Zoogeography of Pacific Ocean islands: a comparison of the rotifer faunas of Easter Island and the Galápagos archipelago

During September 1990, an extensive sampling of the freshwaters of Easter Island was conducted. The resulting list of rotifer species, supplemented by taxa present in samples collected during a previous trip to the island, is compared with that of another oceanic island of volcanic origin, namely Santa Cruz, Galápagos archipelago. In spite of less research, Santa Cruz has a richer rotifer fauna which, unlike Easter Island, includes endemic species. Possible causes for the faunal poverty of Easter Island are: large source-to-target distance, small target size, uniformity of the target island's ecosystems and limited age of its aquatic biotopes.     

A hitchhikers guide to the Galápagos: co-phylogeography of Galápagos mockingbirds and their parasites

Background

Parasites are evolutionary hitchhikers whose phylogenies often track the evolutionary history of their hosts. Incongruence in the evolutionary history of closely associated lineages can be explained through a variety of possible events including host switching and host independent speciation. However, in recently diverged lineages stochastic population processes, such as retention of ancestral polymorphism or secondary contact, can also explain discordant genealogies, even in fully co-speciating taxa. The relatively simple biogeographic arrangement of the Galápagos archipelago, compared with mainland biomes, provides a framework to identify stochastic and evolutionary informative components of genealogic data in these recently diverged organisms.

Results

Mitochondrial DNA sequences were obtained for four species of Galápagos mockingbirds and three sympatric species of ectoparasites - two louse and one mite species. These data were complemented with nuclear EF1α sequences in selected samples of parasites and with information from microsatellite loci in the mockingbirds. Mitochondrial sequence data revealed differences in population genetic diversity between all taxa and varying degrees of topological congruence between host and parasite lineages. A very low level of genetic variability and lack of congruence was found in one of the louse parasites, which was excluded from subsequent joint analysis of mitochondrial data. The reconciled multi-species tree obtained from the analysis is congruent with both the nuclear data and the geological history of the islands.

Conclusions

The gene genealogies of Galápagos mockingbirds and two of their ectoparasites show strong phylogeographic correlations, with instances of incongruence mostly explained by ancestral genetic polymorphism. A third parasite genealogy shows low levels of genetic diversity and little evidence of co-phylogeny with their hosts. These differences can mostly be explained by variation in life-history characteristics, primarily host specificity and dispersal capabilities. We show that pooling genetic data from organisms living in close ecological association reveals a more accurate phylogeographic history for these taxa. Our results have implications for the conservation and taxonomy of Galápagos mockingbirds and their parasites.     

Phylogeography of the Galápagos hawk (Buteo galapagoensis): a recent arrival to the Galápagos Islands

Galápagos hawks (Buteo galapagoensis) are one of the most inbred bird species in the world, living in small, isolated island populations. We used mitochondrial sequence and nuclear minisatellite data to describe relationships among Galápagos hawk populations and their colonization history. We sampled 10 populations (encompassing the entire current species range of nine islands and one extirpated population), as well as the Galápagos hawk's closest mainland relative, the Swainson's hawk (B. swainsoni). There was little sequence divergence between Galápagos and Swainson's hawks (only 0.42% over almost 3kb of data), indicating that the hawks colonized Galápagos very recently, likely less than 300,000 years ago, making them the most recent arrivals of the studied taxa. There were only seven, closely related Galápagos hawk haplotypes, with most populations being monomorphic. The mitochondrial and minisatellite data together indicated a general pattern of rapid population expansion followed by genetic isolation of hawk breeding populations. The recent arrival, genetic isolation, and phenotypic differentiation among populations suggest that the Galápagos hawk, a rather new species itself, is in the earliest stages of further divergence.     

Phylogeography and history of giant Galápagos 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.     

Pollination patterns and plant breeding systems in the Galápagos: a review

Background

Despite the importance of the Galápagos Islands for the development of central concepts in ecology and evolution, the understanding of many ecological processes in this archipelago is still very basic. One such process is pollination, which provides an important service to both plants and their pollinators. The rather modest level of knowledge on this subject has so far limited our predictive power on the consequences of the increasing threat of introduced plants and pollinators to this unique archipelago.

