Changes in parrot diversity after human arrival to the Caribbean.

Humans did not arrive on most of the world's islands until relatively recently, making islands favorable places for disentangling the timing and magnitude of natural and anthropogenic impacts on species diversity and distributions. Here, we focus on Amazona parrots in the Caribbean, which have close relationships with humans (e.g., as pets as well as sources of meat and colorful feathers). Caribbean parrots also have substantial fossil and archaeological records that span the Holocene. We leverage this exemplary record to showcase how combining ancient and modern DNA, along with radiometric dating, can shed light on diversification and extinction dynamics and answer long-standing questions about the magnitude of human impacts in the region. Our results reveal a striking loss of parrot diversity, much of which took place during human occupation of the islands. The most widespread species, the Cuban Parrot, exhibits interisland divergences throughout the Pleistocene. Within this radiation, we identified an extinct, genetically distinct lineage that survived on the Turks and Caicos until Indigenous human settlement of the islands. We also found that the narrowly distributed Hispaniolan Parrot had a natural range that once included The Bahamas; it thus became "endemic" to Hispaniola during the late Holocene. The Hispaniolan Parrot also likely was introduced by Indigenous people to Grand Turk and Montserrat, two islands where it is now also extirpated. Our research demonstrates that genetic information spanning paleontological, archaeological, and modern contexts is essential to understand the role of humans in altering the diversity and distribution of biota.

Bird populations and species lost to Late Quaternary environmental change and human impact in the Bahamas.

Comparing distributional information derived from fossils with the modern distribution of species, we summarize the changing bird communities of the Bahamian Archipelago across deep ecological time. While our entire dataset consists of 7,600+ identified fossils from 32 sites on 15 islands (recording 137 species of resident and migratory birds), we focus on the landbirds from four islands with the best fossil records, three from the Late Pleistocene (∼25 to 10 ka [1,000 y ago]) and one from the Holocene (∼10 to 0 ka). The Late Pleistocene sites feature 51 resident species that have lost one or more Bahamian populations; 29 of these species do not occur in any of the younger Holocene sites (or in the Bahamas today). Of these 29 species, 17 have their closest affinities to species now or formerly living in Cuba and/or North America. A set of 27 species of landbirds, most of them extant somewhere today, was more widespread in the Bahamas in the prehistoric Holocene (∼10 to 0.5 ka) than they are today; 16 of these 27 species were recorded as Pleistocene fossils as well. No single site adequately captures the entire landbird fauna of the combined focal islands. Information from all sites is required to assess changes in Bahamian biodiversity (including endemism) since the Late Pleistocene. The Bahamian islands are smaller, flatter, lower, and more biotically depauperate than the Greater Antilles, resulting in more vulnerable bird communities.

Ancient DNA from the extinct Haitian cave-rail (Nesotrochis steganinos) suggests a biogeographic connection between the Caribbean and Old World.

Worldwide decline in biodiversity during the Holocene has impeded a comprehensive understanding of pre-human biodiversity and biogeography. This is especially true on islands, because many recently extinct island taxa were morphologically unique, complicating assessment of their evolutionary relationships using morphology alone. The Caribbean remains an avian hotspot but was more diverse before human arrival in the Holocene. Among the recently extinct lineages is the enigmatic genus Nesotrochis, comprising three flightless species. Based on morphology, Nesotrochis has been considered an aberrant rail (Rallidae) or related to flufftails (Sarothruridae). We recovered a nearly complete mitochondrial genome of Nesotrochis steganinos from fossils, discovering that it is not a rallid but instead is sister to Sarothruridae, volant birds now restricted to Africa and New Guinea, and the recently extinct, flightless Aptornithidae of New Zealand. This result suggests a widespread or highly dispersive most recent common ancestor of the group. Prior to human settlement, the Caribbean avifauna had a far more cosmopolitan origin than is evident from extant species.

Origin, paleoecology, and extirpation of bluebirds and crossbills in the Bahamas across the last glacial-interglacial transition.

