Seed dispersal by Galápagos tortoises

Aim Large‐bodied vertebrates often have a dramatic role in ecosystem function through herbivory, trampling, seed dispersal and nutrient cycling. The iconic Galápagos tortoises (Chelonoidis nigra) are the largest extant terrestrial ectotherms, yet their ecology is poorly known. Large body size should confer a generalist diet, benign digestive processes and long‐distance ranging ability, rendering giant tortoises adept seed dispersers. We sought to determine the extent of seed dispersal by Galápagos tortoises and their impact on seed germination for selected species, and to assess potential impacts of tortoise dispersal on the vegetation dynamics of the Galápagos. Location Galápagos, Ecuador. Methods To determine the number of seeds dispersed we identified and counted intact seeds from 120 fresh dung piles in both agricultural and national park land. To estimate the distance over which tortoises move seeds we used estimated digesta retention times from captive tortoises as a proxy for retention times of wild tortoises and tortoise movement data obtained from GPS telemetry. We conducted germination trials for five plant species to determine whether tortoise processing influenced germination success. Results In our dung sample, we found intact seeds from > 45 plant species, of which 11 were from introduced species. Tortoises defecated, on average, 464 (SE 95) seeds and 2.8 (SE 0.2) species per dung pile. Seed numbers were dominated by introduced species, particularly in agricultural land. Tortoises frequently moved seeds over long distances; during mean digesta retention times (12 days) tortoises moved an average of 394 m (SE 34) and a maximum of 4355 m over the longest recorded retention time (28 days). We did not find evidence that tortoise ingestion or the presence of dung influenced seed germination success. Main conclusions Galápagos tortoises are prodigious seed dispersers, regularly moving large quantities of seeds over long distances. This may confer important advantages to tortoise‐dispersed species, including transport of seeds away from the parent plants into sites favourable for germination. More extensive research is needed to quantify germination success, recruitment to adulthood and demography of plants under natural conditions, with and without tortoise dispersal, to determine the seed dispersal effectiveness of Galápagos tortoises.     

Giant Tortoises as Ecological Engineers: A Long-term Quasi-experiment in the Galápagos Islands

Giant tortoises were once a megafaunal element widespread in tropical and subtropical ecosystems. The role of giant tortoises as herbivores and seed dispersers, however, is poorly known. We evaluated tortoise impacts on Opuntia cactus (Cactaceae) in the Galápagos Islands, one of the last areas where giant tortoises remain extant, where the cactus is a keystone resource for many animals. We contrasted cactus populations immediately inside and outside natural habitats where tortoises had been held captive for several decades. Through browsing primarily and trampling secondarily tortoises strongly reduced densities of small (0.5–1.5 m high) cacti, especially near adult cacti, and thereby reduced densities of cacti in larger size classes. Tortoises also caused a shift from vegetative to sexual modes of reproduction in cacti. We conclude that giant tortoises promote a sparse and scattered distribution in Opuntia cactus and its associated biota in the Galápagos Islands.     

Annotated bibliography of Galapagos botany. Supplement I

This supplement to a bibliography published in 1973 lists 112 new references on Galápagos botany. The availability of accurate information in a new flora of the Galápagos Islands has brought about an increase in botanical research. Very little new work has been done on cryptogams. Many recent studies concentrate on ecology and conservation of the unique Galápagos plants.     

How a heterostylous plant species responds to life on remote islands: a comparative study of the morphology and reproductive biology of Waltheria ovata on the coasts of Ecuador and the Galápagos Islands

Heterostylous reproductive systems are usually absent on oceanic island. Self-compatibility would, generally, be advantageous for long-distance dispersing species, as it provides reproductive assurance when density of mates is low. The heterostylous reproductive system, often associated with an incompatibility system, may be a constraint on the colonization of remote habitats. It is, therefore, surprising that the distylous shrub Waltheria ovata has colonized all of the Galápagos Islands, situated more than a thousand kilometres off the shore of Ecuador. The present study confirmed the reciprocal herkogamy of W. ovata. A comparison of mainland and the Galápagos Island populations showed a reduction in flower size, including distance between anthers and stigmas and size of anthers on the islands. Some reductions are quite large but not significantly different, mainly due to a high degree of variation among populations on the islands. The pin morph of W. ovata has undergone the most radical adaptive changes in morphology. Pollination experiments of W. ovata disclosed a leak in the incompatibility system on the Galápagos Islands, allowing higher selfing rates as well as intra-morph seed set compared to the mainland populations. This was most pronounced in the thrum morph. The deficient distylous reproductive system may be an adaptation to a pollinator and mate sparse environment on the Galápagos Islands. We conclude that the heterostylous mating system has changed in response to colonization of the Galápagos Islands, giving room for reproductive assurance by seed set after selfings and intra-morph pollinations.     

