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Fluctuating Asymmetry As an Early Warning System in the Critically Endangered Taita Thrush

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Fluctuating Asymmetry As an Early Warning System in the Critically Endangered Taita Thrush Fluctuating Asymmetry as an Early Warning System in the Critically Endangered Taita Thrush LUC LENS,*†‡ STEFAN VAN DONGEN,* AND ERIK MATTHYSEN* *Laboratory of Animal Ecology, Department of Biology, University of Antwerp (UIA), Universiteitsplein 1, B-2610 Wilrijk, Belgium †Department of Ornithology, National Museums of Kenya, P.O. Box 40658, Nairobi, Kenya Abstract: Environmental and genetic factors increasingly stress natural populations, and conservationists need simple tools to measure the effect of these stresses before populations become irreversibly affected. The inability of an organism to withstand random perturbations during its development—so-called developmen- tal instability—has been proposed as a potential early indicator of stress. To act as a true early warning sys- tem, however, stress-mediated changes in developmental instability should be manifest in the phenotype be- fore major changes occur in more direct components of fitness. We tested this hypothesis by estimating the survival probabilities of 260 Taita Thrushes ( Turdus helleri) inhabiting three differentially disturbed forest fragments ( little, moderately, and highly deteriorated) and relating these to individual estimates of tarsus asymmetry (a measure of developmental instability), two other putative indices of expected fitness (size and body condition), and a coefficient of inbreeding. Tarsus symmetry, but not survival, was lower in the moder- ately disturbed population than in the least disturbed one, whereas both symmetry and survival were lower in the most disturbed population. Thus, higher levels of habitat disturbance were reflected by increased popu- lation levels of asymmetry before a decrease in survival became apparent. In contrast, none of the other vari- ables showed a significant response to habitat disturbance. At the individual level, asymmetric thrushes showed lower probabilities of survival than more symmetric ones, and the magnitude of the relationship in- creased with habitat disturbance. Birds in better condition (i.e., higher residual body mass) survived better, irrespective of the quality of the habitat. The key finding that stress-mediated increase in fluctuating asymme- try may precede decrease in survival suggests that single-trait asymmetry can serve as an early warning sys- tem in conservation. Fluctuación de Asimetría como un Sistema de Alerta Temprana en el Tordo Taita Críticamente en Peligro Resumen: Los factores ambientales y genéticos incrementan la presión sobre poblaciones naturales, y los conservacionistas requieren de herramientas simples para medir el efectos de esas presiones antes de que afecten a las poblaciones irreversiblemente. La incapacidad de un organismo de soportar perturbaciones ale- atorias durante su desarrollo, la llamada inestabilidad del desarrollo, se ha propuesto como un potencial in- dicador temprano de los efectos de la presión. Sin embargo, para funcionar como un verdadero “sistema de alerta temprana” los cambios en la inestabilidad del desarrollo por la presión deben manifestarse en el fenotipo antes de que ocurran cambios mayores en los componentes más directos de la adaptabilidad. Proba- mos esta hipótesis estimando las probabilidades de supervivencia de 260 tordos Taita ( Turdus helleri) habi- tantes de tres fragmentos de bosque perturbados diferencialmente (deterioro bajo, moderado y alto) y las rel- acionamos con estimaciones individuales de asimetría del tarso (una medida de inestabilidad del desarrollo), con otros dos índices putativos de adaptabilidad esperada (tamaño y condición del cuerpo) y con un coefi- ciente de endogamia. La simetría del tarso, pero no la supervivencia, fue menor en la población moderada- mente perturbada que en la menos perturbada, mientras que tanto la simetría como la supervivencia fueron menores en la población más perturbada. Así, los mayores niveles de perturbación de hábitat reflejaron un incremento en los niveles de asimetría antes de que fuera aparente una disminución en la supervivencia. En contraste, ninguna de las otras variables mostró respuesta significativa a la perturbación del hábitat. A nivel ‡email [email protected] Paper submitted December 1, 2000; revised manuscript accepted May 20, 2001. 