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.     

Cutlassfishes of the genusLepidopus (Trichiuridae), with two new eastern pacific species

Three of the five known species ofLepidopus occur in the eastern Pacific.Lepidopus manis sp. nov. is described from a single specimen from the Galápagos Islands. The holotype ofL. xantusi Goode et Bean, 1895, supposedly from Cape San Lucas, Lower California, is shown to be conspecific withL. caudatus (Euphrasen, 1788). The species heretofore reported under the nameL. xantusi is described, and namedL. fitchi sp. nov. It ranges from Oregon to the Gulf of California and occurs disjunctly in southern Ecuador and northern Peru. A key to the described species ofLepidopus is given and certain morphological features ofL. caudatus are described. Geographic variability ofL. caudatus andL. fitchi is discussed.     

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.     

Protective and injuring action of visible light on photosynthetic apparatus in wheat plants during hyperthermia treatment

Illumination of wheat (Triticum aestivum L.) leaves during heat treatment produced either additional injury or protection of photosynthetic apparatus depending on irradiance and the heating dose. Furthermore, illumination of leaves during hyperthermia exerted differential impacts on thermal tolerances of photosynthesis and photosystem II-driven electron transport assessed from the reduction of 2,6-dichlorophenolindophenol (DCPIP). Measurements with infrared gas analyzer showed that mild heating of leaves in darkness (10 min at 38–40°C) had stronger inhibitory effect on CO₂ uptake than heating of leaves exposed to low and moderate complex irradiances (3–30 klx), as well as excessive irradiance (75–100 klx). When the leaves were heated at higher temperatures (42–44°C), the low and moderate irradiances had a protective action, while high-intensity light aggravated the inhibition of photosynthesis. Illumination of leaves with weak light during heat treatment mitigated the impairment of chloroplast ultrastructure, whereas irradiation with high-intensity light (100 klx) destroyed the sensitive population of chloroplasts. The heat-stimulated photoinhibition was stronger for leaf photosynthesis than for DCPIP reduction in chloroplasts isolated from heat-treated leaves. No correlation was observed between the extent of violaxanthin deepoxidation, zeaxanthin accumulation, and the protective effect of light on photosynthetic apparatus during heat treatments.     

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.     

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.     

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.     

Low MHC variation in the endangered Galápagos penguin (<Emphasis Type="Italic">Spheniscus mendiculus</Emphasis>)

The major histocompatibility complex (MHC) is one of the most polymorphic regions of the genome, likely due to balancing selection acting to maintain alleles over time. Lack of MHC variability has been attributed to factors such as genetic drift in small populations and relaxed selection pressure. The Galápagos penguin (Spheniscus mendiculus), endemic to the Galápagos Islands, is the only penguin that occurs on the equator. It relies upon cold, nutrient-rich upwellings and experiences severe population declines when ocean temperatures rise during El Niño events. These bottlenecks, occurring in an already small population, have likely resulted in reduced genetic diversity in this species. In this study, we used MHC class II exon 2 sequence data from a DRB1-like gene to characterize the amount of genetic variation at the MHC in 30 Galápagos penguins, as well as one Magellanic penguin (S. magellanicus) and two king penguins (Aptenodytes patagonicus), and compared it to that in five other penguin species for which published data exist. We found that the Galápagos penguin had the lowest MHC diversity (as measured by number of polymorphic sites and average divergence among alleles) of the eight penguin species studied. A phylogenetic analysis showed that Galápagos penguin MHC sequences are most closely related to Humboldt penguin (Spheniscus humboldti) sequences, its putative sister species based on other loci. An excess of non-synonymous mutations and a pattern of trans-specific evolution in the neighbor-joining tree suggest that selection is acting on the penguin MHC.     

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.     

Nocturnal and diurnal pollination of Clerodendrum molle (Verbenaceae) in the Gal��pagos Islands

The primary hypothesis of this study was that in the Galápagos Islands, fruit and seed set via nocturnal pollination would exceed that of diurnal pollination because of the greater insect activity at night typical of hot, arid regions. Clerodendrum molle, a widespread member of the Galápagos flora was submitted to pollination experiments, visitor observations, nectar sampling, pollen transfer studies, pollen?Covule ratio studies, and pollen measurements. Flowers set fruit and seed via open pollination, autonomous autogamy, facilitated autogamy, facilitated cross-pollination, diurnal pollination, and nocturnal pollination. Results indicate no significant difference in fruit set. Cross-pollinated flowers showed a significant increase in seed set over all treatments except facilitated autogamy. Nocturnal and diurnal fruit and seed set did not differ significantly. Nocturnal visitors included ants, spiders, hawk moths, and roaches whereas diurnal visitors included carpenter bees and ants. Galápagos members of C. molle exhibit incomplete protandry and set fruit via autonomous autogamy as a result of natural selection in an environment with few faithful pollinators. Overall low fruit and seed set are likely because of a combination of pollen and resource limitation, the latter exacerbated by nectar robbing. Studies of island angiosperms are crucial for complete understanding of the population dynamics of indigenous plants, which can assist conservation officials in protecting these species.     

