Part 13: Columbiaform Behavioral Science
1. Summary of Dove Behavior
2. Development of Pecking in Doves
SYNOPSIS OF BEHAVIOUR TRAITS OF THE RINGNECK DOVE

Knowledge of normal behavior of a species is of great value in interpreting results of experimental studies. For some purposes, it is desirable for a student to be free of preconceived ideas when he begins a study of natural behavior. Nevertheless, it is useful in other cases to acquaint a worker quickly with the units of behavior for any particular species so that he may go on to more advanced studies. Concise descriptions of the voice, postures, and movements of a species of bird, for example may accomplish this, with a brief indication of how such traits fit into the general life history. Such an outline also would help biologists and animal caretakers in handling and understanding their experimental animals. The following brief synopsis presents original observations on the ring neck dove, Streptopelia risoria, a domestic dove also known as Barbary or blond dove. The senior author has maintained reproductively active groups of this dove in captivity for the past fifteen years and has made continuous observations during six years on the large dove colony maintained by the Department of Genetics, at the University of Wisconsin.
The various displays and postures are grouped under six headings indicating the phase activity in which they occur. The units listed are heterogeneous but in a number of cases (e.g. B 1, 2, 3, 9 and C 1, 8) it seemed more prudent to group a number of related traits than to list each separately. The names are primarily descriptive but at times include reference to the situation of occurrence. An attempt has been made to minimize subjective interpretation in reporting observations; however, often it seems useful to indicate the apparent function of these movements.
A study by Craig (1909) on "emotion" in this species has been published. This work was stimulated by the earlier observations of Whitman (1919). Goodwin (1952) supplemented the earlier studies with a report on doves kept at semi-liberty, and presented comparative studies in 1956. The present authors were pleased to find so many points of agreement with Craig and Goodwin. There are a few minor areas of disagreement, but these are relatively unimportant to the present approach. In an outline such as this, it is difficult to indicate properly the sequence of postures in a given situation; therefore the reader is urged to read the more fluent but less complete reports by Craig and Goodwin. Another pertinent study is that by Lehrman (1955) which is concerned mainly with parental feeding behavior. A few disagreements of the present authors with statements in the latter paper have been reconciled by personal communication. The studies by Bennett (1939, 1940) on behavior in ring neck doves are also interesting and significant, but are not pertinent to the approach of the present study.
This list of "unit" behavior movements is not regarded as complete. For example, the authors are aware that parent birds may assist their young in hatching, resulting in a "T-shaped" shell breakage line. The frequency and details are not known sufficiently, however, to describe it satisfactorily.
A. Infantile and Juvenile Behavior (in approximate order of development)
1. Clutching. The newly hatched squab clutches the nest sticks or toes of its brooding parent with its feet, and hangs on tightly if disturbed. This behavior persists until the squab is nearly full fledged (about 3 weeks). It might serve in providing a solid purchase for the vigorous regurgitation feeding (B 9).
2. Head Waggle. Very young squabs (decreasingly true for older ones) may shake or waggle the head as if the muscles were unable to properly maneuver the head. It apparently occurs when the squab is searching for food or seeking a new position.
3. Squab Note. Apparently when hungry, the squab will give a prolonged shrill, sometimes ascending whistle of low intensity. Rarely the whistle tends to descend the scale. The duration is 1-3 seconds, but it may be longer in older squabs and repeated several times. It is usually accompanied by the squab wing shake (A 4) and bill searching (A 5). A very faint "peep" occasionally may be heard in the piping egg, and the strength of this squab note increases with each day of growth.
4. Squab Wing Shake. The squab may shake its wings rapidly (perhaps two or four shakes per second) for a few seconds and repeat intermittently in food begging movements (A 3, A 5). It becomes increasingly obvious beyond the first week after hatching.
5. Bill Searching. Accompanying A 3 and 4, an older squab thrusts its bill towards the parent's body in rapid "wiggling" movements. The squab learns to aim at and thrust its bill near and into the parent's mouth (see B 9), but very hungry older squabs will thrust at the tail, rump, legs or wings of the parents, the nest mate squab or even their own wings. It may represent a more advanced form of the head waggle (A 2).
6. Nest Defecation. As the squabs grow they tend to back toward the edge of the nest to defecate. Not until the pinfeathers are well developed do the squabs manage to defecate out of the nest.
7. Bill Snapping. Squabs and immatures may "click" or snap their bills one or more times when closely accosted by an unfamiliar object or movement. It develops rather suddenly (as the pin feather open) as does the fight or flight stance (see D 4) which appears with bill snapping and hissing (A 8). Bill snapping may be given by nesting adults in an extremely soft version.
8. Hissing and Puffing. Squabs and immatures may fluff the feather, especially those of the breast, and "hiss" when accosted as above. The wings may be raised as in the fight or flight stance (D 4). Nesting adults may express a faint hiss.
9. Squeaker Notes. Immature birds about four to eight weeks of age are termed "squeakers" by fanciers. Their voice is "squeaky", somewhat harsh and variable. As they become older, a similarity of the squeaker notes with the adult alarm note (E 6), "challenge" note (D 3) and the bow-coo (C 1) becomes evident.
