Hierarchical feeding behaviour in the leopard frog (Rana pipiens)

Anim. Behav.,1969,17,474-479

HIERARCHICAL

FEEDING BEHAVIOUR IN THE LEOPARD FROG (RANA PIPIENS) BY ROBERT

Department

BOICE & DAVID

W. WITTER

of Psychology, University of Missouri, Columbia, Missouri 65201

The extent to which findings of studies on dominance hierarchies in other vertebrates can be applied to amphibia is unclear (Hinde 1966). Furthermore, studies which do indicate territoriality (Pearson 1955) or dominance (Haubrich 1961) in amphibians have not included the species most commonly used in laboratory research, the leopard frog, Rana pipiens. The neglect of hierarchical behaviours in the leopard frog is surprising since many experimenters have noticed the development of gathering at the feeding place prior to feeding in frogs which are regularly fed in aquaria (Noble 1954; Thorpe 1956). If leopard frogs do aggregate prior to feeding as do other Rana (Van Bergeijk 1967), then perhaps some stable order in feeding might develop. Such a feeding hierarchy might resemble that described in Bufo marinus (Alexander 1964) where the smaller toads remain in the background until allowed to feed by the larger toads. Similarly, Haubrich (1961) found that aggressive South African clawed frogs (Xenopus Zaevis) eat more than fess aggressive pair-mates. Experiment 1 The purpose of this experiment was the investigation of individual feeding behaviour in leopard frogs. Specific attention was directed at factors which might affect the feeding response: the placement and character of the prey. Method Thirty-one adult leopard frogs were obtained from E. G. Hoffman & Son, 657 Florida Avenue, Oshkosh, Wisconsin 54901. Equal numbers of males and females were assigned to all groups. Distinctions as to sex on the basis of thumb size were difficult, since the thumbs of most subjects were partly decomposed upon receipt from the supplier. Judgments made from mating behaviour, however, indicated that males were generally larger in size than females. Thirteen were housed in one and eighteen in another O-076 m3 aquarium with 5 cm of water and flat rocks. The temperature of the laboratory varied between 20 and 23” C. The experimental period was from 1 October 1967 to 15 December 1967.

All frogs were fed individually, once a week, in a separate O-019 m3 aquarium. Its sides were covered with black construction paper except for two 5-cm2 openings on one side. One opening was 10 cm above and one was 8 cm below the frog’s eye level when he was positioned on the end of brick, 23 cm away from that side. Redworms were placed on the glass on either opening when appropriate. In the first treatment, all frogs were tested with worms in the ‘above’ position for three trials and with worms in the ‘below’ position for three trials. Three trials were administered in each of two weekly sessions. In the second treatment, all frogs were given two trials in two weekly sessions with artificial rubber worms (Creme Wiggle Baits) placed in the ‘above’ position. The artticial worms were held loosely against the glass and on half of the presentations were made to move in a manner closely resembling that of the live worms. This movement was induced by the use of thin threads the same colour as the backdrop to the experimental area. ReSUlt!S There was no systematic difference in either number of responses (actual jumps following an orienting response) or in average latency of feeding response as a function of above or below placement (Table I). There were few responses to the artificial worms (Table I) and all but two of those occurred when movement was ‘realistic’. A chi-square test for statistical independence showed a significant relationship (~2 = 70.15, P
BOICE & WITTER:

FROG HIERARCHICAL FEEDING BEHAVIOUR

415

Table I. Jumping Responsesby IndividaaI Frogs When Positionor Type of Bait was varied (Experiment 1) Experimental

condition

Possible responses

Actual jumps

Mean responses latency (see)

Worm above eye level

90

52

32.6

Worm below eye level

93

56

38.2

120

13

42.8

Rubber worm Experiment 2

Social behaviour can be defined as that which occurs differently in the presence as opposed to the absence of a conspecific (Bragg & Brooks 1958). The purpose of experiment 2 was the investigation of social feeding behaviour in leopard frogs. Specific attention was directed at factors which might affect the development of a feeding hierarchy : the amount of experience of the frogs as a group and the role of aggression. Methods

