Induced Parental Care In Male Convict Cichlid Fish VERA ABER KRISCHIK Lake Otitario Environmental Laboratory, Oswego, New York PETER G. WEBER Biological Sciences State University of New York, College a t Oswego Oswego, New York

Three parameters of parental care were recorded for pairs of cichlid fish (Cichlasoma niprofasciatum) caring for their own young to determine the normal parental role of the male. Nonreproductive adult males were induced to exhibit parental behavior (e.g., herding, fin-digging, and defense of young) by daily presentation of free-swimming conspecific young. This process of sensitization to young appears to be species-specific in that males did not exhibit parental care toward alien (Hemichromisbimculatus) young. Parental behavior in reproductive and nonreproductive males, as well as the implications and function of sensitization in these fish, is discussed.

A variety of vertebrate species may be induced to exhibit parental behavior toward young when nonreproductive (Burrows & Byerly, 1938; Ginsberg, 1965; Noriot, 1972; Rosenblatt, 1967; Rowell, Hinde, & Spencer-Booth, 1964). Parental behavior in nonreproductive females does not appear immediately, as it does in the puerperal female, but requires a period of exposure to young. The presentation of young to nonreproductive animals to induce parental care is a process termed sensitization. Induction of parental care has been accomplished in male rats (Leblond, 1938; Rosenblatt, 1967) and male fish (Van Iersel, 1953; Kramer & Liley, 1971; Kramer, 1974). In virgin female rats induced parental behavior is indistinguishable from that of the puerperal female (Leon, Numan, & Moltz, 1973). The first part of this study was designed to determine the normal parental role of male cichlid fish in caring for free-swimming young. The second part of this study was designed t o determine whether nonreproductive males will exhibit parental behavior toward young after a period of sensitization, a situation analogous to that in other vertebrates. The last part of this study was designed to determine whether nonreproductive males could be induced to care for young of an alien species, another situation analogus to other vertebrates (Denenberg, Hudgens, & Zarrow, 1964; Ramsay, 1953).

Received for publication 1 November 1973 Revised for publication 25 February 1974 Developmental Psychobiology, 8(1): 1-1 l(1974) 0 1 9 7 5 by John Wiley ti Sons, Inc.

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KRISCHIK AND WEBER

Synopsis of Reproductive Cycle of Cichlasoma Nigrofasciatum The convict cichlid, C. nigrofasciatum,is a teleost fish found in fresh water lakes and streams of Central America. The reproductive behavior of these fish is generally typical of substrate breeding species (Baerands & Baerends-van Roon, 1950). In 75- to 115-liter aquaria, courtship involves mutual display largely dominated by the male and generally lasting 1-7 days. The latter portion of courtship, involving selection and preparation of the spawning site, is dominated by the female. Spawning (30-60 min duration) occurs within a territory defended largely by the male. The egg-care phase (about 72 hr duration at 26'C) begins immediately after spawning. The female vigorously fans the eggs. The male is behaviorally subdominant, defending the vicinity of the eggs and only reluctantly exchanging roles with the female. In the subsequent larval period (about 96 hr duration at 26°C) both parents defend the larvae and occasionally transfer them to new pit nests in the substratum. During the subsequent free-swimming phase of the young (25-35 day duration) both sexes participate in parental care, defending and herding the young into a compact school. The male is capable of assuming the entire parental role in the event that the female is incapable of caring for the young. Morphological changes occur in both parents during the reproductive cycle. In the male the genital pore is extruded fully as spawning approaches and retracted somewhat afterwards, but remains visible throughout the cycle. The color change in the male, which lasts throughout the parental period, involves a heightening of the contrast between the lateral light and dark bars, giving an overall darker appearance.

Methods and Results Animals The fish used in this study were adult cichlid fish (Cichlasoma nigrofasciatum Gunther) 4 generations removed from the wild (British Museum [Natural History] registration number BMNH 1971, 10.27: 4-16). These fish were of unknown breeding experience and were taken from stock tanks.