Scope

As a first step toward building a unified view of the state of pollination in the Galápagos, a thorough literature search was conducted on the breeding systems of the archipelago''s flora and compiled all documented flower–visitor interactions. Based on 38 studies from the last 100 years, we retrieved 329 unique interactions between 123 flowering plant species (50 endemics, 39 non-endemic natives, 26 introduced and eight of unknown origin) from 41 families and 120 animal species from 13 orders. We discuss the emergent patterns and identify promising research avenues in the field.

Conclusions

Although breeding systems are known for <20 % of the flora, most species in our database were self-compatible. Moreover, the incidence of autogamy among endemics, non-endemic natives and alien species did not differ significantly, being high in all groups, which suggests that a poor pollinator fauna does not represent a constraint to the integration of new plant species into the native communities. Most interactions detected (approx. 90 %) come from a single island (most of them from Santa Cruz). Hymenopterans (mainly the endemic carpenter bee Xylocopa darwinii and ants), followed by lepidopterans, were the most important flower visitors. Dipterans were much more important flower visitors in the humid zone than in the dry zone. Bird and lizard pollination has been occasionally reported in the dry zone. Strong biases were detected in the sampling effort dedicated to different islands, time of day, focal plants and functional groups of visitors. Thus, the existing patterns need to be confronted with new and less biased data. The implementation of a community-level approach could greatly increase our understanding of pollination on the islands and our ability to predict the consequences of plant invasions for the natural ecosystems of the Galápagos.     

Colonization and diversification of Galápagos terrestrial fauna: a phylogenetic and biogeographical synthesis

Remote oceanic islands have long been recognized as natural models for the study of evolutionary processes involved in diversification. Their remoteness provides opportunities for isolation and divergence of populations, which make islands remarkable settings for the study of diversification. Groups of islands may share a relatively similar geological history and comparable climate, but their inhabitants experience subtly different environments and have distinct evolutionary histories, offering the potential for comparative studies. A range of organisms have colonized the Galápagos Islands, and various lineages have radiated throughout the archipelago to form unique assemblages. This review pays particular attention to molecular phylogenetic studies of Galápagos terrestrial fauna. We find that most of the Galápagos terrestrial fauna have diversified in parallel to the geological formation of the islands. Lineages have occasionally diversified within islands, and the clearest cases occur in taxa with very low vagility and on large islands with diverse habitats. Ecology and habitat specialization appear to be critical in speciation both within and between islands. Although the number of phylogenetic studies is continuously increasing, studies of natural history, ecology, evolution and behaviour are essential to completely reveal how diversification proceeded on these islands.     

Hematology, serum chemistry, and serology of Galápagos penguins (Spheniscus mendiculus) in the Galápagos Islands, Ecuador

The Galápagos penguin (Spheniscus mendiculus) is an endangered species endemic to the Galápagos Islands, Ecuador. In 2003 and 2004, 195 penguins from 13 colonies on the islands of Isabela and Fernandina in the Galápagos archipelago were examined. Genetic sexing of 157 penguins revealed 62 females and 95 males. Hematology consisted of packed cell volume (n = 134), white blood cell differentials (n = 83), and hemoparasite blood smear evaluation (n = 114). Microfilariae were detected in 22% (25/114) of the blood smears. Female penguins had significantly higher eosinophil counts than males. Serum chemistry on 83 penguins revealed no significant differences between males and females. Birds were seronegative to avian paramyxovirus type 1-3, avian influenza virus, infectious bursal disease virus, Marek's disease virus (herpes), reovirus, avian encephalomyelitis virus, and avian adenovirus type 1 and 2 (n = 75), as well as to West Nile virus (n = 87), and Venezuelan, western and eastern equine encephalitis viruses (n = 26). Seventy-five of 84 (89%) penguins had antibodies to Chlamydophila psittaci but chlamydial DNA was not detected via polymerase chain reaction in samples from 30 birds.     

A comparison of genetic diversity between the Galápagos Penguin and the Magellanic Penguin

The Galápagos Penguin (Spheniscusmendiculus) is a United States federallylisted endangered species with populations onthe Galápagos Islands of Fernandina andIsabela. Although the waters around theislands are normally productive, lowproductivity during El Niño years resultsin high adult penguin mortality and lowrecruitment in following years. We usedmicrosatellite markers developed for Spheniscus penguins to study the long termgenetic effects of serial bottleneck events inthe Galápagos Penguin, and compared thisvariation to that of its congener, theMagellanic penguin (Spheniscusmagellanicus). The observed heterozygosityfor the Galápagos Penguin was 3%,significantly lower than the 46%heterozygosity of the Magellanic Penguin. Thislow level of heterozygosity is directly relatedto its low effective population size. Whilethis population has survived long term,presumably without high levels of geneticvariation, we feel that the greater frequencyof El Niño events, coupled with increasedhuman impacts such as introduced disease, oildischarge, and competition with fisheries, mayput the species in particular danger ofextinction.     