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.     

Photosynthesis in frost-hardened and frost-stressed leaves of Hedera helix L.

Abstract The purpose of this study was to determine the respective extents to which winter reduction of photosynthetic capacity in ivy (Hedera helix L.) is caused by direct frost injury to the photosynthetic apparatus and by preceding protoplasmic changes connected with the acquisition of frost tolerance. Potted juvenile ivy plants were placed in the open under natural weather conditions whilst others were hardened under controlled conditions and subjected to the desired frost stress. Low non-freezing temperatures induced frost tolerance in ivy leaves down to about – 12°C (50% injury = TL₅₀) without impairing net photosynthetic rate as measured under standard conditions (20°C, light saturation, natural CO₂ level; = Standard-F_n. Only if the leaves froze (below ? 3°C to ?4°C) was a reversible inhibition of Standard-F_n observed. As long as the temperatures did not fall below approximately ?8°C the inhibition was small and Standard-F_n reached about 80–90% of the control. In this case the stomatal opening narrowed, giving a poorer supply of CO₂ to the mesophyll cells. Maximal frost tolerance (TL_5O?20°C to ?24°C) developed only with severe frosts below about ? 10°C. After such frosts, Standard-F_n was reduced to less than 20% of the control. The dependence of the rate of net photosynthesis on the internal CO₂ concentration showed a lower initial slope, thus indicating disturbances of chloroplast functions. However, neither in outdoor plants nor in those artificially frosted at – 20°C could there be found an appreciable inhibition of the electron transport capacity from H₂O to dichlorophenol indophenol or of ribulose bisphosphate carboxylase. If intact, severely frosted ivy plants were then held at higher temperatures (20/15°C), Standard-F_n recovered completely in approximately 10 d. Furthermore, following a frost period with temperatures down to ?12°C, mild weather caused a distinct improvement in Standard-F_n in outdoor plants, and there was no loss of maximum frost tolerance. Thus it can be concluded that the inhibition of Standard-F_n after severe frosts is not due to the development of maximal frost tolerance, but rather may be attributed to frost damage to the photosynthetic apparatus.     

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.     

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.     

Response of the photosynthetic apparatus in maize leaves grown at low temperature on transfer to normal growth temperature

Low temperatures are known to restrict chloroplast development and prevent the attainment of photosynthetic competence in maize leaves. The responses of the photosynthetic apparatus of mature maize leaves grown at 14°C on transfer of the plants to 25°C are examined. The synthesis of thylakoid proteins increased immediately on transfer of leaves from 14 to 25°C, with a dramatic accumulation of thylakoid proteins and chlorophylls occurring after 3 d at 25°C. Thylakoid structure and organization also became similar to those observed in leaves grown at 25°C over this period. However, no comparable development of photosynthetic competence in photosystems I and II or in the rate of CO₂ assimilation was observed on transfer of leaves from 14 to 25°C. Immunocytological analyses demonstrated heterogeneity in the distribution of a range of thylakoid proteins (cy tochrome f, the α and β subunits of the coupling factor, Dl of the photosytem II reaction centre, the 33kDa protein of the extrinsic oxygen-evolving complex of photosystem II, and subunit II of photosystem I between mesophyll cells in leaves grown at 14°C, and in the responses of individual proteins to transfer of the leaves to 25°C. Such heterogeneity between mcsophyll cells would account for the inability of the leaves to develop the expected degree of photosynthetic competence on transfer to 25°C. The effects of low growth temperatures on chloroplast biogenesis are complex, as are the changes induced by the transfer ofleaves grown at low temperatures to optimal growth temperature, and both these factors may limit the canopy development and photosynthetic productivity of crops in temperate regions.     

The Galápagos Islands: biogeographic patterns and geology

In the traditional biogeographic model, the Galápagos Islands appeared a few million years ago in a sea where no other islands existed and were colonized from areas outside the region. However, recent work has shown that the Galápagos hotspot is 139 million years old (Early Cretaceous), and so groups are likely to have survived at the hotspot by dispersal of populations onto new islands from older ones. This process of metapopulation dynamics means that species can persist indefinitely in an oceanic region, as long as new islands are being produced. Metapopulations can also undergo vicariance into two metapopulations, for example at active island arcs that are rifted by transform faults. We reviewed the geographic relationships of Galápagos groups and found 10 biogeographic patterns that are shared by at least two groups. Each of the patterns coincides spatially with a major tectonic structure; these structures include: the East Pacific Rise; west Pacific and American subduction zones; large igneous plateaus in the Pacific; Alisitos terrane (Baja California), Guerrero terrane (western Mexico); rifting of North and South America; formation of the Caribbean Plateau by the Galápagos hotspot, and its eastward movement; accretion of Galápagos hotspot tracks; Andean uplift; and displacement on the Romeral fault system. All these geological features were active in the Cretaceous, suggesting that geological change at that time caused vicariance in widespread ancestors. The present distributions are explicable if ancestors survived as metapopulations occupying both the Galápagos hotspot and other regions before differentiating, more or less in situ.     

