Is a new paradigm emerging for oceanic island biogeography?

Following several decades during which two dissimilar and incompatible models (equilibrium and vicariance) dominated island biogeography, recent publications have documented patterns that point the way towards a new paradigm that includes elements of both models, as well as some novel aspects. Many of these seminal contributions have been made possible by the recent development of robust, temporally calibrated phylogenies used in concert with increasingly precise and reliable geological reconstructions of oceanic regions. Although a new general model of oceanic island biogeography has not yet been proposed, in this brief overview I present six hypotheses that summarize aspects of the emerging paradigm. These hypotheses deal with: the frequency of dispersal over oceanic water barriers by terrestrial organisms; the existence of substantial variation in the amount of dispersal (and gene flow) within a given set of related species within a given archipelago; the frequency, extent and impact on species richness of diversification within archipelagos; the frequent correlation of island age and the age of the species that live on the island; the long-term persistence of species on oceanic islands; and the occasional recolonization of continents by species from clades that diversified on islands. Identifying, testing, and seeking means of synthesizing these and other emerging hypotheses may allow a new conceptual paradigm to emerge.     

Deep intra‐island divergence of a montane forest endemic: phylogeography of the Puerto Rican frog Eleutherodactylus portoricensis (Anura: Eleutherodactylidae)

Aim Hypotheses proposed for lineage diversification of tropical montane species have rarely been tested within oceanic islands. Our goal was to understand how basin barriers and Pleistocene climatic fluctuations shaped the distribution of diversity in Eleutherodactylus portoricensis (Eleutherodactylidae), a frog endemic to the montane rain forests of Puerto Rico. Location The north‐eastern (Luquillo) and south‐eastern (Cayey) mountains of Puerto Rico. Methods We generated mitochondrial DNA (mtDNA) control region sequences (c. 565 bp) from 144 individuals of E. portoricensis representing 16 localities, and sequenced 646 bp of cytochrome b and 596 bp of nuclear DNA (nDNA) rhodopsin exon and intron 1 from a subset of individuals. We conducted a phylogenetic analysis on the mtDNA sequence data and explored population substructure with maximum parsimony networks, a spatial analysis of molecular variance, and pairwise F_ST analysis. Coalescent simulations were performed to test alternative models of population divergence in response to late Pleistocene interglacial periods. Historical demography was assessed through coalescent analyses and Bayesian skyline plots. Results We found: (1) two highly divergent groups associated with the disjunct Luquillo and Cayey Mountains, respectively; (2) a shallow mtDNA genetic discontinuity across the La Plata Basin within the Cayey Mountains; (3) phylogeographic congruence between nDNA and mtDNA markers; (4) divergence dates for both mtDNA and nDNA pre‐dating the Holocene interglacial (c. 10 ka), and nDNA suggesting divergence in the penultimate interglacial (c. 245 ka); and (5) historical demographic stability in both lineages. Main conclusions The low‐elevation Caguas Basin is a long‐term barrier to gene flow between the two montane frog populations. Measures of genetic diversity for mtDNA were similar in both lineages, but lower nDNA diversity in the Luquillo Mountains lineage suggests infrequent dispersal between the two mountain ranges and colonization by a low‐diversity founder population. Population divergence began prior to the Holocene interglacial. Stable population sizes over time indicate a lack of demonstrable demographic response to climatic changes during the last glacial period. This study highlights the importance of topographic complexity in promoting within‐island vicariant speciation in the Greater Antilles, and indicates long‐term persistence and lineage diversification despite late Pleistocene climatic oscillations.     

