 6 7

D A Y S P O S T - H A T C H I N G

FIG. 1 PERCENF SQUABS SURVIVING WHEN [,REATEb WI[H FRUIT SCENT: Fewer odor painted than oil-painted squabs survived on days 6 and 7 (P< 0.05, P < 0.025, Kolomogirnov- Schmirnotf test, two-tailed) Fewer "alone" than odor painted squabs lived on days 4 and 5 (P < 0.05, K . -S test, two-tailed)

nor new nests (due to changing of nest material) accounts for the death of the squabs in the odor group.

Although many of the odor-painted squabs died, a greater percentage of them survived longer than "alone" squabs (P< 0.02, day 5, Fisher Exact test, two-tailed), suggesting that parents of the odor-painted squabs were feeding them. Our daily behavioral record during three to four visits per day showed that parents of both odor and oil-painted squabs regularly sat on their nests. Daily body weights of odor-painted squabs that survived were equivalent to those of oil- painted squabs (Table 1). The body weights of odor-painted squabs that died were lower than those of oil-painted squabs (P< 0.05, Mann- Whitney U-tests), but were greater than "alone" squabs. Apparently the parents were feeding these squabs either less frequently or with less crop milk than normal.

We also noted that when squabs and nest were returned to the cage following each treatment, parents of oil-painted squabs settled quickly,

while those of odor-painted squabs shifted their position and investigated the squabs with pecks. Moreover, although parents of odor-painted squabs appeared to sit regularly, the quality of their brooding differed from that of oil-painted squabs in at least two respects: (a) the sitting of parents of odor-painted squabs was frequently interrupted by body movements such as investigative peckings, body shifting and half- standing, thus probably providing insufficient thermal protection for the nestlings; and (b) the investigative peckings of parents sometimes resulted in expulsion of the squab from the nest. In the ring dove, the squabs that fall out of the nest invariably die since parents fail to feed them. In many odor-painted squabs, we observed small wounds which appeared to have been inflicted by peckings. Although aggressive pecking of the squab by the parent is not known in laboratory ring doves, its occurrence has been reported in the field for laughing gulls [12] and in the laboratory for turkeys [13].

The possibility remained that the odor-painted squabs died due to toxicity of the fruit-scented substance. In a test of this hypothesis, squabs were injected with either the odor or oil substance used above. All squabs lived and were raised to the end of the experiment by their parents. Their daily body weights did not differ (for example, on day 7 median = 45.4 g, odordnj, vs 46.9 g. oil-inj.) and were comparable with those of the oil-treated group in the first experiment. These data suggest that we could not account for squab mortality in terms of systemic toxicity.

Our next questT0n is v{/i~at are the sensory cues in the fruit scent that mediate the changes in parental behavior? The possibility that olfactory cues are involved is tested by severing the olfactory nerves of parents of odor- and oil- treated squabs. As indicated in Table 2, bilateral olfactory nerve section in both parents significantly increased the per cent survival of squabs treated with fruit scents (P< 0.05, Fisher Exact test, one-tailed). However, 37% of the fruit-scented squabs of the parents that

TABLE 1. SQUAB BODY WEIGH-[ AT 5 DAYS OF AGE [.ABLE 2 EFFEC F OF OLFAC tORY NERVE CU [, DN SQUAB SURV)VAL

Treatment N Body weight (g) Per cent of squabs survlv~(J

Oil 19 30.8 (25.6-320) Day 4 Day 7

Odor - Lived 7 32 6 (28.1-32 7) (3d~or---[~/ O~t(~rr--()Jl Odor- Died 5 25 4 (13.4-266J . . . . . . . . . . . . . . . . . . . . . . . .

Bilateral olfactory nerve cut 63 I(X) 63 )()() Alone 1 12.5( ) )both parents)(N:Spairs)

Note: odor painted squabs are divided into those that lived through 7 days post-hatching and those that died before 7 days Sham or incomplete operallon ~-~ K)(} ~ f~,} Body weights are medians with quartile ranges. (N = 12 pairs)

OLFACTION AND PARENTAL BEHAVIOR IN RING DOVES 353

underwent olfactory nerve cuts died just the same. Odor-scented squabs belonging to parents with either sham-operations or incomplete olfactory nerve cuts died, and the percentage of mortality was comparable to that of intact parents in experiment 1.

In summary, the present data provide the first evidence that olfactory cues, in addition to visual, tactile [8, 9] and auditory [10] cues, may play a role in the rearing of a brood in ring doves. In addition these findings add to those suggesting that olfaction is one of the sensory cues which can influence avian behavior.

Discussion Our observation that a high percentage of squab mortality .following application of a fruit-scented substance to the young's back is due to altered parental care is supported by (a) the change in parental feeding, suggested by the result that fruit-scented squabs that die have lower body weights than oil-treated squabs; (b) the behavioral observations that parents of odor- painted squabs do not sit properly on the young and peck at them; and (c) the failure of sub- cutaneous injections of the fruit substance to induce squab death, thereby ruling out systemic toxicity. Furthermore, the change in parental behavior leading to squab mortality can be pre- vented, in part, by bilateral olfactory nerve cuts in both parents, suggesting that this effect is mediated by olfactory cues.

