The typical life cycle of an amphibian is often exemplified by that employed by Ireland’s native Common Frog (Rana temporaria). A large number of eggs are laid in a lentic water body and externally fertilized. The young undergo an aquatic larval stage before emerging on land as froglets. Once the eggs have been laid, the parents afford no further care to the young (McDiarmid, 1978).
This, somewhat hands-off approach to parenthood is, however, but one of the many reproductive strategies employed by amphibians, and in particular frogs: for some species go to extraordinary lengths to ensure their offspring get the best possible start to life.
To better understand the significance of these reproductive strategies and why they make such interesting subject matter, it may help to discuss these strategies in the context of the r/K selection theory.
The concept of r and K selection was first presented by ecologists MacArthur and Wilson (Pianka, 1970). The basic premise is that animals adopt one of two techniques for reproduction. Animals that are r-selected have a large number of small young in which they invest no parental care following birth. K-selected animals have a small number of relatively large young in which they invest a huge amount of energy. In reality, the r/K division is more of a continuum than two separate strategies.
Which technique is used is often a reflection of the stability of the environment in which the animal lives. According to r/K selection, unstable conditions should favour r-selected species because they have the ability to produce large numbers of young quickly, allowing the population to rapidly recover from a crash. Invertebrate pests are a commonly cited example of r-selected species. Insecticides can kill the vast majority of a population of pests, but the remaining individuals can restore the population to its former strength in a relatively short period of time.
K-selected species thrive in stable conditions and produce small numbers of highly developed young. These young have much higher survival rates due to parental investment, but these species have a poor ability to recover from population crashes. Whales are an example of a K selected species. While the young receive a great deal of maternal investment and are often too large to be considered prey, it may take decades to restore the population to its former levels if the population suffers a crash (from excessive whaling for example).
The difference in clutch/offspring size is essentially a consequence of metabolic budgeting. The animals devote a fixed amount of energy to reproduction, so if they invest less energy in zygote production then they can afford to offer further energetic investment afterwards.
While the “typical” amphibian reproduction strategy would fall under the r end of the continuum, those that fall closer to the K end are some of the most remarkable and unbelievable adaptations that the animal kingdom has ever produced.
Parental investment among the urodella is not particularly common, but there are some very interesting exceptions.
The Alpine salamander (Salamandra atra) retains the eggs in its oviduct for between 2 and 5 years (Blackburn, 1999). They give birth to 2 fully developed young (one from each oviduct). For the first year of gestation the young feed on unfertilized ova and ova that were fertilized later than the first ovum. After the first year, this resource is exhausted. At this point, a small section of the mother’s oviductal epithelium, the zona trophica, becomes highly secretory. The young feed on these secretions for the duration of their gestation (Pough, 2007, Wake, 1993).
A more common form of parental investment in salamanders is egg attendance. Female Mountain Dusky Salamanders (Desmognathus ochrophaeus) stay with the eggs until such time as they hatch. The level of aggression utilized in defence of the eggs increases as time progresses. This is in essence an insurance policy. Should she lose the clutch early on, she may still be able to produce another clutch that season. If she loses the clutch late on, she will have suffered too great a loss in condition to produce a new clutch (Forester, 1983).
Caecilians are perhaps the least well documented amphibian group, which is unfortunate because they display some very unique behaviours, particularly when it comes to reproduction.
The caecilian Boulengerula taitana lays eggs that develop directly to miniature adults. Both mother and offspring possess unusual adaptations. The mother produces a lipid rich monolayer of skin periodically. The young have specialised dentition that they use to feed on this nutritious layer of skin. As the offspring develop, their dentition changes to suit their adult lifestyle (Kupfer et al., 2006, Muller et al., 2009).
Caecilians of the genus Typhlonectes retain larval young in the oviduct. The young have a pair of large sac like gills which function as a pseudo-placenta, absorbing nutrients from the mother (Wake, 1993).
The Mexican Caecilian (Dermophis mexicanus) also retains the young in its oviduct. Once the egg yolk has been exhausted, the young feed on a nutritious secretion of the oviductal epithelium. The young have special foetal dentition that they use to scrape the oviductal lining. After the birth the young shed their foetal dentition and acquire their adult dentition quickly (Muller et al., 2009).
