Howard L. Snell

Galápagos Birds and Diseases: Invasive Pathogens as Threats for Island Species

Exotic diseases and parasites have caused extinctions on islands and continents, particularly when they spread through assemblages of immunologically naive species. Hawaii has lost a substantial part of its endemic bird fauna since the introduction of avian malaria at the beginning of the 20th century. In contrast, the Galapagos archipelago still possesses its entire endemic avifauna. Several of these Galapagos bird populations are in decline, however, and wildlife managers seek guidance to counteract a potential man-made ecological disaster. We recommend that endemic birds be tested for susceptibility to disease outside the Galapagos so that protection efforts can be better designed to deal with actual threats. At present, the best and perhaps only management option is to protect the isolation of these island communities because treating or vaccinating wild bird populations against diseases is almost impossible. If the isolation of the Galapagos Islands is successful, we will preserve the complete avifauna of an archipelago for the first time in the history of human colonization in the Pacific eco- region.

Intrapopulation variation in predator-avoidance performance of Galápagos lava lizards: The interaction of sexual and natural selection

SummaryThe interaction of sexual and natural selection in shaping variation in defensive behavior was explored via three steps. (1) Three predictions from the hypothesis that varying responses to predation account for intrapopulation variation in locomotory performance and wariness were tested. One measure of locomotory performance and two measures of wariness were compared between lava lizards (Tropidurus albemarlensis) inhabiting sparsely (1% cover) and heavily (33% cover) vegetated areas of Isla Plaza Sur in the Galapagos Archipelago. (2) Variation in morphology was examined to identify proximate mechanisms for differences seen in (1). (3) Levels of predation were compared between males and females to test a prediction from a model explaining the observed variation in defensive behavior. Male, but not female, lizards from sparsely vegetated areas were faster than those from heavily vegetated areas. Both male and female lizards from sparsely vegetated areas were significantly warier than those from heavily vegetated areas. Multiple regression, covariance, and residual analyses identify relatively longer hindlimbs of males as the proximate cause of their greater speed over that of females, rather than differences in body size, but neither body nor hindlimb size account for the microgeographic differences in speed of males. Significantly higher predation on males provided a positive test of the major prediction from our model of selective forces in which sexual selection for territory defense by males favors short approach distances (by minimizing time away from the territory caused by erroneous flight) and leads to natural selection for their increased hindlimb size and speed.

PHYLOGEOGRAPHY AND HISTORY OF GIANT GALAPAGOS TORTOISES

Abstract.— We examined the phylogeography and history of giant Galàpagos tortoise populations based on mito‐chondrial DNA sequence data from 161 individuals from 21 sampling sites representing the 11 currently recognized extant taxa. Molecular clock and geological considerations indicate a founding of the monophyletic Galàpagos lineage around 2–3 million years ago, which would allow for all the diversification to have occurred on extant islands. Founding events generally occurred from geologically older to younger islands with some islands colonized more than once. Six of the 11 named taxa can be associated with monophyletic maternal lineages. One, Geochelone porteri on Santa Cruz Island, consists of two distinct populations connected by the deepest node in the archipelago‐wide phylogeny, whereas tortoises in northwest Santa Cruz are closely related to those on adjacent Pinzón Island. Volcan Wolf, the northernmost volcano of Isabela Island, consists of both a unique set of maternal lineages and recent migrants from other islands, indicating multiple colonizations possibly due to human transport or multiple colonization and partial elimination through competition. These genetic findings are consistent with the mixed morphology of tortoises on this volcano. No clear genetic differentiation between two taxa on the two southernmost volcanoes of Isabela was evident. Extinction of crucial populations by human activities confounds whether domed versus saddleback carapaces of different populations are mono‐ or polyphyletic. Our findings revealed a complex phylogeography and history for this tortoise radiation within an insular environment and have implications for efforts to conserve these endangered biological treasures.

Historical fragmentation of islands and genetic drift in populations of Galápagos lava lizards (Microlophus albemarlensis complex)

The formation of islands following a rise in sea level at the end of Pleistocene is expected to disrupt the equilibrium between genetic drift and gene flow in species with limited ability to disperse. Here, we test the hypothesis that genetic drift in isolation has caused the differentiation of Galápagos lava lizards (Microlophus albemarlensis complex) found on 12 islets that are likely to have been connected to a larger island, Isla Santa Cruz, during the late Pleistocene. Using 11 microsatellite loci, screened on 524 individuals from 17 localities distributed among and within 15 islands, we found marked differences in allelic richness and heterozygosity. Genetic differentiation was strong (global FST = 0.44), with pairwise differences found among populations on islets being larger than differences among three localities sampled within Isla Santa Cruz. As expected under a scenario of drift in isolation, there was a positive correlation of genetic diversity with island size, no relationship between genetic and geographical distance and a strong negative correlation between heterozygosity and measures of genetic differentiation. We conclude that seawater is a significant barrier to gene flow in lava lizards on this timescale. Our results suggest that the shallow diversification of the M. albemarlensis complex is not due to recent gene flow and that genetic drift may have played a substantial role in observed patterns of phenotypic variation among islands.

