Using Bird Distributions to Assess Extinction Risk and Identify Conservation Priorities in Biodiversity Hotspots

Habitat loss, fragmentation, and degradation threaten the World’s ecosystems and species. These, and other threats, will likely be exacerbated by climate change. Due to a limited budget for conservation, we are forced to prioritize a few areas over others. These places are selected based on their uniqueness and vulnerability. One of the most famous examples is the biodiversity hotspots: areas where large quantities of endemic species meet alarming rates of habitat loss. Most of these places are in the tropics, where species have smaller ranges, diversity is higher, and ecosystems are most threatened.

Species distributions are useful to understand ecological theory and evaluate extinction risk. Small-ranged species, or those endemic to one place, are more vulnerable to extinction than widely distributed species. However, current range maps often overestimate the distribution of species, including areas that are not within the suitable elevation or habitat for a species. Consequently, assessment of extinction risk using these maps could underestimate vulnerability.

In order to be effective in our quest to conserve the World’s most important places we must: 1) Translate global and national priorities into practical local actions, 2) Find synergies between biodiversity conservation and human welfare, 3) Evaluate the different dimensions of threats, in order to design effective conservation measures and prepare for future threats, and 4) Improve the methods used to evaluate species’ extinction risk and prioritize areas for conservation. The purpose of this dissertation is to address these points in Colombia and other global biodiversity hotspots.

In Chapter 2, I identified the global, strategic conservation priorities and then downscaled to practical local actions within the selected priorities in Colombia. I used existing range maps of 171 bird species to identify priority conservation areas that would protect the greatest number of species at risk in Colombia (endemic and small-ranged species). The Western Andes had the highest concentrations of such species—100 in total—but the lowest densities of national parks. I then adjusted the priorities for this region by refining these species ranges by selecting only areas of suitable elevation and remaining habitat. The estimated ranges of these species shrank by 18–100% after accounting for habitat and suitable elevation. Setting conservation priorities on the basis of currently available range maps excluded priority areas in the Western Andes and, by extension, likely elsewhere and for other taxa. By incorporating detailed maps of remaining natural habitats, I made practical recommendations for conservation actions. One recommendation was to restore forest connections to a patch of cloud forest about to become isolated from the main Andes.

For Chapter 3, I identified areas where bird conservation met ecosystem service protection in the Central Andes of Colombia. Inspired by the November 11th (2011) landslide event near Manizales, and the current poor results of Colombia’s Article 111 of Law 99 of 1993 as a conservation measure in this country, I set out to prioritize conservation and restoration areas where landslide prevention would complement bird conservation in the Central Andes. This area is one of the most biodiverse places on Earth, but also one of the most threatened. Using the case of the Rio Blanco Reserve, near Manizales, I identified areas for conservation where endemic and small-range bird diversity was high, and where landslide risk was also high. I further prioritized restoration areas by overlapping these conservation priorities with a forest cover map. Restoring forests in bare areas of high landslide risk and important bird diversity yields benefits for both biodiversity and people. I developed a simple landslide susceptibility model using slope, forest cover, aspect, and stream proximity. Using publicly available bird range maps, refined by elevation, I mapped concentrations of endemic and small-range bird species. I identified 1.54 km2 of potential restoration areas in the Rio Blanco Reserve, and 886 km2 in the Central Andes region. By prioritizing these areas, I facilitate the application of Article 111 which requires local and regional governments to invest in land purchases for the conservation of watersheds.

Chapter 4 dealt with elevational ranges of montane birds and the impact of lowland deforestation on their ranges in the Western Andes of Colombia, an important biodiversity hotspot. Using point counts and mist-nets, I surveyed six altitudinal transects spanning 2200 to 2800m. Three transects were forested from 2200 to 2800m, and three were partially deforested with forest cover only above 2400m. I compared abundance-weighted mean elevation, minimum elevation, and elevational range width. In addition to analyzing the effect of deforestation on 134 species, I tested its impact within trophic guilds and habitat preference groups. Abundance-weighted mean and minimum elevations were not significantly different between forested and partially deforested transects. Range width was marginally different: as expected, ranges were larger in forested transects. Species in different trophic guilds and habitat preference categories showed different trends. These results suggest that deforestation may affect species’ elevational ranges, even within the forest that remains. Climate change will likely exacerbate harmful impacts of deforestation on species’ elevational distributions. Future conservation strategies need to account for this by protecting connected forest tracts across a wide range of elevations.