Offspring genetic structure reveals mating and nest infestation behaviour of an invasive parasitic fly (<Emphasis Type="Italic">Philornis downsi</Emphasis>) of Galápagos birds

The natural reproductive behaviour of invasive insects is pivotal knowledge for managing species of ecological or economic concern. We use microsatellites to examine female multiple mating and multiple nest infestations in the introduced parasitic fly, Philornis downsi, which causes high mortality in endemic birds on the Galápagos Islands. We analyse larvae and pupae within 57 nests from Santa Cruz and Floreana Islands in both the highland and lowland habitats. Sib-ship reconstructions of offspring revealed that up to five females may infest a single nest, while multiple mating in females was frequent (65% of reconstructed maternal genotypes), with an average of 1.91 (±0.06 SE) males per female. Genetic relatedness (R) of offspring within nests was generally low, though lowland nests on Floreana had higher R than highland nests. Knowledge of the reproductive behaviour of P. downsi is necessary for modelling appropriate management strategies, in particular, the sterile insect technique, for which success is greatly influenced by female multiple mating.     

Lineage Identification and Genealogical Relationships Among Captive Galápagos Tortoises

Genetic tools have become a critical complement to traditional approaches for meeting short‐ and long‐term goals of ex situ conservation programs. The San Diego Zoo (SDZ) harbors a collection of wild‐born and captive‐born Galápagos giant tortoises (n = 22) of uncertain species designation and unknown genealogical relationships. Here, we used mitochondrial DNA haplotypic data and nuclear microsatellite genotypic data to identify the evolutionary lineage of wild‐born and captive‐born tortoises of unknown ancestry, to infer levels of relatedness among founders and captive‐born tortoises, and assess putative pedigree relationships assigned by the SDZ studbook. Assignment tests revealed that 12 wild‐born and five captive‐born tortoises represent five different species from Isabela Island and one species from Santa Cruz Island, only five of which were consistent with current studbook designations. Three wild‐born and one captive‐born tortoise were of mixed ancestry. In addition, kinship analyses revealed two significant first‐order relationship pairs between wild‐born and captive‐born tortoises, four second‐order relationships (half‐sibling) between wild‐born and captive tortoises (full‐sibs or parent‐offspring), and one second‐order relationship between two captive‐born tortoises. Of particular note, we also reconstructed a first‐order relationship between two wild‐born individuals, violating the founder assumption. Overall, our results contribute to a worldwide effort in identifying genetically important Galápagos tortoises currently in captivity while revealing closely related founders, reconstructing genealogical relationships, and providing detailed management recommendations for the SDZ tortoises. Zoo Biol 31:107;–120, 2012. © 2011 Wiley Periodicals, Inc.     

A cryptic taxon of Galápagos tortoise in conservation peril

As once boldly stated, 'bad taxonomy can kill', highlighting the critical importance of accurate taxonomy for the conservation of endangered taxa. The concept continues to evolve almost 15 years later largely because most legal protections aimed at preserving biological diversity are based on formal taxonomic designations. In this paper we report unrecognized genetic divisions within the giant tortoises of the Galápagos. We found three distinct lineages among populations formerly considered a single taxon on the most populous and accessible island of Santa Cruz; their diagnosability, degree of genetic divergence and phylogenetic placement merit the recognition of at least one new taxon. These results demonstrate the fundamental importance of continuing taxonomic investigations to recognize biological diversity and designate units of conservation, even within long-studied organisms such as Galápagos tortoises, whose evolutionary heritage and contribution to human intellectual history warrant them special attention.     