Conditions The tap water in the aquaria was maintained at 28°C ? 2", filtered by subgravel filters, and changed every 3 weeks. Illumination came from four 40-W fluorescent ceiling lights and six 100-W incandescent bulbs placed around the periphery of the room. Mean light intensity at aquarium level was 366 lux. Lights were on at 0800 hours; off at 2000 hours. Fish were fed once daily between 0800 and 1200 hours; adults, with commercial food (TetraMin); free-swimming young, with brine shrimp (Artemia naupZii).

PARENTAL CARE IN CICHLID FISH

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Experiment A: Normal Role of Male in Parental Care Experimental Arrangement and Procedure Three 80-liter (55 x 35 x 31 cm) aquaria were divided in half by black Plexiglas partitions. Each compartment contained a mated pair with young. A 2 x 2 cm clear panel provided visual access between compartments. Each compartment also contained 2 clay pots and gravel 7 cm deep. Six pairs of C. nigofasciaturn were observed through the normal parental cycle to determine the role of the male in parental care. Data from an aberrant female of 1 pair were discarded when she escaped into the adjacent compartment and was killed by the neighboring pair. Three components of parental care given by each male and female toward their own 12-30 day old, free-swimming young were recorded during daily 10-min observations taken between 1100 and 1400 hours. The 3 components of parental care recorded have been fully discussed by Williams (1972) and are briefly described here : (Z) Looking-at-young. The parent tilts approximately 40" from the horizontal with the head lowered or elevated depending upon the position of the young. The eyes are directed at the group of young or at an individual in the group. The ventral and dorsal fins are usually folded. This act indicates parental attentiveness toward the young. (2)Fin-diging. The fish lowers its head to the substrate and pushes through the gravel, often scooping gravel with its opened jaws. Carrying off and spitting the gravel may conclude the act. During this act young gather around the parent and may obtain uncovered food particles. (3) Attack. The parent swims at a fish on the opposite side of the partition. The opercula and brachio-stergal mambrane may be spread and the act may end in biting at the clear partition. Attack serves to exclude potential predators from the vicinity of the young. The frequency of the action pattern, the number of bouts, and the duration per bout, per act, or per observation period were recorded for each behavior on a Rustrak event recorder.

Results The data shown in Figure 1 indicate that, with the exception of attack frequency and duration per act of looking-at, the male's mean duration and frequency scores were generally lower khan those of the female. A 2-way analysis of variance with Sex and Days as the factors showed that the mean male performance was significantly lower for all parameters except attack frequency and duration per act of lookingat (Table 1 ) . Combining the data for sexes and analyzing differences between days gave significance only for attack frequency and total duration of looking-at. No significant interaction was found for any of the parameters.

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KRISCHIK AND WEBER

Fig. 1 . Mean performance (frequency or duration) per lOmin observation period taken once per day (closed circles, solid lines = female means; open circles, broken lines = male means; n = 6 males and 5 females).

Experiment B: Parental Care in Nonreproductive Males Experimental Arrangement and Procedure Ten adult C. nigrofasciatum males were isolated for 2 weeks to ensure their nonreproductiveness, in 30-liter ( 4 5 x 2 5 ~25 cm) aquaria with visual access to 2

bp < .01. ' p < ,005. dp < .001

< .05.

15.84lC 6.24gd 1.486

1/9 18/162 18/162

s ex Days Interaction

al-,

Total Duration

df

Source

Frequency of Acts 9.1 05a 1.675 1.083

Duration per Act 2,066 1.161 1.253

Looking-at

.485 2.608d .5 84

Frequency of Acts

__Attacks

16.719' 1.448 1.178

Total Duration

10.33ga 1.117 353

Duration per Rout

Findigging

11.300b 1.626 .662

Frequency of Bouts

TABLE 1. Surnmaty of F Values from 2-Way Analysis of Variance with Repeated Measures of 1 Factor.