Effect of temperature on senescing detached rice leaves: I. Photoelectron transport activity of chloroplasts

Detached rice(Oryza sativaL cv Mousouri)leaves were induced to senesce in darkness at 0°C(cold), 27°C(room temperature) and 40°C(heat). 2,6-dichlorophenol indophenol (DCPIP) Hill reaction activity of chloroplasts isolated from senescing leaves under all experimental temperatures with H₂O, Mn²⁺ or diphenyl carbazide (DPC) as electron donor declined during the period of incubation. Since DPC and Mn²⁺ augmented 2,6-dichlorophenol indophenol photoreduction by chloroplasts from senescing leaves, damage and/or change in the conformation of a site between H₂O and DCPIP in photosystem II (PS II) is suggested. Heat caused a faster decline of the Hill activity compared to cold or room temperature. However, cold treatment showed no significant effect on the photoelectron transport from H₂O to DCPIP compared with room temperature.     

Climate Warming May Facilitate Invasion of the Exotic Shrub Lantana camara

Plant species show different responses to the elevated temperatures that are resulting from global climate change, depending on their ecological and physiological characteristics. The highly invasive shrub Lantana camara occurs between the latitudes of 35°N and 35°S. According to current and future climate scenarios predicted by the CLIMEX model, climatically suitable areas for L. camara are projected to contract globally, despite expansions in some areas. The objective of this study was to test those predictions, using a pot experiment in which branch cuttings were grown at three different temperatures (22°C, 26°C and 30°C). We hypothesized that warming would facilitate the invasiveness of L. camara. In response to rising temperatures, the total biomass of L. camara did increase. Plants allocated more biomass to stems and enlarged their leaves more at 26°C and 30°C, which promoted light capture and assimilation. They did not appear to be stressed by higher temperatures, in fact photosynthesis and assimilation were enhanced. Using lettuce (Lactuca sativa) as a receptor plant in a bioassay experiment, we also tested the phytotoxicity of L. camara leachate at different temperatures. All aqueous extracts from fresh leaves significantly inhibited the germination and seedling growth of lettuce, and the allelopathic effects became stronger with increasing temperature. Our results provide key evidence that elevated temperature led to significant increases in growth along with physiological and allelopathic effects, which together indicate that global warming facilitates the invasion of L. camara.     

Eight polymorphic microsatellite markers isolated from the widespread avian louse Colpocephalum turbinatum (Phthiraptera: Amblycera: Menoponidae)

We report eight novel microsatellite loci for Colpocephalum turbinatum, a parasitic louse of the endangered Galápagos hawk (Buteo galapagoensis). Two island populations of C. turbinatum (N = 30) were genotyped for each locus. We found between two and 12 alleles per locus, polymorphic information content from 0.268 to 0.798, observed heterozygosity from 0.067 to 0.667 and no linkage disequilibrium was detected between loci. These markers will be useful in understanding contemporary gene flow of C. turbinatum among islands in the Galápagos and in understanding transmission dynamics between B. galapagoensis hosts, within and between social groups. Because this louse is unusually widespread among avian host taxa, parasitizing at least 53 bird species in the Falconiformes, Strigiformes and Columbiformes, these markers are likely to be useful outside the context of the Galápagos Islands.     

Low genetic diversity and lack of population structure in the endangered Galápagos penguin (<Emphasis Type="Italic">Spheniscus mendiculus</Emphasis>)

Long-term monitoring of the endangered Galápagos penguin (Spheniscus mendiculus) has indicated poor reproductive periods and severe population fluctuations in association with El Niño – Southern Oscillation events. An earlier mark and recapture study indicated that adults exhibit some degree of breeding-site and mate fidelity, and that juveniles potentially move more frequently than adults; however, the extent to which migrants and gene flow occur between islands within the Galápagos archipelago is largely unknown. This study tested the hypothesis that geographic isolation and adult breeding philopatry has led to a degree of genetic differentiation between island subpopulations within the archipelago. We examined the genetic diversity within and among different subpopulations and the extent to which gene flow occurs between island subpopulations. Estimates of allelic richness and gene diversity were not significantly different between subpopulations. Tests to detect genetic heterogeneity failed to reject the H ₀ of no difference in allele frequencies for chi-square (P = 0.28) and Fisher’s exact test (P = 0.19). All pairwise values of the F _ST variant θ were not significant, while a power analysis revealed a >99% probability of detecting a biologically true F _ST of 0.05. Migration estimates in BAYESASS+ suggest symmetrical gene flow throughout the species’ distribution. Our results indicate a low level of genetic diversity throughout the population and a seemingly high level of gene flow between subpopulations. We argue that the Galápagos penguin should be managed as one panmictic population and we discuss the risk of disease threats in the archipelago.