Anim. Behav., 1995, 49, 623-631
Fin digging and leaf lifting by the convict cichlid, Cichlusoma nigrofasciatum: examples of parental food provisioning
BRIAN D. WISENDEN*, TANYA L. LANFRANCONI-IZAWA & MILES H.’ A. KEENLEYSIDE Department of Zoology, University of Western Ontario, London, Ontario, N6A 5B7 Canada
(Received 25 October 1993; initial acceptance 3 December 1993; final acceptance 4 February 1994: MS. number: ~6848~)
AI&act. In fish, the predominant form of parental care is brood defence. The convict cichlid, a biparental fish native to Central America, also engages in two types of brood provisioning: tin digging and leaf lifting. These behaviour patterns were studied in the field, and in outdoor experimental ponds and laboratory aquaria. In the ponds, females fin dug 51 times more often when guarding fry than when unmated; males fin dug three times more frequently when guarding fry than when unmated. After the young became free-swimming, females performed four times (field) and two times (pond and laboratory) more fin digging and twice as many leaf lifts (field) as males. Females in the field increased leaf lifting with brood age but males did not. Fin digging frequency by parental females and males increased with brood age. Frequency of adult feeding bites at the substrate did not change with brood age except in the field, where female feeding bites increased with brood age. In the field, females performed more feeding bites than males but in the laboratory males fed more often than females. Thus changes in fin digging frequency with brood age do not seem to be strongly linked to the feeding requirements of the parents. In the laboratory, fin digging frequency was influenced by substrate quality (P=O.OS)but not by ration (P>O.lO). Taken together, these data support the hypothesis that parental fin digging and leaf lifting help increase food availability to their young.
Typical components of parental care in mammals protein-rich mucus along the sides of their bodies and altricial birds are protection of the offspring upon which their young feed (Hildemann 1959). from predators and the elements, and the pro- In several other species, the young nip at the sides visioning of food to the young. Both patterns of of their parents and ingest mucus (Ward L Barlow behaviour increase offspring survival (Trivers 1967; Noakes & Barlow 1973; Robertson 1973; 1972; Clutton-Brock 1991) and ultimately increase Ward & Wyman 1977). Females of two cichlid the fitness of the parents (Hamilton 1964). Paren- species (Tropheus sp.) in Lake Tanganyika, tal care in fish is uncommon, occurring in about Africa, browse while orally brooding their young 20% of fish families (Bhrmer 1982), and differs (Yanagisawa & Sato 1990). Bagrid catfish, Bagrus in form from that of other vertebrate groups meridionalis, in Lake Malawi, provide food for (McKaye 1981). The most common form of their young directly (McKaye 1986). Unfertilized parental care in fish is for the male parent to eggs produced by the female and benthic inverte- aerate and defend one or more clutches of eggs in brates foraged by the male are fed to the young. a nest until the eggs hatch and the young disperse Cichhds are unusual among fish because paren- (Blamer 1982). There is generally no provisioning tal care continues for several weeks after their of food to the young, even in speciesthat defend young have begun free-swimming (Keenleyside their free-swimming young for some time after 1991). Convict cichlids are small freshwater hatching (Perrone & Zaret 1979). However, there fish native to Central America, ranging from are. a few exceptions. Parental discus cichlids Guatemala to Panama (Miller 1966; Bussing (Symphysodon spp.) produce copious amounts of 1987). These fish are substrate brooders, which lay their eggs inside small caves they excavate under “Present address: Department of Biology, University of stones. Convict cichlids have cooperative, bi- Saskatchewan, Sdskatoon, Saskatchewan. S7N OWO parental care of their eggs, wrigglers (non- Canada. swimming hatchlings) and fry (free-swimming
