zyxwvutsrq zyxwvut zyxwvutsrqp zyxwv zyxwv Ethology 104, 771L779 (1998) 1998 Blackwell Wissenschafts-Verlag, Berlin ISSN 0179-1613 c> zyxw Laboratory of Lower Vertebrates Behaviour, A . N . Severtsoo Institute of' Ecology and Evolution, Russian Academy of' Sciences, Moscow Parental Fin Digging by Cichlasorna octofasciaturn (Teleostei: Cichlidae) and the Effect of Parents' Satiation State on Brood Provisioning Dmitry D. Zworykin Zworykin, D. D. 1998: Parental fin digging by C'ichlusomu ocfqfusciutum (Teleostei: Cichlidae) and the effect of parents' satiation state on brood provisioning. Ethology 104, 771-779. Abstract Although parental care in fishes does not usually include provisioning offspring after hatching, various types of brood provisioning have been documented for some bony fishes, and in particular, for cichlids. For example, fin digging occurs among biparental substrate brooding cichlids of the 'genus' C'ichlusoma sensu lato. Parental fin digging by Cichlu.vomu octofirsciatum was investigated under laboratory conditions. Fin digging was performed significantly more often by females than by males. For both sexes, the frequency of fin digging increased significantly with brood age, especially from ages 3 to 10 d of fry: this was more pronounced in females. The parents' own current satiation state during performance of fin digging influenced the fin digging frequency: for both sexes it was higher in hungry than in satiated parents. zyxwvutsrqp Corresponding author: Dmitry D. Zworykin, Laboratory of Lower Vertebrates Bchaviour. A . N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninsky prospect 33, Moscow, 11 7071, Russia. E-mail: irene(u irene.msk.ru Current address: d.zworykin@gmail.com Introduction Parental food provisioning of young after birth or hatching is an important component of parental care in many viviparous as well as oviparous animals (Clutton-Brock 1991). This is beneficial because it increases the offspring survival and ultimately the fitness of the parents themselves (Hamilton 1964; Trivers 1972). Many types of provisioning young after birth or hatching have been documented in leeches (Kutschera 1992), insects (Wilson 1971) spiders (Kaston 1965), crabs (Diesel 1989), birds (Lack 1966), mammals (Ewer 1973) and in other animals. Various forms of this type of investment are known in fishes. In bony fishes, brood provisioning may occur with ectodermal mucus (e.g. Synzphysodori discus, Hildemann 1959; Acanthochrornispolyacantkus, Robertson 1973), trophic eggs (e.g. B q r u s rneridionulis, Lovullo et al. 1992), partly chewed food (e.g. C i c h l m m a longimianus, Konings 1989; Peloicachrornis pulclwr, D. D. Zworykin, pers. obs.), U. S Copyright Clearance Center Code Statement: 0 179-16 ~3/98/1049-0771$~4.00/0 772 zyxwvu zyx zyxwvu D. D. Zworykin by means of buccal feeding (e.g. Trupheus duboisi, Yanagisawa & Sato 1990; Cyphotilupiu frontosu, Yanagisawa & Ochi 1991), pasture of brood, that is movements of parents and the young to more profitable feeding areas (e.g. Cichlusoma muculicuuda, Perrone 1978; Boulengerochromis microlepis, Kuwamura 1986) and by leaf lifting and fin digging (e.g. Cichlusoma nigrofusciutunz, Keenleyside et al. 1990). Although various forms of parental food provisioning have been documented in substrate brooding cichlids of the ‘genus’ Cichlusoma sensu lato, it is fin digging that is most typical for these fishes. In addition to convict cichlids, Cichlusoma (Archocentrus) nigrofhsciutum, this type of brood provisioning has also been observed in C. (Amphilophus) uljari, C. (Archocentrus) nunoluteus, C. (Archocentrus) octofusciutum, C. (Purupeteniu) lubridens and in some other Cichlusoma species (Konings 1989; Artigas Azas 1992; Wisenden et al. 1995; A. Stalsberg, pers. comm.; D. D. Zworykin, pers. obs.). However, only Wisenden et al. (1 995) have analysed this behaviour in the convict cichlid in detail. Fin digging occurs when a fish settles its body onto the substrate and stirs up detritus and other loose material containing microbenthos by a short bout of rapid, vigorous beating of its pectoral fins and undulating movements of the body. In