The parasites of Anolis lizards in the northern Lesser Antilles

Summary The helminth communities from ten species of lizard on seven islands in the Caribbean were sampled by collecting one hundred specimens of each species. Nine genera of parasites were identified; these included six nematodes, two digeneans and an acanthocephalan. No relationship was discernible between parasite density or abundance and island area or altitude, although dry islands tend to have fewer species of parasites. Anolis lizards of the bimaculatus and wattsi series share similar parasites with four out of nine species common to both series. The parasite community of lizards on these islands is depauperate with respect to similar surveys on the larger islands of the Greater Antilles.On three of the islands lizards were sub-sampled by collecting from moist woodland and more xeric habitats. These data suggest that differences between habitats are as significant as differences between islands in determining parasite burdens. Worm burdens of the commonest parasite species, T. cubensis, increased monotonically with host body size and no evidence was found to suggest that these parasites affect either host survival or fecundity. The sex-ratio of this species correlated with mean abundance of the parasite, with females the dominant sex on islands or in habitats where the parasite was common. This pattern may reflect haplodiploid sexual determination in this species.     

Interspecific interactions tested: two species of malarial parasite in a West African lizard

Plasmodium giganteum and P. agamae, parasites of the rainbow lizard, Agama agama, in West Africa were studied to determine the nature of any interspecific interactions between the two malaria species. The plasmodia are distributed in A. agama throughout the mesic zone of Africa; P. agamae is sometimes found as a solitary malaria species in populations of the lizard, but P. gigateum has not been found alone. In 3170 lizards from Sierra Leone the prevalence of lizard malaria at 22 sites varied considerably (8–90% of lizards were infected), but the ratio of the two species was similar among sites (52–91% P. agamae). Larger lizards were more often infected. Mixed infections occurred 2–5 times more often than expected by chance. Parasite density within individual hosts, or parasitemia, was similar for each species when alone or in mixed infection. Natural infections followed in laboratory lizards stayed at constant levels for as long as 211 days. The two species use different classes of host cells (P. giganteum in immature cells and P. agamae in mature erythrocytes) and may have different periods of peak transmission. Analysis of the data does not support a neutral relationship between P. giganteum and P. agamae, nor ongoing competition for resources or heterologous immunity. The data best support facilitation in which P. agamae alters the host in a way that allows more successful establishment of P. giganteum.     

Distribution anomalies in avian haemosporidian parasites in the southern Lesser Antilles

We compared the haemosporidian parasite faunas (Plasmodium and Haemoproteus) of small land birds on the islands of St Lucia, St Vincent and Grenada in the southern Lesser Antilles. The islands differ in distance from the South American source of colonists, proximity to each other, and similarity of their avifaunas. On each island, we obtained 419–572 blood samples from 22–25 of the 34–41 resident species. We detected parasite infection by PCR and identified parasite lineages by sequencing a portion of the mitochondrial cytochrome b gene. Parasite prevalence varied from 31% on St Lucia to 22% on St Vincent and 18% on Grenada. Abundant parasite lineages differed between the three islands in spite of the similarity in host species. As in other studies, the geographic distributions of the individual parasite lineages varied widely between local endemism and broad distribution within the West Indies, including cases of long‐distance disjunction. St Vincent was unusual in the near absence of Plasmodium parasites, which accorded with low numbers of suitable mosquito vectors reported from the island. Parasites on St Vincent also tended to be host specialists compared to those on St Lucia and Grenada. Similarity in parasite assemblages among the three islands varied in parallel with host assemblage similarity (but not similarity of infected hosts) and with geographic proximity. Parasite prevalence increased with host abundance on both St Lucia and St Vincent, but not on Grenada; prevalence did not vary between endemic and more widespread host species. In addition, the endemic host species harbored parasites that were recovered from a variety of non‐endemic species as well. These results support the individualistic nature of haemosporidian parasite assemblages in evolutionarily independent host populations.     