479 Conservation Biology, Pages 479–487 Volume 16, No. 2, April 2002 480 Asymmetry and survival in T. helleri Lens et al. individual, los tordos asimétricos tuvieron menor probabilidad de supervivencia en comparación con los simétricos, con lo que la magnitud de la relación se incrementó con la perturbación del hábitat. Aves con me- jor condición (es decir, mayor masa corporal residual) sobrevivieron mejor, independientemente de la cal- idad del hábitat. El hallazgo clave de que el incremento de la asimetría fluctuante debido a la presión puede preceder una disminución de la supervivencia sugiere que la asimetría de un solo carácter puede funcionar como un sistema de alerta tempana en conservación. Introduction not destructive, it has become a popular measure of the quality and health of individuals and populations (re- As the loss and deterioration of indigenous habitat in- views by Markow 1995; Leung & Forbes 1996; Møller creasingly stresses natural populations, ecologists need 1997a; Clarke 1998b; Møller & Thornhill 1998). Al- simple estimators to measure their impact (Cairns et al. though population-level FA generally increases with ex- 1993). In particular, they are challenged to identify pop- posure to stressors of environmental or genetic origin ulations subject to stress before these populations are ir- (or underlying processes such as the mating system or reversibly affected, because this would greatly increase population structure that are manifested in a measurable the effectiveness of conservation programs (Leary & Al- genetic response) (Parsons 1990, 1992; Palmer & Stro- lendorf 1989; Clarke 1995a). Developmental instability, beck 1992; Manning & Chamberlain 1994; Polak & Triv- the inability of an organism to withstand random pertur- ers 1994; Møller & Swaddle 1997; but see Bjorksten et bations during its development, could be such an esti- al. 2000), relationships between FA and fitness are mator (Leary & Allendorf 1989; Kieser & Groeneveld highly heterogeneous among studies, often weak, and at 1991; Palmer & Strobeck 1992; Parsons 1992; Clarke present poorly understood (Leung & Forbes 1996, 1997a, 1993, 1995a; Polak & Trivers 1994). Developmental in- 1997b; Clarke 1998a; Dufour & Weatherhead 1998; but stability may be a more sensitive estimator than tradi- for a different opinion see Møller 1999). tional life-history traits such as survival (Clarke & Mc- Inconsistency in the reported relationships of FA with Kenzie 1992) because organisms under stress may need other variables of interest has been attributed to a vari- to allocate more energy to processes necessary to survival, ety of causes, such as weak between-trait correlation or hence compromising the maintenance of their develop- low repeatability of individual FA estimates (Leamy mental stability (Sommer 1996). For developmental in- 1993; Whitlock 1996; Houle 1997; Clarke 1998b; Van stability to predict future stress-mediated changes in di- Dongen 1998a, 1998b), or an admixture of “true” FA rect components of fitness—which are often more with other types of bilateral asymmetry that may have a cumbersome to measure—and hence use as an “early genetic basis (Palmer & Strobeck 1992; Palmer 1994; warning system” (sensu Clarke 1995a)—the following as- Van Dongen et al. 1999a; Lens & Van Dongen 2000). sumptions need to be fulfilled: (1) individuals are subject Consequently, it has been argued that FA in individuals to biologically relevant stress(es) and suffer a significant may not be a universal measure of quality or fitness and decrease in fitness under severe stress; (2) increased ex- that other phenotypic measures, such as mean or maxi- posure to stress is reflected in increased levels of devel- mum trait size (Hunt & Simmons 1997; Bennett & Hoff- opmental instability; and (3) stress-mediated changes in mann 1998; David et al. 1998; Van Dongen et al. 1999c; developmental instability are manifest in the phenotype Woods et al. 1999; Bjorksten et al. 2000) or measures of before major changes occur in more direct components organismal condition (Leung & Forbes 1997b; Dufour & of fitness, such as survival or fecundity. Weatherhead 1998; Gage 1998), might perform better. The degree of developmental instability among indi- Although newly developed programs accommodate viduals and populations is most commonly expressed by most of the statistical problems intrinsic to estimation of their level of fluctuating asymmetry (FA; Ludwig 1932). individual developmental instability (review by Van The underlying assumptions of FA analysis are that the Dongen et al. 2002), nonstatistical factors such as trade- development of both sides of bilaterally symmetrical offs between different fitness components may further traits is influenced by identical genes, that nondirec- confound attempts at finding universal relationships be- tional differences between the sides are of environmen- tween asymmetry and fitness (M. Tracy, C. Freeman, T. tal origin and reflect accidents during development, and Huff, A. Alados, & J. Graham, unpublished data). Be- that high levels of FA indicate high levels of develop- sides, phenotypic quality is a function of both genetic mental instability (Clarke 1993; Palmer 1994; Møller and environmental factors. Whereas in stressful environ- 1997a). Because the measurement and
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