RUN-OF-THE-MILL ECOLOGY TO SEXUAL BRUTALITY AND EVOLUTION: ANNALS OF AN AROUSED TORTOISE POPULATION

Abstract : The following story offers a humble example of islands as natural laboratories, stressing the significance of insights gained from free-ranging animals in a somewhat simplified context. Two generous data-sharing populations of promiscuous sexually coercive Hermann’s tortoises (Testudo hermanni, a species with delayed maturity [~10 years]) from the Prespa Lake Region in Macedonia were scrutinized. Comparisons between island (Golem Grad, divided into narrow shores and a large plateau) and mainland (Konjsko) populations revealed age-specific life-history trends and behavioural peculiarities. The island context brought to attention very unusual demographic processes, eventually resonating with a seemingly inevitable population doom brought upon by insufferable sexual conflict. Neonates to three-year old tortoises exhibit slow growth and low variation in body size (VBS) among individuals, likely illustrating the impact of a soft shell and lack of parental care. The subsequent gradual approach of a survival plateau (annual survival rate increase: 0.30 to 0.70) parallels a gradual increase in confidence and a slowly hardening shell that promotes better foraging capabilities reflected onto a phase of fast linear growth. Unlike long-lived mammals that are in a hurry to reach maturity at a certain size (lowering VBS) that will increase survival and ensure reproduction during a non-growing adult phase, tortoises have the potential for indeterminate growth (estimated individual asymptotic sizes from incremental growth after maturity on Golem Grad range from ~153 to ~224). When protected by a hard carapace that translates into a survival plateau (0.90) at the age of five, indeterminate growth leaves room for young tortoises to express individuality in growth regimes, promoting an ever increasing VBS prior to adulthood. Size-at-maturity is thus a blurred notion in these tortoises. Testosterone levels and sexual activity indicate that minimal size at maturity in precocious males is somewhere between 115- 120mm straight carapace length (SCL), whereas VBS and literature point to a range of 140-150mm. Clearly some tortoises mature early, while others are in no rush at all. Sexual size dimorphism in the Testudo genus suggests most larger-atmaturity tortoises are likely females; Golem Grad population-mean female asymptotic size estimates make no exception. Nevertheless, actual body sizes on the island do not reflect estimates from incremental growth – the largest individuals are males. At ~100 individuals/ha with an operational sex ratio (OSR [♂/♀]) of ~11, male sexual coercion from constantly aroused tortoises drastically increased female mating costs, wreaking havoc on Golem Grad. Adult survival estimates are considerably higher in males (0.97) than in females (0.84). This is accompanied with low female bodycondition, intense cloacal injuries inflicted by males, that can even push females from the island’s high cliffs. Overall, island females do not live long and are also discouraged from reproduction (dissections data). Even implementing species' average fecundity, simulations predict recruitment insufficiency and a decline in the number of females, exacerbating OSR-bias. Tortoises are long-lived animals; adult cohorts ensure population growth despite environmental fluctuations. Nevertheless, on the island the temporal-variance of adult female survival has succumbed to the pressure stirred up by male sexual coercion and will likely lead to population extinction. Perhaps most surprisingly, cloacal injuries indicate that even immature females (~8 years old) have become the target of the maladaptive sexual appetite of males. After reaching nine years, females that inhabit the island’s macho Plateau (only 5% of adults are females) are harassed and exhibit lower average annual survival probabilities. This unfortunate demographic drift does not seem to be the only consequence of OSR bias and high density – island frustrated males court and mount other males more frequently than females. They even exhibit extravagant sexual behaviours, attempting to copulate with dead conspecifics, empty shells, and stones. Golem Grad tortoises elucidated the first natural example of a “prison effect,” whereby a high population density combined with female deprivation (but not accompanied with abnormal testosterone levels) triggered same-sex sexual behaviours (SSB) as a mere outlet of sexual stimulation. More generally, this supports the hypothesis that SSB can be a nonadaptive consequence of unusual proximate factors rather than reflecting physiological disorders. Finally, SSB may even benefit females by diluting aggressive male mounting efforts among males as well. In light of the expensive conservation endeavours on the endangered Hermann’s tortoises in western Europe, life-history insight gained from Golem Grad tortoises can provide a valuable conservation lesson: taking into account Hermann’s tortoises’ environmental sex determination, captive breeding programs can easily create dense female biased colonies that will stand the best chance of creating a prosperous breeding population in the shortest time. Such valuable advice can reduce conservation costs, and help reverse the artificial separation of fundamental research from conservation, particularly evident in the developing (e.g. Macedonia) and third world. After all, applied conservation should only be the inevitable and likely unavoidable side-effect of research, rather than a short term must!
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Dragan Arsovskic. RUN-OF-THE-MILL ECOLOGY TO SEXUAL BRUTALITY AND EVOLUTION: ANNALS OF AN AROUSED TORTOISE POPULATION. Environmental Sciences. Université de la Rochelle, 2018. English. ⟨tel-02265290⟩

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