A PHYLOGENETIC ANALYSIS OF CHARACTER DISPLACEMENT IN CARIBBEAN ANOLIS LIZARDS

Twenty-seven islands in the Lesser Antilles contain either one or two species of Anolis lizards. On nine of the ten two-species islands, the species differ substantially in size; 16 of the 17 one-species islands harbor an intermediate-sized species. Two processes could produce such a pattern: size adjustment (or character displacement), in which similar-sized species evolve in different directions in sympatry; and size assortment, in which only different-sized species can successfully colonize the same island together. Previous analyses implicitly have assumed that size is evolutionarily plastic and determined solely by recent ecological conditions, and consequently have tested the hypothesis that character displacement has occurred on each of the ten two-species islands. Other studies have focused only on size assortment. By analyzing such patterns in a phylogenetic context, I explicitly consider historical effects and can distinguish between size adjustment and size assortment. Using a minimum evolution algorithm, I assess evidence for size adjustment by partitioning changes in size along branches of the phylogenetic tree. Size evolution appears rare (a minimum of 4-7 instances of substantial size evolution). In the northern (but not the southern) Lesser Antilles, size change was significantly greater when a descendant taxon occurred on a two-species island and its hypothetical ancestor occurred on a one-species island, thus supporting the size adjustment hypothesis, though size adjustment might have occurred only once. The relative rarity of size evolution suggests that size assortment might be responsible for nonrandom patterns. In both the northern and southern Lesser Antilles, a null model of no size assortment is convincingly rejected. Closely related taxa, however, are usually similar in size, and hybridization between species has been reported. Consequently, similar-sized species might not coexist because they interbreed and coalesce into one gene pool. A null model that only allows species from different “clades” to co-occur is rejected for the northern Lesser Antilles, but is ambiguous with regard to the southern Lesser Antilles. Thus, competitive exclusion is probably responsible for the pattern of size assortment in the northern Lesser Antilles; both competitive exclusion and interbreeding of closely related species of similar size might be responsible for the patterns evident in the southern Lesser Antilles.     

Saurian malaria in the Caribbean: Plasmodium azurophilum sp. nov., a malarial parasite with schizogony and gametogony in both red and white blood cells

A survey of 466 Caribbean lizards found Plasmodium parasites present in Anolis species only of five islands. Parasites presently considered to be P. floridense occurred on Grand Cayman, North Bimini, Jamaica, Hispaniola (Haiti), and Puerto Rico. A second species, P. azurophilum, is described as new from Anolis cybotes of Haiti, A. krugi of Puerto Rico, and A. lineatopus and A. grahami of Jamaica. It lacks visible pigment in erythrocytic host cells but can produce it occasionally. Both asexual and sexual forms occur in a variety of white blood cells, notably in azurophil granulocytes and polymorphonuclear leucocytes. Experimental infections indicate that the leucocytic phase occurs after the acute erythrocytic infection declines, thus suggesting that the schizogonic and gametogonic cycles in white cells may represent an adaptive defense against immune mechanisms of the host. Mean numbers of nuclei in schizonts and mean gametocyte size are influenced by host species and type of host cell.     

Parasite-mediated competition in Anolis lizards

Summary On many small Caribbean islands, two species of Anolis lizard coexist, but the two are typically very different in body size. The two Anolis of St. Maarten, however, are exceptional because they are similar in size and are known to be strongly competitive. One species, A. gingivinus, appears the stronger competitor and occurs throughout the island; the other, A. wattsi, is found only in the central hills. The malarial parasite Plasmodium azurophilum very rarely infects A. wattsi, but in some locations is very common in A. gingivinus. Wherever malaria infects A. gingivinus, A. wattsi is present, but wherever malaria is absent, only A. gingivinus occurs. This pattern of coincidence of malaria and coexistence of both Anolis is observed over distances of only a few hundred meters. The parasite infects both red and white blood cells of A. gingivinus and causes important pathology: immature erthrocytes increase in abundance, blood hemoglobin decreases, monocytes and neutrophils increase, and infected white cells are less likely to produce acid phosphatase. These results argue that malaria mediates competition between the two species and determines the present distribution of the lizards on St. Maarten. This kind of parasite-mediated competition could be common if susceptibility to parasitic infection varies among competitors. The distribution of malaria in the Anolis of Caribbean islands suggests this parasite can play an important role in Anolis community ecology.     