Origin and population history of a recent colonizer, the yellow warbler in Galápagos and Cocos Islands

The faunas associated with oceanic islands provide exceptional examples with which to examine the dispersal abilities of different taxa and test the relative contribution of selective and neutral processes in evolution. We examine the patterns of recent differentiation and the relative roles of gene flow and selection in genetic and morphological variation in the yellow warbler (Dendroica petechia aureola) from the Galápagos and Cocos Islands. Our analyses suggest aureola diverged from Central American lineages colonizing the Galápagos and Cocos Islands recently, likely less than 300 000 years ago. Within the Galápagos, patterns of genetic variation in microsatellite and mitochondrial markers suggest early stages of diversification. No intra-island patterns of morphological variation were found, even across steep ecological gradients, suggesting that either (i) high levels of gene flow may be homogenizing the effects of selection, (ii) populations may not have had enough time to accumulate the differences in morphological traits, or (iii) yellow warblers show lower levels of 'evolvability' than some other Galápagos species. By examining genetic data and morphological variation, our results provide new insight into the microevolutionary processes driving the patterns of variation.     

Phylogeographic history and gene flow among giant Galápagos tortoises on southern Isabela Island

Volcanic islands represent excellent models with which to study the effect of vicariance on colonization and dispersal, particularly when the evolution of genetic diversity mirrors the sequence of geological events that led to island formation. Phylogeographic inference, however, can be particularly challenging for recent dispersal events within islands, where the antagonistic effects of land bridge formation and vicariance can affect movements of organisms with limited dispersal ability. We investigated levels of genetic divergence and recovered signatures of dispersal events for 631 Galápagos giant tortoises across the volcanoes of Sierra Negra and Cerro Azul on the island of Isabela. These volcanoes are among the most recent formations in the Galápagos (<0.7 million years), and previous studies based on genetic and morphological data could not recover a consistent pattern of lineage sorting. We integrated nested clade analysis of mitochondrial DNA control region sequences, to infer historical patterns of colonization, and a novel Bayesian multilocus genotyping method for recovering evidence of recent migration across volcanoes using eleven microsatellite loci. These genetic studies illuminate taxonomic distinctions as well as provide guidance to possible repatriation programs aimed at countering the rapid population declines of these spectacular animals.     

Ecosystem resilience and threshold response in the Galápagos coastal zone

Background

The Intergovernmental Panel on Climate Change (IPCC) provides a conservative estimate on rates of sea-level rise of 3.8 mm yr⁻¹ at the end of the 21^st century, which may have a detrimental effect on ecologically important mangrove ecosystems. Understanding factors influencing the long-term resilience of these communities is critical but poorly understood. We investigate ecological resilience in a coastal mangrove community from the Galápagos Islands over the last 2700 years using three research questions: What are the ‘fast and slow’ processes operating in the coastal zone? Is there evidence for a threshold response? How can the past inform us about the resilience of the modern system?

Methodology/Principal Findings

Palaeoecological methods (AMS radiocarbon dating, stable carbon isotopes (δ¹³C)) were used to reconstruct sedimentation rates and ecological change over the past 2,700 years at Diablas lagoon, Isabela, Galápagos. Bulk geochemical analysis was also used to determine local environmental changes, and salinity was reconstructed using a diatom transfer function. Changes in relative sea level (RSL) were estimated using a glacio-isostatic adjustment model. Non-linear behaviour was observed in the Diablas mangrove ecosystem as it responded to increased salinities following exposure to tidal inundations. A negative feedback was observed which enabled the mangrove canopy to accrete vertically, but disturbances may have opened up the canopy and contributed to an erosion of resilience over time. A combination of drier climatic conditions and a slight fall in RSL then resulted in a threshold response, from a mangrove community to a microbial mat.

