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Research model and softwareCLIMEX modelFAW growth and development are primarily related to climate conditions, especially temperature patterns17. The current study used CLIMEX (version 4)42, a semi-mechanistic niche modeling platform, to project FAW distribution in relation to climate. The model parameters that describe the species’ response to climate were overlaid onto FAW occurrence data and climate data to project the species’ potential global distribution. Briefly, the annual growth index (GI) was used to describe the potential for FAW population growth during favorable climatic conditions, while stress indices (SI: cold, wet, hot, and dry) and interaction stresses (SX: hot-dry, hot-wet, cold-dry, and cold-wet) (Table 1) were applied to describe the probability that FAW populations could survive unfavorable conditions. The Ecoclimatic index (EI) was derived from a combination of GI, SI, and SX indices to provide an overall annual index of climatic suitability on a scale of 0–10042. An EI value of 0 indicates that the location is not suitable for the long-term survival of the species, whereas an EI value of 100 indicates maximum climatic suitability comparable to conditions in incubators. EI values of more than 30 indicate the optimal climate for a species. In this study, the climatic suitability was classified into four arbitrary categories; unsuitable for EI = 0, marginal for 0  More

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Deer capture and samplingWe captured 100 mule deer (54 females, 46 males) during November 2018–February 2019, avoiding capture and sampling of juveniles. We attempted to distribute captures throughout the ~23 km2 study area described by Miller et al.5 to minimize spatial disparities in comparing contemporary and past data, and to assure marks were widely distributed for December ground counts to estimate deer abundance5,35,36. Field and sampling methods generally followed those used elsewhere5,31,37. Field procedures were reviewed and approved by the CPW Animal Care and Use Committee (file 14–2018).We pursued deer on foot and darted them opportunistically, delivering sedative combinations intramuscularly via projectile syringe. Premixed immobilization drug combinations included either nalbuphine (N; 0.9 mg/kg) or butorphanol (B; 0.5 mg/kg) combined with azaperone (A; 0.2 mg/kg) and medetomidine (M; 0.2 mg/kg)38, with standard total doses for respective combinations based on an estimated mass of 70 kg (average drug volume per animal was 1.3 ml NMA, 1.4 ml BAM). We collected rectal mucosa biopsies to determine CWD infection status37. We also collected whole blood and marked all deer with individually identifiable ear tags and some with telemetry (n = 51) or visual identification (n = 12) collars. Ages were estimated to the nearest year via tooth replacement and wear patterns39; observers used a pocket reference guide in the field to help assure consistency. To antagonize sedation upon completion of handling and sampling, each deer received 5 mg atipamezole/mg M administered, injected intramuscularly.Prion diagnosticsFormalin-fixed tissue biopsies were processed and analyzed by immunohistochemistry (IHC) at the Colorado State University Veterinary Diagnostic Laboratory (Fort Collins, Colorado USA; CSUVDL) for evidence of CWD-associated prion (PrPCWD) accumulations using monoclonal antibody F99/97.6.1 (VMRD Inc., Pullman, Washington, USA)40 and standard IHC methods24,37,41, except that the CSUVDL’s IHC staining machine (Leica Microsystems Inc., Buffalo Grove, Illinois, USA) was different from that used in earlier studies (Ventana Medical Systems, Oro Valley, Arizona, USA). Biopsies were evaluated microscopically and classified as positive (infected) or not detected (negative) based on PrPCWD presence or absence; the same pathologist (T. R. Spraker) read biopsies for both the current and prior5 studies.We included only data from deer with biopsies providing ≥3 lymphoid follicles in analyses involving infection status in order to maintain a relatively high (≥90%) probability of detecting infected individuals24. Two animals with low follicle counts that died shortly after capture were excepted by substituting postmortem IHC results. Limiting the acceptable follicle count excluded seven females (two 225SS, five 225SF) and two males (one 225SS, one 225SF) from some analyses. One male deer was 225FF and one female deer was missing a blood sample and thus not assigned to a PRNP gene group; these two individuals also were excluded from some analyses (e.g., Table 1).