Molecular evidence for sequential colonization and taxon cycling in freshwater decapod shrimps on a Caribbean island

Taxon cycling, i.e. sequential phases of expansions and contractions in species' distributions associated with ecological or morphological shifts, are postulated to characterize dynamic biogeographic histories in various island faunas. The Caribbean freshwater shrimp assemblage is mostly widespread and sympatric throughout the region, although one species (Atyidae: Atya lanipes) is geographically restricted and ecologically and morphologically differentiated from other Atya species. Using patterns of nucleotide variation at the COI mtDNA gene in five species of freshwater shrimp (A. lanipes, A. scabra, A. innocuous; Xiphocarididae: Xiphocaris elongata; Palaemonidae: Macrobrachium faustinum) from Puerto Rico, we expected to detect a signature of sequential colonization in these shrimp, consistent with the concept of taxon cycling, and expected that A. lanipes would be at a different taxon stage (i.e. an early stage species) to all other species. We also examined patterns of genetic population structure in each species expected with poor, intermediate and well-developed abilities for among-river dispersal. Population expansions were detected in all species, although the relative timing of the expansions varied among them. Assuming that population expansions followed colonization of Puerto Rico by freshwater shrimp, results bear the hallmarks of sequential colonization and taxon cycling in this fauna. A. lanipes had a star phylogeny, low mean pairwise nucleotide differences and recent (Holocene) estimates for an in situ population expansion in Puerto Rico, and it was inferred as an early stage species in the taxon cycle undergoing a secondary phase of expansion. All other species were inferred as late stage species undergoing regional population expansions, as their mean pairwise nucleotide differences were relatively high and phylogenetic patterns were more complex than A. lanipes. High rates of gene flow without isolation by distance among rivers were detected in all species, although results should be treated cautiously as some populations are unlikely to be in mutation-drift equilibrium. Nested clade analysis produced inconsistent results among species that all have high rates of gene flow and expanding populations.     

Biogeographical kinetics on mainland and island volcanoes

Aim To compare post‐eruption biotic recolonization times on mainland and island volcanoes. Location The research involved the study of the recolonization kinetics of Mt Vesuvius (a mainland volcano in southern Italy) and the Island of Vulcano (southern Italy). Comparisons were also made with Jorullo Volcano (Mexico) and Mount St Helens (USA) (two mainland volcanoes) and with Krakatau (Indonesia) (an island volcano). Methods Island volcanoes are expected to possess inherently impoverished faunas and floras, and recolonization after eruption is expected to occur to a low level. In comparison, the recolonization kinetics for a mainland volcano should be characterized by a higher plateau of species, and by species with low dispersal ability. To test this model, recolonization times after the small‐scale Plinian eruption of 1631 were calculated for various insect groups of Mt Vesuvius and compared with recolonization times calculated for the Island of Vulcano, which erupted dramatically in 1888. For this purpose, thorough insect checklists, based on exhaustive samplings, were extracted from the literature. Results obtained from Mt Vesuvius and Vulcano were also compared with recolonization times calculated for biotas of other mainland and island volcanoes. Results Insect recolonization times from the 1631 Vesuvius eruption varied according to the ecology of the animal group considered and appeared very long when compared with those obtained for the island volcano of Vulcano. Results obtained from Vulcano also suggest the possibility that this island hosts more species than expected at equilibrium, a state of affairs also found for the butterflies of Krakatau. Main conclusions In keeping with the predictions of multi‐phase models developed in island biogeography theory, island volcanoes have a lower species richness at equilibrium than do mainland volcanoes, but might host, in a first phase of recolonization, more species than expected at equilibrium, because ecological space is unsaturated and inter‐specific interactions are limited. The lower isolation of mainland volcanoes (allowing higher immigration rates) leads to higher rates and longer periods of recolonization and hence to higher species richness at equilibrium.     

A new species of Litarachna (Acari,Hydrachnidia, Pontarachnidae) from a Caribbean mesophotic coral ecosystem

New records of pontarachnid mites (Acari: Hydrachnidia) from the Caribbean island of Puerto Rico are presented. Litarachna lopezae sp. n., from substrata collected from Bajo de Sico, a mesophotic coral reef ecosystem in Mona Passage off Puerto Rico, is described as new to science. The new species was collected from nearly 70 m depth, the greatest depth from which pontarachnid mites have been found until now. In addition, a Litarachna sp. was also found in association with the tube of the polychaete Sabellastarte magnifica (Shaw, 1800) at the shallow waters of north Puerto Rico.     