m

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KRISCHIK AND WEBER

similarly housed males. At the start of a test, a male was placed in a 70-liter (91 x 26 x 3 1 cm) aquarium, containing a 7.5-cm diameter clay pot and an air stone. Each aquarium floor was covered with 2 cm of coarse gravel. Water was filtered through an outside charcoal filter. The experimental aquaria also housed 3 to 4 adult males of another cichlid species, Tilapia mossambica, which were 2-3 times larger than the C. nigrofasciatum males. The Tilapia functioned as objects for the males’ aggression during the later induced parental care. The size of a male’s territory could be estimated by observing the area of the aquarium from which he chased the Tilapia. After the experimental fish had been acclimated to the new aquarium situation for 1 week, introduction of young was begun. Daily between 1300 and 1800 hours, 5 free-swimming young were decanted into the test aquarium (Table 2). The young were either conspecific or an alien cichlid, the jewel fish (Hemichromis bimaculatus). The mean age of the 970 introduced conspecific young was 17.6 days, with a range of 3-48 days free-swimming age. The 1275 alien young averaged 26.2 days with a range of 8-59 days free-swimming age. At these ages C. nigrofasciatum young show vertical light and dark stripes which become prominent by 10 days. Hemichromis young are smaller and show 2 horizontal stripes during the free-swimming stage. Ten-minute observations of the male’s color, aggressive state, size of genital pore, and response to the young were recorded. Five behavioral states toward introduced young were observed in male C. nigrofascia tum (Fig . 2): ( I ) No response. Males remained inside the clay pot, eating young that entered to escape predation by the Tilapia. Males were blanched, had no visibly protruding genital pore, and did not defend the pot vicinity against Tilapia.

TABLE 2. Age of Introduced Conspecific Young Presented to each of 10 Male C. nigrofasciatum. Age of Young Determined )?om 1st day of Free-Swimming. (C.n. = C. nigrofasciatum,H.b. = H. bimaculatus). Free-swimming Age (days) of Young Male Weight (g)

Total No. Stock Young

No. Stock Broods

Range

Mean and S.D.

2 3 3 5

20.30 17.55 16.94 19.44 17.47

150 C.n. 150 C,n. 150 C.n. 270 C.n. 250 C.n.

2 2 2 10 9

3-31 3-31 3-31 648 10-26

16.70k 8.18 16.70% 8.18 16.70t 8.18 20.85 k 9.63 16.84 f 15.90

6 7 8 9 10

26.33 29.53 32.86 23.99 23.9 1

255 H.b. 255 H.b. 255 H.b. 255H.b. 255 H.b.

5 5 5 4 4

8-32 8-32 8-32 15.59 15-59

18.70 t 18.21 18.70 t 18.21 18.70k 18.21 37.53 t 37.90 37.53 k 37.90

Male No.

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.I

I

1

TIME (DAYS)

Fig. 2. Changes in the behavior of 5 males C. nigrofaschrum toward introduced conspecific young. Open bars = chase and eat; cross hatchings = chase; vertical stripes = intermediate; dots = herd; horizontal stripes = no response.

(2) Chase aizd eat. Males actively chased and ate the young in the pot vicinity. Males were dark, with a slightly visible genital pore. The pot vicinity was occasiondlly defended against Tilapia. ( 3 ) Chase. Males chased the young in the pot vicinity but did not eat them. Males were dark, with the genital pore extruded. The pot vicinity was vigorously defended against Tilapia. Males remained inside the pot, allowed young to enter without being ( 4 ) Ignore. pursued or eaten, but did not display parental care toward them. Males were very dark, with the genital pore completely extruded. The pot vicinity was vigorously defended against Tilapia. (5) Herd. Males collected and herded the young into the pot or into a pit excavated in the gravel. Coloration and genital pore condition were the same as in the preceding phase. Males enlarged the defended pot vicinity by attacks on the Tilapia, which were forced into a small area of the aquarium. Only 1 of the a b w e 5 stages was shown by a given male during a given observation period. Introduction of young was terminated after 1 week of herding by the male, or 51 days without attaining the herding phase.