The greatest diversity of reproductive strategies can be seen in the frogs and toads.
The Western Nimba Toad (Nimbaphrynoides occidentalis) is a viviparous species that feeds the young on oviductal secretions for the final 2 months of gestation. The gestation lasts 9 months. For the first seven, the female resides in an underground nest to escape the dry season (Wake, 1993).
The Creole Frog (Leptodactylus ocetlatus) lays a foam nest which floats on the surface of the water body. In this way the young are protected from aquatic predators for the early stages of their development. Once the eggs hatch, the young form a school that moves around the pond feeding. The mother follows the school around and attacks potential predators attempting to feed on the larvae (McDiarmid, 1978).
The Surinam Toad (Pipa pipa) has quite a unique method of brooding its young. During amplexus the female turns herself upside down so that the eggs are rolled up on to her back with some assistance from the male. The females back will become swollen and puffy. The eggs sink into the modified skin and become almost completely enveloped by it. The young undergo metamorphosis in these pockets and emerge 3-5 months later as fully developed froglets (Rabb & Snedigar, 1960, Rabb & Raab, 1960, 1963).
Those frogs having pouches (Amphignathodon, Flectonus, and Gastrotheca) are termed marsupial frogs (Duellman & Maness, 1980). Of these, some retain the young until metamorphosis is complete, while others retain them until an advanced stage of metamorphosis. All of these frogs brood their young in dermal pouches. The shape, position and capacity of the pouches vary between species. The sex of the brooding parent also varies between species. In Flectonotus pygmaeus, eggs are laid one at a time at one minute intervals. As the male fertilizes each egg he assists in its insertion into the pouch. When the eggs hatch, the female moves to a small water body, such as a bromeliad, allowing the advanced tadpoles to swim out of the pouch. The young then complete metamorphosis in approximately two weeks (Elinson et al., 1990).
The now extinct Gastric Brooding Frog (Rheobatrachus silus) as its name suggests, maintained their young in the female’s stomach. Once the eggs had been fertilised she would swallow them. The eggs would secrete Prostoglandin E2, which caused gastro-intestinal stasis and prevented the mother from producing gastric acid (De La Lande et al., 1984). During the brooding period, the stomach becomes highly distended and expanded to the point of inhibiting normal function of the mother’s lungs. Eight weeks later, the young were regurgitated as fully developed froglets. Eight days after the birth, the gastrointestinal tract of the mother returned to normal functionality (Gibbins & Tyler, 1983, Wake, 1993).
Darwin’s Frog (Rhinoderma darwinii) maintains their young in the vocal sac of the father. For the first 20 days after fertilisation development of the eggs occurs in moist ground. At this stage, they begin to exhibit muscular activity and it is this cue that prompts the male to pick them up one by one and guide them into his vocal sac. The average clutch size is 11. The young develop fully inside the father’s vocal sac and emerge about 52 days later (Busse, 1970). There is some evidence to suggest that the father may supply the young with nutrition during the brooding period (Goicoechea et al., 1986).
Some species exhibit direct development of the eggs. Large eggs allow the young to forego the vulnerable aquatic
larval stage. The Jamaican Frog (Eleutherodactylus cundalli) goes one step further. They deposit their eggs deep inside caves where they are less vulnerable to predation and the environment is stable. The female attends the clutch until they hatch. The froglets then climb on her back and she transports them outside the cave where food is more plentiful (Diesel et al., 1995).
When it comes to parental care, it is the Dart frogs that are the most renowned. Frogs of the genus Dendrobates exhibit complex parental care. In species such as Dendrobates auratas, Dendrobates tinctorius azureus and Dendrobates tinctorious a small clutch is laid in leaf litter. The male then attends the clutch until they hatch, at which point he transports them to phytotelma (water bodies held by plants such as pitcher plants) where they complete their development (Summers et al., 1999).