Adaptive radiation versus intraspecific differentiation: morphological variation in Caribbean Anolis lizards

Lizards in the genus Anolis have experienced adaptive radiation in the Greater Antilles, producing a suite of species morphologically adapted to use different parts of the environment. In the Lesser Antilles, adaptive radiation has not occurred, but on some islands, interpopulational variation is high and represents adaptation to different habitats. We compared the extent of morphological differentiation among Greater Antillean habitat specialists with that exhibited among populations of two species, Anolis marmoratus and A. oculatus, from the Lesser Antillean islands of Guadeloupe and Dominica. Although extensive, intraspecific divergence in the Lesser Antilles is substantially less in magnitude than the differences among habitat specialists in the Greater Antilles. All populations of A. marmoratus are most similar to Greater Antillean trunk‐crown habitat specialists, but populations of A. oculatus differ in their affinities: some are similar to trunk‐crown anoles, but others are more similar to trunk‐ground habitat specialists.     

Identification of microsatellite markers in Plasmodium mexicanum,a lizard malaria parasite that infects nucleated erythrocytes

Reptile and bird hosts of malaria parasites (Plasmodium) have nucleated erythrocytes. Infected blood thus contains a mix of abundant host and scant parasite DNA which has prevented identification of Plasmodium microsatellites. We developed a protocol for isolation of microsatellite markers for Plasmodium mexicanum, a parasite of lizards. The ATT repeat was common in the genome of P. mexicanum, but most (87%) of these repeats were exceptionally long (50–206 + repeats). Seven microsatellite markers with polymerase chain reaction primers are described. The protocol should allow discovery of microsatellites of malaria parasites (with AT‐rich genomes) infecting bird and reptile hosts.     

THE PARADOX OF THE PHYLOGENY: CHARACTER DISPLACEMENT OF ANALYSES OF BODY SIZE IN ISLAND ANOLIS

The evolution of body size in Anolis lizards of the Lesser Antilles Islands has been the subject of intensive, if divisive, study. Early research by Schoener revealed a regularity in the number of Anolis species that coexisted on islands and the difference in body size between coexisting congeners in the Northern Lesser Antilles. This consistent pattern of body size was suggested to be the result of competitive character displacement. Two recent studies critically evaluated this hypothesis by incorporating information about the phylogenetic relationships of insular Anolis. Roughgarden and Pacala suggested that the patterns of body-size differences in the Northern Lesser Antilles could be explained as a cyclical phenomenon that they labeled a taxon cycle. However, Losos supported the character-displacement hypothesis (“size adjustment”). The conflict between these two studies is important because both investigations were based on the same phylogenetic hypothesis. We investigated body-size evolution in Lesser Antilles Anolis to resolve the differences in the conclusions of these studies. Our new analysis supported the taxon-cycle hypothesis but nevertheless failed to reject the character-displacement hypothesis. We argue that this curious scenario is largely a function of the method by which phylogenetic information is incorporated in comparative analyses. Different comparative analyses may lead to dramatic differences in results and ambiguity in the conclusions to be drawn. We suggest that ecologists and evolutionary biologists specifically consider the underlying assumptions and models of character evolution inherent to each of the phylogenetically based analytical methods now available.     

Composition and structure of Caribbean bat (Chiroptera) assemblages: effects of inter‐island distance,area, elevation and hurricane‐induced disturbance

