Fry Recognition and Foster-Parenting in Geophagine Cichlids

Transcription

1 Fry Recognition and Foster-Parenting in Geophagine Cichlids by Wayne S. Leibel Geophagus-Aequidens Study Group 620 Monroe Street Easton, PA Introduction My interest in fry recognition began, as usual, quite serendipitously one day when spawnings of the African Jewelfish (Hemichromis guttatus) and Gymnogeophagus balzanii occurred within minutes of each other. Already up to my armpits in Gg. balzanii fry, and having commenced a series of behavioral experiments that involved manipulating eggs and fry of this species (see Leibel, 1983a), I began to pursue a series of informal fry-swapping experiments that have proven quite interesting and provocative. These manipulations involved various mouthbrooding and substrate-spawning members of the closely-related genera Geophagus and Gymnogeophagus, and are reported herein. They seem to support the primacy of visual, primarily behavioral, cues in the recognition and adoption of fry in this group of neotropical cichlids. Fry Escape and Buccal Sheltering in M ixed H. guttatus-gg. balzanii Schools The co-spawned clutches of Hemichromis guttatus and Gymnogeophagus balzanii eggs developed more or less synchronously: both were free swimming and feeding by day eight postspawn, although the H. guttatus fry were conspicuous for their distinctive coloration, even at 5 mm hatching size. In fact, the H. guttatus fry bore two dark brown horizontal stripes from head to tail, whereas the Gg. balzanii fry were uniformly light brown. Thus, it was easy to distinguish the two fry when mixed, even from a distance. Hemichromis guttatus, you will recall, are typical substrate spawners in contrast to the delayed mouthbrooding strategy of Gg. balzanii (Leibel, 1983b). The experiment suggested itself: If H. guttatus and Gg. balzanii fry of similar age and sizes were mixed together, would they school and swarm together when threatened; if so, would the female Gg. balzanii accept these strangers into her buccal cavity? Three dozen H. guttatus fry were added to the 300+ school of Gg. balzanii fry. I sat back to watch. The fry did indeed school together and were quite compatible. When threatened both species alike made a beeline for the brooding female Gg. balzanii, but the H. guttatus fry (distinguishable due to their conspicuous double striping) always balked when the gaping mouth and moment of truth drew near. In fact, I never witnessed t he uptake of any H. guttatus fry. The balkiness of these three dozen strangers slowly affected the Gg. balzanii fry s response. The swarming tapered down to a slow equivocal mouthward procession, and even the female seemed somehow reluctant to pick up her own fry. Although she did harbor some of the fry, it was always a minority of the total shoal, which were now fairly unimpressed by my threatening knocks, owing to the H. guttatus fry s apparent bravado. The next morning, all 36 H. guttatus fry had vanished. However, the amount of Gg. balzanii contemporaries was undiminished, and they now responded to my threatening knocks with renewed vigor and typical swarming behavior. Buntbarsche Bulletin 101/ 3

