Buckley and colleagues (Buckley et al., 2010) describe parental care in discus cichlids of the genus Symphysodon, demonstrate that immunoglobulin is present in the mucus secreted by breeding discus, and propose that discus might be an interesting novel model system for studies of mammal-like parental care.
Hildemann (Hildemann, 1959) appears to have been the first to describe parental care in discus, providing detailed analyses of the behaviours re-visited by Buckley and colleagues (Buckley et al., 2010). Parental investment is provided after fertilization of the eggs not just in discus but in all cichlids (ca. 1600 species), and many other families of fish (for reviews, see Blumer, 1979; Breder and Rosen, 1966; Gross and Sargent, 1985). In fact, parental care is exhibited in around 22% of teleost fish, and in 72% of non-teleost fish (Sargent and Gross, 1993). Sargent and Gross also review the literature and the proposed models that investigate the cost of reproduction and the parent–offspring conflict within fish (Sargent and Gross, 1993), citing early examples, just after the publication of Robert Trivers' theory (Carlisle, 1982; Presley, 1976; Trivers, 1974).
In most fish parental care involves fry guarding or provisioning; for example, breeding convict cichlids (species name) actively disturb the substrate using their pectoral fins to release micro-organisms for their fry to feed on, even though the parents themselves do not feed on such small prey items (Keenleyside, 1981; Krischik and Weber, 1975; Williams, 1972).
The highly developed bi-parental care and fry mucus-feeding behaviour observed in Symphysodon spp. is also widespread – at least 28 species have been reported to exhibit fry mucus-feeding behaviour in four families (Noakes, 1979), and this behaviour has evolved many times, in species separated on distant branches of the fish phylogeny, including the Osteoglossiforme Arapaima gigas (Liiling, 1964; Menezes, 1951).
Fry feeding on the mucus secreted onto the skin of their parents is called ‘contacting’ and has been studied in detail in Midas cichlids (Amphilophus citrinellus), orange chromides (Etroplus maculatus) and discus (Symphysodon spp.), in both the laboratory and the wild (Noakes, 1973; Noakes and Barlow, 1973; Ward and Barlow, 1967). The results of Buckley and colleagues (Buckley et al., 2010) on the role of the parents in this behaviour confirm earlier work on the Midas cichlid (A. citrinellus) (Schütz and Barlow, 1997).
Whilst it has been well documented that the fry of Symphysodon spp. are feeding on the mucus secreted by their parents (Chong et al., 2005; Noakes, 1979; Perrone and Zaret, 1979) [see also Hildemann (Hildemann, 1959) and references therein], it has also been shown that, in contrast to mammals, mucus is not the only meal they are getting. Critically, Bremer and Walter (Bremer and Walter, 1986) found that there are more secretocytes undergoing mitosis in breeding individuals of S. discus than in non-breeders and analysis of the faeces of the contacting fry showed that they were consuming these cells and other micro-organisms that are present on the skin of the adults.
However, one area in which the analogy may break down is in Buckley and colleagues' description of weaning (Buckley et al., 2010). The time at which the ‘weaning’ behaviour is proposed to occur coincides with the time when juvenile fish in the wild would naturally disperse from their parents. At this point in the breeding cycle, parental care has finished in the wild for most cichlids, including those that exhibit contacting behaviour (Noakes and Barlow, 1973). In fact, under aquarium conditions, if Midas cichlid (A. citrinellus) fry are left with their parents they eat from them so vigorously in the fourth week that they create wounds on the parental skin (Barlow, 2000). In the wild, such a situation would never occur, as dispersal would have already separated the young fish from their parents (Barlow, 2000).
The most interesting result reported by Buckley and colleagues (Buckley et al., 2010) is that immunoglobulin concentrations are higher in breeding discus than non-breeding discus, and are highest in wild breeding individuals. This result is fascinating and opens up opportunities for future research. What we need to know now is whether this immunoglobulin is passed on to the contacting fry in the same concentrations as it is found in the mucus. If it is, how does the increased amount of immunoglobulin affect the growth and survival of these fry? Away from the immunoglobulin result, there remain other interesting questions for contacting behaviour. The secretocytes found on discus by Bremer and Walter (Bremer and Walter, 1986) appear to be specialized cells; are these types of cell present in other fish that are known to have contacting fry?
The case of parental care in fish is indeed a fascinating model system for answering a variety of questions about the cost of reproduction, and the parent–offspring conflict, and many investigations have already been conducted. It is my hope that modern technologies and techniques can help us to better understand these systems and their problems.
Acknowledgements
I thank Justine Aw and Adrian Thomas for helpful comments on the manuscript, and Andrea Flack for helping me understand the Bremer and Walter (Bremer and Walter, 1986) paper, which is written in German. I would also like to thank the Biotechnology and Biological Sciences Research Council for funding (BB/H01103X/1).