response, the fry immediately rush in and begin feeding (Williams 1972; Keenleyside 1991; Artigas Azas 1992; Wisenden et al. 1995). It is typically considered that parental cichlids use fin digging to promote their young in feeding (Keenleyside 1991; Wisenden et al. 1995), which means that they should be able to assess the current nutritive condition of the offspring. At the same time, this behavioural pattern is also associated with the foraging of both non-parental and parental adults, although it is performed more often by parents near the brood (Williams 1972; Wisenden et al. 1995). This is why Wisenden et al. (1995) suggested that parents may use their own nutritive status to judge the ambient food availability for their young. This idea, however, had a rather weak experimental support: the authors found that fin digging was influenced by the substrate quality (poor versus rich), with only marginal significance: and was not influenced by the level of adults’ ration. Even if fin digging is not influenced by the above factors, it may nevertheless be associated with the nutritive status of parents. One could suppose that it is the current satiation state of parents that is of principal importance in the digging frequency. This prediction seems to be quite likely for two reasons. First, provided that fin digging is a form of adult foraging (Williams 1972; Artigas Azas 1992; Wisenden et al. 1995), it should depend upon satiation. Second, feeding of both adults and young of many Central American Cichlusoma species is associated with the benthos and drift (Konings 1989; Wisenden et al. 1995; W. A. Bussing, pers. comm.). Therefore, substrate digging by adults should increase availability of food for both themselves and fry, in which case the satiation levels of parents and offspring would correlate. The aim of the present study was to investigate the dependence of fin digging on the sex of parent and brood stage in C. uctofusciutum and to test whether the current satiation state of breeding adults affects the fin digging frequency. zyxwvut zyxwvut zyxwv zyxwvut Fin Digging in Cichlusomu octqfusciutum 773 zyxwvuts zyxw Methods C. octofusciatum is a biparental substrate brooding cichlid fish occurring in Central America and southern states of the USA. Stock was descended from fishes obtained from a private aquarium breeder. Each pair was maintained in a 100-1 aquarium (70 x 35 x 41 cm) with half a clay flower-pot as a potential spawning substrate. Each aquarium contained a 3 4 cm layer of natural gravel and thin (up to 2 mm) layer of detritus over the gravel. The photoperiod was a 10: 14 h light : dark cycle. Water temperature was maintained at 25 5 1 “C. Both adults and fry were fed daily ad libitum. The diet of adults consisted of large (8-10 mm) live bloodworms (Chironomus sp. larvae) and that of young consisted of commercial fry flakes (TetraMin). The parental fin digging could, in addition, provide fry with particles of detritus, debris of the flake food and probably microbenthos. For ease of comparison of the data with those obtained by Wisenden et al. (1995) on the convict cichlid, brood development was classified into the same five stages: (1) egg stage; ( 2 ) wriggler stage; (3) 3 d as fry; (4) 10 d as fry; ( 5 ) 17 d as fry. The number of parental fin digs during the 15-min observation periods were recorded twice at each brood stage. The first recording session was carried out between 1 1 .OO and 14.00 h, before feeding of both adults and fry; immediately after that the adults were fed. The fry were not able to feed on the adults’ diet because the bloodworms were too large (8-10 mm). Shortly (10-15 min) after feeding of parents was terminated, the second recording session was conducted. Thus, these sessions were separated by an interval (not more than 30 min) that was short enough to avoid undesirable effects of diurnal changes of the fishes’ behaviour. After termination of the second recording session, the fry were fed. The two recording sessions differed in satiation of adults (parents were hungry during the first session and satiated during the second one) but not in satiation