2 Had the Gg. balzanii fry or the brooding female dispatched them? One dozen more H. guttatus fry were added to the shoal of Gg. balzanii and the same sequence of H. guttatus balkiness and eventual Gg. balzanii reluctance was observed. Next morning the second batch of H. guttatus fry were gone. I removed the female Gg. balzanii and added the remainder of the H. guttatus fry to the shoal of Gg. balzanii. After two weeks I still hadn t lost one H. guttatus fry: Apparently their selective disappearance in the presence of the brooding female Gg. balzanii female was due neither to fry-fry belligerence nor to some H. guttatus-specific disease condition, but rather selective infanticide on the part of the female Gg. balzanii. Conclusions from these simple experiments are several. Although the highly social interaction we call schooling seems to meld fry of such disparate genetic backgrounds as African Hemichromis guttatus and Neotropical Gymnogeophagus balzanii into a more or less cohesive unit, schooling is not sufficient to induce buccal escape behavior in a species for which such escape behavior is not a normal part of the behavioral repertoire. There does seem to be some social factor which works strongly in the opposite direction, as witnessed by the negative influence of the balking H. guttatus fry on the swarming school made up overwhelmingly of Gg. balzanii. Moreover, and not unexpectedly, the female Gg. balzanii recognized H. guttatus fry as foreign, will not accept them and eventually practiced selective infanticide as a solution to her dilemma. The most obvious recognition factor would seem to be a marked difference in fry coloration, but as subsequent experiments to be detailed below seem to suggest, it is fry behavior and not coloration which is the important parameter in determining whether foreign fry are accepted or eaten. Interspecific Fry Swapping These highly interesting results with mixed H. guttatus-gg. balzanii schools prompted a number of interspecific fry swaps between species of various geophagine cichlids, as luck, timing and the amazing fecundity of Gg. balzanii permitted. Brooding Gg. balzanii females will readily accept Geophagus steindachneri (Red Hump) fry of similar age, as does the brooding G. steindachneri female with Gg. balzanii fry. Although the two fry are visually distinguishable (by me, though not so dramatically different as are Gg. balzanii and H. guttatus), both species practice buccal sheltering as a normal part of their brood care and the same moving black spot releases the behavior in both (see Leibel, 1983a). Brooding Gg. balzanii females will also successfully adopt and rear Geophagus brasiliensis fry despite differing appearance and behavior. Geophagus brasiliensis is a typical non-mouthbrooding substrate spawner which cares for its fry in typical cichlid fashion, although occasional reports of mouthbrooding or buccal sheltering by this species are found in the literature (Reid and Atz, 1958, Breder and Rosen, 1966). Brooding females adopt Apistogramma-like brood dress including vertical eye bar, black-edged pelvics, and mid-lateral blotch. When threatened, alternate flicking of the female s pelvic fins signal G. brasiliensis fry to hit the dirt (drop to the bottom and cease movement). When offered to Gg. balzanii females and similarly threatened, these motionless fry would be gingerly scooped up by their foster mother and buccally sheltered as she would her own fry. Even in mixed Gg. balzanii-g. brasiliensis shoals, once the Gg. balzanii female 4 / Buntbarsche Bulletin 101

3 had accommodated her own swarming fry, she would eagerly and carefully scoop up the remaining clustered, inactive G. brasiliensis fry from the substrate. Similar behavior has been described for Geophagus steindachneri females mixed G. steindachneri-herotilapia multispinosa fry combinations (Eckstein, 1983); the latter, however, apparently learning and adopting the swarming behavior of their G. steindachneri cohorts. The Geophagus brasiliensis was not (H. guttatus) fry. When frightened, the jewel fish did not hit the dirt, but neither did they swarm to the female s lips. She quite patiently collected the fry, one by one, and spat them slateward in a futile attempt to collect and protect them. They, of course, refused to remain stationary, but the G. brasiliensis female seemed never to anger, or to tire of her endless task. She took perfect care of these visually-recognizable strangers and raised them along with or instead of her own fry. Gymnogeophagus balzanii male. It appears from experimentation that brooding female Geophagine cichlids rely primarily on behavioral cues in the recognition and acceptance of fry. photo by Wayne S. Leibel quite so tolerant. She accepted her Gg. balzanii shoal until they were threatened. These scared Gg. balzanii fry behaved as expected: Swarmed and beat themselves senseless on the suprised G. brasiliensis female s pursed lips... But not for long. This puzzled and perhaps even angered the G. brasiliensis female, (please pardon my unabashed anthropomorphism), which quickly dispatched the entire brood... ironically by swallowing them! This same G. brasiliensis female, surprisingly enough, quite placidly adopted a shoal of jewel fish Intraspecific Fry Swapping It would seem, based on the above observations, that the ability of Gg. balzanii females to discriminate their own young is something less than keen. When my dominant male Gg. balzanii male spawned in turn with each of two females within one hour of each other, I saw and grabbed my chance to experiment with intraspecific fry swaps. Both females reared their broods without incident and released their fry eight days post-spawn. I tried the old switcheroo: With crafty flick of the net I Buntbarsche Bulletin 101/ 5