B. Reproductive Behavior (Non-sexual)
1. Stick Nest Building. (May belong with sexual behavior C). Either sex, but more often the male, may walk around the ground picking up "suitable" (small, irregular shaped) sticks with its bill. [Nevertheless, pine needles about 6 inches long are favored.] Many sticks are discarded. The sticks are carried, a single stick at a time, to the nest site and placed near the partner. Usually, a longer section of the stick as held by the dove is carried projecting forward and down. Sticks beneath the nest site are ignored. The female predominates in arranging the sticks. However, a reversal of the roles occurs to some extent. Frequently the partner will "grab" the stick before it is placed and a short "tug-of-war" usually results. Juveniles have been observed to "play" with sticks.
2. Egg Laying. During oviposition, the female will stand and slowly raise the fore body. She appears to be straining for perhaps half a minute before the egg drops. She may ease the straining briefly and start again with a faint "ptk" expressed. During the straining period and especially near its termination, the eyes may be partially closed, or covered by the nictitating membrane. Also, the wings may droop, perhaps to assist the bird maintain balance. As the egg drops, the head may by thrown up and back. The bird usually "rests" five to ten minutes standing over the egg before leaving the nest, or before starting incubation, if the second egg was laid.
(Usually the female will lay the first egg in the afternoon and the second egg about 42
hours later. In this species a clutch usually consists of two eggs, occasionally one.)
3. Incubation. The parent crouches over the eggs, more or less orients then in a fore and aft position with the aid of the bill, the sides of the legs, and the keel, fluffs the ventral feather which exposes bare skin, and then settles down on the eggs. Eggs in an unsuitable position may be retrieved by gently placing the bill over the egg until the egg can be rolled carefully underneath the bird.
(The female parent sets during the night and contiguous light periods. The male sets six to fourteen hours during the middle of the day, 9:30 a.m. to 4 p.m. being typical, and the duration depending largely on the photoperiod. The length of the incubation period to hatching is 14 days.)
4. Feces Retention. During incubation, the faces of the settling parent are retained until the bird has departed from the nest, when a relatively enormous load may be released.
5. "Hiding". When closely approached either sex may remain motionless (crouch and freeze) on a nest of eggs or very young squabs. The head is drawn in and the feathers held tightly. This may be an alternative to the fight-or-flight stance (D 4) which also may be exhibited by a nesting bird. It is characteristic for any one bird to exhibit only one of these reactions in such a situation.
6. "Squared". When hiding (B 5) either sex may further tighten one wing (occasionally both) to the body so that the wing and back nearly form a right angle and tiny coverts near the shoulders are not smoothed to the rest of the wing but stand out.
7. Broken Wing Ruse or Injury Feigning. (Very rare.) When the senior author disturbed its nest, one white ring neck female clearly exhibited this behavior common to mourning doves and other birds in which one or both wings are held awkwardly extended and shaken as the bird hesitatingly moves away from the nest site.
8. Shell Removal. After emergence of the squab from the egg, a parent frequently removes the two shell parts one at a time with the bill and flies some distance from the nest before dropping them.
9. Regurgitation Feeding. Either parent may feed one of both young together by opening its mouth and receiving the bill of the young in its bill. The parent usually lowers its head as it "pumps" food from its crop to the throat by violent "shivering" of the wings and crop. Nearly always the head is raised and the "pumping" process is repeated several times. Regurgitation feeding is sometime initiated by a parent, which may very gently peek or preen the newly hatched squab. During this process the head of the parent is often lowered and the bill partly opened. This peeking and preening usually stimulates the young squab to head waggle and bill search (A 2 and 5), although these may occur without detectable parental stimulation. See Lehrman (1955) for additional comments on this process.
C. Sexual Behavior
1. Bow-coo. (The most frequent of coos.) The neck is inflated ventrally, the head and body held high; then the head is brought low suddenly with the bill pointed at or touching the ground. The pupil of the eye contracts. The first "note" of the call usually starts immediately as the head comes down. The first "note" is short; the middle notes form a rolling coo; and the last "note" is 2-3 times the duration of the first note, sometimes slightly descending the scale. If the observer is close, a strident, low, "appendix" note (one or two) is often heard at the end of the last note in the coo, as if the bird were regaining its breath or redistributing its air. The call may be indicated as huk' prrrroooo wah (wah). The bow-coo is always directed to or at a particular bird. It may by repeat as rapidly as 5 per ten seconds but usually longer interval occurs between calls. One bow-coo averages about 2 and 1/2 seconds per call. Between repeated bow-coos the male always "stamps" his feet lightly or steps toward the object-dove. However, sometimes one foot is only slightly raised and replaced. This call, occasionally given by unmated females, was never observed to be given by mated females.
2. Perch-coo. The notes are nearly the same as in a bow-coo (C 1), but they are given less hurriedly than the sometimes "frenzied" bow-coo. The perch-coo may be given with the eyes open, or nearly completely closed and is the only coo also given at night. It is never obviously directed at any particular bird in sight.