Aim Although bats of the Caribbean have been studied extensively, previous work is largely restricted to zoogeography, phylogeography or the effects of island characteristics on species richness. Variation among islands in species composition that is related to geographical or environmental variation remains poorly understood for much of the Caribbean. Location Caribbean islands, including the Bahamas, Greater Antilles and Lesser Antilles. Methods Using presence–absence data, we assessed the extent to which island area, maximum island elevation, inter‐island distance and hurricane‐induced disturbance affected patterns of composition and nestedness for bats in the Bahamas, Greater Antilles and Lesser Antilles. Analyses were conducted for all species, as well as for two broadly defined guilds: carnivores and herbivores. Results For the Bahamas, only inter‐island distance accounted for variation in species composition between islands. For the Greater and Lesser Antilles, differences in island area and inter‐island distance accounted for differences in species composition between islands. Variation in species composition was not related significantly to differences in elevation or hurricane‐related disturbance. In general, results of analyses restricted to a particular broad guild (i.e. carnivores or herbivores) mirrored those for all bats. Bat species composition was nested significantly in each island group. Nestedness was stronger in the Greater Antilles and in the Lesser Antilles than in the Bahamas. Carnivore assemblages were nested significantly in the Greater and in the Lesser Antilles, but not in the Bahamas. In contrast, herbivore assemblages were nested significantly in each island group. Main conclusions Inter‐island distance had a greater effect on compositional similarity of Caribbean bat assemblages than did island area, elevation or disturbance related to hurricanes. Differential immigration and hierarchical habitat distributions associated with elevational relief are likely to be primary causes for nestedness of Caribbean bat assemblages.     

Consequences of chronic infections with three different avian malaria lineages on reproductive performance of Lesser Kestrels (Falco naumanni)

We studied the consequences of chronic infections by three different lineages of avian malaria, two Plasmodium (RTSR1, LK6) and one Haemoproteus (LK2), on reproductive performance of Lesser Kestrels (Falco naumanni). Malaria infections in male and female parents had no effect on clutch size, hatching success or nesting success. However, when only successful nests were considered, we found that males parasitized by LK6 raised a lower number of fledglings, suggesting that the level of parental effort by males may be limited by this particular lineage of Plasmodium. This effect was not evident in females, probably due to the higher investment of males during the chick rearing period in this species. Overall, we have found that chronic stages of specific malaria lineages have certain negative consequences on host reproductive performance, highlighting the importance of considering genetic differences among malaria parasites to study their consequences on natural bird populations.     

Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles

We recovered 26 genetically distinct avian malaria parasite lineages, based on cytochrome b sequences, from a broad survey of terrestrial avifauna of the Lesser Antilles. Here we describe their distributions across host species within a regional biogeographic context. Most parasite lineages were recovered from a few closely related host species. Specialization on one host species and distribution across many hosts were both rare. Geographic patterns of parasite lineages indicated limited dispersal and frequent local extinction. The central islands of the archipelago share similar parasite lineages and patterns of infection. However, the peripheral islands harbor well-differentiated parasite communities, indicating long periods of isolation. Nonetheless, 20 of 26 parasite lineages were recovered from at least one of three other geographic regions, the Greater Antilles, North America, and South America, suggesting rapid dispersal relative to rate of differentiation. Six parasite lineages were restricted to the Lesser Antilles, primarily to endemic host species. Host differences between populations of the same parasite lineage suggest that host preference may evolve more rapidly than mitochondrial gene sequences. Taken together, distributions of avian malarial parasites reveal evidence of coevolution, host switching, extinction, and periodic recolonization events resulting in ecologically dynamic as well as evolutionarily stable patterns of infection.     

Lizard habitat partitioning on islands: the interaction of local and landscape scales

Aim This study addresses how species resolve environmental differences into biological habitats at multiple, interacting spatial scales. How do patterns of local habitat use change along an elevation gradient? How do patterns of local habitat partitioning interact with partitioning at a landscape scale? Location Northern and southern Lesser Antilles islands, West Indies. Methods We document how Anolis Daudin, 1802 lizards partition habitat locally at sites along a landscape‐scale elevation gradient. We examine habitat partitioning both with and without interspecific interactions in the predominately flat northern Lesser Antilles islands and in the more mountainous southern islands. Results Anoles partition local habitat along perch‐height and microclimate axes. Northern‐group sympatric anoles partition local habitat by perch height and have overlapping distributions at the landscape scale. Southern‐group sympatric anoles partition local habitat by microclimate and specialize in particular habitats at the landscape scale. In both the northern and southern groups, species use different perch heights and microclimates only in areas of species overlap along the elevation gradient. Main conclusions We demonstrate the interaction between local‐ and landscape‐scale habitat partitioning. In the case of microclimate partitioning, the interaction results from the use of thermal physiology to partition habitat at multiple scales. This interaction prompts the question of whether habitat partitioning developed ‘local‐out’ or ‘landscape‐in’. We pose this dichotomy and present a framework for its resolution.     