PRNP genotypingWe used DNA extracted from whole blood buffy coat aliquots (n = 99) to screen for the presence of sequences at PRNP gene codon 225 that encode for serine (S) and/or phenylalanine (F) in the mature prion polypeptide, classifying individuals as 225SS, 225SF, or 225FF16,36,42. Methods generally followed those described by Jewell et al.16. Briefly, we extracted DNA using the DNeasy® blood and tissue kit (Qiagen, Valenica, California, USA). We amplified the complete open reading frame (ORF) plus 25 bp of 5′ flanking sequences and 53 bp of 3′ flanking sequences in the PRNP coding region using polymerase chain reaction (PCR). Purified DNA was combined in a 0.2 ml PCR tube containing a puReTag Ready-To-Go PCR bead (illustra™, GE Healthcare Bio-Sciences Corp, Piscataway, New Jersey, USA). Each PCR bead contained 2.5 units puReTag DNA polymerase, 10 mM Tris-HCI, 50 mM KCl, 1.5 mM MgCl2, 200 µM of each deoxynucleoside triphosphate, and stabilizers, including bovine serum albumin. For each PCR assay, 1 μL of each primer at 200 nM, 22 μL of RNase-free water and 1 μL of approximately 100 ng total genomic DNA was added for a final volume of 25 μL. Primers used for amplification were forward (MD582F, 5′-ACATGGGCATATGATGCTGACACC-3′) and reverse (MD1479RC, 5′-ACTACAGGGCTGCAGGTAGATACT-3′) described by Jewell et al.16. Reactions were thermal-cycled in a PTC 100 (MJ Research) at 94 C for 5 min and then 32 cycles of 94 C for 7 s, 62 C for 15 s, 72 C for 30 s and a final cycle of 72 C for 5 min, and kept at 4 C until inspected for successful amplification by agarose gel electrophoresis. As confirmed by LaCava et al.19, the MD582F and MD1479RC primers developed by Jewell et al.16 specifically amplify the functional PRNP gene ORF, thereby excluding confounding effects that could arise from the presence of a processed pseudogene that occurs in a majority of deer (Odocoileus spp.)42.We used EcoRI restriction digestion of the PCR-amplified PRNP region16—a validated assay targeting the singular polymorphism at codon 225 in mule deer—to screen all 99 samples for presence of S or F codons. Aliquots (10 μl) of completed PCR reactions were incubated with 10 U EcoRI (New England Biolabs) in a total volume of 12 μl containing 50 mM NaCl, 100 mM Tris/HCl, 10 mM MgCl2, 0.025% Triton X-100 (pH 7.5) at 37 C for 2–16 h followed by the addition of 2.5 μl 6× concentrate gel loading solution (Sigma- Aldrich) per sample, and the inspection of products by agarose gel electrophoresis for the presence of one 897bp-sized band for 225SS, two bands—one 897 bp and one 719 bp—for 225SF, or one 719 bp-sized band for 225FF. As noted by Jewell et al.16, occurrence of TTC (the F codon) at position 225 creates an EcoRI recognition DNA sequence and cleavage site GAATTC from codons 224–225, whereas TCC (the S codon) creates the sequence GAATCC, which is not cut by EcoRI. When incubated with EcoRI, PCR products with a TTC codon at position 225 yielded cleavage fragments of the predictable sizes listed16. Because no other sites within the PRNP ORF DNA sequence are potentially transformable to GAATTC with one base change, this represents a specific genotyping method for assessing the S225F polymorphism in mule deer16.To confirm findings from EcoRI screening, we examined sequences of the complete PRNP ORF from 20 samples that showed evidence of cleavage indicating 225*F and 6 samples without cleavage identified as 225SS. For DNA sequencing, we used primers 245 (5′-GGTGGTGACTGACTGTGTGTTGCTTGA-3′), 12 (5′-TGGTGGTGACTGTGTGTTGCTTGA-3′) and 3FL1 (5′-GATTAAGAAGATAATGAAAACAGGAAGG-3′; Integrated DNA Technologies). Sanger sequencing was done on purified PCR product by Eurofins Genomics (Louisville, Kentucky, USA). Sequence chromatograms were viewed and DNA sequence alignments and comparisons were made using the MAFFT multiple sequence alignment program v7.450 module, software platform v2020.2.3 of Geneious Prime. Sequencing confirmed the presence of coding for F in all samples identified as 225*F by EcoRI digestion, as well as the absence of such coding in samples identified by EcoRI digestion as 225SS. Moreover, presence of AGC at codon 138 in all sequenced samples reconfirmed that the primers we used had amplified the functional PRNP gene42.Statistics and reproducibilityFor analyses, we tabulated IHC-positive and -negative results to estimate apparent prevalence of prion infection. We also tabulated the number of individuals assigned to PRNP genotypes and to age groupings as described. Age groupings were selected based on relevance to CWD epidemiology in mule deer1,5,8,12,16,17,18,20,24,31,37. Assuming a ~2-year disease course5,8,17 and relative scarcity of end-stage disease in 225SS deer More