Testing island biogeography theory with visitation rates of birds to British islands

Aim We consider three hypotheses – MacArthur and Wilson’s island biogeography theory (IBT), Lack’s habitat diversity idea and the ‘target effect’– that explain the pattern of decreased species richness on small and distant islands. Location We evaluate these hypotheses using a detailed dataset on the occurrence and abundance of terrestrial birds on nine islands off the coast of Britain and the Republic of Ireland. Methods  Unlike previous studies, we compile data on species that visit the islands, rather than just those that breed on them. We divided the species into five mutually exclusive categories based upon their migratory status and where they regularly breed: British residents, summer visitors to Britain, winter visitors to Britain, and vagrants from Europe or beyond Europe. For each species group on each island we calculated the average number of species visiting each year. We then regressed the average number of species against island area and distance to the mainland (all variables were log‐transformed). We also compared the average number of species visiting each island with the average number of species breeding on each island. Results  Average number of visiting British residents decreased significantly with increasing island distance, but showed no relationship with island area. There was no significant relationship between island area or island distance and average number of summer or winter visitors. European and non‐European vagrants likewise showed no relationship between numbers of species visiting and island distance. However, the relationship between island area and number of visiting species was significant for both these categories; as island area increases so too does the number of visiting species. Main conclusions  As predicted by IBT, there were fewer visiting species on more distant islands. There were substantially more visitors to each island than breeding species, supporting Lack’s argument that lower bird richness is not a result of varying immigration rates (as predicted by IBT) but rather a result of some other island property, e.g. fewer resources. Birds make a decision to either leave an island or stay and breed. The target effect was also clearly demonstrated by the increase in European and non‐European breeders with increasing island size.     

Hypothesis: the rate and scale of dispersal of freshwater diatom species is a function of their global abundance

We have analysed the geographical records of a representative selection of extant diatom species from a freshwater pond. The more often a species is recorded in the ecological literature, the greater is its apparent global distribution. One explanation is that the frequently recorded species are globally abundant, whereas species that are infrequently recorded are globally rare. We suggest a model in which random dispersal is the dominant force driving large-scale distribution of species, with the rate and scale of dispersal largely determined by global population size. Thus species that are locally rare or abundant are likewise rare or abundant worldwide. It is predicted that many of the rarer diatom species will, with additional sampling effort, be shown to have wide geographical distribution, but this requires intensive studies focused on revealing species that are normally cryptic. The argument in favour of endemic diatom species is untenable, because it is not possible to disprove their existence elsewhere in the biosphere.     

Comparative phylogeography and demographic history of the wood lemming (Myopus schisticolor): implications for late Quaternary history of the taiga species in Eurasia

The association between demographic history, genealogy and geographical distribution of mitochondrial DNA cytochrome b haplotypes was studied in the wood lemming (Myopus schisticolor), a species that is closely associated with the boreal forest of the Eurasian taiga zone from Scandinavia to the Pacific coast. Except for a major phylogeographic discontinuity (0.9% nucleotide divergence) in southeastern Siberia, only shallow regional genetic structure was detected across northern Eurasia. Genetic signs of demographic expansions imply that successive range contractions and expansions on different spatial scales represented the primary historical events that shaped geographical patterns of genetic variation. Comparison of phylogeographic structure across a taxonomically diverse array of other species that are ecologically associated with the taiga forest revealed similar patterns and identified two general aspects. First, the major south-north phylogeographic discontinuity observed in five out of six species studied in southeastern Siberia and the Far East implies vicariant separation in two different refugial areas. The limited distribution range of the southeastern lineages provides no evidence of the importance of the putative southeastern refugial area for postglacial colonization of northern Eurasia by boreal forest species. Second, the lack of phylogeographic structure associated with significant reciprocal monophyly and genetic signatures of demographic expansion in all nine boreal forest animal species studied to date across most of northern Eurasia imply contraction of each species to a single refugial area during the late Pleistocene followed by range expansion on a continental scale. Similar phylogeographic patterns observed in this taxonomically diverse set of organisms with different life histories and dispersal potentials reflect the historical dynamics of their shared environment, the taiga forest in northern Eurasia.     

