Behavioural ecology

Ways to raise tadpoles

To reduce parental care, just add water — that's the conclusion of an intriguing investigation into the extent of the motherly and fatherly devotion that different species of frog extend to their offspring.

Nature documentaries frequently invite their viewers to contemplate that only a tiny minority of the perfectly formed larvae floating in the sea, or crawling on land, can ever hope to make it to the adult stage. Parents of many species seem surprisingly unconcerned, leaving their progeny to fend for themselves. In some species, however, parents provide their offspring with costly, time-consuming services, ranging from protecting them against predators and environmental stresses to giving them shelter or food.

Why does this diversity of solutions exist? Theoreticians state that parents may reduce care to increase the number of young produced and/or to improve the parents' own survival. Both trade-offs reduce the lifetime fecundity of parents, so parents are likely to provide care only if it substantially improves the survival of the offspring they do produce1. A study of frogs by Brown et al.2, just published in The American Naturalist, shows that a species' breeding habitat can influence offspring survival in a surprisingly deterministic way: tadpoles have a chance of surviving on their own only if they live in relatively large pools of water.

It has proved difficult to identify specific ecological factors that affect whether parental care will evolve, yet the answer provided by Brown and colleagues2 is simple and elegant. To start with, they built a phylogeny depicting the evolutionary relationships among 404 frog species that are distributed across the order Anura and that have been investigated for whether and how they provide parental care.

Frog species differ enormously in whether they care for their young and in the type of care given: parents may protect eggs by laying them in terrestrial burrows, or brood the young in pockets of tissue on their back or in the mother's stomach3. Although Brown et al. did not consider all frog species (of which there are more than 5,300), their phylogeny uncovered compelling ecological generalities. Species that deposit eggs and tadpoles into phytotelmata (small pools of water found in hollows in plants) are more likely to provide parental care than those breeding in terrestrial waters such as streams, ponds and rivers. The estimated rate of evolutionary transitions from providing no care to providing care was nine times higher in species that breed in these tiny pools than in those that use terrestrial waters.

Why does a limited water source turn frogs into devoted parents? One possible answer is that the food supply that a small body of water offers is so meagre that parents using these as breeding grounds have been strongly selected to improve the survival of their offspring. To test this idea, Brown et al. investigated one of the evolutionary contrasts in their data set in detail, reporting fascinating differences between two species of poison frog that live in the same habitat in Peru.

Individuals of the variable poison frog species (Ranitomeya variabilis) have large home ranges, and both sexes frequently switch mating partners. Eggs are laid above a suitable phytotelma, and either the tadpoles fall into the water or, more commonly, the male parent returns and helps the tadpoles to rupture the egg membrane. He then transports the tadpoles on his back (Fig. 1) to another hollow. In this species, males place tadpoles in water volumes averaging about half a cup (112 millilitres). In the closely related, similarly sized mimic poison frog (Ranitomeya imitator), mating pairs are often monogamous. Their home ranges are small, and males carry the tadpoles to a tiny phytotelma which is, on average, the volume of half a shot glass (24 ml). The male parent thereafter returns periodically to monitor whether it is time to feed the tadpoles. If he calls incessantly, the female makes her way to the pool and lays a specialized 'trophic' egg, which is promptly eaten by the tadpoles.

Figure 1: Tadpole transport.
figure1

JASON L. BROWN

After tadpoles have emerged from eggs, males of both the variable poison frog (Ranitomeya variabilis; top) and the mimic poison frog (Ranitomeya imitator; bottom) carry these offspring on their back from the place of birth in a phytotelma (a water-filled hollow in a plant) to another phytotelma. Brown et al.2 find that these frogs otherwise differ considerably in the amount of care provided by the parents. The smaller phytotelmata favoured by R. imitator are associated with a greater degree of parental attention being paid to the tadpoles.

Tadpoles of both species are thus cared for, but tadpoles of the variable poison frog develop without being fed and receive care from only one sex (males). Is it a coincidence that variable poison frogs use larger breeding pools than mimic poison frogs, or did feeding evolve in mimic poison frogs specifically to combat a low food supply in tiny pools?

To shed light on this question, Brown et al.2 carried out a translocation experiment. They show that tadpoles of both species grow and survive poorly in small pools when they are denied parental attention, whereas such problems do not arise in larger pools. The fact that tadpoles of both species suffered similar fates is crucial to the interpretation of the experiment. It allowed Brown et al. to circumvent the chicken-and-egg problem that species in which care is routinely given might have evolved tadpoles that obligately rely on parental care, which could have led to an overestimation of the value of parental care in small pools.

The phylogeny constructed by Brown et al.also reveals that the production of trophic eggs is generally associated with breeding in phytotelmata. However, trophic egg production by frogs is rare, so factors other than the need to feed offspring are probably required to explain the patterns of parental care in frogs more fully. For example, breeding in a small body of water could decrease the likelihood of brood parasitism (in cases in which more than one pair are using a breeding pool), because later-hatching tadpoles are often cannibalized by those that hatched earlier4. In addition, the use of a small breeding ground increases the certainty of genetic parentage, making it more likely that parental care will evolve. It also influences which sex provides care — males, females or both parents5 — but evolutionary transitions do not occur as easily in all directions6. It might not be a coincidence that the poison frog species that engages in biparental care is also the one that is genetically more monogamous.

Even so, caution should be exercised in using the argument that monogamy is conducive to biparental care and therefore concluding that circumstances that make offspring needy also favour monogamy. The co-evolution of traits tends to occur with a delay. Thus, the first monogamous parents of a hypothetical species might not reap any benefits from their behaviour as they will not yet have responded to the novel conditions of reliable parentage by switching to a more intensive form of care. It may be, however, that home-range size or other ecological factors make monogamy more likely in some species and that this later selects for care by both parents.

Regardless of the details of the final story, there is little doubt that frogs, with the diverse ways in which they care for their offspring and an increasingly well-resolved phylogeny, are becoming an important group in helping to explain why there is so much variation in parental care among animals7. Unfortunately though, this diversity continues to be lost. For instance, the details of the ecology of the only two species of gastric-brooding frog will never be known, as both became extinct in the mid-1980s.

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Kokko, H., Jennions, M. Ways to raise tadpoles. Nature 464, 990–991 (2010) doi:10.1038/464990b

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