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Results The daily presentation of conspecific young to 5 male C. nigrofasciatum altered the behavior of each from nonparental (i.e., young were eaten), through an intermediate ignore stage, and eventually to a parental stage (i.e., young were protected). As the male began the intermediate stage, the number of young in the aquarium generally began to increase, and by the start of herding the male was caring for more than 15 young per day (Fig. 2). The mean latency for herding to occur was 30 (range 2346) days. In marked contrast, 5 male C. nigrofasciatum never accepted Hemichromis young, nor did they exhibit parental behavior. These males never exhibited Stages 4 or 5, but either showed no response to the alien young or chased and often ate them. These young, upon introduction, were either eaten by the male or by the Tilapia, and their numbers never increased beyond the 5 introduced per day (Fig. 3).

Discussion The results of Experiment A support the observations of Armitage (1960), and the more detailed study of Williams (1972), who found that both cichlid parents are capable of parental care. The lack of significant interaction in all parameters indicates that the pattern of parental behavior is similar for both sexes. Males simply show lower performance levels than the females in terms of most of the parameters quantified. The results of Experiment B indicate that C. nigrofasciatum males isolated from interaction with females and the earlier stages of young, will give parental responses to conspecific free-swimming young after a sensitization period of about 30 days. This result contradicts earlier work with cichlid fish which indicated that parental care in nonreproductive individuals could only be elicited by administration of hormones (Noble, Kumpf, & Billings, 1938). The complex physiological changes involved in producing young facilitate parental behavior, but are not a necessary precursor of parental behavior. Sensitization to young in nonreproductive fishes indicates that the young themselves are a key stimulus in eliciting parental care. Visual, chemical, or auditory stimuli associated with the young can alone trigger parental care in other fish species. For male 3-spined sticklebacks, Gasterosteus aculeatus, Van lersel (1953) has shown that the presence of eggs can induce egg-care behavior without the normal sequence of courtship and fertilization. Likewise, parental eggeating inhibition can be initiated by presenting male blue gouramis, Trichogaster trichopterus, with eggs spawned by other pairs (Kramer &Liley, 1971; Kramer, 1974). Sensitization with young in nonreproductive C. nigrofasciatum males of unknown breeding experience was only successful using conspecific young; Hemichromis young did not elicit parental care (Fig. 3). In previous studies on the ability of cichlid fish to discriminate between alien and conspecific young, the young of reproductive fish have been exchanged for alien young. Noble and Curtis (1939), Baerends and Baerends-van Roon (1950), and Myrberg (1964) found that experienced cichlid parents discriminate against alien young primarily by differences in color, pattern, or size, although olfactory differences may be involved (Kuhme, 1963; Myrberg, 1966). Successful exchanges with free-swimming young have been made with other cichlid species in studies where the developmental stage of the exchanged young matched the parent’s reproductive phase (Collins & Braddock, 1962; Greenberg, 1963 a,b; Noakes & Barlow, 1973).

PARENTAL CARE IN CICHLID FISH

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5

Fig. 3. Changes in the behavior of 5 male C. nigrofasciatum toward introduced H. bimaculatus young. Legend as for Fig. 2.

In the present study, neither the developmental stage of the conspecific nor the Hemichromis young were appropriate at the outset, in that the C. nigrofasciatum males were nonreproductive. However, successive presentations of conspecific young eventually induced appropriate parental care. The failure of the Hemichromis young to induce parental care is perhaps due to the ability of the adult males to discriminate color patterns or olfactory differences, as size and developmental stages of both conspecific and alien young were similar. Thus, the results of Experiment B indicate that whereas conspecific young are a sufficient stimulus to induce parental care without the physiological changes associated with production of young, alien young are an insufficient stimulus to male C. nigrofasciatum. The latency of the parental care response in nonreproductive C. nigrofasciatum males was about 30 days. Latencies of 6-18 days have been reported for mice (Leblond, 1938), rats (Rosenblatt, 1967), and domestic hens (Burrows & Ryerly, 1938; Ramsay, 1953). Ramsay found that nonbroody hens went through stages of incomplete parental care before reaching the normal broody behavior, a situation analogous to that observed here in C. nigrofasciatum. In the fish 7: trichoptems, Kramer (1974) found that the latency for males to become parental was short and varied with the strength of the stimulus.