A possible interpretation of these results is that the fruit scent is aversive in general and resulted in behavioral disruption of which parental care is only one example. In a separate experiment (Cohen, unpublished observations), lemon or control oil was applied to the back of sexually receptive female ring doves who were then observed with normal male partners. This procedure did not induce measurable changes in male courtship behavior. Males continued to perform heteropreening, a display involving tactile contact with the neck region of the female. It appeared, therefore, that the fruit scent that disrupted parental behavior is not aversive in general.

The data from the olfactory nerve sectioning suggest that the fruit-scent squab mortality is in part mediated by olfactory cues. Since 37% of the squabs of parents with bilateral olfactory nerve cuts died, this suggests that either some other sensory cue (gustatory) emanating from the squab is responsible for squab mortality or that the squab olfactory cues are detected by the parents via sensory receptors that bypass the primary olfactory nerve. One other candidate for the detection of olfactory information is the trigeminal system. Pigeons with bilateral olfactory nerve cuts are capable of responding to odorants, and this has been attributed to the trigeminal nerve [14].

Experimental Treated squabs. 30 reproductively experienced male-female pairs of ring doves were introduced into breeding cages each containing food, water, nest material and a nest bowl; they were allowed to court (7-10 days) and incubate two eggs (14-15 days). In the afternoon following the hatching of the second squab, the nest bowl was removed, and the two squabs were weighed. The squabs were then transferred to a new nest (a fresh nest was constructed by the experimenter), treated and returned to their parents. Treatments consisted of swabbing the squab's back with either lemon or apple scented oil (Sunshine Laboratories, Inc.) (odor, n= 12 pairs) or the scentless oil base (oil, n = 11 pairs). The third group I"alone", n=7 pairs), received neither oil treatment or parental care and was kept in an incubator (33 ° ) to determine whether odor-painted squabs were receiving any care. If odor-painted squabs did not receive parental care, their body weights should approximate those of the "alone" group. Squabs were weighed and treated daily until the squabs died, or for 7 days, whichever occurred first.

Spot checks were made on incubating pairs three to four times a day between 09:00 and 17:00 h. Since this is the period when the male normally incubates [11 ], most observa- tions involved male-squab interactions.

Subcutaneous treatment of squabs. Squabs were given subcutaneous injections on the back on each of the first 7 days post-hatching Injections consisted of either 0.02 cm 3 of the lemon-scented oil (odor-inj., n=6 pairs) or scentless oil base (oil-inj., n=7 pairs). The volume injected was approximately the amount of oil that was swabbed on a squab's back as above. Daily body weights were recorded between days 1 and 7 post-hatching.

Bilateral o/factory nerve section of parents. Parents were made anosmic by bilateral olfactory nerve section on the first day the squab was hatched. They were returned to their squabs that were either fruit-scented or oil-treated on their backs (see above). Daily body weights were recorded between days 1 and 7 post-hatching On day 8, the parents were killed and examined with the aid of a dissecting scope for completeness of the nerve cuts.

Acknowledgements-Contribution No. 306 from the Institute of Animal Behavior, Rutgers - The State University. This work was supported by NIMH Grant No. MH-02271 and by Research Scientist Development Award No. MH-70897 to M.-F. Cheng.

References 1. Shorey, H. (1976) Animal Communication by Phero-

mones. Academic Press, New York.

354 JEFFREY COHEN

2. Bang, B. and Cob, S. (1968) A u k ~ , 55. 3. Hartwick, R. F., Foa, A. and Papi, F. (1977) Behav. Ecol.

Sociobiol. 2, 81. 4. Wenzel, B. M. (1968) Nature (London) 220, 1133. 5. Wenze(, B. M. and Raueh, L. S (1977) Ann. N. Y. Acad.

Sci. 2g0, 314. 6. Balthazart, J. and Schoffenieis, E (1979) Naturwissen

schaften 55, 55. 7. Wortis, R. P./1969) Anim. Behav. Mono. 2, 1. 8. Buntin, J. (1977) J. Comp. Physiol. Psycho). gl, 17. 9. Buntin, J. E)., Cheng, M. F. and Hansen, E. (1977)

Horm. Behav. 8, 297.

10. Nottebohm, F. and Nottebohm, M. E (1971) Anim Behav. lg, 313.

11. Gerlach, J. L., Heinrich, W. and Lehrman, D. S. (1975) Verh. Dtsch. Zoo/. Ges. 57, 351.

12. Hahn, D. C. (1977) Doctoral dissertation, Burgers Ur~i versity

13. Schleidt, W. M., Schleidt, M and Mage, M. (1960) Behawour 18, 254.

14. Henton, W. W., Smith, J C and Tucker, D (1966) Science 153, 1138