of fry. As such, any change of the frequency of parental fin digging between the two recording sessions should be accounted for by the satiety of parents but could not reflect changes in the fry satiety. Six pairs of C. octofusciatum mated repeatedly, resulting in 12 runs of the experiment (broods). Repeated measures ANOVA was used for the statistical analysis of the effects of sex and satiation of parents, and brood stage on the frequency of parental fin digging. To control the effect of possible differences between pairs, a randomized block design was applied. Because the pairs were tested difierent numbers of times (from one to three) and the experimental design was unbalanced (pairs and repetitions were initially incorporated into the repeated measures ANOVA), the regression approach was used (I interpreted the type III sum of squares, see Milliken & Johnson 1984). The assumptions of sphericity and compound symmetry were violated (Mauchly W test, p = O.O&O.Ol)and therefore the Greenhouse-Geisser adjustment was applied (Milliken & Johnson 1984; Crowder & Hand 1995). The original values were log-transformed to remove correlation between means and variances and improve the variance homogeneity. For untransformed data, the maximum value of F,, = 7.1 df = I , p < 0.003 and for log-transformed data F,,, = 2.9, df = 1, p = 0.091 (Hartley F test). 774 D. D. Zworykin Results zyxwvu zyxw zyx zyxw zy zyx Observations showed that hungry non-parental C. octqfi7sciatunz rarely performed solitary fin digs: during several hours of observation only it few instances of this behaviour were noted. Satiated non-parental adults never performed this behaviour. This rarity does not allow meaningful statistical analysis. However, during the parental period fin digging became much more common. There were no significant differences (ANOVA, p = 0.98) between pairs of C. ocfofusciatum in the frequency of fin digging (i.e., within-pair variability greatly exceeded that of between-pair). Therefore, pseudoreplication would not have any detrimental effect and individual broods were treated independently. The results of the analysis of variance are presented in Table 1. Parental fin digging was performed significantly more often by females than by males (Table 1, Fig. I). The difference between sexes in the frequency offin digs was most pronounced when fry were 10 d and 17 d old (Tukey HSD test, both p < O.OOl), whereas there was no significant difference between the sexes at other brood stages (Tukey HSD test, p 3 0.124). The frequency of fin digging increased significantly with brood age for both females and males (Table 1, Fig. I). For both sexes, the increase of parental fin digging frequency was most pronounced with the change of offspring age from 3 to 10 d as fry (Tukey HSD test, p = 0.01 for males, p < 0.001 for females), whereas the difference in parental fin digging frequency between other adjacent brood stages (egg and wriggler, wriggler and 3 d as fry, 10 d and 17 d as fry) was not significant (Tukey HSD test, p 3 0.148 for males, p 3 0.243 for females). The interaction between parent sex and brood age was significant (Table 1). Although it was difficult to find an unambiguous interpretation of this interaction (since raw data were log-transformed), it appears that the increase of fin digging frequency with brood age was more pronounced in females than in males (Fig. I). Hungry parents fin dug more often than satiated ones (Table 1, Fig. 2). There was no significant interaction between satiation and sex of parents, satiation and zyxw Tuble I : Effects of sex and satiation of parents, and brood stage on the frequency of parental fin digging (ANOVA results) Effect Sex of parents Brood stage' Satiation df 1 , 22 3, 65.1 I , 22 Interaction between sex of parents and brood stage' 3, 65.1 Interaction between sex of parents and satiation I , 22 Interaction between brood stage and satiation 4, 88 Interaction between sex ofparents, brood stage and satiation 4, 88 ' Greenhouse-Geisser adjustment was used 1: P 39.13 68.01 26.53 5.52 0.41 0.76 I .50 <0.001 <0.001 <0.001 0.002 0.528 0.555 0.210 Egg zy zy zyxwvuts zyxwvu