4 separated each female from their respective free-swimming broods and switched the fry. Each of the two females immediately accepted their foreign fry, which repeatedly and predictably swarmed when startled. I placed both females in a 20 gallon (75 liter) long aquarium. They were separated from each other by a plastic egg crate divider that allowed the fry to swim freely between the two resident females. Each accepted their continually-changing, extended family and guarded them all the more vigorously with another female in clear view. For the finale, I offered each of the two synchronously-brooding females (now ten days post-spawn) some 25 day old fry from a previous spawning, which still swarmed in response to the moving black dot (see Leibel 1983a), now five days following removal from their own, third female. Would these females accept conspicuously older (larger) foreign fry? Apparently not These older fry were chased and dispatched before I could net them out. Summary and Conclusions A number of hypotheses have been advanced to explain how cichlids might recognize their own brood. Myrberg (1975) reviewing literature on cichlid fry recognition, cites evidence for chemically-based discrimination, particularly the jewelfish, but himself reveals data in the paragraphs that follow arguing for the visual basis (color pattern) of fry discrimination; a theory that had been proposed somewhat earlier (Noble and Curtis, 1939). The fry-swapping experiments reported herein would seem to contradict both points of view and strongly argue a third: Brooding female Geophagine cichlids rely primarily on behavioral cues in the recognition and acceptance of fry. In general, mouthbrooding geophagine species (Gg. balzanii, G. steindachneri) will readily adopt and rear fry of other mouthbrooding species or of substrate-spawning cichlids whose fry recognize generalized danger signaling behaviors (fin flicking, etc.) and respond by dropping motionless to the substrate. Fry which fail to react in either of these ways (e.g., the continuously-active Hemichromis guttatus) will be rejected. In contrast, brooding substrate-spawning Geophagine species (e.g., G. brasiliensis) are unable to behaviorally accommodate fry of mouthbrooding species which respond to generalized danger signaling by attempted buccal escape behavior. However, these species seem quite content to accept and successfully rear less passive fry (e.g., Hemichromis guttatus). Within these two categories, however, mouthbrooding species seem quite lacking in discriminatory abilities. Gymnogeophagus balzanii will accept G. steindachneri in both female-fry pairings. Gymnogeophagus balzanii will rear substrate-spawning G. brasiliensis fry and likewise, G. steindachneri will accept Herotilapia multispinosa fry (Eckstein, 1983). With this wide range of visual tolerance, it is not at all surprising that intraspecific fry adoptions between shoals of similar age proceed with no hitch in Gg. balzanii. Such relaxed discriminatory standards are not without precedent in the neotropical cichlid world. Brooding Apistogramma females are particularly notable in this regard, adopting and defending tubifex worms, swarms of daphnia, or even air bubbles in lieu of fry (Myrberg, 1975; Burchard, 1965). I have never witnessed such pathetic behavior on the part of Gg. balzanii females, so apparently they have more neurons than Apistogramma (I knew something had to be lost in miniaturization!). When older, larger and distinc 6 / Buntbarsche Bulletin 101

5 tively-marked Hemichromis fasciatus are substituted for normal broods, female Apistogramma trifasciatum will accept and rear these strangers (Burchard, 1965). Often, mixed shoals are formed naturally when occasional brooding (polygnist) males usurp and rear fry of various developmental stages from their brooding harem (Burchard 1965). It would be interesting to offer brooding Apistogramma females young of any of the mouthbrooding Geophagines to see the kidnapping of Cichlasoma spinossisimum fry by a C. septemfasciatum female whose spawn had been removed. Finally, and most interestingly, McKaye and McKaye (1977) reported kidnapping and communal care practiced by several species of Cichlasoma in Lake Jiloa, Nicaragua. Using SCUBA, these observers recorded mixed-species broods being successfully tended in the natural environment including mixed C. citrinellum - Neetroplus nematopus shoals Parental Cichlasoma citrinellum have been recorded tending mixed broods, which often include fry of the cichlid pictured above, Neetroplus nematopus, here a frytending female. photo by Paul V. Loiselle. how (behaviorally) accommodating they really are. Species of several other genera have been reported to adopt and raise fry of unrelated species. Foth (1939) in a series of intergeneric swapping experiments reported the following successful instances of foster-parenting: Acaronia nassa fry - Cichlasoma facetum parents; Acaronia nassa fry - Tilapia zilli parents; Tilapia zilli fry - Geophagus brasiliensis parents; mixed Aequidens caerulopunctata and Hemichromis fasciatus fry - Hemichromis fasciatus parents. Eckstein (1982) humorously described tended by parental C. citrinellum, mixed C. longimanus - C. citrinellum shoals tended by parental C. longimanus and mixed C. longimanus - C. nicaraguense shoals tended by parental C. nicaraguense. In direct manipulation experiments, McKaye and McKaye (1977) attempted to introduce foreign fry (both intra- and inter-specifically) by netting partial broods and releasing these orphans in proximity to the intended adoptive brooding parents. They successfully introduced orphan Neetroplus nematopus fry into Cichlasoma citrinellum broods Buntbarsche Bulletin 101/ 7