m3-3472/95/030623 +09 $08.00/O P, 1995 The Association for the Study of Animal Behaviour 623 624 Animal Behaviour, 49, 3 young) for about 6 weeks. During the fry stage of also recorded adult feeding rates in the field and brood development (3-4 weeks) both parents adult feeding rates in the laboratory. Second, we actively defend their fry against potential brood measured the influence of substrate quality (clean predators. In addition, they occasionally perform versus silty) and adult food ration (two levels) 04 two activities that have been called fin digging fin digging in a laboratory experiment. Fin dig. (Williams 1972) and leaf lifting (Keenleyside et al. ging should be of greatest potential benefit when 1990). the substrate is silty because small organisms During fin digging, a parent fish settles onto the hidden in the silt may be exposed to foraging fish, substrate and stirs up loose material by a short Therefore fin digging activity should increase on bout of vigorous rapid beating of its pectoral fins. silty substrate and decrease on clean substrate. During leaf lifting, a parent grasps the edge of a Parents may use their own nutrient status to sunken leaf and, with a series of backward judge ambient food availability for their young. tugs and forward pushes, raises the leaf off the When food for the parents is limited, parents may substrate and then releases it. As the leaf sinks perceive food to be limited for their fry and it often turns over, exposing the underside. Paren- increase the frequency of fin digging behaviour to tal fin digging has been observed in Costa provide more food for their young. Therefore, Rican streams, performed by convict cichlids rates of fin digging should be higher for parents on (Keenleyside et al. 1990) and Cichlasoma alfari a low food ration than for those on a high food (B. D. Wisenden, personal observation). It has ration. also been reported for a few other biparental cichlids in the aquarium literature (Loiselle 1985; Azas 1992). Leaf lifting has been reported METHODS from the field for convict cichlids (Meral 1973; Keenleyside et al. 1990) and for C. panamense Field Study (Townshend & Wootton 1985a). Parental care behaviour was monitored during When parental fish perform fin digging or leaf two breeding seasons, January-June 1990 and lifting, their fry immediately converge to feed on December 1990-June 1991. Data were collected suspended or newly exposed food items. Thus, from two study sites in the rio Cabuyo, and two these two activities appear to assist the young in sites in the quebrada Amores at Lomas Barbudal feeding (Keenleyside 1991). Parental food pro- Biological Reserve in Guanacaste province, visioning may increase survival of their offspring northwest Costa Rica, 10”30’N, 8Y23’W. by increasing fry growth and thus decreasing the Quebrada Amores is a small headwater stream time during which fry are vulnerable to brood and a tributary of the rio Cabuyo. predators (Perrone 1978). We monitored pairs of convict cichlids breeding Non-breeding convict cichlids occasionally fin at each site regularly at intervals of 3-10 days dig and leaf lift while foraging for themselves. (usually 7) throughout brood development from However, both acts appear to be performed more oviposition to fiy independence. We identified often by breeding pairs, especially when their individual broods and identified attending parents young are free-swimming fry (Williams 1972). on subsequent sampling dates using sketches of Because both adults and fry feed primarily on parental body markings, stage of brood develop algae and microfauna in the benthos (B. D. ment and location in the stream. After a 5-min Wisenden, personal observation), fm digging, acclimation period, we recorded the frequency of especially on silty substrates, and leaf lifting, parental behaviour patterns performed by each should make more food available for the fry. parent, including fin digging and leaf lifting, for The aim of this research was to explore the 10 min. Observations were made from shore or possibility that fm digging and leaf lifting by while wading nearby, with the aid of polarized parental convict cichlids are ,acts of food pro- sunglassesto reduce surface reflection. Altogether, visioning for their free-swimming young. We did we made 840 lo-min recordings on 195 brooding this in two ways. First, we recorded the frequency pairs; 115 in 1990, 80 in 1991; 102 in quebrada of both behaviour patterns, by breeding adults in Amores, 93 in rio Cabuyo. Immediately after the their natural habitat, and of fin digging in outdoor behavioural recordings, we captured each brood experimental ponds and in the laboratory. We using hand nets, a face mask and snorkel. We Wisenden et al.: Parental.food provisioning by cichlids 625 arbitrarily anaesthetized 15 fry with MS222 flower-pots using a face mask and snorkel. We (tricaine methanesulphonate) and measured their recorded lo-min observations of each parent of 14 standard length (SL) to the nearest 0.5 mm. We pairs consecutively for each of the following allowed the fry to recover from the anaesthetic stages of brood development: (1) 1 day after the and returned them to their parents using a clear