3. Nest-coo. The notes of this call are nearly the same as in a bow-coo (C 1), but the call is softer, less forceful, and more intermittent. It is always accompanied by wing "flipping" (C 4). The head may "nod" at the beginning of each nest-coo. In potential nest site males give this call more frequently than the female before a nest site is chosen, but afterwards the female may give it more frequently. (Apparently, doves sometimes consider a thin perch as a nest site and may even carry sticks to it, B 1).
4. Wing Flip. Either or both sexes in a nest site or more rarely on a perch may jerk their shoulders so that the wings, especially the tips, flip. Rarely only one wing is so flipped. Wing flipping may be constantly repeated and maintained intermittently for several minutes with a frequency of approximately two flips per second. Nearly always the head is held low and the tail high when the wing flip is given.
5. Hetero-preening. The male and female of a pair may "preen" each other especially about the face and neck or head. Hetero preening may be somewhat ritualized since the preening movement is often more cursory than in homo preening. Parents may hetero-preen their young, apparently assisting the feathers to break out of the sheath.
6. Billing. Billing occurs in a situation similar to hetero preening (C 5). Billing is often initiated be the female, which preens the neck and face of the male. After variable amounts of this hetero preening the male may reciprocate and then take the bill of the female in his and apparently feed her as he would a squab. (It is not clear whether or not food is actually passed.) [A very small amount of food likely is taken or tasted by the female.]
7. Sex-crouch. The sex-crouch usually follows billing (C 6). The female squats, lowers her head, and raises her shoulders, which will support the feet of the male.
8. Sex-mount. (Treading). The male's posterior feathers fluff out and he repeatedly "cranes" his neck above the female. He may even "preen" or place his neck above the female. He may "preen" or place his bill between his wing tips and rump. Then he mounts the female (both facing in the same direction), which is in a sex-crouch and maintains his balance by fluttering his wings. The tail of the male bends anterio-ventrally and swings from side to side until copulation. Normally, the sex-mount is always followed by the "laugh" or challenge note (D 3) by both sexes. The sex-mount takes about 5 to 10 seconds for completion, but the "preening" and "neck craning" by the male may be prolonged. Females very rarely try to mount mature males but may mount a partner frequently if paired with another female.
9. Driving. A few days prior to the female laying the first egg of a clutch, the male tends to follow her wherever she goes with occasional incomplete pecking movements (D 5a). Driving in ring neck doves is much less distinct than in C. livia. Goodwin (pers. comm., see 1956a) believes that driving normally occurs only if the potential sexual rivals are present.
10. Display Flight. (see F 16d)
D. Aggressive Behavior.
1. Attack Posture. The head is held low and horizontal and drawn close to the body. Sometimes the head is jerked up and down just before or after challenge notes (D 3) are given. The rump feathers are fluffed, and the pupil of the eye may contract and expand.
2. Rush. Maintaining and attack posture, the dove often runs or rushes at the opponent. At times the dove will fly toward the opponent but cage conditions ten to inhibit a rush by flying.
3. Challenge Note: Kah or "laugh". This note is nearly always given from an attack posture (D 1) and is often preceded or followed by a forward hop or jump. It consists of a series of similar high pitched, rapid, short notes (often five notes), hinh-hinh, hinh-hinh-hinh, frequently in one of the following ways.
OR
They may ascend and descend the scale slightly or alternate notes may go higher; other combinations are more rare. The high notes are accented. The challenge note given by a male often leads to bow-coos (C 1) if the "opponent" is a female and to a fight or flight stance (D 4) if the opponent is a male. Females usually give it only to newcomers, mates or territorial transgressors.
4. Fight or Flight Stance: Fear-threat display. A position nearly broadside to the opponent may be assumed with the wing opposite the opponent half raised. Initially the fore body is often raised slightly. Either escape (E 2, 3, 4, 5) or fighting (D 5a, b) may ensue from the position. It is especially easy to observe contrasting "intention" movements of the aggressive escape "conflict" within a dove in this posture.
5. Fight. (Intermittently accompanied by challenge notes, D 3).
a. Pecking. The aggressor dove pecks intermittently at the head, neck and shoulders of the opponent who may return pecks and wing blows.
b. Wing boxing. From the fight or flight stance (D 4) the opponent may be hit with single or multiple wing blows more or less directed to the head, neck and shoulders. It is the wing nearest the opponent, which does the "boxing". Sometimes the wings of the aggressor in flight hit the opponent.
c. Standing on opponent. The aggressor often flies or hops to stand on the back of the opponent. Thereupon pecking or wing boxing may ensue; but strangely enough these are minimized and standing alone may satisfy the aggressor.
E. Escape Behavior
1. Alert Stance. The body is held erect by straightened legs with the tail low, neck stretched and held high. The plumage is tightened close to the body. It is usually accompanied by the alarm note (E 6). The alert stance and the alarm note may be stimulated by the appearance of hawks, unfamiliar moving objects, or by humans, cats, rats, and snakes.
2. Flight Stance. The bird crouches, stretches the head forward, and raises the tail somewhat. It may follow an alert stance (E 1).