Evidence that 19-hydroxyandrostenedione is secreted by the adrenal cortex and is under the control of ACTH and the renin-angiotensin system in man

Plasma 19-hydroxyandrostenedione (19-OH-A-dione) concentrations in man were evaluated using a specific and sensitive radioimmunoassay. Plasma 19-OH-A-dione concentrations (mean ± SE) in normal subjects are 151 ± 14 pg/ml (n=13) in males and 141 ± 9 pg/ml (n=14) in females. Plasma 19-OH-A-dione (mean ± SE) rises significantly during ACTH stimulation (116 ± 25 pg/ml vs 288 ± 38 pg/ml; P<0.01; n=5), declines significantly during dexamethasone suppression (180 ± 30 pg/ml vs 36 ± 14 pg/ml; P<0.01; n=4) and rises significantly during angiotensin II infusion (89 ± 10 pg/ml vs 159 ± 27 pg/ml; P<0.05; n=5). Plasma 19-OH-A-dione in the adrenal vein is much higher than that in the inferior vena cava (2076–3076 pg/ml vs 115–184 pg/ml; n=2). These results demonstrate that 19-OH-A-dione is directly secreted by the adrenal cortex and is under the control of ACTH and the renin-angiotensin system.     

Male reproductive success and its behavioural correlates in a polygynous mammal,the Galápagos sea lion (Zalophus wollebaeki)

Sexual selection theory predicts competitive males and choosy females. Nevertheless, since molecular marker‐based studies, paternity outside the expected mating patterns has increasingly been described. Even in highly polygynous systems, where paternity is expected to be strongly skewed towards large, dominant males, alternative mating tactics have been suggested. We examined reproductive success in the polygynous Galápagos sea lion (Zalophus wollebaeki). Semiaquatic territoriality allows females to move freely and may lower the degree of polygyny otherwise suggested by both territorial behaviour and strong sexual dimorphism. We assigned paternities with 22 microsatellites and analysed how male reproductive success was related to size, dominance status, intra‐sexual agonistic behaviour, proximity to females, and attendance in the colony. Male behaviour was consistent across two seasons for all parameters under consideration. Attendance was by far the most important determinant of paternal success. Skew in reproductive success towards large, dominant males was weak and dominance status played no role. This appears to be caused by an extremely long reproductive season lasting five or more months, making it difficult for any male to monopolize receptive females. Females seem to choose displaying males that were present in the colony for a long time rather than dominance per se. Sexual dimorphism in Galápagos sea lions may thus be more influenced by selection for fasting than fighting ability. Our data provide further evidence for alternative mating tactics, as several males gained relatively high reproductive success despite short attendance and hardly any involvement in agonistic interactions.     

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.     

Primary motivations of tourists visiting Galápagos: do tourists visit the archipelago to learn about evolution?

Background

The Galápagos archipelago is known worldwide for its contributions to Charles Darwin’s theory of evolution by natural selection, and the islands continue to support studies in evolutionary biology. Yet despite the strong association of Galápagos with evolutionary biology, it is unknown if tourists—approaching 200,000 individuals annually—come to Galápagos with a specific interest in learning about evolution. Prior work has established that Galápagos National Park guides are proud of the association between the islands and evolution, yet on average do not do well on a test of basic evolutionary concepts. The work described herein is an attempt to clarify, via in-person surveys on tourists during the summer of 2016, whether tourists are motivated to visit Galápagos by an interest in evolution.

Results

Of the 109 tourists who answered the question “How interested were you in this trip to Galápagos?” all but one indicated that they were interested or extremely interested in their trip. Only two mentioned a specific interest in learning about evolution or the relationship between the islands and the history of evolutionary thought. For most people, seeing animals—in general or specifically identified animals such as the giant tortoises—was the primary motivation for coming to Galápagos. Unusual animals, snorkeling, and visiting a remote location all averaged above 4.0 on a 5.0-point scale, indicating that these aspects of the archipelago are very-to-extremely appealing to tourists. When average responses for 22 items were ranked from most to least appealing, evolution-related items came in 14th, 17th, 18th, and 20th. However, consequences of evolutionary processes, such as unusual animals and biodiversity, rank higher than either of the four evolution-specific items.

Conclusions

Given tourists’ primary interest in the islands’ endemic wildlife, we find little reason for concern over the guides’ lack of specific evolution-related content knowledge. More critical to both guides and tourists are the impacts of population growth and increased tourism to the islands. Stakeholders can best serve the interests of the growing tourist population and the vigor of the Galápagos economy via conservation efforts—by developing and supporting programs that mediate the concerns raised by ecologists, protecting the islands’ fragile habitat, and regulating commercial land use. In addition, a better understanding of tourists’ motivations may provide opportunities to explore connecting evolutionary concepts to visitor interests.

     

Fruit and pedicel characters derived from Galápagos Tomatoes’

By relatively simple breeding procedures, seven different modifications of fruit and pedicel have been successfully transferred from wild tomatoes of the Galápagos Islands to large-fruited cultivars. Some of these traits, the majority of which are simply inherited, may have horticultural value. Such introgression from the wild forms is expedited by the remarkable freedom from barriers at any stage of the breeding processes.     