fish spawned (egg stage); (2) 1 day after the eggs plastic tube (Wisenden & Keenleyside 1992). hatched (wriggler stage); (3) 3 days free-swimming Because the exact date of spawning was often not (fry stage); (4) 10 days as fry; and (5) 17 days as known, we used fry size to classify brood devel- fry. The fifth stage corresponded with the opment into five stages: (1) cave; when the brood 8-1Omm SL fry stage of the field study. We was still concealed inside the spawning cave as recorded the number of fin digs performed with either eggs or wrigglers; (2) fry lessthan 6 mm SL, the brood (within two body lengths) and away (3) fry 6-8 mm SL; (4) fry 8-10 mm SL; and (5) from the brood during each lo-min observation fry greater than 10 mm SL. Fry first emerged period. We also recorded the frequency of tin from their cave at 4-4.5 mm SL and began dis- digging behaviour by randomly selected unmated persing soon after reaching 10 mm SL (personal males (N=13) and females (N=13) for compari- observation). son with fin digging by parental fish. Because of the limited number of adults in the experimental ponds, the behaviour of some fish was recorded pond Observations while parental and non-parental, some fish were We used four outdoor ponds measuring recorded only while parental, others only while 7 x 10 m at the University of Western Ontario non-parental. In the analyses, these data were (43”01’N, 81”17’W). The ponds had sloping treated as independent points. Leaf lifting did not bottoms; water entered at the shallow end (depth occur in the ponds because very few leaves fell 65 cm) and drained by a vertical standpipe at the into them during the experimental period. deep end (depth 100 cm). Pond substrate was 1Ocm of fine sand over 5 cm of coarse gravel. Laboratory Experiment Scattered clumps of algae (Chara sp.) grew in all ponds and a layer of organic debris, detritus and Pairs of convict cichlids from the laboratory algae accumulated on the substrate during the stock were placed into 96-litre aquaria (80 x experimental period. Clay flower-pots (20 cm top 40 x 30 cm high) with 3 cm of naturally coloured diameter) were cut in half and placed concave side gravel, a clay flower-pot cut in half placed at one down on the substrate to serve as spawning sites. end, and a plastic plant in the centre. Water Eight halt-pots were placed in each pond in a temperature was maintained between 27 and 29°C regular pattern, separated by 1.5 m. by aquarium heaters and the photoperiod was a All experimental fish were obtained from the 14:lO h 1ight:dark cycle. Each pair was in visual University of Western Ontario laboratory stock, contact with one neighbouring pair. composed of fish purchased from local aquarium Two factors were tested for their effect on fin dealers back-crossed with fish captured in Costa digging: substrate quality and food availability. Rican streams in 1984 and 1990. Past breeding We used two levels of substrate quality (enriched; experience of the fish was unknown. Each fish was clean) and two levels of ration (high, low) to form anaesthetized with MS222, weighed, measured a 2 x 2 factorial design. Trials with ‘clean’ sub- and tagged with a unique combination of strate started with freshly cleaned gravel. Trials coloured beads attached to the dorsal musculature with ‘enriched’ substrate had 250 ml (506.6 f with stainless steel wire. We observed six males 21.2 g) of detritus and sand added to a tank with and six females in each pond from 28 June to 6 clean gravel, forming a 0.25~cm layer of fine September 1990. Fish fed on accumulated detritus material on top of the gravel. Sand and detritus and algae on the substrate; additional food was were collected from the experimental ponds. We not provided. fed each pair of adults in the low-ration treatment Each day between 0900 and 1500 hours we 1 g of commercial cichlid pellets (Tropic Aquaria, recorded the mating status of all adults and the Brampton, Ontario) three times per week and location and developmental stage of each brood those in the high-ration treatment daily. Fry were being guarded. We visually checked broods inside fed 0.1 g of FryFeedKyowa B-250 (BioKyoma, 626 Animal Behaviour, 49, 3
12t n Females 1.3 -0 Males
4 1.2 - s -g 0.9 - 3 .S 0.6 - Er 0.3 -
Fry SL (mm) Fry SL (mm)
Figure 1. Mean (+sE) fin digging frequency per 10 min Figure 2. Mean (+SE) leaf lifting frequency per 10 min by parental female and male convict cichlids in Costa by parental female and male convict cichlids in Costa Rica at each of five stages of brood development. Data Rica (both watersheds) at each of five stages of brood from both watersheds combined. development.