zyxwvuts zyxwvut Fin Digging in Cichlusomu octofuscicrrum 0 - Males A -Females T Wriggler 3d 10 d 775 zyx T 17 d Brood stage Fig. 1: Fin digging frequency per 15 min by parental males and females of C'ichkmor~7a octofasciatum at five stages of brood development. The box plots give the median (point), 25 and 75 % inter-quartiles (upper and lower ends of box), and minimum and maximum values (whisker). Data before and after parents were fed are combined brood stage or satiation, sex and brood stage (Table I). Thus, the fin digging frequency of hungry adults was higher than that of satiated ones, for both males and females, and increased with brood age both in hungry and satiated males, as well as both in hungry and satiated females (Fig. 2). Discussion Two main features of the parental fin digging are similar in the convict cichlid, C. nigrqfasciuturn (Wisenden et al. 1995) and in C. octofusciaturn. First, in both species it is performed more often by females than by males. Second, as in the convict cichlid, the fin digging frequency in C. octufasciatum increases with brood age. This corresponds to the data on another type of parental provisioning in Cichlasoma species, namely leaf lifting (Keenleyside et al. 1990). Generally, among biparental substrate brooding cichlids, the two parents do not share all parental duties equally. Males patrol the brood-rearing territory and repulse predators, while females concentrate on promotion of growth and development of young, including brood provisioning (Keenleyside 199I). This also agrees with previous data on the parental care in C. octofasciaturn (Zworykin 1993, 1995). Increase of the parental brood provisioning with offspring age is one of the general predictions of parental investment theory and has been revealed for many animals (Clutton-Brock 1991). As the present study found, the increase of parental fin digging frequency was most pronounced with the change in offspring age from days 3 to 10 as fry. This fact probably reflects that during the first three days of free-swimming the food demands of the fry were low, but during the next week they increased rapidly. Artigas Azas (1992) observed that not only parental but also non-breeding 776 zyxwvu zyxwv zyxwvuts zyxwvuts zyxwvutsrq zyxwvuts D. D. Zworykin 3.5 a 3 2.5 .-c 0 -Hungryrnales A - Satiated males E I7 n 2 . g, .- 1.5 0 f ’ .- 0.5 ___ 0 Egg Wriggler 3 days 10 days 17 days Brood stage b A Egg - Hungry females - Satiated females Wriggler T 3day Brood stage T n T zyxwvut 10 day 17 day Fig. 2: Effect of satiety on frequency of fin digs by males (a) and females (b) per 15 min by parents of Cichlasoma octofasciatum at five stages of brood development. Conventions are as in Fig. 1 C. labridens occasionally fin dug while foraging for themselves in nature. Similar data have been reported for the convict cichlid (Williams 1972; Wisenden et al. 1995; A. Stalsberg, pers. comm.). I observed that under aquarium conditions hungry non-parental C. octofusciutum rarely performed fin digging, whereas satiated ones never fin dug. Because fin digging is associated with both the adults’ own feeding and parental food provisioning, Wisenden et al. (1995) suggested that parents may use their own nutritive status to estimate food availability for their fry. This hypothesis appears reasonable but it is based on the speculative premise that both adults and fry of species such as the convict cichlid feed in nature zyxwvutsr zyxwvu zyxwv zyxwvutsr Fin Digging in Cichlusoma octofasciutum 777 primarily on the same food (algae and microfauna in the benthos). Indeed, parental provisioning with the adult diet is widely distributed among various animals (Clutton-Brock 1991).Yanagisawa & Sato (1990) also supposed that in the Tanganyikan mouthbrooding cichlid Tropheus duboisi the essential condition for parental food provisioning by means of buccal feeding is the same diet for both adults and young. However, while this assumption may be true for buccal feeding, it is probably not adequate for fin digging. The natural food of adult convict cichlids consists primarily of aquatic insect larvae, zoobenthos and partly of plants (Bussing 1993; Winemiller et al. 1995). Adult C. octofusciutum feed on insect larvae and imagines, and zoobenthos. Large adults may hunt for small fishes (Jennings 1986; Konings 1989; J. M. Artigas Azas, pers. comm.). Unfortunately, I was not able to find welldocumented data on the juvenile diet of Cichlusomu species, but in habitats that are poor in plankton, the young probably feed mainly on drift and the epibenthos (W. A. Bussing, pers. comm.). Consequently, feeding of both adult and young cichlids in such habitats is associated with bottom substrate and, regardless of the differences between adult and juvenile diets, fin digging is likely to increase the food availability for adults and, perhaps to a greater extent, for fry. According to Wisenden et a]. (1 9 9 9 , general food availability and the abundance of the adult ration had no significant influence on the frequency of parental fin digging in convict cichlids. In this study I showed that this type of parental behaviour in a related species, C. actofusciaturn, was significantly associated with the satiation state of adults. The current physiological state of parents rather than an assessment of food availability probably determined their behaviour. Provided that the digging of substrate improved feeding opportunities of both adults and fry, the changes in parents and offspring satiation would correlate. Therefore, adult cichlids could be able to infer the fry food demands through their own satiety, i.e. there could be a single proximate mechanism regulating fin digging for both adults foraging and fry provisioning. Natural selection is more likely to maintain such economical mechanism than to create an independent one dedicated to the estimation of fry satiety. My data confirm this idea: the young in my study (unlike in natural conditions) were unable to feed simultaneously with the parents and so the fry satiation itself was unlikely to determine the behaviour of parents. Most probably, it was the parents’ own current level of satiety that influenced the frequency of their fin digging. There might be a generalized short-term effect of satiation, but my previous study (Zworykin 1993) showed that both overall activity and certain types of parental behaviour in females of C. octofasciutum did not decrease with satiation. Based on literature data and my own observations I suggest the possible evolutionary scenario. Fin digging may have been a pattern of adult foraging in the ancestors of the contemporary Cichlusomu species and natural selection may have favoured individuals that fin dug more actively during the breeding period because this would increase offspring survival. Selection could therefore preserve the mechanism regulating the frequency of fin digging associated with adults’ feeding behaviour, but it should create an adjustment for parental fin digging performance for optimization of parental investment. Such a process seems to be a 778 D D. Zworykin zyxwvuts typical case of the evolutionary expansion and/or change of function (see Severtsov 1987) of behaviour. It should be noted that the important condition for the development of this form of parental food provisioning by the method described is exploitation of the same food source, namely the bottom substrate, by both adults and fry. zyxwvutsrq zyxwvutsrq zyxwvuts zyxwvutsrq zyxw zyxwvu Acknowledgements I especially wish to thank S . V. Budaev for statistical advice, constructive comments and correction of English. 1 am very grateful to M. H. A. Keenleyside for active interest in my work. for encouragement and help, and A. Stalsberg, H. M . Artigas Azds, B. D. Wisenden and W. A. Bussing for useful consultations on the feeding and breeding of Central American cichlids. My greatest appreciation goes to M . Taborsky, M.V. Mikheev, A. D. Mochek and A. Yu. Zhuikov for their helpful comments. The help and support of A. A. Vlasova is also gratefully acknowledged. Literature Cited Artigas Azas, J . M. 1992: The “Cichiusomu” /uhr-ir/~,L.tzs-complex.In: The Cichlid Yearbook. Vol. 2. (Konings, A,, ed.). Cichlid Press, St Leon-Rot. pp. 65-70. Bussing, W. A. 1993: Fish communities and environmental characteristics of it tropical rain forest river in Costa Rica. Rev. Biol. Trop. 41, 791 - 809. Clutton-Brock, T. H. 1991: The Evolution of Parental Care. Princeton Univ. Press, Princeton. Crowder, M . J. & Hand, D. J. 1995: Analysis of Repeated Measures. Chapman & Hall, London. Diesel, R. 1989: Parental care in an unusual environment: Metopcrulius depressus (Decapoda: Grapsidae), a crab that lives in epiphytic bromeliads. Anim. Behav. 