On low islands or island groups such as the Bahamas, surrounded by shallow oceans, Quaternary glacial-interglacial changes in climate and sea level had major effects on terrestrial plant and animal communities. We examine the paleoecology of two species of songbirds (Passeriformes) recorded as Late Pleistocene fossils on the Bahamian island of Abaco-the Eastern bluebird (Sialia sialis) and Hispaniolan crossbill (Loxia megaplaga). Each species lives today only outside of the Bahamian Archipelago, with S. sialis occurring in North and Central America and L. megaplaga endemic to Hispaniola. Unrecorded in the Holocene fossil record of Abaco, both of these species probably colonized Abaco during the last glacial interval but were eliminated when the island became much smaller, warmer, wetter, and more isolated during the last glacial-interglacial transition from ∼15 to 9 ka. Today's warming temperatures and rising sea levels, although not as great in magnitude as those that took place from ∼15 to 9 ka, are occurring rapidly and may contribute to considerable biotic change on islands by acting in synergy with direct human impacts.

Ancient DNA from a 2,500-year-old Caribbean fossil places an extinct bird (Caracara creightoni) in a phylogenetic context.

Since the late Pleistocene humans have caused the extinction of species across our planet. Placing these extinct species in the tree of life with genetic data is essential to understanding the ecological and evolutionary implications of these losses. While ancient DNA (aDNA) techniques have advanced rapidly in recent decades, aDNA from tropical species, especially birds, has been historically difficult to obtain, leaving a gap in our knowledge of the extinction processes that have influenced current distributions and biodiversity. Here we report the recovery of a nearly complete mitochondrial genome from a 2,500 year old (late Holocene) bone of an extinct species of bird, Caracara creightoni, recovered from the anoxic saltwater environment of a blue hole in the Bahamas. Our results suggest that this extinct species is sister (1.6% sequence divergence) to a clade containing the extant C. cheriway and C. plancus. Caracara creightoni shared a common ancestor with these extant species during the Pleistocene (1.2-0.4 MYA) and presumably survived on Cuba when the Bahamas was mostly underwater during Quaternary interglacial intervals (periods of high sea levels). Tropical blue holes have been collecting animals for thousands of years and will continue to improve our understanding of faunal extinctions and distributions. In particular, new aDNA techniques combined with radiocarbon dating from Holocene Bahamian fossils will allow us to place other extinct (species-level loss) and extirpated (population-level loss) vertebrate taxa in improved phylogenetic, evolutionary, biogeographic, and temporal contexts.

Predictable evolution toward flightlessness in volant island birds.

Birds are prolific colonists of islands, where they readily evolve distinct forms. Identifying predictable, directional patterns of evolutionary change in island birds, however, has proved challenging. The "island rule" predicts that island species evolve toward intermediate sizes, but its general applicability to birds is questionable. However, convergent evolution has clearly occurred in the island bird lineages that have undergone transitions to secondary flightlessness, a process involving drastic reduction of the flight muscles and enlargement of the hindlimbs. Here, we investigated whether volant island bird populations tend to change shape in a way that converges subtly on the flightless form. We found that island bird species have evolved smaller flight muscles than their continental relatives. Furthermore, in 366 populations of Caribbean and Pacific birds, smaller flight muscles and longer legs evolved in response to increasing insularity and, strikingly, the scarcity of avian and mammalian predators. On smaller islands with fewer predators, birds exhibited shifts in investment from forelimbs to hindlimbs that were qualitatively similar to anatomical rearrangements observed in flightless birds. These findings suggest that island bird populations tend to evolve on a trajectory toward flightlessness, even if most remain volant. This pattern was consistent across nine families and four orders that vary in lifestyle, foraging behavior, flight style, and body size. These predictable shifts in avian morphology may reduce the physical capacity for escape via flight and diminish the potential for small-island taxa to diversify via dispersal.

Vertebrate community on an ice-age Caribbean island.

We report 95 vertebrate taxa (13 fishes, 11 reptiles, 63 birds, 8 mammals) from late Pleistocene bone deposits in Sawmill Sink, Abaco, The Bahamas. The >5,000 fossils were recovered by scuba divers on ledges at depths of 27-35 m below sea level. Of the 95 species, 39 (41%) no longer occur on Abaco (4 reptiles, 31 birds, 4 mammals). We estimate that 17 of the 39 losses (all of them birds) are linked to changes during the Pleistocene-Holocene Transition (PHT) (∼ 15-9 ka) in climate (becoming more warm and moist), habitat (expansion of broadleaf forest at the expense of pine woodland), sea level (rising from -80 m to nearly modern levels), and island area (receding from ∼ 17,000 km(2) to 1,214 km(2)). The remaining 22 losses likely are related to the presence of humans on Abaco for the past 1,000 y. Thus, the late Holocene arrival of people probably depleted more populations than the dramatic physical and biological changes associated with the PHT.

Tropical ancient DNA reveals relationships of the extinct Bahamian giant tortoise Chelonoidis alburyorum.