Chesterfield, Missouri) three times per week in all 50 treatments. We recorded the frequencies of fin WFemales 0 Males digging (within two body lengths and away from 40 T the brood), and of feeding bites at the substrate .g for each parent during consecutive lo-min obser- 2 30 7 vations. Seven pairs were used for each treatment B combination, for 28 pairs. 2 20 i? 3 RESULTS 8 10 E Field Study 0 ~ Cave <6 6-8 8-10 r10 Fin digging was performed significantly more rlFry SL (mm) often by female convict cichlids than by males Figure 3. Mean (+SE) frequency of feeding bites at the (repeated-measures ANOVA, P I.5 2o 1 n Females 1 Females T T Brood stage Brood stage Figure 5. Mean ( + SE) fin digging frequency per 10 min in Figure 4. Mean (+SE) fin digging frequency per 10 min in aquaria by parental female and male convict cichlids at outdoor ponds by parental female and male convict five stages of brood development. cichlids at five stages of brood development, and by unmated, non-parental females (Yd) and males (H). Fin digging near and away from the brood is combined. performed near and away from the brood were combined for the analyses. Sex of the parent and brood stage had the same effects on fin digging away from the brood (parental females: tz5.31, frequency in the laboratory setting as in the P ’ n Enriched substrate n High ration r r T 1 0 Clean substrate 0 Low ration .9 6- -r+ T y. i Enriched Brood stage Substrate type Figure 6. Effect of substrate quality on frequency of fin Figure 8. Overall effects on fin digging (x+SE) per digging (X+SE) per 10 min by parental convict cichlids 10 min, of the substrate and ration treatments used in (sexes combined) in aquaria at five stages of brood the laboratory experiment. Sexes and brood stages are development. combined. 1 8 High ration I HFemales q Males T 0 Low ration .S 6 E 1 s T Brood stage Brood stage Figure 7. Effect of food ration on frequency of fin Figure 9. Frequency of feeding bites (F+SE) per 10 mia digging (X+SE) per 10 min by parental convict cichlids by parental female and male convict cichlids in aquaria (sexes combined) in aquaria at five stages of brood at five stages of brood development. development. during 280 observation periods or 1261 feeding not follow the same pattern (Fig. 9). In the events). laboratory, the feeding frequency of females was lower than that of males (repeated-measures DISCUSSION ANOVA, P=O.O23) and neither sex changed feeding frequency with brood stage (repeated- Fin digging data from the field, experimental measures ANOVA, PzO.906). ponds and laboratory, and leaf lifting data from Within each sex, rates of feeding bites were the field, indicate that parental convict cichlids use uniformly high except for the combination of these two behaviour patterns to assist their young clean substrate and high ration, when feeding in feeding. The strongest evidence that these are activity was significantly reduced in both methods of food provisioning is that in all parts of sexes (Fig. 10). Consequently there was a sig- the study, fin digging by both parents seldom nificant interaction between substrate and occurred when their young were at the egg and ration (repeated-measures ANOVA, P=O.O46). wriggler stages, and were thus incapable of exe Fin digging events were not closely associated genous feeding, but increased in frequency with with adult feeding activity (fewer than 30 increasing age of their free-swimming young. feeding bites occurred within 1 s of a fin dig Also, in the ponds, unmated, non-parental adults, Wisenden et al.: Parental food provisioning by cichlids 629 egg or wriggler stage. This suggests that leaf lifting n High ration 0 Low ration is an important foraging technique for adult con- vict cichlids and is not solely a form of food provisioning for their young. In general, parental investment should increase with offspring age because the probability of offspring survival and thus the potential value of the offspring to parental fitness increase with offspring age (Clutton-Brock 1991). Parental investment often declines towards the end of the period of parental care as the young become ClMll Enriched Chn Enrich< sd self-sufficient and their survival is less dependent Females Males on parental care. This pattern of increasing then Figure 10. Frequency of feeding bites (X+SE) per 10I min decreasing levels of parental investment with by parental female and male convict cichlids in aquaria increasing offspring age has been modelled during trials differing in substrate and ration treatments. (Sargent & Gross 1993) and supported by empiri- cal studies of brood defence in fish, birds and and parents away from their brood, seldom per- some mammals (reviewed in Montgomerie & formed tin digging. In addition, the frequency of Weatherhead 1988; Clutton-Brock 199 1; Sargent leaf lifting by parental females in the field & Gross 1993). increased with offspring age. This corresponds Parents may have increased fin digging fre- with the data on leaf lifting by parental convict quency with brood age because the food re- cichlids in Costa Rican streams by Keenleyside quirements of the fry increase as they grow. et al. (1990). Unfortunately we were not able to collect data on In the field, ponds and laboratory, after the fry foraging rates to confirm this. Williams (1972) young became free-swimming, females performed and Krischik & Weber (1974) found an increase in more fin digging, and in the field more leaf lifting fin digging frequency by male and female parental than males. This finding concurs with other convict cichlids