Avian Plasmodium infection in field‐collected mosquitoes during 2012–2013 in Tarlac,Philippines

Global warming threatens to increase the spread and prevalence of mosquito‐transmitted diseases. Certain pathogens may be carried by migratory birds and transmitted to local mosquito populations. Mosquitoes were collected in the northern Philippines during bird migration seasons to detect avian malaria parasites as well as for the identification of potential vector species and the estimation of infections among local mosquito populations. We used the nested PCR to detect the avian malaria species. Culex vishnui (47.6%) was the most abundant species collected and Cx. tritaeniorhynchus (13.8%) was the second most abundant. Avian Plasmodium parasites were found in eight mosquito species, for which the infection rates were between 0.5% and 6.2%. The six Plasmodium genetic lineages found in this study included P. juxtanucleare ‐GALLUS02, Tacy7 (Donana04), CXBIT01, Plasmodium species LIN2 New Zealand, and two unclassified lineages. The potential mosquito vectors for avian Plasmodium parasites in the Philippines were Cq. crassipes, Cx. fuscocephala, Cx. quinquefasciatus, Cx. sitiens, Cx. vishnui, and Ma. Uniformis; two major genetic lineages, P. juxtanucleare and Tacy7, were identified.     

Avian Plasmodium lineages found in spot surveys of mosquitoes from 2007 to 2010 at Sakata wetland,Japan: do dominant lineages persist for multiple years?

The ecology and geographical distribution of disease vectors are major determinants of spatial and temporal variations in the transmission dynamics of vector‐borne pathogens. However, there are limited studies on the ecology of vectors that contribute to the natural transmission of most vector‐borne pathogens. Avian Plasmodium parasites are multihost mosquito‐borne pathogens transmitted by multiple mosquito species, which might regulate the diversity and persistence of these parasites. From 2007 to 2010, we conducted entomological surveys at Sakata wetland in central Japan, to investigate temporal variation in mosquito occurrence and prevalence of avian Plasmodium lineages in the mosquito populations. A polymerase chain reaction (PCR)‐based method was used to detect Plasmodium parasites and identify the blood sources of mosquitoes. Culex inatomii and C. pipiens pallens represented 60.0% and 34.8% of 11 mosquito species collected, respectively. Our results showed that the two dominant mosquito species most likely serve as principal vectors of avian Plasmodium parasites during June, which coincides with the breeding season of bird species nesting in the wetland reed beds. Fourteen animal species were identified as blood sources of mosquitoes, with the oriental reed warbler (Acrocephalus orientalis) being the commonest blood source. Although there was significant temporal variation in the occurrence of mosquitoes and prevalence of Plasmodium lineages in the mosquitoes, the dominant Plasmodium lineages shared by the two dominant mosquito species were consistently found at the same time during transmission seasons. Because vector competence cannot be confirmed solely by PCR approaches, experimental demonstration is required to provide definitive evidence of transmission suggested in this study.     

Parasites and the evolution of extravagant male characters: Anolis lizards on Caribbean islands as a test of the Hamilton-Zuk hypothesis

Anolis lizards from Puerto Rico (five species from one site), Curaçao and Aruba in the southern Caribbean (2 populations), and 22 populations from 14 islands in the eastern Caribbean were surveyed for blood parasites (two species of Plasmodium and haemogregarines). Literature records for gut helminths from nine of these populations were added to the data set. Dorsal body color and dewlap color of males were also observed and classified into objective classes with no subjective view of showiness. These data were used to test the among-species prediction of the Hamilton-Zuk hypothesis which states that species harboring more harmful parasites over their evolutionary history will be more likely to evolve extravagant sexually dimorphic traits. Critics have noted important shortcomings in previous tests of the prediction; here we corrected for these errors. Parasite loads (prevalence and number of species) and dorsal and dewlap color varied substantially among the populations sampled. However, there was no association of parasite load with color either in a broad analysis or when correcting for phylogenetic relationships among the lizard species.     