3. Avoidance. The head us held low and away from the attacker with the body in a crouch and sometimes leaning to one side; or, less often, the head may be held high, as the bird attempts to climb out of reach. It may be an intermediate form of the flight stance (E 2).
4. Flight. (See F 16). Outright flight often occurs immediately after aggressor approaches, as when one dove is in another's territory. Flight usually terminates any persistent attack. When frightened from the ground by a hawk, the dove most commonly flies forward and upward with a noisy clatter or wings, according to Goodwin (1952).
5. Wings Vertical. Adults, juveniles or older squabs may spread the tail, fluff the feathers, and hold one or usually both wings vertically over the body, which is sometimes inclined away from the attacker. It may follow a fight or flight stance (D 4).
6. Alarm Note. A soft "hinnnnh" may be given, often repeatedly. The character of this note may vary from time to time in the same individual, occasionally approaching a louder harsh quality. The latter may occur during feeding of the young. The duration of a single note is nearly one second, but a repeat note may be given every 5 to 10 seconds.
F. Other Behavior
1. Sunbathing. In direct sunshine, a dove may spread the tail, incline the body to one side and lift the wings, alternately holding one aloft during a few seconds or minutes.
2. Water Bathing. Doves may step into shallow water or sit on a perch near water level and fluff the feathers, crouch, and flutter the wings so that the water is "sprayed" throughout the plumage. The head is rapidly dipped or passed through the surface of the water a few times in a "sideswipe" motion. Often the wing is held vertical, but the tail is seldom spread. This response may also occur at the beginning of a light rain or spray of water. The bird always preens and shakes afterwards, if undisturbed.
3. Relaxed Resting. Beyond the usual "perching" a dove may lean its body to one side so that one wing is partly laid upon. Sometimes both wings are at an unusual angle (shoulders out, wrists in near feet). It occurs frequently in immatures and more rarely in adults.
4. Stretch
a. Gape. The neck is stretched forward and the mouth opened widely and moved forward and up.
b. Back stretch. Both wings are held vertically over the body but not spread. The tail and head are depressed. It frequently precedes or follows a foot stretch.
c. Foot Stretch. (or foot and wing stretch). One foot and leg are stretched backwards; the tail and one wing are spread and extended toward the leg being stretched.
d. Upper Mandible Stretch. The terminal half (distal) of the upper mandible is sometimes lifted above the lower bill while the mouth is held closed.
5. Rapid Peering. The head is moved more or less up, forward, and back in what appears to be visual "searching" movements. The head also may be turned side to side allowing each eye in turn to see the object of attention.
6. Questioning Bill. When no escape behavior is exhibited and when the bird is watching action or objects seemingly peculiar or unfamiliar to the bird, a "silent" rapid opening and closing of the bill occurs singly or repeatedly.
7. Huddled. When cold, ill, or "frustrated" (?) the bird may fluff the feathers, draw its head in very close to the body and perhaps even close its eyes. It may remain thus for hours in extreme cases.
8. Shivering. When very cold, ill or "ill at ease" (?) a shivering of the body and especially of the wings may occur.
9. Sneeze. The bird may be stimulated by illness, [eating too much salt], or by unknown factors to "sneeze" in a sharp "pttk" accompanied by a sudden sideways jerk of the bill and head. If the bird does have a "cold," the sneeze may be followed by a wheezing sounds.
10. Preening (homo-preening). The dove may arrange its feathers and their parts with the bill, each feather being passed between the mandibles in turn. A dove cannot reach its own head and many of the neck feathers for preening. The uropygial gland is used relatively infrequently.
11. Ruffling and Shaking. Practically all the feathers of the body are raised or "fluffed" and the wings and body are shaken vigorously. The feathers smooth down quickly afterwards. It often occurs during or after preening (F 10).
12. Tail Wag. Often after preening or ruffling and shaking or if an object drops on the bird's tail, the dove may shake the tail sideways somewhat like a duck but with only one or two shakes.
13. Scratching. The dove scratches its head and neck with its toes. The leg is not held dorsal to the wing as occurs in some birds when they scratch.
14. Eye Wipe. When a feather or foreign object adheres to the eye or when illness affects it, the dove may wipe its eye on its shoulder.
15. Flight Exercise or Wing Fanning. Immatures and adults after a period of relative inactivity may beat their wings somewhat as in flight but remain grasping the perch or floor. (Click here to see wing fanning)
16. Flight
a. Pen Flight or "hovering flight." The characteristic details of a dove flying in a pen or for short distances of a few feet have not been adequately distinguished. However, there seems to be a "hovering" quality distinct from distance flight.
b. Distance Flight. Since this species is usually caged, such flight is only rarely observed, but it is swift and direct according to Goodwin (1952).
c. Gliding Flight. The distance flight may be interrupted by gliding or sailing aspects with the wings held nearly motionless.
d. Display Flight. The male flies upward wing-clapping, then with the wings and tail spread widely he glides down, often in a half-circle (Goodwin, 1952). In wing-clapping, common in the domestic pigeon but less marked in the ring neck dove, the wings meet above the body in flight, producing a clapping sound.
17. Defecation. In normal defecation the vent feathers are fluffed, a semi-solid mass is expelled and the vent muscles are rhythmically contracted a few times.