as their fry developed, followed by reports of parental fin digging (Krischik & Weber a gradual decline over the next 10 days. Glancing 1974; Lavery & Keenleyside 1990) and leaf lifting behaviour and associated micronipping at the by convict cichlids (Keenleyside et al. 1990). parents’ body, by fry of the Asian cichlid, Etroplus Parental care duties among biparental cichlids maculatus, increased significantly between the ages are usually not divided equally between the sexes of 9 and 19 days free-swimming (Ward & Barlow (see Keenleyside 1991 for a review). Females are 1967). more directly involved in the care of the eggs and The decline in female fin digging at late fry wrigglers than are males, and generally spend stages in the field may be related to the increasing more time closely associated with the young abilities of young convict cichlids to forage inde- throughout the brood-rearing period than do pendently on the substrate as they grow and males. Males patrol the breeding territory and develop, even though they are still being guarded then join the female in active brood defence when by their parents (Williams 1972). However, the the young become free-swimming. The sex differ- decline in hn digging is also associated with ences in fin digging and leaf lifting in this study increased feeding rates of females. This raises an were consistent with this pattern. Females rarely alternate hypothesis, that the increase in fin left the spawning cave when the brood was at the digging frequency with brood age by parental egg and wriggler stages (especially in the field females is partially attributable to a general where brood predators were abundant), and con- increase in female feeding activity, perhaps in sequently fin digging and leaf lifting by females response to gonad exhaustion from spawning or occurred infrequently at the cave stage. During somatic exhaustion from the metabolic demands these early brood stages, males were not con- of brood defence. This hypothesis is countered by strained by egg and wriggler care and used leaf data from the pond study where fin digging fre- lifting to forage for themselves. However, parental quency by females and males did not change with males did not fin dig when their broods were at the brood stage while they were away from the brood, 630 Animal Behaviour, 49, 3 presumably when they were feeding only for ACKNOWLEDGMENTS themselves, and there was also a low level of direct temporal association between feeding bites and fm Statistical advice was provided by Roger H. digging. Furthermore, the frequencies of feeding Green whose sagacity and tenacity for repeated- bites by females and males in the laboratory measures ANOVA designs, balanced and other- (Fig. 9) and males in the field (Fig. 3) were not wise, made the analyses possible. In the field, influenced by brood age. In addition, an earlier assistance in data collection was provided by Bee study of convict cichlid parental behaviour in the Wisenden, Jeff Christie, Gillian de Gannes, Owen same ponds found that the feeding frequency of Steeleand Randy Jose Jimtnez. Logistical support male and female parents did not change with in the field was provided by Gordon and Jutta increasing age of the brood (Keenleyside et al. Frankie and Friends of Lomas Barbudal. 1990). The feeding frequency of non-parental con- Permission to work at the field sites was granted vict cichlids in the field is more than three times by El Servicio de Parques Nacionales de Costa higher than that of parental fish (Keenleyside Rica and the Stewart family. Rob Mackereth et al. 1990). assisted with data collection at the outdoor exper- In the laboratory, fin digging was somewhat imental ponds. Terence Laverty and Roger Green reduced on clean, silt-free substrates regardless of were advisors for Tanya Lanfranconi-Izawa’s ration level (Fig. 8), while the frequency of paren- undergraduate thesis (laboratory experiment). We tal feeding bites on clean substrate was reduced thank Shannon Fraser and three anonymous ref- for the trials with high ration (Fig. 10). Substrate erees for helpful comments on the manuscript. type had a weak effect on parental fin digging This research was financially supported by an (P=O.O84) and food ration had no effect. Adult operating grant to M.H.A.K. and summer hunger levels may have been satisfied by the high research grants to T.L.L.-I. from the Natural food ration and thus adults were less motivated to Sciences and Engineering Research Council of forage on sterile substrate. An alternate hypoth- Canada. esis,that the low food ration may have limited the amount of energy available to parents to invest in REFERENCES their offspring (Townshend & Wooton 1985b), was not supported by the results of the ration Azas, .I. M. A. 1992. The ‘Cichlasoma’ labridens- treatment. complex. In: The Cichlids Yearbook, Vol. 2 (Ed. Fin digging occurred most frequently in the by A. Konings), pp. 65-70. St Leon-Rot: Cichlid experimental ponds and least frequently in the Press. Blumer, L. S. 1982. A bibliography and categorization field. This was probably because the substrate of bony fishes exhibiting parental care. 2001. J. Linn. in the ponds contained more silt and detritus Sot., 76, l-22. than the field sites where convict cichlids reared Bussing, W. A. 1987. Peces de las Aquas Continentales de their broods. The relatively low fin digging fre- Costa Rica. San Jose: Editorial de la Universidad de Costa Rica. quency in the field may also reflect the greater Clutton-Brock, T. 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