Conclusions/Significance

Palaeoecological records can provide important information on the nature of non-linear behaviour by identifying thresholds within ecological systems, and in outlining responses to ‘fast’ and ‘slow’ environmental change between alternative stable states. This study highlights the need to incorporate a long-term ecological perspective when designing strategies for maximizing coastal resilience.     

Review Oribatid mites of the Galápagos Islands – faunistics, ecology and speciation

The results from investigations on oribatid mites of the Galápagos archipelago during 10 years are presented. Samples were taken on all larger and most smaller islands of the archipelago, as well as in all vegetation zones and some special habitats such as grass or cactus litter and fumaroles. A total of 202 oribatid species belonging to 64 families were encountered; among them 81 species are new to science. The Oribatida occur from the littoral zone to the summit of the volcanoes. Diversity and abundance increases from the arid to the moister zones at higher elevations. Most species prefer moist habitats at medium to higher elevations of the islands, in some parts reaching remarkably high abundances (in the Scalesia zone of Santa Cruz approximately 18 000 individuals m–2). The species richness of an island depends on the altitude and number of available habitats rather than the area of the island. Many oribatid species on the Galápagos Islands have a wide biogeographical distribution. The majority originate from the Central and South American mainland, but several Pacific and even Holarctic elements were also found. In comparison with the species composition of the adjacent mainland, the oribatid mite fauna of the Galápagos Islands can be regarded as disharmonic. Sea surface transportation has been proved at least between the islands, which also applies to oribatid species living at higher elevations. Long distance dispersal can be assumed to be mainly hydrochorous. The oribatid fauna of the littoral and arid vegetation zones is presented in detail. Some species even inhabit such extreme habitats as warm fern litter in fumaroles or hot volcanic soils. Others were mainly found in or near agricultural areas, suggesting human introduction. Striking distribution patterns within the archipelago are discussed. The distribution of endemic forms in the genera Aeroppia, Scapheremaeus, Scheloribates and Cultrobates indicates both speciation on different islands, as well as speciation on the same island by occupying different habitats.     

Population Genetic Structure and Conservation of the Galápagos Petrel (Pterodroma phaeopygia)

The Galápagos petrel (Pterodroma phaeopygia) is endemic to the Galápagos archipelago, where it is known to breed only on five islands. The species has been listed as critically endangered due to habitat deterioration and predation by introduced mammals. Significant morphological and behavioural differences among petrels nesting on different islands suggest that island populations may differ genetically. Furthermore, nesting phenology suggests that genetically differentiated seasonal populations may exist within at least one island. We analysed variation in six microsatellite loci and part of the mitochondrial ATPase 6/8 gene in 206 Galápagos petrels sampled from all five islands. No evidence of genetic structuring within islands was found, although statistical power was low. In contrast, significant differences occurred among island populations. For the microsatellite loci, private alleles occurred at all islands, sometimes at high frequency; global and pairwise estimates of genetic differentiation were all statistically significant; Bayesian analysis of genotypes frequencies provided strong support for three genetic populations; and most estimates of migration between populations did not differ significantly from zero. Only two ATPase haplotypes were found, but the geographic distribution of haplotypes indicated significant differentiation among populations. For conservation purposes, populations from Floreana, Santa Cruz, San Cristóbal and Santiago should be regarded as separate genetic management units. Birds from Isabela appear to be derived recently from the Santiago population, and the population on San Cristóbal appears to be a mixture of birds from other populations. However, considering ecological and behavioural differences among birds from different islands, we recommend that all five populations be protected.     

Plant community composition and structural characteristics of an invaded forest in the Galápagos

Non-native species have invaded habitats worldwide, greatly impacting the structure and function of native communities and ecosystems. To better understand mechanisms of invasion impacts and how to restore highly impacted and transformed ecosystems, studies are needed that evaluate invader effects on both biotic communities and structural characteristics. On Santa Cruz Island in Galápagos we compared biotic (plant species richness, diversity, and community composition) and structural (canopy openness, forest height, and leaf litter) characteristics of a relic forest dominated by an endemic and highly threatened tree and a forest dominated by an invasive tree. The forests are located within the historical distribution of the endemic tree, which now occupies only 1% of its original extent. We found that the invaded forest had 42% lower native plant species richness and 17% less plant diversity than the endemic tree dominated forest. Additionally, with the invader there was 36% greater non-native plant species richness, 37% higher non-native plant diversity, and highly dissimilar plant composition when compared to the endemic-dominated forest. Additionally, the invaded forest had a more open and taller tree canopy and greater leaf litter cover than native forest. The presence of the invasive tree and the associated forest structural changes were the primary factors in models that best explained higher non-native diversity in the invaded forest. Our correlational results suggest that an invasive tree has significantly altered plant assemblage and forest structural characteristics in this unique ecosystem. Experiments that remove the invader and evaluate native plant community responses are needed to identify thresholds for practical restoration of this threatened and biologically unique native forest.     