6 and vice-versa. As previous intraspecific manipulation with C. citrinellum has shown (Noakes and Barlow, 1973), the important factor for successful adoption in these experiments is the age of the orphan fry. As long as these were the same age or younger than the parents own brood, introductions were usually successful. Most interesting, McKaye and McKaye (1977) describe communal tending of young by multiple pairs of Cichlasoma citrinellum. By their own account:... Three pairs of C. citrinellum communally protected from predators a large school of four to five week old fry. When danger threatened, the young would split into three groups and follow the pair back into their respective caves. When the danger passed they emerged and mixed freely in the school. Individual fry were observed switching parents. (page 675). Moreover, routine interspecific kidnapping and adoption in this same species was observed. This is not surprising given the apparent inability of C. citrinellum fry to chemically recognize their own mother (Barnett, 1982). It is doubtful they possess the visual acuity to do so, as well. Similar communal care has been reported in the Green Chromide (Etroplus suratensis) in their natural habitat (Ward and Wyman, 1975) and inter- and intraspecific kidnapping and adoption between Tilapia melanopleura and Tilapia mariae (Burchard, 1967). However, in all of the cases documented above, the fry being exchanged are from substratespawning species, and not amongst mouthbrooding species or between mouthbrooding and substrate-spawning species. Ribbink (1977) has reported defense of mixed species broods by several mouthbrooding cichlids from Lake Malawi (Haplochromis polystigma, H. macrostoma and Serranchromis robustus). When threatened, each of the parental species buccally accommodated the mixed fry. One obviously mixed shoal of fry being tended by S. robustus was caught and subsequently reared to identifiable size in aquaria. These turned out to be both S. robustus and Haplochromis chyrsonotus. Apparently a similar laxness of fry recognition exists in mouthbrooding species from Africa. Greenberg (1963; based on similar intra- and inter-specific fry switches between Aequidens portalegrensis and Hemichromis guttatus) concluded that acceptance of foster broods depends on: 1) the stage of the parent s brooding cycle (i.e., how soon after spawning fry are manipulated, 2) the correspondence in developmental stage of the experimentally-provided foster young with the adoptive parent s own brood, and 3) the behavior of the young. While the last criterion remains virtually unaddressed (or explained) in the body of the paper, Greenberg reports that on average brooding pairs of both species tend to reject and eat more advanced foster fry and to accept and rear foster fry of the same age or younger age than their own biological young. These younger fry apparently easily fit into the proper phase of the parental care cycle and are thus easily accepted. Noakes and Barlow (1973) and McKaye and McKaye (1977) found similar age dependency for successful fry adoption as outlined above. While I have not yet extensively attempted fry switches of varying synchronicity in Gg. balzanii, one experiment, that of involving 25 day old Gg. balzanii fry slipped to each of two 10 day post-spawn females, would support Greenberg s view. Both females rejected (and ate) these older fry even though they still responded appropriately to danger signaling behaviors. 8 / Buntbarsche Bulletin 101