Ancient DNA of extinct species from the Pleistocene and Holocene has provided valuable evolutionary insights. However, these are largely restricted to mammals and high latitudes because DNA preservation in warm climates is typically poor. In the tropics and subtropics, non-avian reptiles constitute a significant part of the fauna and little is known about the genetics of the many extinct reptiles from tropical islands. We have reconstructed the near-complete mitochondrial genome of an extinct giant tortoise from the Bahamas (Chelonoidis alburyorum) using an approximately 1 000-year-old humerus from a water-filled sinkhole (blue hole) on Great Abaco Island. Phylogenetic and molecular clock analyses place this extinct species as closely related to Galápagos (C. niger complex) and Chaco tortoises (C. chilensis), and provide evidence for repeated overseas dispersal in this tortoise group. The ancestors of extant Chelonoidis species arrived in South America from Africa only after the opening of the Atlantic Ocean and dispersed from there to the Caribbean and the Galápagos Islands. Our results also suggest that the anoxic, thermally buffered environment of blue holes may enhance DNA preservation, and thus are opening a window for better understanding evolution and population history of extinct tropical species, which would likely still exist without human impact.

Phylogenomic evidence for multiple losses of flight in ratite birds.

Ratites (ostriches, emus, rheas, cassowaries, and kiwis) are large, flightless birds that have long fascinated biologists. Their current distribution on isolated southern land masses is believed to reflect the breakup of the paleocontinent of Gondwana. The prevailing view is that ratites are monophyletic, with the flighted tinamous as their sister group, suggesting a single loss of flight in the common ancestry of ratites. However, phylogenetic analyses of 20 unlinked nuclear genes reveal a genome-wide signal that unequivocally places tinamous within ratites, making ratites polyphyletic and suggesting multiple losses of flight. Phenomena that can mislead phylogenetic analyses, including long branch attraction, base compositional bias, discordance between gene trees and species trees, and sequence alignment errors, have been eliminated as explanations for this result. The most plausible hypothesis requires at least three losses of flight and explains the many morphological and behavioral similarities among ratites by parallel or convergent evolution. Finally, this phylogeny demands fundamental reconsideration of proposals that relate ratite evolution to continental drift.

Ancient mitogenomics elucidates diversity of extinct West Indian tortoises.

We present 10 nearly complete mitochondrial genomes of the extinct tortoise Chelonoidis alburyorum from the Bahamas. While our samples represent morphologically distinct populations from six islands, their genetic divergences were shallow and resembled those among Galápagos tortoises. Our molecular clock estimates revealed that divergence among Bahamian tortoises began ~ 1.5 mya, whereas divergence among the Galápagos tortoises (C. niger complex) began ~ 2 mya. The inter-island divergences of tortoises from within the Bahamas and within the Galápagos Islands are much younger (0.09-0.59 mya, and 0.08-1.43 mya, respectively) than the genetic differentiation between any other congeneric pair of tortoise species. The shallow mitochondrial divergences of the two radiations on the Bahamas and the Galápagos Islands suggest that each archipelago sustained only one species of tortoise, and that the taxa currently regarded as distinct species in the Galápagos should be returned to subspecies status. The extinct tortoises from the Bahamas have two well-supported clades: the first includes one sample from Great Abaco and two from Crooked Island; the second clade includes tortoises from Great Abaco, Eleuthera, Crooked Island, Mayaguana, Middle Caicos, and Grand Turk. Tortoises belonging to both clades on Great Abaco and Crooked Island suggest late Holocene inter-island transport by prehistoric humans.

Exceptionally well preserved late Quaternary plant and vertebrate fossils from a blue hole on Abaco, The Bahamas.