The subjects were four groups of leopard frogs, estimated to be 1 year of age. The first two, groups A and B, consisted of frogs used in experiment 1. Their housing continued as before. They were fed weekly as groups for 3 months prior to the start of testing. The testing period was from 1 January to 15 May 1968. Members of group A (N = 10) were not removed after obtaining a worm but were allowed to continue trying to obtain more worms until all frogs had ingested at least one worm. Frogs in group A had a mean length of 69.7 cm and a mean weight of 34.4 gm. Members of group B (N = 14) were removed after ingesting one worm but were replaced when all had eaten. Frogs in group B had a mean length of 67.0 cm and a mean weight of 28.7 gm. The second two groups consisted of adult leopard frogs obtained from E. G. Steinhilber & Co. Inc., Oshkosh, Wisconsin 59401. Both groups were maintained and fed the same as group B except that each was housed in a O-019m3 aquarium and both were tested as soon as the frogs were grouped. Group C (N = 8) had a mean length of 60.4 cm and a mean weight of 30.2 gm. Group D (N = 8) had a mean length of 59.6 cm and a mean weight of 27.9 gm. The presentation of food was the same for all groups. Red worms were placed against the glass of one side of the aquarium, one worm at a time (Fig. 1). In group A, the jumping order aaQ number of wOrms obtained were rworded?

In group B, only the jumping order was recorded. Groups C and D were added to permit testing from the start of grouping and to allow measurements of feeding order, jumping order, and number of jumps per session. The two original groups (A and B) were tested for a total of 12 and 14 weeks, respectively. The two newer groups (C and D) were tested for 8 and 9 weeks, respectively. All frogs were identified by their individual markings. Sketches of dorsal spots were used as referents. Results Table II summarizes the development of hierarchical feeding orders in all groups. The Kendall coefficient of concordance (W) (Siegel 1956) reflects the extent of agreement betkeen weekly rank-orders. This coefficient is also expressed as an average rank intercorrelation (rsaV) and as a ~2 statistic to permit a test of the hypothesis of no difference in mean rank over sessions. The resultant probabilities indicate the likelihood that the consistency of feeding orders over sessions could have occurred by chance. At the conclusion of the experiment (Table IIB) probabilities had decreased and agreement between rankings had increased over those based on testing at the midway point (Table HA). The correlation between summed ranks of feeding order and the number of worms obtained in group A was significant at the end of eight sessions (rho = O-873, P
476

ANIMAL

BEHAVIOUR,

Table II.* C-y

17,

3

of Fealing Order

A. Midway in Experiment 2 Number weeks tested

W

‘Sav

A

7

0.360

0.254

2522

0.01

B

8

0.354

0.262

28.34

0.01

C

4

0.182

-0Q91

5.08

0.70

D

4

0.185

-0.087

5.17

0.70

Group

X2

P<

B. At Conclusion of Experiment 2 A

12

0.371

0.314

40.07

0.001

B

14

0.430

0.386

70.25

0.001

C

8

0.318

0221

18.71

0.02

D

9

0,210

0.111

13.23

o-10

*The averageSpearmanrank correlations observedby use of the following (Siegel 1956): rSav=kW-1 k-l in which rSav = averagers or rho; k = number of setsof rankings; W = Kendall coefficientof concordance. The Kendall w’s were testedfor signiticanceby useof the following chi-squared formula (Siegel1956): ~2 = k(N - l)W, in which k = number of setsof rankings; N = number of individualsranked; W = Kendall coethcientof concordance. Table III. Correlati~~Bete~S$e

and Feeding Order

X

Group

rho

P<

A

0.685

0.05

B

o-495

0.05

C

0.321

ns

D

0.387

ns

Groups C and D demonstrate that frogs which jump first also tend to get a worm first (Table IV). Also frogs which tend to get worms first, tend to do so with the fewest jumps. Diiuwion The finding that placement of the worm above or below the eye level of the leopard frogs resulted in similar jumping behaviour (Table I) is not surprising since other species of Rana apparently capture food above and beneath the water sur-

face (Hamilton 1948). The finding that the frogs could discriminate live worms from rubber worms which were moved ‘realistically’ is contrary to results obtained in earlier studies. For example, Drake (1914) notes that the frog’s food is almost anything small enough to be seized and swallowed. Bragg (1957) contends that frogs will even jump at a dangled piece of cloth. Frogs in experiment 1 persisted in their preference for live worms even though the jumping distance prevented actual contact with the bait. This discriminative ability is pertinent later in interpreting nipping of other frogs as aggressive responses and not just feeding responses to movement. The stereotypy of sequential individual feeding postures is essentially identical to that noted by Hemplemann (1926). These same postures characterized orientation and grouping of the frogs in experiment 2. Prior to presentation of the worm, the grouped frogs were not aggregated and did not face in any particular direction. Wb?n a, worn was placed on the side of t4e

BOICE & WITTER:

FROG HIERARCHICAL

PLATE

FEEDING

BEHAVIOUR

XI

Fig. 1. Normal positioning of a testing group beneath a redworm; orienting postures show stereotypy of response. The white object on the surface of the water is a ruler of 15 cm in length.