In Chapter 5, I refine the ranges of 726 species from six biodiversity hotspots by suitable elevation and habitat. This set of 172 bird species for the Atlantic Forest, 138 for Central America, 100 for the Western Andes of Colombia, 57 for Madagascar, 102 for Sumatra, and 157 for Southeast Asia met the criteria for range size, endemism, threat, and forest use. Of these 586 species, the Red List deems 108 to be threatened: 15 critically endangered, 29 endangered, and 64 vulnerable. When ranges are refined by elevational limits and remaining forest cover, 10 of those critically endangered species have ranges < 100km2, but then so do 2 endangered species, seven vulnerable, and eight non-threatened ones. Similarly, 4 critically endangered species, 20 endangered, and 12 vulnerable species have refined ranges < 5000km2, but so do 66 non-threatened species. A striking 89% of these species I have classified in higher threat categories have <50% of their refined ranges inside protected areas. I find that for 43% of the species I assessed, refined range sizes fall within thresholds that typically have higher threat categories than their current assignments. I recommend these species for closer inspection by those who assess risk. These assessments are not only important on a species-by-species basis, but by combining distributions of threatened species, I create maps of conservation priorities. They differ significantly from those created from unrefined ranges.

Delimiting species without nuclear monophyly in Madagascar's mouse lemurs.

BACKGROUND: Speciation begins when populations become genetically separated through a substantial reduction in gene flow, and it is at this point that a genetically cohesive set of populations attain the sole property of species: the independent evolution of a population-level lineage. The comprehensive delimitation of species within biodiversity hotspots, regardless of their level of divergence, is important for understanding the factors that drive the diversification of biota and for identifying them as targets for conservation. However, delimiting recently diverged species is challenging due to insufficient time for the differential evolution of characters--including morphological differences, reproductive isolation, and gene tree monophyly--that are typically used as evidence for separately evolving lineages. METHODOLOGY: In this study, we assembled multiple lines of evidence from the analysis of mtDNA and nDNA sequence data for the delimitation of a high diversity of cryptically diverged population-level mouse lemur lineages across the island of Madagascar. Our study uses a multi-faceted approach that applies phylogenetic, population genetic, and genealogical analysis for recognizing lineage diversity and presents the most thoroughly sampled species delimitation of mouse lemur ever performed. CONCLUSIONS: The resolution of a large number of geographically defined clades in the mtDNA gene tree provides strong initial evidence for recognizing a high diversity of population-level lineages in mouse lemurs. We find additional support for lineage recognition in the striking concordance between mtDNA clades and patterns of nuclear population structure. Lineages identified using these two sources of evidence also exhibit patterns of population divergence according to genealogical exclusivity estimates. Mouse lemur lineage diversity is reflected in both a geographically fine-scaled pattern of population divergence within established and geographically widespread taxa, as well as newly resolved patterns of micro-endemism revealed through expanded field sampling into previously poorly and well-sampled regions.

Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor.

BACKGROUND: The availability of multiple avian genome sequence assemblies greatly improves our ability to define overall genome organization and reconstruct evolutionary changes. In birds, this has previously been impeded by a near intractable karyotype and relied almost exclusively on comparative molecular cytogenetics of only the largest chromosomes. Here, novel whole genome sequence information from 21 avian genome sequences (most newly assembled) made available on an interactive browser (Evolution Highway) was analyzed. RESULTS: Focusing on the six best-assembled genomes allowed us to assemble a putative karyotype of the dinosaur ancestor for each chromosome. Reconstructing evolutionary events that led to each species' genome organization, we determined that the fastest rate of change occurred in the zebra finch and budgerigar, consistent with rapid speciation events in the Passeriformes and Psittaciformes. Intra- and interchromosomal changes were explained most parsimoniously by a series of inversions and translocations respectively, with breakpoint reuse being commonplace. Analyzing chicken and zebra finch, we found little evidence to support the hypothesis of an association of evolutionary breakpoint regions with recombination hotspots but some evidence to support the hypothesis that microchromosomes largely represent conserved blocks of synteny in the majority of the 21 species analyzed. All but one species showed the expected number of microchromosomal rearrangements predicted by the haploid chromosome count. Ostrich, however, appeared to retain an overall karyotype structure of 2n=80 despite undergoing a large number (26) of hitherto un-described interchromosomal changes. CONCLUSIONS: Results suggest that mechanisms exist to preserve a static overall avian karyotype/genomic structure, including the microchromosomes, with widespread interchromosomal change occurring rarely (e.g., in ostrich and budgerigar lineages). Of the species analyzed, the chicken lineage appeared to have undergone the fewest changes compared to the dinosaur ancestor.

Distribution and Conservation of the Antillean Manatee in Hispaniola

Antillean manatees (Trichechus manatus manatus) were heavily hunted in the past throughout the Wider Caribbean Region (WCR), and are currently listed as endangered on the IUCN Red List of Threatened Species. In most WCR countries, including Haiti and the Dominican Republic, remaining manatee populations are believed to be small and declining, but current information is needed on their status, distribution, and local threats to the species.

