DIET INFLUENCES LIFE SPAN IN PARROTS (PSITTACIFORMES)

Auk, The, Jan 2006 by Munshi-South, Jason, Wilkinson, Gerald S

ABSTRACT.-

Evolutionary hypotheses regarding longevity predict that life span should increase as extrinsic mortality rates decrease. Specifically, a decline in age-specific survival and fertility should evolve and decrease life span in proportion to the magnitude of the mortality risk. We examined these ideas using a new data set on maximum longevity, ecology, and life history of 162 parrot species (Psittaciformes). Parrots are generally long-lived but exhibit remarkable variation in life span between similar-sized genera, with particularly long-lived species occurring in the Cacatua, Calyptorhynchus, and Amazona. After controlling for both body size and phylogenetic ancestry using a phylogenetic supertree of all 352 parrot species, type of diet and communal roosting explain significant variation in parrot life span, but the influence of communal roosting is statistically dependent on an association with diet type. We suggest that extreme longevity in parrots has evolved in response to species-specific characteristics of diet, habitat, and behavior that influence extrinsic mortality rates. Received 24 July 2004, accepted 8 June 2005.

Key words: life history, longevity, parrots, Psittaciformes.

La Dieta Influencia la Longevidad en los Psittaciformes

RESUMEN.-Las hipótesis evolutivas relacionadas con la longevidad predicen que la duración de la vida debe incrementarse cuando las tasas de mortalidad extrínseca disminuyen. Específicamente, se esperaria una disminución evolutiva en la supervivencia y la fertilidad a edades específicas, causando una disminución en la longevidad proporcional a la magnitud del riesgo de mortalidad. Examinamos estas ideas empleando una base de datos nueva sobre la longevidad máxima, la ecología y las historias de vida de 162 especies de Psittaciformes. Los Psittaciformes son generalmente longevos pero existe amplia variación en la longevidad entre géneros con especies de tamaño corporal similar; las especies particularmente longevas pertenecen a los géneros Cacatua, Calyptorhynchus y Amazona. Luego de controlar por el tamaño corporal y la ancestría filogenética empleando un superárbol filogenético de las 352 especies de Psittaciformes, el tipo de dieta y el uso de perchas comunales explicaron significativamente la variación en la longevidad, pero la influencia del uso de perchas comunales depende estadísticamente de una asociación con el tipo de dieta. Sugerimos que la extrema longevidad de los Psittaciformes ha evolucionado como respuesta a características de la dieta, el hábitat y el comportamiento específicas de las especies que influencian las tasas extrínsecas de mortalidad.

EVOLUTIONARY THEORIES OF longevity predict that average life span should increase as the rate of extrinsic mortality decreases (Austad and Fischer 1991). For example, the ability to fly may contribute to long life span in birds and bats through decreased vulnerability to environmental contingency (Holmes and Austad 1994). Probability of dying from extrinsic factors, such as prédation, disease, or accidents, is believed to influence life span because the force of natural selection decreases with age. If extrinsic sources of mortality are important, then late-acting deleterious mutations in the population will not be exposed to selection, thus accumulating over time. Late-acting deleterious mutations that also have beneficial effects early in life result in antagonistic pleiotropy, and can further influence the evolutionary relationship between aging and extrinsic mortality (Partridge 2001). Under either the mutation-accumulation or antagonistic-pleiotropy mechanism, a decline in age-specific survival and fertility (i.e. senescence) should evolve and decrease life span in proportion to the magnitude of the mortality risk (Austad 1997). In support of this view, the rate of aging has been directly related to the risk of mortality for birds and mammals (Ricklefs 1998, Ricklefs and Scheuerlein 2001).

We present the first comparative examination of the evolution of longevity within the parrots (Psittaciformes). Parrots have been poorly studied in the wild, and a history of association with humans has only recently provided reliable longevity data for many species in captivity (Brouwer et al. 2000). The anecdotal reputation of parrots as very long-lived is not undeserved; they are the longest-lived order of birds for their body size (Prinzinger 1993). Psittacids also exhibit striking variation in life span between similar-sized taxa. We examined the evolution of life span in parrots using modern comparative methods and an extensive new database of longevity, life history, and ecological variables that seemed likely to reflect species differences in the rate of extrinsic mortality. Given this assumption, we predicted that mortality risk is associated with body size, foraging group size, communal roosting, diet type, aridity of habitat, latitude, and restriction to islands.

We predicted that the mortality risk from predation should be lower for larger-bodied species because they should have fewer predators than small-bodied species. Because many parrots are restricted to islands where predation or interspecific competition may be lower than in mainland habitats (Miller et al. 2000), we also predicted that insular species should exhibit greater longevity. We expected parrots with large foraging-group sizes and communal roosting to exhibit longer life spans, because flocking and communal roosting should reduce the per-capita risk of predation through predator dilution, enhanced vigilance, or both. Nesting habits that provide protection from predators (such as cavity- or colonial-nesting) are associated with lower mortality rates (Martin 1995), lower fecundity, and the evolution of longer life span in birds (Owens and Bennett 1995) and bats (cave-roosting; Wilkinson and South 2002). Sociality has been implicated in the extended life spans of some taxa (Carey and Judge 2001), with eusocial insects providing the most convincing case (Keller and Genoud 1997). The gregarious nature of most parrots while foraging or roosting may result in lower extrinsic mortality in unpredictable environments. We also examined the influences of diet type, latitude, and aridity of habitat on longevity, because social behavior and the risk of starvation may be associated with diet, habitat, and foraging behavior (Cannon 1984, Jullien and Clobert 2000).