Fig. 2. An example of nipping (arrow) following the frog being nipped.

the obtaining of food by Boice & Witter,

Anim.

Be/w.,

17, 3

ANIMAL

BEHAVIOUR,

PLATE

Fig.

3. Confrontation

(arrow)

between

17,

3

X11

two

toads

in the presence

Boicc

of a redworm.

61 Witter,

A/C/u.

Behm.,

17,

3

BOICE & WITI’ER: FROG I-UERARCHCAL FEEDING Bl%lAVfOuR TableIV. CTmddom BetweenJmn&

Group

Feeding order and jumping order

477

Order&Nm&er)ofJampsBeforesueeesg,and Feeding

Feedingorde-rand number of jumps

Jumping order and nuder of jumps

C

rho = O-655(P-cO.05)

rho = 0.286 (ns)

rho = O-238(ns)

D

rho = O-512(ns)

rho = O-863(P-CO-01)

rho = O-625(ns)

aquarium, most frogs turned their heads toward the stimulus simultaneously. This simultaneous movement seems to represent some sort of contagion effect but the’mediating cues were not readily apparent. Head movement was always followed by movement of the trunk toward the worm and the initiation of crawling toward the worm. Similarly, Snedigar (1963) notes that toads abandon hopping for a fast crawl when stalking, a gait less likely to attract the attention of the prey. This movement brought the frogs into rather stereoptyped positions under the worm (Fig. 1). Aggressive responses were critical at this time as the frogs pushed into position. When the frogs were in position to try for the worm, they raised or lowered their heads and drew up their legs in a symmetrical position. Even though most frogs in a group were apparently ready to jump simultaneously, jumps at the worm were usually successive. Each jump response was followed by disorientation. A frog which has jumped and missed has to ‘notice’ the worm again each time. However, once initial arousal is present responses occur more readily and more often. For example, the frog may look back toward the worm about 1 set after jumping. Thus even though the frog must repeat the sequence of postures leading to feeding each time (Hemplemann 1926), the whole process can apparently be quickened by heightened arousal. While the feeding hierarchy which developed in experiment 2 lacks the precision of linear dominance hierarchies in domestic chickens (Allee 1951), it does resemble hierarchical relationships in many vertebrates. The results of experiment 2 indicate that the outcome of a social encounter in leopard frogs is predictable if the situation is repeated enough times. Frogs which had been fed as a group for 12 or 14 weeks showed highly significant reliability of feeding order (Table II). Frogs which were housed together before testing (groups A and B) showed greater stability after around eight sessions than did those tested from the start of housing (groups C and D).

Because the feeding orders took time to de velop, the question of practice is raised. That is, do frogs which get worms first do so because they have had more practice in jumping? In group A, where frogs were allowed nearly unlimited practice, the higher-ranking frogs actually had the least exercise. The significant correlation (rho = 0.939, P
ANIMAL

418

BEHAVfOUk,

of drawing back to the periphery of the group and making one big leap at the worm. This afforded them medium rankings in slight excess of that permitted others of their size. An instance was observed of one frog which had been accidentally removed from its own group (B) and placed in another (A). Although it was ranked No. 3 in feeding order for its own group, it did not obtain a worm in the strange.group; frogs of 1, 2, 5, 6.5, 6.5 (tied ranks) obtained food in its presence. It was returned to its own group after frogs ranked 1,2,4,6, 12, 13 had eaten and were removed. It then oriented, crawled toward, and obtained a worm with unusual speed, experiencing little apparent competition from the remaining frogs. Similarly, Braddock (1949) found that prior residence in fish ‘. . . confers upon an individual a greater potential for dominance than it would otherwise have’ (p. 168). The most obvious form of aggression, nipping, occurred infrequently. Figure 2 shows a typical nipping response which has followed a successful jump by the frog being nipped. Nipping typically occurred between frogs who were similarly ranked and who contended actively for worms. Nips were exclusively directed at frogs who had just obtained a worm and usually occurred down the ranks. The fact that the frogs did not otherwise respond to movement patterns except those of live worms suggests that nipping was aggressive and not just misdirected feeding behaviour. There was also a marked