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Development of Pecking in Ring Doves

The development of pecking in ring doves is described and analyzed as a model system for understanding the roles of learning in behavioral development. Ring dove squab go from complete dependence on their parents to independent feeding during the third and fourth week post-hatch. They learn to identify food and to consume it through their interaction with food and their parents. This chapter describes experiments that analyze the specific learning mechanisms involved in the development of pecking and what it is that squabs learn from their experience. More generally, the chapter illustrates the utility of applying learning principles to the analysis of behavioral development.

Chapter Outline & Navigation

I. Learning and Behavioral Development

II. Pecking

III. Development of Pecking
Thrusting and Gaping
Role of Feedback
Scaling of Gape to Seed Size
Synopsis: Learning and the development of pecking

IV. Learning and Behavioral Development

V. References

I. Learning and Behavioral Development

In this chapter we focus on how learning principles can be used to understand the development of pecking in the ring-necked dove (Steptopelia risoria). We study this system as a model for understanding how learning contributes to behavioral development (Balsam & Silver, 1994). First, we describe the character of adult pecking. Next, we describe how this response emerges during development followed by a summary of our research on how birds learn what to peck at and how they learn to make the skilled adult motor response. Lastly, we return to the general implications of this work for an analysis of behavioral development.

II. Pecking

The beak is the primary means by which most birds influence the world. It is used for prehension in a similar way to how primates use fingers and hands to reach, grasp, and manipulate objects. The beak is used to pick up and ingest food, preen the feathers, and build the nest. In many altricial species the beak is used to feed the young, either by grasping the beaks of the young and delivering food regurgitatively or by using the beak to seize food and carry it back to the nest. Additionally, the beak is sometimes used to drink, inflict injury, and to produce song. All of these actions involve different topographies of movement that are tuned to the specific stimuli and functions. These behaviors are highly skilled in adults.

For example, picking up a piece of seed is a
highly skilled action. An accurate response clip requires that information about the spatial location and properties of the target seed be rapidly acquired. This information is then used to precisely guide the motion of the head and the coordinated movement of the beak in grasping a seed. This is a remarkably flexible system in the fine adjustments that are made during each unique occurrence of the behavior. The trajectory of the head must change with each change in body position and the opening of the beak must be scaled to each change in seed size. In adults, the behavior is stereotyped and efficient, but it does not start out that way.

Prehension in avians, like that in primates requires the coordination of two response components the effector must be transported to the target object and then closed around it. In primates the transport component is typically called reaching or simply transport; for avians we prefer the term thrust. Closing around and securing of the target is called grasping. A successful peck requires that thrusting and grasping be well coordinated.

The duration of thrusting and the accompanying opening phase of grasping is so short (about 50-120 ms) in the Columbidae that either high speed motion picture photography or direct transduction by attached sensors is necessary to measure these movements precisely . A system for the direct measurement of the gape component was developed in the pigeon. A small rare-earth magnet is glued to the bird's lower beak and a small magnetic sensor to the upper beak. The intensity of the magnetic field detected by the sensor decreases as the beak opens. The signal from the sensor is input into a computer and the changes in interbeak distance are recorded in real time.