Tantalizing Tortoises and the Darwin-Galápagos Legend

During his historic Galápagos visit in 1835, Darwin spent nine days making scientific observations and collecting specimens on Santiago (James Island). In the course of this visit, Darwin ascended twice to the Santiago highlands. There, near springs located close to the island’s summit, he conducted his most detailed observations of Galápagos tortoises. The precise location of these springs, which has not previously been established, is here identified using Darwin’s own writings, satellite maps, and GPS technology. Photographic evidence from excursions to the areas where Darwin climbed, including repeat photography over a period of four decades, offers striking evidence of the deleterious impact of feral mammals introduced after Darwin’s visit. Exploring the impact that Darwin’s Santiago visit had on his thinking – especially focusing on his activities in the highlands – raises intriguing questions about the depth of his understanding of the evolutionary evidence he encountered while in the Galápagos. These questions and related insights provide further evidence concerning the timing of Darwin’s conversion to the theory of evolution, which, despite recent claims to the contrary, occurred only after his return to England.     

Recent colonization of the Galápagos by the tree Geoffroea spinosa Jacq. (Leguminosae)

This study puts together genetic data and an approximate bayesian computation (ABC) approach to infer the time at which the tree Geoffroea spinosa colonized the Galápagos Islands. The genetic diversity and differentiation between Peru and Galápagos population samples, estimated using three chloroplast spacers and six microsatellite loci, reveal significant differences between two mainland regions separated by the Andes mountains (Inter Andean vs. Pacific Coast) as well as a significant genetic differentiation of island populations. Microsatellites identify two distinct geographical clusters, the Galápagos and the mainland, and chloroplast markers show a private haplotype in the Galápagos. The nuclear distinctiveness of the Inter Andean populations suggests current restricted pollen flow, but chloroplast points to cross‐Andean dispersals via seeds, indicating that the Andes might not be an effective biogeographical barrier. The ABC analyses clearly point to the colonization of the Galápagos within the last 160 000 years and possibly as recently as 4750 years ago (475 generations). Founder events associated with colonization of the two islands where the species occurs are detected, with Española having been colonized after Floreana. We discuss two nonmutually exclusive possibilities for the colonization of the Galápagos, recent natural dispersal vs. human introduction.     

The vector ecology of introduced Culex quinquefasciatus populations,and implications for future risk of West Nile virus emergence in the Galápagos archipelago

Culex quinquefasciatus Say (Diptera: Culicidae), an important vector of West Nile virus (WNV) in the U.S.A., was first detected on the Galápagos Islands (Ecuador) in the 1980s. However, little is known of its ecology, distribution or capacity for arbovirus transmission in the Galápagos. We characterize details of lifecycle (including gonotrophic period), temporal abundance, spatial distribution, vector competence and host‐feeding behaviour. Culex quinquefasciatus was detected on five islands of the Galápagos during 2006–2011. A period of 7–14 days was required for egg–adult emergence; water salinity above 5 ppt was demonstrated to hinder larval development. Blood‐meal analysis indicated feeding on reptiles, birds and mammals. Assessment of WNV vector competency of Galápagos C. quinquefasciatus showed a median infectious dose of 7.41 log₁₀ plaque‐forming units per millilitre and evidence of vertical transmission (minimal filial infection rate of 3.7 per 1000 progeny). The distribution of C. quinquefasciatus across the archipelago could be limited by salt intolerance, and its abundance constrained by high temperatures. Feeding behaviour indicates potential to act as a bridge vector for transmission of pathogens across multiple taxa. Vertical transmission is a potential persistence mechanism for WNV on Galápagos. Together, our results can be used for epidemiological assessments of WNV and target vector control, should this pathogen reach the Galápagos Islands.     

Ten novel dinucleotide microsatellite loci cloned from the Galápagos sea lion (Zalophus californianus wollebaeki) are polymorphic in other pinniped species

We isolated and characterized 10 novel dinucleotide microsatellite loci from the Galápagos sea lion (Zalophus californianus wollebaeki) and tested their amplification utility in four further otariid species (Zalophus californianus californianus, Arctocephalus gazella, Arctocephalus australis and Eumetopias jubatus) and three phocid species (Hydrurga leptonyx, Halichoerus grypus and Phoca vitulina). All of the loci amplified polymorphic polymerase chain reaction (PCR) products in at least three species other than the Galápagos sea lion. These markers will be useful for studies of pinniped mating systems, genetic structure and genetic diversity.     