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KRISCHIK AND WEBER

Differences in sensitization latencies in various species may also reflect differences in the relative importance of physiological change in producing an appropriate parental response. Thus, long latencies might be expected in species where parental care is preceded by complex physiological changes associated with reproduction. Sensitization studies are designed to determine the relative role of the young as stimuli in eliciting and maintaining appropriate parental care. Parental care of free-swimming young by C. nigrofasciatum males in the typical reproductive sequence may be regarded as a result of 2 sets of interacting causal factors. One set is the visual, chemical, or auditory environmental stimuli, first of the female and then of the female and offspring. The other set of causal factors are the largely unknown physiological changes that accompany various stages of the normal reproductive sequence in these fish. Thus we postulate for C. nigrofasciatum a complex “stimulus -+. physiological change -> response” chain analogous to that described for ring doves (Lehrman, 1965) and canaries (Hinde, 1965). In this study we are concerned with the: free swimming young (stimulus)

--+

postulated physiological change

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parental care (response) toward free-swimming young (object of response)

portion of this reproductive chain. Fiedler (1962), Blum and Fiedler (1964, 1965), and Blum (1966) have shown that administration of exogenous prolactin alone can elicit and maintain a parental behavior (fanning) in nonreproductive fish in the absence of an appropriate stimulus. We have shown that the stimuli of free-swimming young can elicit and maintain parental behavior toward those young in nonreproductive fish, perhaps by induction of appropriate physiological changes (see discussion of latency above). The adaptive significance of this postulated stimulus-response chain is that if the stimuli are removed (e.g., destruction of eggs or death of young), the response of the adult soon ceases. The absence of the stimulus, then, dampens energy-wasteful or inappropriate behaviors.

Notes Alan Bostrom performed the computer analyses and provided statistical advice; the authors gratefully acknowledge his aid. They are indebted to P. Colgan, K. M. Rosenberg, and S. P. Weber for critically reading earlier stages of the manuscript and contributing toward its improvement. Request reprints from: Dr. Peter G. Weber, Biological Sciences, State University of New York at Oswego, Oswego, New York 13126, U.S.A.

References Armitage, K. B. (1960). Observations of parental behavior of Cichlasoma nigrofasciaturn (Gilnther). nans. Kans. Acad. Sci.,63: 269-273. Baerends, G . P., and Baerends-van Roon, J. M. ( 1 950). An introduction to the study of the ethology of eichlid fishes. Behaviour, Suppl. 1. Blum, V. (1966). Zur hormonalen Steuerung der Brutpflege einiger Cichliden. 2001.Jahrb., Ab?. Allgen?. Zool. Physiol. Tiere, 72: 264-290. Bluni, V., and Fiedler, K. (1964). Der Einfluss von Prolactin auf das Brutpflegverhalten von Symphysodon aequifasciata axelrodi I,. P. Schultz (Cichlidae, Teleostei). Naturwissenschaften, 51: 149-150.