We employed this system to record the gape of adult ring doves. The movement of the head is synchronized with that of the beak. The gape sensor record is also synchronized. The top panel of the gape sensor record shows displacement and the bottom panel velocity. Negative velocities indicate reclosure of the beak. As an ingestive sequence begins, the head is briefly fixated above the seed and then drives downward toward the seed. During this thrusting movement the beak opens. Gape reaches its maximum (1-2mm wider than the seed) while the head is being thrust downward. As the beak reaches the seed it is reclosed around it creating a plateau in the record. After reclosure with the seed secured at the beak tip, there is a set of higher velocity beak opening movements that typically have only a single velocity peak and result from moving the seed to the back of the beak for swallowing. The movement of the seed in the beak is called mandibulation, and is often assisted by the tongue which sticks to the seed and pulls it backwards. At the end of the ingestive sequence the beak opens one final time. This opening appears on the gape record as a peak with rounded shoulders. According to Van Gennip (1988), this epoch of the signal is caused by movement of the tongue to allow swallowing.

III. Development of Pecking

The Columbidae family (pigeons and doves) provides good model of how adult feeding responses emerge during development. The general developmental pattern is similar in all members of this family and has been described in detail for the ring dove.

After a male and female ring dove have mated, the female typically lays a clutch of two eggs that are incubated by both parents for 14-15 days prior to hatching. Initially, the young are unable to feed themselves. The parents feed the squab "crop-milk", a cheese-like substance produced in the crop. Both parents participate in the regurgitative feeding of the young. These feedings are initiated by the parents after hatching, but by the time the young leave the nest on about post-natal day 10 (PD 10), the squab beg vigorously to obtain parental feeding. The begging consists of the squab thrusting its beak at the parent's beak while making very rapid fluttering motions with its wings. The begging is sometimes accompanied by a chirping-like call. During regurgitative feeding, the parent grasps the bill of the squab between its mandibles and makes vigorous pumping movements with its upper body, particularly with its neck and head. From around the third day post-hatching until the squab begin getting food on their own, the parents feed the squab crop-milk mixed with increasing amounts of seed. The amount of crop-milk fed to the squab increases through about PD 5 and declines thereafter. The amount of seed fed to the squab steadily increases until they are eating seed on their own during the fourth week after hatching.

The squab's and parents' behavior surrounding feeding interactions changes during the feeding transition from dependent to independent feeding. All of the young that we have observed will beg for food at least through the time of weaning (PD 21). The next figure shows that Parental feeding of young begins to decline near the end of the third week and usually ceases by the end of the fourth week post-hatch. Pecking begins around PD 14 and increases in frequency. Squab begin to successfully ingest seed by about PD 16 and continue to improve in efficiency. By PD 28 they are nearly as efficient as adults at ingesting seeds. We used the hall-effect system to follow the changes in gaping from the time squab start pecking until they independently feed. There were three types of gapes that were dominant during different steps in the development of feeding. Over 90% of all pecks could be sorted into the three types shown in the next figure. All of the squab moved through the same sequence of changes in topography as pecking became more efficient. Each transition in form was associated with improved efficiency of pecking. These were just the sort of changes that one might expect if the squab's experience with seed was contributing to the changes in response form.

Thrusting and gaping

In our first approach to the question of whether normal development of pecking depends on experience, we reared squab without any exposure to seed. We achieved this by grinding seed into a fine powder and gradually making this the only source of food available to parents prior to hatching. This powdered seed was also the only source of food available to the families after the squab hatched. We have found no differences between these powder-reared squabs and seed-reared squabs in growth and general behavior. Beginning on PD 14 and on all subsequent days, squabs were put into a chamber with seed on the floor for twenty minutes. We found that powder-reared squabs pecked very little during these test sessions as compared to seed-reared subjects indicating that direct experience with seed is important for development of the adult response.

We then began to analyze whether and what kind of experiences are necessary for normal development to occur. First, we have found that 2-3 week old squabs have an unconditioned tendency to thrust at seed. This response will habituate unless the sight of seed is followed by positive ingestional consequences. These Pavlovian pairings increase the rate of thrusting at seed and these pairings occur in natural parent-squab interactions.

The pairings of seed and food, while increasing head thrusts toward seed, do not result in the release of the skilled adult response. Initially, the opening and closing of the beak is only loosely coupled to head movement and seems to be elicited by the head movement. These gapes are not scaled to seed size and there is limited accuracy in the targeting of the peck. Suspecting that feedback from successful and unsuccessful pecks was necessary for sustaining pecking and for shaping the squab's behavior toward the adult form, we turned our attention to analyzing the roles of feedback in the development and maintenance of pecking.