NEWS
11 January 2022

Landmark Colombian bird study repeated to right colonial-era wrongs

A re-run of a 100-year-old, US-led bird survey will inform future conservation efforts — but be helmed by local researchers.

Luke Taylor

Luke Taylor

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Ornithologist Andrés Cuervo takes a selfie of a team of Colombia Resurvey Project researchers during an expedition in Caquetá.Credit: Andrés M. Cuervo

Colombia has more animal and plant species per square kilometre than anywhere else in the world. Pioneering US bird scientist Frank Chapman once said that the country was so rich in biodiversity that when his research team explored the area in the early twentieth century, it could have studied a single mountain range for five years and still not have mapped all of its fauna.More than 100 years later, Colombian researchers are redoing his legendary bird survey, which is a reference for ornithologists the world over. They are surveying the areas that Chapman catalogued between 1911 and 1915, to investigate how a century of war, global warming and industrialization has affected the landscape and its biodiversity.
The world’s species are playing musical chairs: how will it end?
But this project will not snatch birds and whisk them to a museum abroad — as Chapman’s team did. Instead, local scientists will keep specimens in Colombia and engage with local communities during their expeditions, to include them in the momentous endeavour, improve the quality of the research and set an ethical standard for future fieldwork.Chapman and at least 5 other collectors shot many of the nearly 16,000 birds that they hauled back to the American Museum of Natural History in New York City, offering local residents little explanation — or credit. “You wouldn’t like it if I came to your house, surveyed it without permission, took photos and then went back to Colombia without telling you what I had found,” says Nelsy Niño-Rodríguez, the Colombia Resurvey Project’s community-relations coordinator, who is an ornithologist at the Alexander von Humboldt Biological Resources Research Institute in Bogotá. Without local guides knowledgeable about Colombia and its birds, Chapman couldn’t possibly have located and collected so many specimens, says Natalia Ocampo-Peñuela, a research partner on the resurvey project and a conservation ecologist at the University of California, Santa Cruz. Yet Chapman’s logs hardly mention guides; when they are discussed, it’s usually in racist or pejorative terms, she says.“His interest was to feed his curiosity, his scientific intellect and the museum,” she adds, but not to inform the wider population — and definitely not the local populations.A changed landscape Colombian researchers have dreamt of re-running Chapman’s expeditions for decades. But it wasn’t possible until the past few years, because many areas were inaccessible owing to armed conflict. Following a landmark peace deal in 2016, remote regions that had been under the control of the Revolutionary Armed Forces of Colombia (FARC), a left-wing guerrilla group, once again opened to exploration. That, and an infusion of funding from the Colombian government and international donors, meant researchers could attempt a resurvey.

Birds of Colombia: top, many-banded araçari (Pteroglossus pluricinctus); left, pileated finch (Coryphospingus pileatus); right, white-fringed antwren (Formicivora grisea).Credit: Andrés M. Cuervo