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Blum, V., and Fiedler, K. (1965). Hormonal control of reproductive behaviour in some cichlid fish. Cen. Comp. Endocrinol., 5 : 186-196. Burrows, W. H., and Byerly, T. C. (1938). The effect of certain groups of environmental factors upon the expression of broodiness. Poult. Sci., I 7 324-330. Collins, H. L., and Braddock, J. C. (1962). Notes on fostering experiments with the cichlid fishes, Tilapia sparrmani and Aequiderzs portalegrensis (Abstract). Am. Zool., 2: 400. Denenberg, V. H., Hudgens, G. A., and Zarrow, M. X. (1964). Mice reared with rats: Modification of behavior by early experience with another species. Science, 143: 380-381. Fiedler, K. (1962). Die Wirkung von Prolactin auf das Verhalten das Lippfisches Crenilabrus ocellatus (Forskg). Zool Jalzrb., Aht. Allgem. Zool.Physwl. Tiere, 69: 609-620. Ginsberg, B. E. (1965). Coaetion o f genetical and nongenetical factors influencing sexual behavior. In F . R . Beach (Ed.), Sex and Behavior. New York: Wiley. Pp. 53-75. Greenberg, B. (1963a). Parental behaviour and recognition of young in Cichlasoma hwcellatum. Anim. Behav., 11: 578-582. Greenberg, B. (1963b). Parental behaviour and imprinting in CicNid fishes. Behoviour, 21: 127-144. Hinde, R. A . (1965). Interaction of internal and external factors in integration of canary reproduction. In P. R. Beach (Ed.), Sex and Behavior. New York: Wiley. Pp. 381415. Kramer, D. L. (1974). Parental behaviour in the blue gourami, Trichogaster tricoptetus (Pisces, Belontiidae) and its induction during exposure to varying numbers of conspecific eggs. Behoviour, 47: 14-32. Kramer, D. L., and Liley, N. R. (1971). The role of spawning behaviour and stimuli from the eggs in the induction of a parental response in the blue gourami, Trichogaster tricopterus (Pisces: Belontiidae). Anim Behmi., 19: 87-92. KUhme, W. (1963). Chemisch ausgelaste Brutpflege - und Schwarmreaktionen bei Hemichromis himaculatus (Pisces). Z. Tierpsychol., 20: 688-704. Leblond, C. P. (1938). Extra-hormonal factors in maternal behavior. B o c . SOC.Exp. Biol. Med., 38: 66-70. Lehrman, D. S. (1965). Interaction between internal and external environments in the regulation of the reproductive cycle of the ring dove. In F. R . Beach (Ed.), Sex and Behavior. New York: Wiley. Pp. 355-379. Leon, M., Numan, M., and Moltz, H . (1973). Maternal behavior in the rat: Facilitation through gonadectomy. Science, 179: 1018-1019. Myrberg, A. A., Jr. (1964). An analysis of the preferential care of eggs and young by adult cichlid fishes. Z. Tierpsychol., 21: 53-98. Myrberg, A. A., Jr. (1966). Parental recognition of young in cichlid fishes.dnim. Behav., 1 4 : 565-571. Noakes, D. L. G . , and Barlow, G . W. (1973). Cross-fostering and parental-offspring responses in Cichlasoma citrinellum (Pisces, Cichlidae). Z. Tierpsychol., 33: 147-152. Noble, G . K. and Curtis, B. (1939). The Social behaviour of the jewel fish,f€emichrornishimculatus, Gill. Bull. Am. Mus. Natur. Hist., 76: 1-46. Noble, G . K., Kumpf, K. F. and Billings, V. N. (1938). The induction of brooding behavior in the Jewel Fish. J. Endocrinol., 23: 353-359. Noirot, E. (1972). The onset of maternal behavior in rats, hamsters, and mice a selective review. In D. S. Lehrman, R. A. Hinde, and E. Shaw (Eds.), Advances in rhe Srudy of Behavior. New York: Academic Press. Pp. 107-145. Ramsay, A. 0. (1953). Variations in the development of broodiness in fowl. Behaviour, 5 : 51-57. Rosenblatt, J. S. (1967). Nonhormonal basis ofmaternal behavior in the rat. Science, 156: 1512-1514. Rowell, T. E., Hinde, R. A,, and Spencer-Booth, Y. (1964). “Aunt”-infant interaction in captive rhesus monkeys. Anim. Behav., 12: 219-226. Schneirla, T. C., and Rosenblatt, J. S. (1961). Behavioral organization and genesis of the social bond in insects and mammals, Am. J. Orthopsychiatry, 31: 223-253. Van lersel, J . J. A. (1953). An analysis of the parental behavior or the male three-spined stickleback (Gasterosteus aculeatus L.). Behaviour, Suppl. 3. Williams, N. J. (1972). On the ontogeny of behavior of the cichlid fish Cichlasonis nigrofasciatum (Gunther). Unpublished doctoral thesis, University of Gronigen, The Netherlands.

Induced parental care in male convict cichlid fish.

Three parameters of parental care were recorded for pairs of cichlid fish (Cichlasoma nigrofasciatum) caring for their own young to determine the norm...
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