The effects of island ontogeny on species diversity and phylogeny

A major goal of island biogeography is to understand how island communities are assembled over time. However, we know little about the influence of variable area and ecological opportunity on island biotas over geological timescales. Islands have limited life spans, and it has been posited that insular diversity patterns should rise and fall with an island''s ontogeny. The potential of phylogenies to inform us of island ontogenetic stage remains unclear, as we lack a phylogenetic framework that focuses on islands rather than clades. Here, we present a parsimonious island-centric model that integrates phylogeny and ontogeny into island biogeography and can incorporate a negative feedback of diversity on species origination. This framework allows us to generate predictions about species richness and phylogenies on islands of different ages. We find that peak richness lags behind peak island area, and that endemic species age increases with island age on volcanic islands. When diversity negatively affects rates of immigration and cladogenesis, our model predicts speciation slowdowns on old islands. Importantly, we find that branching times of in situ radiations can be informative of an island''s ontogenetic stage. This novel framework provides a quantitative means of uncovering processes responsible for island biogeography patterns using phylogenies.     

Influence of a simulated hurricane on aquatic insect recolonization in the phytotelma of Heliconia caribaea (Heliconiacaea)

Disturbances like hurricanes can affect diversity and community composition, which may in turn affect ecosystem function. We examined how a simulated hurricane disturbance affected insect communities inhabiting the phytotelma (plant-held waters) of Heliconia caribaea in the Luquillo Experimental Forest of eastern Puerto Rico, a tropical island that frequently experiences hurricanes. We hypothesized that disturbance would alter diversity and that larger Heliconia would attract more species following disturbance due to the area-diversity relationship described by the Theory of Island Biogeography. Individual flower parts (bracts) of Heliconia inflorescences (racemes) were artificially disturbed via removal of existing insect communities, then after refilling with water, cohorts of Heliconia were destructively sampled biweekly for 6 weeks to assess recolonization patterns of α (bract level), β, and γ (summed across bracts; raceme level) diversity over time and across raceme sizes. Although we found no support for our hypothesis about the effect of raceme size on recolonization, our hypothesis regarding recolonization patterns over time was supported; species richness, evenness, and abundance of bracts increased directly after the disturbance and then decreased below pre-disturbance levels, and community composition at the raceme level changed significantly over time during recolonization. β Diversity was also greater in smaller racemes compared to larger racemes, suggesting high heterogeneity across bracts of Heliconia racemes exacerbated by raceme size and age. Overall, our results highlight the importance of scale and appropriate measurements of diversity (particularly α) in experiments aiming to extrapolate conclusions about the ecological impacts of disturbances across different habitats and ecosystems.     

Patterns of colonization, evolution and gene flow in species of the genus Patella in the Macaronesian Islands

The study of phylogeographical patterns may contribute to a better understanding of factors affecting the dispersal of organisms in ecological and historical times. For intertidal organisms, islands are particularly suitable models allowing the test of predictions related to the efficacy of pelagic larvae dispersal. Here, we study the phylogeographical patterns and gene flow within three groups of species of the genus Patella present in the Macaronesian Islands that have been previously shown to be monophyletic. The genetic variability of around 600 bp of the mitochondrial gene cytochrome c oxidase subunit I was studied by single strand conformation polymorphism and/or sequencing for seven species of limpets. A total of 420 samples were analysed from the Macaronesian archipelagos, North Africa, and Atlantic and Mediterranean shores of the Iberian Peninsula. No clear geographical pattern or temporal congruence was found between the three groups of species, pointing to independent histories and colonization events. However, for the three groups, the split between the Macaronesian and the mainland forms most probably occurred before 3.9 million years ago, predating the establishment of the current circulation patterns. The presence of pelagic larvae in these species is shown to be insufficient to ensure gene flow between continental and Macaronesian populations and between the Macaronesian archipelagos. In the endangered Azorean populations of Patella candei, there is restricted gene flow to Flores and Graciosa.     