Chapman visited Colombia because he thought that its geography made it one of the most biodiverse places in the world. He theorized that the presence of the Andes Mountains, combined with the country’s position bridging South and Central America, made it an evolutionary melting pot.
FARC and the forest: Peace is destroying Colombia’s jungle — and opening it to science
Although Colombia is still home to around 10% of the world’s biodiversity, the forests once explored by Chapman have changed immensely. Pristine jungles have been cleared to create uniform pastures resembling golf courses, says Andrés Cuervo, an ornithologist at the National University of Colombia in Bogotá who is one of the directors of the resurvey project. The dirt tracks that Chapman and his team traversed on mules are now roads. And climate change has pushed birds to higher elevations and altered their migratory patterns.Seeking to understand the effects of these changes on biodiversity, researchers launched the Colombia Resurvey Project in 2019. The main objective is to gather bird specimens, including DNA and tissue samples, to compare the modern population with Chapman’s collection. The team, which includes US researchers as well as local ones, has so far conducted 6 expeditions, visiting 14 of Chapman’s original sites — leaving 60 to go. A useful catalogue The researchers are finding that they have to venture deep into the forest to find birds that were once a stone’s throw from Chapman’s campsites, Cuervo says. And some species are nowhere to be found, including the red-ruffed fruitcrow (Pyroderus scutatus) — almost certainly lost when the trees in its territory were cut down to grow avocados, he adds.

Resurvey project researchers Jessica Diaz (right) and Andrés Sierra (left) record data from a mist net, used to collect birds during expeditions.Credit: Andrés M. Cuervo

The team has also confirmed that birds dependent on unique ecosystems are being replaced by generalist species — which are more adaptable to fragmented forest and a disrupted diet — reducing the country’s biodiversity1. Larger species and fruit eaters seem to have been hit particularly hard over the past century, because they require vast expanses of forest to thrive.
Illegal mining in the Amazon hits record high amid Indigenous protests
The effects of climate and landscape changes on bird populations in the tropics are not well understood, so the project will inform future conservation efforts, researchers say. “It’s almost impossible to imagine all the ways in which this data can potentially be used down the road,” says John Bates, curator and head of life sciences at the Field Museum of Natural History in Chicago, Illinois. Members of the resurvey project hope their catalogue will have as much impact as Chapman’s. It will include resources such as a genomic map illustrating birds’ evolution, generated from DNA samples. “We are collecting the most complete set of specimens that one can imagine so that scientists from now and the future can answer questions that we haven’t thought of,” Ocampo says.Taking chargeThe Colombia Resurvey Project team especially hopes that its anti-colonial approach will resonate with the scientific community. The researchers run workshops before each excursion to inform local communities about why they are planning to kill some birds, and how this is important for conservation and science. They are storing the specimens at the National University of Colombia, where the birds will be digitally catalogued, so that people can view them online, listen to audio of their song and scroll through interactive maps of the expeditions. And the team is creating birdwatching tours at the expedition sites to boost tourism.
Brazilian road proposal threatens famed biodiversity hotspot
Involving communities leads to better results, Niño-Rodríguez says. For instance, even if some Indigenous people do not know the scientific names for birds, they might be able to identify them on sight and know where they are most likely to be found. And community knowledge of how the forests have changed has passed from generation to generation, so local residents are able to fill gaps when satellite data and research logs aren’t available.It’s equally important to the researchers that those leading the project are from Colombia. They say it’s common for local experts to help visiting foreign researchers to find new species and make discoveries, but be excluded from the scientific process and the credit. “We don’t want to be the guys with the permits or the guys who facilitate the logistics of someone else’s research,” Cuervo says. “We want to do our own high-quality research, and we want it to be available for people to use.” This time around, the American Museum of Natural History is a partner on the project, rather than its lead. “Although the Chapman expedition was conducted with help and permissions from the Colombian government, today’s expeditions appropriately look much different than they did in Chapman’s time,” says a museum spokesperson, adding that the museum “is proud of the very active relationship it maintains with Colombia’s scientific institutions through education and research”.
Colombia: after the violence
Meanwhile, project researchers are training curious members of local communities in how to identify birds scientifically, so they can continue to log species with their cameras and mobile phones once the researchers leave the forest. Areas previously ruled by FARC guerrillas are now falling under the control of other armed groups, which might not let outsiders in, so local residents could soon be the only people who have access to some of Colombia’s most biodiverse jungles and the birds that inhabit them.“Hopefully we won’t have to wait another hundred years for scientists to return to these sites and assess their bird fauna,” Cuervo says. “Communities can do it with empowerment and interest in their biodiversity and surroundings.”

Nature 601, 178-179 (2022)
doi: https://doi.org/10.1038/d41586-021-03527-x

References1.Gómez, C., Tenorio, E. A. & Cadena, C. D. Conserv. Biol. 35, 1552–1563 (2021).PubMed 
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