We report Quaternary vertebrate and plant fossils from Sawmill Sink, a "blue hole" (a water-filled sinkhole) on Great Abaco Island, The Bahamas. The fossils are well preserved because of deposition in anoxic salt water. Vertebrate fossils from peat on the talus cone are radiocarbon-dated from approximately 4,200 to 1,000 cal BP (Late Holocene). The peat produced skeletons of two extinct species (tortoise Chelonoidis undescribed sp. and Caracara Caracara creightoni) and two extant species no longer in The Bahamas (Cuban crocodile, Crocodylus rhombifer; and Cooper's or Gundlach's Hawk, Accipiter cooperii or Accipiter gundlachii). A different, inorganic bone deposit on a limestone ledge in Sawmill Sink is a Late Pleistocene owl roost that features lizards (one species), snakes (three species), birds (25 species), and bats (four species). The owl roost fauna includes Rallus undescribed sp. (extinct; the first Bahamian flightless rail) and four other locally extinct species of birds (Cooper's/Gundlach's Hawk, A. cooperii/gundlachii; flicker Colaptes sp.; Cave Swallow, Petrochelidon fulva; and Eastern Meadowlark, Sturnella magna) and mammals (Bahamian hutia, Geocapromys ingrahami; and a bat, Myotis sp.). The exquisitely preserved fossils from Sawmill Sink suggest a grassy pineland as the dominant plant community on Abaco in the Late Pleistocene, with a heavier component of coppice (tropical dry evergreen forest) in the Late Holocene. Important in its own right, this information also will help biologists and government planners to develop conservation programs in The Bahamas that consider long-term ecological and cultural processes.

A new genus and species of pigeon (Aves, Columbidae) from the Kingdom of Tonga, with an evaluation of hindlimb osteology of columbids from Oceania.

The region from New Guinea through Oceania sustains the world's most diverse set of columbids. We describe osteological characters of the hindlimb (femur, tibiotarsus, tarsometatarsus) that divide the Papuan-Oceanic pigeons and doves into three groups based on functional morphology: "arboreal" (Hemiphaga, Ducula, Ptilinopus, Drepanoptila, Gymnophaps), "intermediate" (Columba, Macropygia, Reinwardtoena), and "terrestrial" (Gallicolumba [includes Alopecoenas], Trugon, Microgoura, Goura, Chalcophaps, Geopelia, Henicophaps, Caloenas, Didunculus, Otidiphaps). The arboreal and terrestrial groups are each distinctive osteologically, especially in the tibiotarsus and tarsometatarsus, which are short relative to the femur in the arboreal group, and long relative to the femur in the terrestrial group. The intermediate pigeons are more similar to arboreal than to terrestrial pigeons, but nonetheless fit in neither group. To estimate the phylogenetic relationships among or within these three groups is somewhat tentative using hindlimb osteology alone, although all five genera of arboreal pigeons have independent molecular evidence of relatedness, as do most of the genera of terrestrial pigeons.                Using the hindlimb and other osteological data as a framework, we describe a new extinct genus and species of pigeon, Tongoenas burleyi, from Holocene archaeological and Pleistocene paleontological sites on six islands (Foa, Lifuka, `Uiha, Ha`afeva, Tongatapu, and `Eua) in the Kingdom of Tonga. Tongoenas was a large-sized member of the "arboreal" pigeon group, with osteological characters that relate it to Ducula, Gymnophaps, and Hemiphaga (generally canopy frugivores) rather than with the "terrestrial" pigeons (more ground-dwelling and granivorous) such as Gallicolumba, Trugon, Microgoura, Goura, etc. (others listed above). Among volant columbids, living or extinct, only the species of Goura (from New Guinea) are larger than Tongoenas. From most of the same prehistoric sites, we also report new material of the nearly as large, extinct pigeon Ducula shutleri Worthy Burley, recently described from islands in the Vava`u Group of Tonga. Thus, D. shutleri also was widespread in Tonga before human impact. The prehistoric anthropogenic loss in Tonga of Tongoenas burleyi, Ducula shutleri, and other columbids undoubtedly had a negative impact on the dispersal regimes of Tongan forest trees. At first human contact about 2850 years ago, at least nine species of columbids in six genera inhabited the Tongan islands, where only four species in three genera exist today.

Ancient DNA and high-resolution chronometry reveal a long-term human role in the historical diversity and biogeography of the Bahamian hutia.

Quaternary paleontological and archaeological evidence often is crucial for uncovering the historical mechanisms shaping modern diversity and distributions. We take an interdisciplinary approach using multiple lines of evidence to understand how past human activity has shaped long-term animal diversity in an island system. Islands afford unique opportunities for such studies given their robust fossil and archaeological records. Herein, we examine the only non-volant terrestrial mammal endemic to the Bahamian Archipelago, the hutia Geocapromys ingrahami. This capromyine rodent once inhabited many islands but is now restricted to several small cays. Radiocarbon dated fossils indicate that hutias were present on the Great Bahama Bank islands before humans arrived at AD ~800-1000; all dates from other islands post-date human arrival. Using ancient DNA from a subset of these fossils, along with modern representatives of Bahamian hutia and related taxa, we develop a fossil-calibrated phylogeny. We found little genetic divergence among individuals from within either the northern or southern Bahamas but discovered a relatively deep North-South divergence (~750 ka). This result, combined with radiocarbon dating and archaeological evidence, reveals a pre-human biogeographic divergence, and an unexpected human role in shaping Bahamian hutia diversity and biogeography across islands.

