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| Laborde's Chameleon Furcifer labordi Christopher Raxworthy / Public domain |
Twelve years ago came the news from Madagascar of an ‘annual’ chameleon—one that spent more time in the egg than as an adult.
In short, Laborde’s Chameleon, Furcifer labordi, was found to grow rapidly after hatching in November, to reach sexual maturity and breed by January-February and then to senesce and die. The adult lifespan was found to be 4-5 months. For the dry season of April to October there were no adults alive, just the eggs remained waiting to hatch at the start of the wet season in November.
The discovery excited a great deal of interest for all sorts of reasons. Not least was that among those studying the phenomenon and mechanisms of ageing, comparative life histories and longevity. Laborde’s Chameleon joined a few species of marsupials amongst tetrapods known to have a short lifespan and to die after a first breeding.
This is not the place to describe the large and controversial field of ageing. However, some of those involved may have been tempted to speculate that these short-lived chameleons might be exemplars of one theory of ageing which contends—erroneously in my view—that organisms have a built-in programme that, around a certain age, leads to death. However, what played on my mind, having once known a bit but never enough about chameleons, was what caused the chameleons to die after reproducing. Would they, for example, live longer if breeding did not take place? Was there something about the environment, a lack of food for example, that prevented their survival as adults?
A clue that Laborde’s Chameleon is not always strictly ‘annual’ came from a different location. Kirindy, where the warm, wet season is longer. There, females were found which had bred more than once and one survived into a second year after a particularly long rainy season. When these chameleons were kept in cages in the same region, some males were found to survive until the next season.
Still, I contend, the best way of looking at differences in lifespan between species is the Disposable Soma Hypothesis of Tom Kirkwood. In essence, because the availability of nutrients within the body is limited, animals balance the amount invested in reproduction and in repair. At one extreme, with Laborde’s Chameleon being an exemplar, the animal goes for rapid growth and reproduction at the expense of essential repairs to its cells, to its DNA, to fighting infection and infestation, to healing its wounds etc; as a result it dies when relatively young. At the other extreme, the slow-growing, slowly reproducing animal invests in keeping the adult in good condition for much longer; as a result it does not fall victim to tumours caused by errors in DNA copying or to infection and thus may live for a very long time; think elephant.
Thus, one might expect, with its defences down, Laborde’s Chameleon to fall victim to something in the environment that a longer-lived species which lives in the same habitat (like the Warty Chameleon, F. verrucosus, which aestivates during the dry season) would be expected to see off. I suggested some time ago to people in conversation that one of the factors that might be involved in the death of short-lived chameleons might be parasites. The reason I argued thus was that I had seen the incredible parasite loads of other species of chameleon after a short time in captivity: worms, protozoans and coccidial spores abounded. I was about to write this article when I came across a paper published in 2019 which examined that very idea—that a low resistance to parasites in Laborde’s Chameleon is what is the proximate cause of death of the adults.
The German group who reported the work from Kirindy joined forces with veterinary colleagues. They found that the parasite load in the alimentary canal increased dramatically during the last three months of life. Males had a greater parasite load internally and externally than females. Some animals were kept in cages—again in their habitat in Madagascar. Those individuals had a lower parasite burden and lived longer than their counterparts living in the wild. The authors concluded that the increased prevalence of gastrointestinal and blood parasites is entirely compatible with less investment in the immune system of these fast-growing, fast reproducing lizards—just as would be predicted from a trade-off between a rapid lifestyle and internal defence and repair.
Males might have been expected to be less affected than females producing eggs. However, it seems that males also put everything into reproduction. There is intense rivalry and bloody combat during the short breeding season as males guard their mates.
The indication of lower parasite loads in, and longer lifespan of, Laborde’s Chameleons kept in captivity in Madagascar suggests the need for further experiments. The animals were fed on invertebrates caught in the wild, some of which would presumably contain parasites. What would happen if, say, newly-hatched individuals were fed on parasite-free livefood? What would be their lifespan and what would they die of?
Finally, this article started off as one about a remarkable chameleon from a remarkable island fauna but it has to end as one about parasites and co-evolution with their hosts. In general, parasites evolve so as to be less lethal to their hosts. They have their own trade-off between going for growth and reproduction and killing the host by taking too much food and causing physical damage. So has co-evolution delivered a suite of parasites that like the chameleon itself go for broke and then in vast numbers lurk in an intermediate species for the onset of the next rainy season?
…and really finally. We did not see Laborde’s Chameleon when we were in southwest Madagascar in 2003. When I realised that was in October I now see why—the eggs were in the ground ready to start hatching in November.
Eckhardt F, Kappeler PM. Kraus C. 2017. Highly variable lifespan in an annual reptile, Labord’s chameleon (Furcifer labordi). Scientific Reports 7: 11397 doi:10.1038/s41598-017-11701-3
Eckhardt F, Strube C, Mathes KA, Mutschmann F, Thiesler H, Kraus C, Kappeler PM. 2019. Parasite burden in a short-lived chameleon, Furcifer labordi. International Journal for Parasitology: Parasites and Wildlife 10, 231-240. https://doi.org/10.1016/j.ijppaw.2019.09.010
Karsten KB, Andriamandimbiarisoa LN, Fox SF, Raxworthy CJ. 2008. Proceedings of the National Academy of Sciences of the USA 105, 8980-8984. doi10.1073pnas.0802468105
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