Role of feedback

We guessed that feedback from the beak during the movement and feedback about the consequent success and failure of pecks was essential for the skill to develop. We thought that the feedback might be important for sustaining and strengthening the peck response. Additonally, unless the mapping from the visual cue to the size of the gape was "hard-wired", the afferent feedback from particular gapes must be associated with the success and failure of pecks at specific targets. In two different lines of experiments we have examined the role of feedback on the development of pecking.

To examine the role that feedback plays in sustaining the overall level of pecking, we exposed a group of powder-reared squab to seed for 20 minutes each day during the second week post hatch, but did not allow them to experience the seed in their beak. We did this by gluing the seed to the floor of the test chamber. These squab were immediately fed by the experimenter after the test session. The level of pecking observed in this group on day 22 when they were tested with loose seed on the floor was substantially less than the pecking observed in a second group who was given unglued seed throughout the prior training and testing days. Subjects exposed to the glued seed and deprived of feedback provided by successful pecks responded considerably less than the subjects that got to handle seed with the beak during testing. In fact, the glued-seed subjects pecked at exactly the same level as subjects that only received pairings of the sight of seed with food. Pavlovian pairings promote pecking but the opportunity to handle seed results in a higher peck rate. Thus one role of the feedback is to increase the overall rate of pecking. It is plausible that when parents regurgitatively feed offspring the sensation of seed in the beak becomes a conditoned reinforcer because of its association with positive nutritional consequences. Once the squab starts pecking successful responses provide this immediate reinforcement which would lead to a higher peck rate.

In sum, feedback about success and failure seems to contribute to every aspect of the skill. It contributes to the overall level of pecking and affects the targeting, grasping, and handling of the seed. When normal feedback is present during development the highly flexible adult response emerges. The bird pecks very precisely at a wide range of seeds from a range of positions. We wondered what learning underlies this flexibility. How does the bird build such a flexible repertoire?

Scaling of Gape to Seed Size

We already knew that maturation alone could not account for the development of the adult gaping response. Squabs reared on the powder diet do not show the adult gape form even when tested at an age when seed-reared squabs are quite proficient. The skilled adjustment to seeds of different size exhibited by adults depends on experience. Thus we turned our attention to identifying the specific experiences necessary for this aspect of the adult skill.

Our doves are usually raised on a standard dove mix. This mixture contains seeds of many sizes and shapes which range from about 1mm (millet) to about 12 mm (peas). It is possible that doves must separately learn to handle all of the different seeds before they show the precise and flexible adult response. Alternatively, the doves may acquire a generalized motor program. One characteristic of a generalized motor program is that quantitative adjustments of behavior occur in novel situations. For example, once we are skilled walkers we adapt to new terrain with little loss of skill. Similarly, we adjust the opening phase of our grasp to the width of any new object we pick-up. Presumably, once the motor program is functioning we are able to extract the necessary information to use the program from visual cues provided by the novel object.

It was an open question as to whether experience is necessary for the development of motor programs. Though skill surely improves with experience, but it is not clear whether or not the initial induction of motor programs requires experience. Because we can limit the doves' experience with seed during development we can study this question with respect to pecking. We know from our powder-reared subjects that they are not able to pick up seed when they first encounter it – even at an age when normally reared subjects would be quite proficient (Deich & Balsam, 1994). Perhaps experience with a single seed would be sufficient for inducing the motor program. Alternatively, experience with two or more points along a dimension may be necessary for the development of a generalizable skill.

To test this hypothesis, we compared the pecking of normally reared doves to a group reared on a single size pellet. In the group reared on a single size pellet their diet consisted solely of pellets, 2 mm in diameter. This was the only food available to the parents and squab until the time of weaning and the only food available to the squab until they were 18-24 months old. A second group of subjects was reared on mixed grain until they were between 18 and 20 months old. This group was switched to a diet of only 2 mm pellets by gradually increasing the proportion of their food that consisted of pellets over the course of a week. These subjects were then maintained solely on these pellets for at least two months prior to testing.