A model-independent test for the presence of regulatory equilibrium and non-random structure in island species trajectories

Aims To test a key prevision of the dynamic equilibrium theory of island biogeography, namely that changes in species numbers on islands over time (hereafter, species trajectories) are equilibrial, and to characterize aspects of the dynamical properties of species change over time using a model‐independent test. Methods We tested for regulatory equilibrium and non‐random structure in species numbers through time by comparing observed correlation coefficients at lag‐k for species trajectories from four true islands and two habitat islands. First, we estimated the shape of the autocorrelation function for each observed species trajectory by calculating correlation coefficients of the observed data between pairs of values N_t?k and N_t separated by lag‐k (k = 1, 2, …, N ? 1). Second, we tested the observed correlation coefficients at each lag against a distribution of correlation coefficients generated by randomly ordering observed numbers in the species trajectories. Results The patterns of autocorrelation functions for all but one of the observed species trajectories did not exhibit evidence of regulatory equilibrium, and, in fact, closely matched what would be expected from a non‐stationary or ‘random walk’ process. The majority of the correlation coefficients generated from the observed species trajectories did not deviate significantly from correlation coefficients produced by the randomized trajectories. However, there was strong evidence of unusual positive autocorrelation at small time lags for birds on islands measured annually (2‐ to 4‐year lags) and for arthropods on islands measured weekly (7‐ to 8‐week lags), suggesting some degree of structure in change in species richness over time. Main conclusions The autocorrelation function patterns for all but one of the observed species trajectories showed various forms of non‐stationarity. These types of patterns suggest that the numbers of species through time gradually wandered away from their initial sizes. Our model‐independent test of individual correlation coefficients revealed significant structure in the observed species trajectories. These trajectories appear to be non‐random at relatively short lag intervals, indicating a process with short memory.     

Population structure and phylogeography of Aphyocypris kikuchii (Oshima) based on mitochondrial DNA variation

Aphyocypris kikuchii is a cyprinid species endemic to northern and eastern Taiwan and is the only primary freshwater fish native east of the Coastal Mountain Range. In total, 92 individuals of A. kikuchii from seven populations in three regions of the island were surveyed for mitochondrial DNA (mtDNA) variation. High haplotype diversity ( h = 0·989) and low nucleotide diversity ( π = 0·009) of mtDNA were detected. Negative values of Tajima's D and unimodal mismatch distributions probably reflect a history of recent demographic expansions from small populations. Three major haplotype clusters displayed geographically non-overlapping distributions, indicating a long-term isolation between regions. Hierarchical analysis of molecular variance showed significant genetic structuring among populations ( Φ _ST= 0·66). Significant haplotype heterogeneity was also detected among populations within regions ( Φ _SC= 0·41, P < 0·001) and among regions ( Φ _CT= 0·43, P < 0·05). Molecular clock estimates of coalescence in the three major mtDNA lineages indicated coalescence in the most recent common ancestor c. 0·11–0·39 million years ago. Haplotypes of cluster B nested as interior nodes in the haplotype network, indicating that migrations from Shueilian (SL) populations to the northern region (cluster A) and to the eastern region (cluster C) may have occurred independently. Lineages A and B + C should be managed as two distinct evolutionarily significant units, while the northern, SL and southern groups should be managed as separate management units.     

Effect of island geological age on the arthropod species richness of Azorean pastures

Species richness of six pasture arthropod assemblages (total arthropod species, total herbivore species, sucking and chewing herbivores, total predatory species and spiders) were regressed against several geographical variables (area, distance from the nearest mainland, maximum elevation and geological age of the islands) of three Azorean islands (S. Maria, Terceira and Pico). The species were sampled by the fixed-quadrat size sampling method and the results obtained are consistent with the geological age hypothesis, i.e. the species richness of the six indigenous arthropod assemblages increases with the geological age of the islands, both at local and regional scales. Higher values of indigenous and endemic species richness were consistendy found on the older island (S. Maria), and the lowest values on the most recent island (Pico). Moreover, when considering the age of Faial (an older island probably once connected with Pico) as a estimate of the age of Pico, correlations between species richness and island age were improved, thereby strengthening the relationship. The older island (S. Maria) has more specialized herbivores and a greater proportion of herbivores in relation to predatory arthropods. Ecological and biogeographical studies in the Azores should take into account the effects of the time each island has been available for colonization and evolution.     