38, 561-575. Ewer, R. F. 1973: The Carnivores. Weidenfeld and Nicolson. London. Hamilton. W. D. 1964: The genetical evolution of social behaviour. 1. 11. J . Theor. Biol. 7. I---52. Hildemann, W. H. 1959: A cichlid fish, Sjmplzj~vodondi.scus, with unique nurture habits. Am. Nat. 93, 27-34. Jennings, D. P. 1986: Characterization of a localized Jack Dempsey, Cic/iiu.so~.tncrocloftrscicrrurn. population in Alachua Country, Florida. Fla. Sci. 49, 255----259. Kaston, B. J. 1965: Some little known aspects of spider behavior. Am. Midl. Nat. 73, 336---356. Keenleyside, M. H. A. 1991: Parental care. In: Cichlid Fishes: Behaviour, Ecology and Evolution. (Keenleyside, M. H. A,, ed.). Chapman & Hall, London. pp. 191-208. Keenleyside, M. H. A,. Bayley, R. C. & Young, V. H. 1990: Variation in the mating system and associated parental behaviour of captive and free-living Cichlu.sonru f f ~ ~ ~ u / ~(Pisces, ~ c i ~ ~ / u ~ Cichlidae). Behaviour 112,202--220. Konings, A. 1989: Cichlids from Central America. T F H Publ., Neptune City. Kutschera, U. 1992: Reproductive behavior and parental care of the leech Hr/obdel/u iriwr-idis (Hirudinea, Glossiphoniidae). Zool. Anz. 228, 7+81. Kuwamurd, T. 1986: Substratum spawning and biparental guarding of the Tanganyikan cichlid BouIengerochromis microkepis, with notes on its life history. Physiol. Ecol. Jap. 23, 31-43. Lack, D. 1966: Population Studies of Birds. Clarendon Press, Oxford. Lovullo, T. J., Stauffer, J. R. & McKaye, K. R. 1992: Diet and growth o f a brood of B q r u s nwridiunrtlis Gunther (Siluriformes, Bagridae) in Lake Malawi, Africa. Copeia 1084 - 1088. Milliken, G. A. &Johnson, D. E. 1984: Statistical Analysis of Messy Data. van Nostraiid Reinhold, New York. Perrone, M . 1978: Mate size and breeding success in a monogamous cichlid fish. En!.. Biol. Fish. 3, 193---20 I . Robertson, D. R. 1973: Field observations on the reproductive behaviour of ii pomacentrid fish, Acanihochromis poljmanthus. Z. Tierpsychol. 32, 3 19--324. Severtsov, A. S . 1987: The Principles of Evolutionary Theory. Moscow Univ. Press, Moscow. (In Russian). - zyxwvut zyxwvut zyxwvutsrqp zyxwvut zyxwv zyxw Fin Digging in Cichkrsoniu ocrofb.sriurum 779 Trivers, R. L. 1972: Parental investment and sexual selection. In: Sexual Selection and the Descent of Man, 1871--1971.(Campbell, R., ed.). Heinemann, London. pp. 136-179. Williams, N . J . 1972: On the ontogeny of behaviour of the cichlid fish C i c l i l ~ ~ tirymfuscia/utiI ~ni~ (Giinther). PhD Diss., Univ. of Groningen, Groningen. Wilson, E. 0. 1971: Insect Societies. Harvard Univ. Press, Cambridge. Winemiller, K. 0.. Kelso-Winemiller, L. C. & Brenkert, A. L. 1995: Ecomorphological di\ersification and convergence in fluvial cichlid fishes. Env. Biol. Fish. 44,235--261. Wisenden. B. D., Lanfranconi-Izawa, T. L. & Keenleyside, M . 14, A. 1995: Fin digging and leaf lifting by the convict cichlid, Cichlusoniu nigr~fr~sciarirni: examples of parental food provisioning. Anim. Behav. 49,623-63 I . Yanagisawa, Y. & Ochi, H. 1991: Food intake by mouthbrooding females of Cjphotilapia j k n l o s a (Cichlidae) to feed both themselves and their young. Env. Biol. Fish. 30, 353--358. & Sato. T. 1990: Active browsing by mouthbrooding females of T w p h w s rluhoivi and Tropheus rnoorii (Cichlidae) to feed the young and/or themselves. Env. Bid. Fish. 27,43---SO. Zworykin, D. D. 1993: Peculiarities of parental investment of male and female in (‘ic~hlcisomam u fusciurum (Regan, 1908) (Teleostei: Cichlidae). MSc. Diss., Moscow State Univ., Moscow. (In Russian). 1995: Male and female parental investment in Cichlasoma ocrofusciutuni (Cichlidac). J . Ichthyol. 35.135-141. ~ ~ -- RrecJiced:March 24. 1997