On the first test day, subjects were given 1 mm, 2 mm, and 3.6 mm pellets to eat. On test trials ten seeds of each size were presented. All pecks were videotaped and scored for accuracy. The set-up was similar to the one illustrated in the video. The seeds and beak were visible from below and from the side of the test aquarium. We classified the types of errors made by the birds into the six categories described in the figure showing the data from this test. The result of this test showed that subjects reared on mixed seed (not shown in the figure) had little trouble Click here to see results handling the 1 and 3.6 mm pellets even though they had only handled 2 mm seeds in the recent past. The subjects who had only experienced a 2 mm diet (shown in the figure) exhibited a different pattern of results during the generalization test. These subjects had little trouble with the 1mm seed. They made a few errors in which they contacted the seed but failed to grasp it. This was about the same number and type of error that they made when handling the very familiar 2 mm pellet. In contrast, the subjects reared on the restricted diet did very poorly on the 3.6 mm seed. They often contacted the seed and failed to grasp it or got their beaks around it briefly until the pellet squirted out as the beak closed. They were not scaling the gape to the size of the seed or positioning the beak to securely grasp the seed. It seems likely that the gape they had learned for 2mm seeds was wide enough and targeted well enough to handle the smaller, 1 mm, seed but not adequate for the larger seed. Over the next few days they readily learned to handle the larger seeds. In fact, they made very few errors after 50 or so experiences with the 3.6 mm seed. After a week of this testing, we introduced a 7.2 mm pellet during testing. None of the birds had any trouble with the new seed. Apparently, it takes experience with two or three points on a dimension to induce the generalizable skill.

Synopsis: Learning and the development of pecking

There is an unconditioned tendency for squabs to thrust at grain-like objects. However, this response habituates quickly unless the squab experiences Pavlovian pairings of the sight of grain with feeding. The Pavlovian induced thrusts do not have the coordinated gape found in the adult peck. There is only a loose coordination of gape and thrust, induced by the thrusting motion, itself. Squabs must have experience with handling and ingesting seed for the adult topography and coordination to emerge. Through differential feedback from successful and unsuccessful pecks, the gape component and its coordination with the thrust component are moved toward the more effective adult form by a process of response shaping. Operant conditioning is proposed as the underlying operative process because neither maturation nor extensive Pavlovian training is sufficient to produce the stereotyped adult response. Furthermore, reduction in the oro-sensory feedback as a result of beak deafferentation interferes with the development of the coordination.

All of these processes are important in the normal developmental context. From the time that parents start to feed squab seed the feel of seed in the mouth becomes associated with positive nutritional consequences. During the second week after hatching the parents stop consistently feeding the begging squab and, instead, go to peck at seed themselves (Wortis, 1969). The squabs follow the parents to the seed and make some unconditioned thrusts at food. Additionally, we have found that squabs tend to peck when their parents do (Iskrant & Balsam, 1994; see Zentall & Akins (2001) for more on social learning) and have documented that this social coordination is present in the undisturbed interactions of parents and squabs (Hirose & Balsam, 1995). The unconditioned tendency and the social enhancement guarantee the squabs visual exposure to seed. During this stage, parents generally feed squabs within a minute or two of this exposure (Hirose & Balsam, 1995). This allows for the sight of seed to be paired with food. The frequency of thrusting toward seed is increased by the Pavlovian pairings (Balsam et al., 1992). The squab's thrusting movement elicits loosely coordinated gapes (Wall et al., 1996). Some of these thrust-gape coordinations result in seed in the beak. Feedback from the seed in the beak reinforces the successful actions. The gape component and its coordination with the thrust component are moved toward the more effective adult form by a process of response shaping by reinforcement.

IV. Learning and Behavioral Development

The highly skilled and adaptable adult pecking response is produced by an intricate interplay between the squab's reflexes, the teaching of the parent, and the very precise feedback that is provided by the environment for success and failure. In these regards the development of pecking shares many features of behavioral development that are common to altricial species.

Within the context of the parent-offspring interaction there is typically a great deal of flexibility in development as a result of experience. For example, in the case of feeding, local conditions of food availability can determine the rate at which weaning occurs, the specific foods that a juvenile learns to find and to consume, and the specific responses that are used for foraging and eating (Balsam et al., 1992). Thus experiences are a critical influence on development. An important question is how to understand the specific ways in which experience affects these behaviors.

A number of developmentalists have articulated the view that laboratory learning principles do not capture the ways that experience affects development. Gottlieb (1976, p. 232) wrote, "Traditional forms of learning (habituation, conditioning and the like) have not proven very useful in explaining the species-typical development of behavior…" In this context, we view the studies described in this paper as a true test of validity for laboratory learning principles and believe that they have done pretty well. At least in the case of pecking, laboratory-derived learning principles have served us well by providing an analytic tool for understanding how specific experiences contribute to the development of specific aspects of behavior.

The emergence of new behavior is also a significant aspect of development that is influenced by experience. New response forms can be induced by elicitation, Pavlovian conditioning, habituation, and shaping (Balsam & Silver, 1994). Again the learning principles seem useful for understanding the ways in which experience accomplishes these changes in development. Furthermore, one can conceive of the transitions in functionally equivalent behaviors as the product of changing relative reinforcement rates. For example, the transition from dependent to independent feeding is likely modulated by the pay-off that each affords. The selection of specific feeding topographies is likely determined by the successes and failures of those actions in the past. In sum, we believe that learning principles provide a very useful framework for understanding the roles of experience in the ontogeny of behavior.