To assess the past and current distribution and conservation status of the Antillean manatee in Hispaniola, I conducted a systematic review of documentary archives dating from the pre-Columbian era to 2013. I then surveyed more than 670 artisanal fishers from Haiti and the Dominican Republic in 2013-2014 using a standardized questionnaire. Finally, to identify important areas for manatees in the Dominican Republic, I developed a country-wide ensemble model of manatee distribution, and compared modeled hotspots with those identified by fishers.

Manatees were historically abundant in Hispaniola, but were hunted for their meat and became relatively rare by the end of the 19th century. The use of manatee body parts diversified with time to include their oil, skin, and bones. Traditional uses for folk medicine and handcrafts persist today in coastal communities in the Dominican Republic. Most threats to Antillean manatees in Hispaniola are anthropogenic in nature, and most mortality is caused by fisheries. I estimated a minimum island-wide annual mortality of approximately 20 animals. To understand the impact of this level of mortality, and to provide a baseline for measuring the success of future conservation actions, the Dominican Republic and Haiti should work together to obtain a reliable estimate of the current population size of manatees in Hispaniola.

In Haiti, the survey of fishers showed a wider distribution range of the species than suggested by the documentary archive review: fishers reported recent manatee sightings in seven of nine coastal departments, and three manatee hotspot areas were identified in the north, central, and south coasts. Thus, the contracted manatee distribution range suggested by the documentary archive review likely reflects a lack of research in Haiti. Both the review and the interviews agreed that manatees no longer occupy freshwater habitats in the country. In general, more dedicated manatee studies are needed in Haiti, employing aerial, land, or boat surveys.

In the Dominican Republic, the documentary archive review and the survey of fishers showed that manatees still occur throughout the country, and occasionally occupy freshwater habitats. Monte Cristi province in the north coast, and Barahona province in the south coast, were identified as focal areas. Sighting reports of manatees decreased from Monte Cristi eastwards to the adjacent province in the Dominican Republic, and westwards into Haiti. Along the north coast of Haiti, the number of manatee sighting and capture reports decreased with increasing distance to Monte Cristi province. There was good agreement among the modeled manatee hotspots, hotspots identified by fishers, and hotspots identified during previous dedicated manatee studies. The concordance of these results suggests that the distribution and patterns of habitat use of manatees in the Dominican Republic have not changed dramatically in over 30 years, and that the remaining manatees exhibit some degree of site fidelity. The ensemble modeling approach used in the present study produced accurate and detailed maps of manatee distribution with minimum data requirements. This modeling strategy is replicable and readily transferable to other countries in the Caribbean or elsewhere with limited data on a species of interest.

The intrinsic value of manatees was stronger for artisanal fishers in the Dominican Republic than in Haiti, and most Dominican fishers showed a positive attitude towards manatee conservation. The Dominican Republic is an upper middle income country with a high Human Development Index. It possesses a legal framework that specifically protects manatees, and has a greater number of marine protected areas, more dedicated manatee studies, and more manatee education and awareness campaigns than Haiti. The constant presence of manatees in specific coastal segments of the Dominican Republic, the perceived decline in the number of manatee captures, and a more conservation-minded public, offer hope for manatee conservation, as non-consumptive uses of manatees become more popular. I recommend a series of conservation actions in the Dominican Republic, including: reducing risks to manatees from harmful fishing gear and watercraft at confirmed manatee hotspots; providing alternative economic alternatives for displaced fishers, and developing responsible ecotourism ventures for manatee watching; improving law enforcement to reduce fisheries-related manatee deaths, stop the illegal trade in manatee body parts, and better protect manatee habitat; and continuing education and awareness campaigns for coastal communities near manatee hotspots.

In contrast, most fishers in Haiti continue to value manatees as a source of food and income, and showed a generally negative attitude towards manatee conservation. Haiti is a low income country with a low Human Development Index. Only a single dedicated manatee study has been conducted in Haiti, and manatees are not officially protected. Positive initiatives for manatees in Haiti include: protected areas declared in 2013 and 2014 that enclose two of the manatee hotspots identified in the present study; and local organizations that are currently working on coastal and marine environmental issues, including research and education on marine mammals. Future conservation efforts for manatees in Haiti should focus on addressing poverty and providing viable economic alternatives for coastal communities. I recommend a community partnership approach for manatee conservation, paired with education and awareness campaigns to inform coastal communities about the conservation situation of manatees in Haiti, and to help change their perceived value. Haiti should also provide legal protection for manatees and their habitat.