Introduction history and genetic diversity of the invasive ant <Emphasis Type="Italic">Solenopsis geminata</Emphasis> in the Galápagos Islands

The Galápagos Islands constitute one of the most pristine tropical systems on Earth. However, the complex and fragile equilibrium of native species is threatened by invasive species, among which is one of the most successful ants in the world, the tropical fire ant, Solenopsis geminata. We characterized the genetic structure and diversity of populations of S. geminata in the Galápagos Islands and unravelled the archipelago colonization by combining Bayesian clustering methods and coalescent-based scenario testing. Using 12 microsatellite markers and one mitochondrial DNA fragment (COI), we analysed individuals collected in all main invaded islands of the archipelago and from the native areas in Costa Rica and mainland Ecuador. We also used mitochondrial DNA to infer evolutionary relationships of samples collected in Galápagos Islands, Ecuador, Costa Rica and other Latin American countries. Our results showed that genetic diversity was significantly lower in Galápagos Islands and mainland Ecuador populations when compared to Costa Rican populations, and that samples from Galápagos Islands and mainland Ecuador (Guayaquil) clustered in a single group and all share a single mtDNA haplotype. Approximate Bayesian Computation favoured a scenario assuming that populations from Galápagos Islands diverged from mainland Ecuador. The city of Guyaquil, an obligatory hub for tourism and trade, could act as a bridgehead.     

Characterization of canarypox-like viruses infecting endemic birds in the Galápagos Islands

The presence of avian pox in endemic birds in the Galápagos Islands has led to concern that the health of these birds may be threatened by avipoxvirus introduction by domestic birds. We describe here a simple polymerase chain reaction-based method for identification and discrimination of avipoxvirus strains similar to the fowlpox or canarypox viruses. This method, in conjunction with DNA sequencing of two polymerase chain reaction-amplified loci totaling about 800 bp, was used to identify two avipoxvirus strains, Gal1 and Gal2, in pox lesions from yellow warblers (Dendroica petechia), finches (Geospiza spp.), and Galápagos mockingbirds (Nesomimus parvulus) from the inhabited islands of Santa Cruz and Isabela. Both strains were found in all three passerine taxa, and sequences from both strains were less than 5% different from each other and from canarypox virus. In contrast, chickens in Galápagos were infected with a virus that appears to be identical in sequence to the characterized fowlpox virus and about 30% different from the canarypox/Galápagos group viruses in the regions sequenced. These results indicate the presence of canarypox-like viruses in endemic passerine birds that are distinct from the fowlpox virus infecting chickens on Galápagos. Alignment of the sequence of a 5.9-kb region of the genome revealed that sequence identities among Gal1, Gal2, and canarypox viruses were clustered in discrete regions. This indicates that recombination between poxvirus strains in combination with mutation led to the canarypox-like viruses that are now prevalent in the Galápagos.     

Genetic distinctiveness of brown pelicans (<Emphasis Type="Italic">Pelecanus occidentalis</Emphasis>) from the Galápagos Islands compared to continental North America

We examined population differentiation across a substantial portion of the range of the brown pelican (Pelecanus occidentalis) to assess (1) the genetic distinctness of the Galápagos subspecies (P. o. urinator) and (2) genetic differentiation between subspecies that inhabit the coasts of North and Central America (P. o. californicus and P. o. carolinensis). Birds were sampled from coastal California, coastal Florida, and the Galápagos Islands. Using a 957 bp (bp) fragment of the NADH dehydrogenase subunit 2 (ND2) gene, 661 bp of the mitochondrial control region, and eleven microsatellite loci we characterize population genetic differentiation among 158 brown pelicans. The Galápagos subspecies is genetically distinct from the sampled continental subspecies, possessing a unique ND2 haplotype and unique mitochondrial control region haplotypes. Samples from the two continental subspecies all possessed the same ND2 haplotype and shared four mitochondrial control region haplotypes. Bayesian clustering in STRUCTURE placed the Galápagos subspecies in a distinct genetic group with high probability, but could not differentiate the continental subspecies from one another. Estimates of migration rates from BayesAss indicated substantial migration between continental subspecies, but no migration between the Galápagos subspecies and either continental subspecies. There are clearly two Evolutionarily Significant Units within the range of the brown pelican, which warrants conservation attention. Further investigation should determine how the un-sampled subspecies (P. o. murphyi and P. o. occidentalis) fit into the broader picture.