7 There are several additional experiments that would further amplify the simplistic and dogmatic statement that fry recognition and adoption is based on behavioral parameters in Neotropical, Geophagine cichlids. As of yet, I have not been fortunate enough to enjoy synchronous spawnings of Gg. balzanii and the Egyptian Mouthbrooder, Pseudocrenilabrus multicolor, and to pull the obvious and desired intercontinental switcheroo between the two very unrelated species with convergent, reproductive strategies (i.e., mouthbrooding). However, based on the above observations, I would predict that foster parenting would proceed without incident. It would be of considerable value to repeat the substrate spawner (fry) to Gg. balzanii (female) swap with species whose fry offer a more distinctive and different color pattern than G. brasiliensis does, e.g., Cichlasoma atromaculatum which has a wide, black, vertical band down the center of an otherwise light-colored body. Would behavior (brasiliensis-like, therefore acceptable ) or coloration (easily discriminated) prove the determinant in the success or failure of the attempted fry adoption? Even better replacement of the Gg. balzanii brood with a shoal of conspicuously different mouthbrooding fry (suggestions any of you African aficionados?). And, is this hierarchy of cues generalizable to other mouthbrooding species of the genus Geophagus? There is clearly much fun to be had in experimenting with, as well as simply propagating members of the family Cichlidae. As Dr. James Atz pointed out at Convention 82, the hobbyist has much to contribute to science in the way of behavioral observations (see Reid and Atz, 1958, for example). I am, myself, an avocational ethologist whose lab is the fishroom and whose observations are made in my own spare time. And while my experiments are neither rigorous nor statistically significant, I would like to think that they do/will contribute to our general understanding of fish behavior and to the aquarium hobby. Here is hoping some of you will accept the challenge of observing your aquarium inhabitants and sharing your observations in these pages. Acknowledgment. Special thanks to Drs. James Atz and Paul Loiselle for suggesting relevant bibliographic material. Portions of this article appeared previously in The Sifter 1(4):6. REFERENCES: Barnett, C The Chemosensory Response of Young Cichlid Fish to Parents and Predators. Animal Behavior 30: Breder, Jr., C.M. and D.E. Rosen Modes of Reproduction in Fishes. TFH Publications, Inc., Neptune City, NJ. Burchard, Jr., J.E Family Structure in the Dwarf Cichlid Apistogramma trifasciatum Eigenmann and Kennedy. Zeit. fur Tierpscyhol. 22: Burchard, Jr., J.E The Family Cichlidae, in: W. Reed, Fish and Fisheries of Northern Nigeria. Min. Agricul. Northern Nigeria, pp (cited in McKaye and McKaye 1977). Eckstein, G Sez You. Cichlasoma Power 2(3). Eckstein, G Interspecific Fry Adoption in Geophagine Cichlids: Geophagus steindachneri. The Sifter 1(4): 5. Foth, L Intelligenzprufungen bei Cichliden. Wochenschr. Aquar.- Terrarienk. 36(47): (cited and summarized by Breder and Rosen 1966). Greenberg, B Parental Behavior and Imprinting in Cichlid Fishes. Behavior 21: Buntbarsche Bulletin 101/ 9

8 Leibel, W.S. 1983a. Fry Escape and Buccal Sheltering Behaviors in Geophagine Mouthbrooders. Buntbarsche Bulletin 99: 2-7. Leibel, W.S. 1983b. Gymnogeophagus balzanii (Perugia 1891). Buntbarsche Bulletin 97: McKaye, K.R. and G.W. Barlow Chemical Recognition of Young by the Midas Cichlid Cichlasoma citrinellum. Copeia (2) McKaye, K.R. and N.M. McKaye Communal Care and Kidnapping of Young by Parental Cichlids. Evolution 31: Myrberg, Jr., A.A The Role of Chemical and Visual Stimuli in the Preferential Discrimination of Young by the Cichlid Fish Cichlasoma nigrofasciatum (Gunther). Zeit. fur Tierpsychol. 37: Noakes, D. and G.W. Barlow Cross-fostering and Parent-Offspring Response in Cichlasoma citrinellum (Pisces, Cichlidae). Zeit. fur Tierpsychol. 33: Noble, G.K. and B. Curtis The social behavior of the jewelfish. Hemichromis bimaculatus Gill. Amer. Mus. Nat. Hist. Bull. 76: Reid, W. and J. Atz Oral Incubation in the Cichlid Fish Geophagus jurupari Heckel. Zoologica 43: Ribbink, A.J Cuckoo Among Lake Malawi Fish. Nature 267: 243. Ward, J.A. and R.A. Wyman The cichlids of the resplendent isle. Oceans. 8: / Buntbarsche Bulletin 101