11,

3

short retention span and responds to aversive stimulation rather slowly (McGill 1960) he is capable of establishing feeding hierarchies which would suggest the presence of differing survival potentials in competitive situations. Summary Hierarchical feeding orders are expressed in grouped leopard frogs by an increasing stability of rank ordering in respect to frequency of capturing worms. The feeding hierarchy reaches significant reliability only after frogs are housed together for several months. Frogs which obtain worms most quickly tend to weigh the most and show the greatest degree of accuracy. Hierarchical feeding behaviours are primarily subtle, including pushing and climbing in an apparent attempt to gain position to jump at the worm. Occasional instances of nipping occur in closely competitive frogs after the worm has been ingested. Acknowledgments We are indebted to Dr Louis G. Lippman, now of Western Washington State College, who originally pointed out the feeding hierarchy in leopard frogs to the senior author when both were graduate students at Michigan State University in 1966. We thank Dr Robert Haubrich of Denison University, for making valuable criticism of an earlier version of this study. This research was supported in part by NIMH Grant MH 16093-01.

Table V. Consistency of Feeding Order in Toads N 16

Number weeks

tested 4

w

*Sav

0.660

0.547

tendency for other frogs to orient toward the frog who had just obtained a worm. These behaviours are apparently similar to aggressive confrontations in toads (Bufo americanus) kept in our laboratory in similar situations. The toads engage in striking face to face positions with eyes bulging (Fig. 3). These same toads showed a consistency of feeding order which exceeds that of the leopard frogs (Table V). Other investigators have noted that toads surpass frogs in the retention of learned responses (Thorpe 1956). The significance of the results of experiment 2 for the study of aggression is that the principles of feeding hierarchies extend to the leopard frog. Although the leopard frog has a relatively

X2

3960

P< 0401

REFERENCES Alexander, T. R. (1964). Observations of the feeding behavior of Bufo ma&us (Linne). Herpetologica, 20,255-259. Allee, W. C. (1951). Cooperation among Animals. New York: Henry Schuman. Braddock, J. C. (1949). The effect of prior residence upon dominance in the fish, Platypoecilus macula&s. Physiol. Zool., 22, 161-169. Bragg, A. N. (1957). Some factors in the feeding of toads. Herpetologica, 13, 189-191. Bragg, A. N. & Brooks, M. (1958). Social behavior in juveniles of Bufo cognatus Say. Herpetologica, 14, 141-147. Drake, C. J. (1914). The food of Ranu pipiens Shreber. Ohio Nat., 14, 257-263. Hamilton, W. J. (1948). The food and feeding behavior of the green frog, Runa clamitans Latrielle, in New York State. Copeia, 3,203~207.

EOICB & WUTBR: FROG ?HERARCHICAt Haubrich, R. (1961). Hierarchical behaviour in the South African clawed frog, Xenopus laevis Daudin. Anim. Behav., 9, 71-76. Hemplemann, F. (1926). Tierpsycholgie vom Standpunkte des Biologen. Leipzig: Akad. Verlagsges. (Cited in N. R. F. Maier & T. C. Schneirla, Principles of Animal Psychology). New York: Dover, 1964. Hinde, R. A. (1966). Animal Behaviour. New York: McGraw-Hill. McGill, T. E. (1960). Response of the leopard frog to electric shock in an escape-learning situation. J. comv. vhvsiol. Psvchol.. 53, 43345. Noble, G. K: (i9i4). The Riology of the Amphibia. New York: Dover. Pearson, P. G. (1955). Population ecology of the spade-

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BEHAVrOtrR

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foot toad, Scaphiopus h. holbrooki: (Harlan). Ecol. Monogr., 25,233-267. Siegel, S. (1956). Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill. Snedigar, R. (1963). Our Small Native Animals: Their Habits and Care. New York: Dover. Test, F. H. (1954). Social aggressiveness in an amphibian. Science, 126, 140-141. Thorpe, W. H. (1956). Learning and Instinct in Animals. Cambridge, Mass.: Harvard Univ. Press. Van Bergeijk, W. A. (1967). Anticipatory feeding in $s buuT3gg (Rana catesbeina). Anim. Behav., , (Received 21 August 1968; revised 1 November 1968; Ms. number: A741)