Another new species of flightless Rail (Aves: Rallidae: Rallus) from Abaco, The Bahamas.

We describe a late Pleistocene species of extinct rail, Rallus gracilipes n. sp., from Sawmill Sink blue hole on Abaco Island, Little Bahama Bank, The Bahamas. The only other extinct rail known from any Bahamian island is the smaller Rallus cyanocavi, also from late Pleistocene contexts at Sawmill Sink. No fossils of R. gracilipes or R. cyanocavi have been found in Holocene sites on Abaco; the loss of both of these species is likely to be due to changes in climate, habitat, and island area during the Pleistocene-Holocene Transition.

The bat community of Haiti and evidence for its long-term persistence at high elevations.

Accurate accounts of both living and fossil mammal communities are critical for creating biodiversity inventories and understanding patterns of changing species diversity through time. We combined data from from14 new fossil localities with literature accounts and museum records to document the bat biodiversity of Haiti through time. We also report an assemblage of late-Holocene (1600-600 Cal BP) bat fossils from a montane cave (Trouing Jean Paul, ~1825m) in southern Haiti. The nearly 3000 chiropteran fossils from Trouing Jean Paul represent 15 species of bats including nine species endemic to the Caribbean islands. The fossil bat assemblage from Trouing Jean Paul is dominated by species still found on Hispaniola (15 of 15 species), much as with the fossil bird assemblage from the same locality (22 of 23 species). Thus, both groups of volant vertebrates demonstrate long-term resilience, at least at high elevations, to the past 16 centuries of human presence on the island.

A new extinct species of Snipe (Aves: Scolopacidae: Gallinago) from the West Indies.

We describe an extinct species of snipe (Gallinago kakuki, new species) from late Quaternary fossils in the Bahamian Archipelago (Abaco, New Providence, Little Exuma, Long, and Middle Caicos islands). The new species is known as well from fossils on Cuba, and Cayman Brac in the Cayman Islands. This rather large species of snipe was volant, although because of its relatively short carpometacarpus, the primary flight feathers probably were short. The only other species of Gallinago from the West Indies is the extant, migratory G. delicata, which breeds only in North America. Gallinago kakuki shares more osteological characters with two Eurasian species (G. media, G. hardwickii) than with either of the New World species we examined (G. delicata, G. paraguaiae). A possible inter-hemispherical relationship has been proposed as well for the two extinct, late Quaternary species of woodcocks from the West Indies (Scolopax anthonyi of Puerto Rico, S. brachycarpa of Hispaniola).

A new species of Woodcock (Aves: Scolopacidae: Scolopax) from Hispaniola, West Indies.

Several hundred late Holocene fossils from Trouing Jean Paul, a cave in Massif de la Selle, Haiti, represent an extinct species of woodcock (Scolopax brachycarpa, new species). Scolopax brachycarpa is known from most major skeletal elements; although volant, its carpometacarpus was very short relative to its humerus. The only other species of Scolopax from the West Indies is the extinct and presumably closely related S. anthonyi of Puerto Rico, which also had a relatively short carpometacarpus compared to continental congeners. Both Scolopax brachycarpa and S. anthonyi share more osteological characters with the Eurasian S. rusticola than with the North American S. minor.

Fossils reject climate change as the cause of extinction of Caribbean bats.

We combined novel radiocarbon dates of bat fossils with time-scaled ecological niche models (ENM) to study bat extinctions in the Caribbean. Radiocarbon-dated fossils show that late Quaternary losses of bat populations took place during the late Holocene (<4 ka) rather than late Pleistocene (>10 ka). All bat radiocarbon dates from Abaco (Bahamas) that represent extirpated populations are younger than 4 ka. We include data on six bat species, three of which are Caribbean endemics, and include nectarivores as well as insectivores. Climate-based ENMs from the Last Glacial Maximum to the present reflect overall stability in distributions, with suitable climatic habitat being present over time. In the absence of radiocarbon dates, bat extinctions had been presumed to take place during the last glacial-interglacial transition (ca. 10 ka). Now we see that extirpation of bats on these tropical islands is more complex than previously thought and primarily postdates the major climate changes that took place during the late Pleistocene-Holocene transition.