A similar strategy is utilized by frogs in the genus Oophaga. The Strawberry Dart-Frog (Oophaga pumilio) is perhaps the best known. In this species, the male attends the clutch until they hatch, but it is the female that transports the young to phytotelma (Limerick, 1980). She returns to the pools periodically and deposits unfertilized ova for the young to feed on (Brust, 1993, Summers et al., 1999).
While the assemblage of reproductive strategies utilized is diverse, they seldom deviate far from basic ideals. To understand why a particular strategy may work for a species one must weigh up its benefits against its costs.
So what advantages does clutch attendance offer? It reduces predation during early life stages as parents can defend the clutch by attacking would-be predators. One particularly interesting case of attendance is that of Centroienella valerioi, a species of Glass Frog. The male has a reticulated appearance that makes him look very similar to his clutch. In this way, if egg-feeding predators mistake the male for the clutch and are attacked, they may be dissuaded from attacking the clutch in future. This form of camouflage also serves to protect the male from predators who are uninterested in amphibian eggs (McDiarmid, 1978).
Another major advantage of egg attendance is the ability to monitor the eggs condition and prevent developmental problems. Parents can help prevent desiccation of the eggs and can remove eggs that show signs of fungal infection. Large eggs are more susceptible to developmental anomalies, which the parents can counteract through frequent manipulation of the eggs (McDiarmid, 1978).
This strategy is not without its costs. Egg attendance reduces the parent’s ability to feed and mate, though in many species the male will continue to call for mates and may attend clutches from multiple partners (Beck, 1998, Burrowes, 2000).
This strategy is particularly helpful for species who continue to care for their young during the aquatic larval stage because the small enclosed bodies of water make the young easy to locate. By leaving the young in a small pool, such as those formed by a bromeliad axil, the parents ensure the young are safe from aquatic predators. The downside is that food is limited, so species that exhibit phytotelm breeding are often capable of completing metamorphosis without feeding or are provisioned with food from their mother in the form of infertile ova (Alves-Silva & da Silva, 2009, Brust, 1993).
Viviparity is commonly utilized by species in colder environments. By retaining the young until they’re fully developed, the mother protects them from extreme weather, and helps ensure that the temperature of the eggs is sufficient for development. The downside is that a lengthy gestation will prevent females from mating again and large developing young may impede the female’s efforts to feed and move. In species where the young feed on oviductal secretions, there is also the added energetic cost of nourishing the young.
Internal brooding in modified structures (stomach, vocal sac etc.) and dermal brooding provide the young with a moist, stable environment in which to develop. The young also gain extra protection from predation, because they are only ever as vulnerable as the brooding parent. There is a cost to the parent. As with viviparity, the young may impede the parent’s movement, and may even interfere with proper organ function (Gibbins & Tyler, 1983).
While parental care would appear to be more complex than the “traditional” amphibian life cycle, the complexity does not necessarily imply that parental care is a better strategy. The traditional strategy has its own pros and cons. The parents expend all their reproductive energy in a short time, allowing them more time to recover for the next season. The young have the benefit of numbers to reduce each individual’s risk from predation. Larger clutches will have a higher diversity of mutations, some of which may prove beneficial. The cons are quite obvious. The eggs are susceptible to predation and the young can do little to avoid it, the aquatic larvae are also highly vulnerable to predation. If fungal infections develop on the eggs, there are no parents present to reduce its spread etc.
Regardless of the strategy employed, amphibians are always at the mercy of their aquatic origins. The young must be kept moist at all costs. By evolving complex parental strategies that allow them to brood young successfully in terrestrial environments, amphibians can exploit a more diverse range of niches and reduce their dependence on fixed water bodies.
About the Author: Rob is a zoologist specialising in invasive freshwater bivalves. He is the PR Officer for The Herpetological Society of Ireland. Find him on Twitter here.
This article was originally produced for the HSI’s publication Lacerta. Reproduced here with minor additions.
Trish Hartmann’s Flickr. Photo used under license.
Brian Gratwicke’s Flickr. Photos used under license.
Wagon16’s Flickr. Photo free from copyright.
All other photos are property of Rob Gandola.
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