Adaptation to habitat unpredictability and some consequences

The subject of this essay is rain pools – specifically those on rock surfaces in tropical Africa. Rain pools are at the extreme of short duration among fresh waters, some lasting just hours after rain. Yet they are inhabited by immense populations of midge larvae – strictly a single species to each pool. Over the past thirty five years, on and off, I have been interested in adaptations enabling these extraordinary animals to survive and flourish in what would appear an unpromising place. In the end this work has hinged on a comparison of the adaptations of two principal inhabitants, larvae of Chironomus species on the one hand and larvae of Polypedilum vanderplanki, on the other. What has not previously received attention are the consequences following from adaptation to habitat desiccation. I refer to exposure to parasites and predators.

For the first time I consider costs as well as benefits to adaptive strategies to habitat unpredictability. To develop my arguments I adopt the comparative method practised by John Crook and by Peter Jarman, among others (Krebs & Davies, 1993), pp. 25-29. In other words, I compare strategies and in so doing attempt to bring out the relationships between ecology and accompanying adaptation. As pointed out by John Krebs and Nick Davies 1993, p. 25, this is rather like looking at the results of an experiment done over evolutionary time with species acting as controls for each other.

To begin, some background.  The rain pool faunas include three species of midge, Chironomus imicola, Chironomus pulcher and Polypedilum vanderplanki. I focus on the two Chironomus species taken together in contrast to P. vanderplanki. For my present purposes we need to know only that Chironomus inhabit pools with an average duration close to the average duration of the aquatic larval and pupal stages. P vanderplanki, on the other hand, inhabits pools with an average duration many times shorter than the average duration of the aquatic stages. Chironomus spp have behavioural adaptations enabling them to use cues to imminent pool desiccation and are triggered by these cues to metamorphose and leave the pool as adults. These cues allow, in effect, predictions of what is likely to happen in the future. In this sense adaptation can hinge on future events, a much misunderstood matter (Dawkins, 1986), p71. P. vanderplanki by contrast, survive in the dry home pool as desiccated larvae. As would be expected the choice between stay and leave is universal wherever habitat duration is unpredictable. Maynard Smith, pp262-263, cites the case of fish in transient habitats, for example, lung fish (stay), vs. osteolepid fish (leave) (Maynard Smith, 1975).

I turn now to the costs of the parasites and predators associated with the stay or leave strategies. Both parasites and predators infect aquatic stages of the midges but costs occur in the adult stage. The predicted costs and benefits of the stay or leave strategies are shown in Table 1.

Table 1. Costs and Benefits in terms of changes in fitness due to interactions with predators and parasites. The predators considered are ants and parasites, worms and mites.  

           Taxon                                         cost                                        benefit

Chironomus	Parasites	?
P. vanderplanki	Predators	No parasites

Entries in Table 1 take the form of testable hypotheses. My reasoning is as follows: costs to Chironomus accrue to adults harbouring either mites or worms (McLachlan, 2006). For P. vanderplanki, costs are due to predation by ants mining for larvae in suspended animation (Fig. 1). Benefits accrue because P. vanderplanki individuals escape parasites which are unable to infect desiccated larvae. (Fig. 2) shown a mite (Unionicola ypsilophora) and a worm probably Gastromermis rosea. To a first approximation, I regard both as parasites.

Fig. 1. Top. Spoil tips from ant mining activity in the bed of a dry P. vanderplanki rain pool.

Below left. An ant with a larva in its mandibles. Below right. Two ants fighting over a larva in cryptobiosis. From (McLachlan & Cantrell, 1980).

Fig. 2.  Parasitic mites and worms. a,  a female midge baring several mites. b,  a females midge with a large worm (g), emerging.

All hypotheses are readily tested, for example by capturing adults emerging from pools in the wild to count parasites. Negative fitness effects to ant predation can be determined by counting larvae removed by ants against the number recovering after artificially flooding the home pool.

In conclusion I wish to broaden the scope of this essay and in so doing promote a better understanding of the adaptive landscapes to which the insects are exposed.

I start with Chironomus and the question over the benefits shown for Chironomus (Table 1). Pools do not invariable dry before the full growth of Chironomus larvae is complete (McLachlan & Ladle, 2001). The benefits to Chironomus larvae when the home pool is full include access to super-abundant food with virtually no inter-specific competition. But whenever larvae succeed in metamorphosing there is a considerable cost, i. e. the burden of parasites in the adult stage of the life cycle (McLachlan, 1999). So, for Chironomus, the frequency of early desiccation must be brought into the equation (McLachlan, 2006).

Turning to P. vanderplanki, these larvae enjoy the same benefits as Chironomus when pools contain  water. There is a cost in the larval stage to predication, the extent of which remains to be measured but it can be predicted that there is a very considerable fitness benefit to the absence of parasites. There is more to anhydrobiosis. Referring to my (2013) Blog, it has been suggested that anhydrobiosis is the reason for some desiccation resistant rotifers dispensing with both sex and parasites. As far as can be determined they never have sex! Perhaps, as suggested by Hamilton and Zuk (1982), they don't need sex in the absence of parasites. 

References

Dawkins, R. (1906). The Extended Selfish Gene. Oxford University Press. 

Krebs, J. R., & Davies, N. B. (1993). An Introduction to Behavioural Ecology. Oxford: Blackwell Scientific Publications.

Maynard Smith, J. (1975). The Theory of Evolution. (third ed.). New York: C. Nicholls 

McLachlan, A. J. (1999). Parasites promote mating success: the case of a midge and a mite. Animal Behaviour, 57, 1199-1205.

McLachlan, A. J. (2006). You are looking mitey fine: parasites as direct indicators of fitness in the mating system of a host species. . Ethology Ecology & Evolution 18, 233-239.

McLachlan, A. J., & Cantrell, M. A. (1980). Survival Strategies in Tropical Rain Pools. Oecologia, 47, 344 - 351.

McLachlan, A. J., & Ladle, R. (2001). Life in the puddle: behavioural and life-cycle adaptations in the Diptera of tropical rain pools. Biological Reviews 76, 377-388.

McLachlan, A. J. (2013). Anhydrobiosis, parasites and sex. http://www. atholmclachlan.blogspot,com/

Hamilton, W. D. and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science. 218. 384-387.