Many models of parental investment consider offspring as passive participants where parents decide upon appropriate levels of investment. However, in 1974, Trivers introduced the theory of parent–offspring conflict, which views offspring as active participants soliciting investment from parents (Trivers, 1974). Although parent–offspring conflict in its broadest sense may apply to any sexually reproducing species showing parental investment (Trivers, 1974), in oviparous species, those that lay eggs, pre-parturition conflict between future offspring and parents is unlikely (Crespi and Semenuik, 2004). Post-parturition conflict is often difficult to determine if parental care is confined to parental defence of offspring. The stickleback, Gasterosteus aculeatus, is an example of an oviparous species where females lay eggs and then males guard and fan the developing embryos. To our knowledge there is no concrete evidence in oviparous fish species that developing offspring are able to directly manipulate parental investment. There is clear potential for chemical communication between parents and offspring to occur post-parturition in oviparous fish species (e.g. Mourabit et al., 2010) but a role in parent–offspring conflict remains speculative. Certainly, many previous models of parental investment motivated by teleost fishes focus on factors that influence a parent's decision to invest in offspring only from the perspective of the parent (reviewed by Sargent and Gross, 1993) without active influence by offspring.
In Symphysodon (and some other species of cichlids) parents provide offspring with an opportunity to gain nutrition from parental mucus and offspring perform behaviours (known as contacting, micronipping, parent-touching) to maximise attainment of this food. While not all contacting behaviours in fish are trophic in function (Noakes, 1979), where nutrition is obtained through this behaviour, offspring have the potential to demand more investment than the parent is selected to give (Trivers, 1974). Mucus-feeding behaviour stands out as a situation where measurable parent–offspring conflict post-parturition occurs. Ongoing, unpublished experiments in our laboratory allow us to manipulate both parental investment and offspring demand during this period of conflict in Symphysodon spp. Only a few species of fish (<0.2%) perform such parental care behaviours where parent–offspring conflict can be studied post-parturition.
In the context of mucus feeding, ‘mucus’ is a term used to describe a secretion containing a variety of substances [e.g. Buckley et al. (Buckley et al., 2010) measured immunoglobulin, protein, hormones and ions] in the same way that mammalian ‘milk’ refers to a liquid containing fats, proteins, sugars, immunoglobulins and microorganisms. Therefore, provision of fish ‘mucus’ as a form of parental care could be considered analogous to mammalian ‘milk’. In lactating species, postnatal parental care can be divided into three periods according to the age of the offspring (Trivers, 1974). The last of these periods is the weaning period where most contact between parent and offspring is initiated by the offspring, with parents showing open avoidance and even aggression towards offspring (Trivers, 1974). Only by studying the behaviour of both parent and offspring is it possible to determine whether a weaning conflict exists. Our study (Buckley et al., 2010) documents changes in parental care during the breeding period of Symphysodon and highlights that in week three, open avoidance by the parents can be observed in this species and offspring actively seek out their parents during this period. These observations of both parental and offspring behaviour are directly in line with Trivers' description of the third period of parental care in mammals (Trivers, 1974).
This fascinating behaviour seen in Symphysodon spp. certainly raises many questions. Currently we are investigating, among other things, whether parental immunoglobulins found in this mucus meal are measurable in discus fry. We have recently demonstrated that mucus of adult fish inhabiting metal-contaminated waters or eating a metal-contaminated diet contains measurable levels of contaminants that can be passed on to offspring through mucus feeding (R. J. Maunder, J.B., A.L.V. and K.A.S., unpublished results).
Acknowledgements
We thank Dr Sigal Balshine for comments on a previous draft of our Response.