The influence of geographical and ecological factors on island beta diversity patterns

Aim To investigate the importance of various island characteristics in determining spatial patterns of variations in beta diversity for various animal groups. Location Analyses are presented for 10 animal groups living on the Aeolian Islands, a volcanic archipelago in the central Mediterranean, near Sicily. Methods Three hypotheses were formulated to explain patterns of beta diversity: the target‐area–distance effect, stepping stone dispersal and island age. Matrices of inter‐island dissimilarities were constructed under each hypothesis and correlated with matrices of faunal dissimilarities using Mantel tests. For the ‘target‐area–distance effect’ hypothesis, inter‐island dissimilarities were calculated using island sizes and distances to nearest mainland areas. For the ‘stepping stone dispersal’ hypothesis, inter‐island distances were measured. Finally, for the ‘island age’ hypothesis, inter‐island dissimilarities were calculated on the basis of the geological age of the islands. Cluster analysis was used to investigate inter‐island faunal relationships. Results Support for a target‐area–distance effect was found only for birds. For these highly mobile animals, inter‐island distances had no significant effects on beta diversity. Birds are known to colonize islands by crossing large sea barriers and thus they can easily reach the Aeolian Islands, which are close to source areas (notably Sicily). Inter‐island distances had a significant role in determining patterns of beta diversity in most invertebrates. For Mollusca, Opiliones, Chilopoda, Heteroptera, coprophagous Scarabaeoidea, and Tenebrionidae, even relatively short distances preclude invertebrates from colonizing an island regularly from the mainland, and most colonization probably results from inter‐island faunal exchanges. Island age was proved to be important only for orthopterans. Main conclusions The origin of most of the Aeolian invertebrate fauna is quite recent, and species appear to have established on the islands predominantly by stepping stone dispersal. Birds, which are highly mobile organisms, follow more direct mainland–island dynamics. As further studies on other islands become available, comparative analyses will confirm whether the factors influencing variations in beta diversity in this study and their relationships with species dispersal ability are consistent across scales and geographical context.     

PACT in practice: comparative historical biogeographic patterns and species–area relationships of the Greater Antillean and Hawaiian Island terrestrial biotas

Aim To compare the evolutionary and ecological patterns of two extensively studied island biotas with differing geological histories (the Hawaiian Islands and the Greater Antilles). We evaluated the results from PACT (phylogenetic analysis for comparing trees), an innovative approach that has been proposed to reveal general patterns of biotic expansion (between regions) and in situ (within a region) diversification, as well as species–area relationships (SAR) and the taxon pulse dynamic. Location The Hawaiian Islands and Greater Antilles. Methods We used the PACT algorithm to construct general area cladograms and identified biotic expansion and in situ nodes. We analysed the power‐law SAR and relative contribution of biotic expansion and in situ diversification events using power‐law and linear regression analyses. Results Both biotic expansion and in situ nodes were prevalent throughout the PACT general area cladograms (Greater Antilles, 55.9% biotic expansion, 44.1% in situ; Hawaiian Islands, 40.6% biotic expansion, 59.4% in situ). Of the biotic expansion events, both forward and backward events occurred in both regions (Greater Antilles, 85.1% forward, 14.9% backward; Hawaiian Islands, 65% forward, 35% backward). Additionally, there is a power‐law SAR for the Greater Antilles but not for the Hawaiian Islands. However, exclusion of Hawai'i (the youngest, largest Hawaiian Island) produced a power‐law SAR for the Hawaiian Islands. Main conclusions The prevalence of in situ events as well as forward and backward biotic expansion events reveals that both Hawaiian and Greater Antillean biotas have evolved through alternating episodes of biotic expansion and in situ diversification. These patterns are characteristic of the taxon pulse dynamic, for which few data have previously been recorded on islands. Additionally, our analysis revealed that historical influences on the power‐law SARs are pronounced in both assemblages: old, small islands are relatively species rich and young, large islands are relatively species poor. Thus, our PACT results are consistent with hypotheses of geological influence on the evolution of island biotas and also provide greater insight into the role of the taxon pulse dynamic in the formation of island equilibria.