Morphometrics Parallel Genetics in a Newly Discovered and Endangered Taxon of Galápagos Tortoise

Galápagos tortoises represent the only surviving lineage of giant tortoises that exhibit two different types of shell morphology. The taxonomy of Galápagos tortoises was initially based mainly on diagnostic morphological characters of the shell, but has been clarified by molecular studies indicating that most islands harbor monophyletic lineages, with the exception of Isabela and Santa Cruz. On Santa Cruz there is strong genetic differentiation between the two tortoise populations (Cerro Fatal and La Reserva) exhibiting domed shell morphology. Here we integrate nuclear microsatellite and mitochondrial data with statistical analyses of shell shape morphology to evaluate whether the genetic distinction and variability of the two domed tortoise populations is paralleled by differences in shell shape. Based on our results, morphometric analyses support the genetic distinction of the two populations and also reveal that the level of genetic variation is associated with morphological shell shape variation in both populations. The Cerro Fatal population possesses lower levels of morphological and genetic variation compared to the La Reserva population. Because the turtle shell is a complex heritable trait, our results suggest that, for the Cerro Fatal population, non-neutral loci have probably experienced a parallel decrease in variability as that observed for the genetic data.     

Cryptic structure and niche divergence within threatened Galápagos giant tortoises from southern Isabela Island

Although Galápagos giant tortoises are an icon for both human-mediated biodiversity losses and conservation management successes, populations of two species on southern Isabela Island (Chelonoidis guntheri, and C. vicina) remain threatened by hunting and persistence of feral animals. Conservation management of these tortoises has been hampered by lack of clarity regarding their taxonomy, ecological and morphological diversity, and the spatial distribution of evolutionarily significant units that may exist. Analyses of 16 microsatellite loci did not group samples according to current taxonomy. Instead, three (rather than two) genetic clusters were revealed. We show that the three regions of southern Isabela associated with these genetic clusters are significantly different in their ecological niches, which could suggest that ecological divergence may have shaped patterns of genetic differentiation in these tortoises. Furthermore, results suggest limited recent gene flow among sampled localities and between each of the three regions associated with genetic clusters. We discuss the need for further research on the ecological factors shaping the genetic and morphological diversity of southern Isabela tortoises. We suggest that current strategies whereby populations are managed separately are warranted pending further study, but due to mixed ancestry we recommend that Cerro Paloma tortoises be excluded from management programs.     

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 Espa?ola 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 Espa?ola 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.     

Understanding the colonization history of the Galápagos flycatcher (Myiarchus magnirostris)

The Galápagos archipelago has never been connected to any continental land masses, so it is of interest to know the colonization and diversification history of its endemic species. We analyzed the phylogenetic placement of the endemic Galápagos flycatcher, M. magnirostris, within Myiarchus by using the genes ND2 and cytb (1970 bp) to compare 16 of the 22 species that comprise this genus. We also analyzed variability in cytb sequences from 154 M. magnirostris individuals captured on seven Galápagos islands. Our phylogenetic analyses recovered the two main Myiarchus clades that had been described by previous genetic, morphological, and vocal analyses. M. magnirostris is monophyletic and its closest living relative is M. tyrannulus from Mexico and Central America. The average age for the split node between these two groups was approximately 850,000 years (95% C.I. 630,735-1,087,557). M. tyrannulus, M. nugator, M. nuttingi, M. sagrae, and M. stolidus are not monophyletic species. Within M. magnirostris itself, we found low nucleotide and haplotype diversities (π=0.0009 and h=0.4913, respectively) and a high genetic structure among populations. We also detected a star-shaped haplotype network and significantly negative values for Tajima's D and Fu's Fs for this species. Our results suggest that M. magnirostris originated from a single colonization event and had a recent population expansion in the Galápagos archipelago.