Evolutionary consequences of ecological release in Caribbean Anolis lizards

On the large islands of the Greater Antilles, multi-species communities of Anolis lizards are composed of species specialized to use particular habitats; similar sets of specialized species have evolved independently on each island. We studied species of anoles found on small Caribbean islands. Because these islands contain at most only one other species of anole, we predicted that species on these islands should not be as specialized as Greater Antillean species; rather, they might be expected to exhibit a generalized morphology and a greater breadth of habitat use. Our findings, however, do not confirm these predictions. Lesser Antillean species do not exhibit greater breadth of habitat use than Greater Antillean species, nor do they exhibit a generalized morphology. Most species are ecologically and morphologically similar to specialized trunk-crown anoles of the Greater Antilles, although some species exhibit morphologies unlike those seen in Greater Antillean species. Among descendants of specialized Greater Antillean species occurring on one-or two-species islands, most descendants of trunk-crown species have diverged relatively little, whereas several descendants of trunk-ground anoles have diverged considerably. Consequently, we propose that ancestral species in the Greater Antilles may have been trunk-crown anoles.     

Molecular systematics of Selenops spiders (Araneae: Selenopidae) from North and Central America: implications for Caribbean biogeography

The Caribbean region includes a geologically complex mix of islands, which have served as a backdrop for some significant studies of biogeography, mostly with vertebrates. Here, we use the tropical/subtropical spider genus Selenops (Selenopidae) to obtain a finer resolution of the role of geology in shaping patterns of species diversity. We obtained a broad geographic sample from over 200 localities from both the islands and American mainland. DNA sequence data were generated for three mitochondrial genes and one nuclear gene for eleven outgroup taxa and nearly 60 selenopid species. Phylogenetic analysis of the data revealed several biogeographic patterns common to other lineages that have diversified in the region, the most significant being: (1) a distinct biogeographic break between Northern and Southern Lesser Antilles, although with a slight shift in the location of the disjunction; (2) diversification within the islands of Jamaica and Hispaniola; (3) higher diversity of species in the Greater Antilles relative to the Lesser Antilles. However, a strikingly unique pattern in Caribbean Selenops is that Cuban species are not basal in the Caribbean clade. Analyses to test competing hypotheses of vicariance and dispersal support colonization through GAARlandia, an Eocene–Oligocene land span extending from South America to the Greater Antilles, rather than over‐water dispersal. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 288–322.     

Phylogeography of the frog Leptodactylus validus (Amphibia: Anura): Patterns and timing of colonization events in the Lesser Antilles

The frog Leptodactylus validus occurs in northern South America, Trinidad and Tobago, and the southern Lesser Antilles (Grenada and St. Vincent). Mitochondrial DNA sequences were used to perform a nested clade phylogeographic analysis (NCPA), to date colonization events, and to analyze colonization patterns using on a relaxed molecular clock and coalescent simulations. L. validus originated on the mainland and first colonized Trinidad with subsequent independent colonizations of Tobago and the Lesser Antilles from Trinidad. The NCPA suggests a historical vicariant event between populations in Trinidad and Tobago from those in the Lesser Antilles. The colonization of Trinidad occurred 1 million years ago (mya) and the colonization of the Lesser Antillean islands occurred 0.4 mya. The coalescent approach supported the scenario where L. validus dispersed from Trinidad to St. Vincent and from there to Grenada, a dispersal event that could have been mediated by human introduction as recent as 1600 years ago.     

A review of the net-winged midges (Diptera: Blephariceridae) of the West Indies,with description of a new species from Puerto Rico

ABSTRACT

The Caribbean blepharicerid fauna comprises three described species: Paltostoma palominoi Hogue and Garces, 1990, found in eastern Cuba; P. agyrocincta Curran, 1927, widespread in Puerto Rico; and P. schineri Williston, 1896, which occupies most major islands of the Lesser Antilles. In this paper, we describe P. portoricensis Hogue and Courtney, sp. n., a second species from Puerto Rico. We also provide keys to adults, pupae, and larvae of known Caribbean species, re-describe P. argyrocincta and P. schineri, and present a brief discussion of the bionomics and phylogenetic affinities of the net-winged midge fauna.