Life history trade-offs and phenotypic plasticity in the reproduction of Galápagos lava lizards (Microlophus delanonis)

Trade-offs between traits are a fundamental component of life history theory. However, because individuals may differ in the amount of energy available for allocation between traits, expected negative relationships are often difficult to detect or may become positive. The latter can occur when both traits are phenotypically plastic in response to variation in environmental productivity. We tested this hypothesis by analyzing expected trade-offs between egg mass and clutch size, and total clutch mass and post-nesting condition, in a population of Galápagos lava lizards (Microlophus delanonis) that experienced marked annual and seasonal variation in rainfall. Due to its close relationship with overall mass (reproductive plus post-nesting mass), we considered rainfall to be a suitable indicator of environmental productivity. Females that reproduced during periods of low rainfall produced smaller and fewer eggs, and had lower post-nesting body mass independent of body size (snout-vent length). This pattern was found in comparisons both between and within individuals that nested in dry and wet periods, respectively. The relationships between egg mass and clutch size, and total clutch mass and post-nesting mass, were positive when data were combined across years and seasons. Restriction of the analysis to comparisons within time periods (in effect, holding productivity constant), resulted in negative correlations between egg mass and clutch size, and weakened relationships between total clutch mass and post-nesting mass. We conclude that phenotypic plasticity in reproduction obscures life history trade-offs and that plasticity may be more important to the fitness of females than a particular value for an individual reproductive trait.

Genetic analysis of a successful repatriation programme: giant Galápagos tortoises

As natural populations of endangered species dwindle to precarious levels, remaining members are sometimes brought into captivity, allowed to breed and their offspring returned to the natural habitat. One goal of such repatriation programmes is to retain as much of the genetic variation of the species as possible. A taxon of giant Galápagos tortoises on the island of Española has been the subject of a captive breeding–repatriation programme for 33 years. Core breeders, consisting of 12 females and three males, have produced more than 1200 offspring that have been released on Española where in situ reproduction has recently been observed. Using microsatellite DNA markers, we have determined the maternity and paternity of 132 repatriated offspring. Contributions of the breeders are highly skewed. This has led to a further loss of genetic variation that is detrimental to the long–term survival of the population. Modifications to the breeding programme could alleviate this problem.

Island biogeography of Galápagos lava lizards (Tropiduridae: Microlophus): species diversity and colonization of the archipelago.

The “lava lizards” (Microlophus) are distributed throughout the Galápagos Archipelago, and consist of radiations derived from two independent colonizations. The “Eastern Radiation” includes M. bivittatus and M. habeli endemic to San Cristobal and Marchena Islands. The “Western Radiation” includes five to seven historically recognized species distributed across almost the entire Archipelago. We combine dense geographic sampling and multilocus sequence data to estimate a phylogenetic hypothesis for the Western Radiation, to delimit species boundaries in this radiation, and to estimate a time frame for colonization events. Our phylogenetic hypothesis rejects two earlier topologies for the Western Radiation and paraphyly of M. albemarlensis, while providing strong support for single colonizations on each island. The colonization history implied by our phytogeny is consistent with general expectations of an east-to-west route predicted by the putative age of island groups, and prevailing ocean currents in the Archipelago. Additionally, combined evidence suggests that M. indefatigabilis from Santa Fe should be recognized as a full species. Finally, molecular divergence estimates suggest that the two colonization events likely occurred on the oldest existing islands, and the Western Radiation represents a recent radiation that, in most cases, has produced species that are considerably younger than the islands they inhabit.

Population genetics of Galápagos land iguana (genus Conolophus) remnant populations

The Galápagos land iguanas (genus Conolophus) have faced significant anthropogenic disturbances since the 17th century, leading to severe reduction of some populations and the extinction of others. Conservation activities, including the repatriation of captive‐bred animals to depleted areas, have been ongoing since the late 1970s, but genetic information has not been extensively incorporated. Here we use nine species‐specific microsatellite loci of 703 land iguanas from the six islands where the species occur today to characterize the genetic diversity within, and the levels of genetic differentiation among, current populations as well as test previous hypotheses about accidental translocations associated with early conservation efforts. Our analyses indicate that (i) five populations of iguanas represent distinct conservation units (one of them being the recently discovered rosada form) and could warrant species status, (ii) some individuals from North Seymour previously assumed to be from the natural Baltra population appear related to both Isabela and Santa Cruz populations, and (iii) the five different management units exhibit considerably different levels of intrapopulation genetic diversity, with the Plaza Sur and Santa Fe populations particularly low. Although the initial captive breeding programmes, coupled with intensive efforts to eradicate introduced species, saved several land iguana populations from extinction, our molecular results provide objective data for improving continuing in situ species survival plans and population management for this spectacular and emblematic reptile.

Galapagos Islands : Marine iguanas die from trace oil pollution

An oil tanker ran aground on the Galapagos island of San Cristóbal on 17 January 2001, spilling roughly three million litres of diesel and bunker oil. The slick started to spread westwards and was dispersed by strong currents, so only a few marine animals were killed immediately as a result. Here we draw on long-term data sets gathered before the spill to show that a population of marine iguanas (Amblyrhynchus cristatus) on Santa Fe island suffered a massive 62% mortality in the year after the accident, due to a small amount of residual oil contamination in the sea. Another population on the more remote island of Genovesa was unaffected.

Marine iguanas die from trace oil pollution.

An oil tanker ran aground on the Galapagos island of San Cristóbal on 17 January 2001, spilling roughly three million litres of diesel and bunker oil. The slick started to spread westwards and was dispersed by strong currents, so only a few marine animals were killed immediately as a result. Here we draw on long-term data sets gathered before the spill to show that a population of marine iguanas (Amblyrhynchus cristatus) on Santa Fe island suffered a massive 62% mortality in the year after the accident, due to a small amount of residual oil contamination in the sea. Another population on the more remote island of Genovesa was unaffected.