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The use of genetics for the management of a recovering population: temporal assessment of migratory peregrine falcons in North America

Background:Our ability to monitor populations or species that were once threatened or endangered and in the process of recovery is enhanced by using genetic methods to assess overall population stability and size over time. This can be accomplished most directly by obtaining genetic measures from temporally-spaced samples that reflect the overall stability of the population as given by changes in genetic diversity levels (allelic richness and heterozygosity), degree of population differentiation (F ST and D EST ), and effective population size (N e ). The primary goal of any recovery effort is to produce a long-term self-sustaining population, and these measures provide a metric by which we can gauge our progress and help make important management decisions. Methodology/Principal Findings:The peregrine falcon in North America ( Falco peregrinus tundrius and anatum ) was delisted in 1994 and 1999, respectively, and its abundance will be monitored by the species Recovery Team every three years until 2015. Although the United States Fish and Wildlife Service makes a distinction between tundrius and anatum subspecies, our genetic results based on eleven microsatellite loci, including those from Brown et al. (2007), suggest no differentiation and warrant delineation of a subspecies in its northern latitudinal distribution from Alaska through Canada into Greenland. Using temporal samples collected at Padre Island, Texas during migration (seven temporal time periods between 1985-2007), no significant differences in genetic diversity or significant population differentiation in allele frequencies between time periods were observed and were indistinguishable from those obtained from tundrius/anatum breeding locations throughout their northern distribution. Estimates of harmonic mean N e were variable and imprecise, but always greater than 500 when employing multiple temporal genetic methods. These results, including those from simulations to assess the power of each method to estimate Ne, suggest a stable population consistent with data from field-based monitoring indicating that this species is stable or continuing to increase in abundance. Therefore, historic and continuing efforts to prevent the extinction of the peregrine falcon in North America appear successful, further highlighting the importance of archiving samples for continual assessment of population recovery and long-term viability.

PLoS ONE

Decline and present status of breeding Peregrine Falcons in Oregon

Unprecedented declines of the Peregrine Falcon ( Falco peregrinus ) throughout much of the Northern Hemisphere became apparent during the Madison Peregrine Falcon Conference in 1965 (Hickey 1969). Data from Britain were the most detailed; broken or missing eggs were much more common in 1949-56 than they had been in earlier years (Ratcliffe 1958). Subsequently, Ratcliffe (1967) showed a significant decrease in eggshell weight of peregrines in Britain starting in 1947 or 1948. Later, the same finding was demonstrated in North America (Hickey and Anderson 1968). The relation of eggshell thickness to DDE residue levels was established for Alaskan peregrines by Cade et al. (1971) and Peakall et al. (1975). Peakall (1976) stated that pesticides were considered to be a major factor in the decline of the peregrine, and tentatively concluded that the level of DDE in eggs that failed to hatch was 15-20 ppm (wet weight.)

Oregon

Incorporating productivity as a measure of fitness into models of breeding area quality of Arctic peregrine falcons

Using empirical location data from individuals to model habitat quality and species distributions is valuable towards understanding habitat use of wildlife, especially for conservation and management planning. Incorporating measures of reproductive success or survival into these models helps address the role of vital rates (a surrogate of fitness) in affecting a species’ distribution. We used 24-year datasets of Arctic peregrine falcon ( Falco peregrinus tundrius ) nest-site locations and productivity from the Colville River Special Area, Alaska, USA to model suitability of breeding habitat and the relative quality of used and potential nest sites. We used zero-inflated negative binomial regression models and covariates describing nest-site productivity, area of surrounding prey habitat, geology, topography, and land-cover type to model and predict intensity of Arctic peregrine falcon nest-site use along the Colville River, and developed a predictive map of intensity of nest-site use. Regions of higher predicted intensity of use were characterized by steeper slopes, greater area of prey habitat, and higher average productivity, which are likely attributed to minimizing predation risk, gaining advantages for hunting, having sufficient prey resources, site quality, and overall fitness. Including productivity in intensity of nest-site use models improved the models, supporting our supposition that adding a fitness parameter enhanced the predictive capability of the species distribution model. Areas predicted to have higher intensity of use by our model can be used to focus efforts of continued protection of areas with frequently occupied and productive nest sites, and conversely, identify areas where protection of nest sites is likely to have few conservation benefits.

Alaska

Falcons

Four species of Falco occur in the northeastern United States. The gyrfalcon is a rare winter visitor. The peregrine falcon federally listed as endangered, is a migrant and through reestablishment is breeding and wintering locally throughout the northeast. The merlin is a migrant and uncommon winter bird. The American kestrel breeds, winters, and migrates in the northeast. A 22-year analysis of the American kestrel Breeding Bird Survey data showed populations to be stable in less developed areas and declining in more developed areas. By states, declines occurred in the more developed areas of New Hampshire, Massachusetts, Connecticut and Pennsylvania, and data indicate a decrease in American kestrels from 1957 to 1966, a decrease in merlins between 1967 and 1974 and a decrease in peregrine falcons between 1940 and 1975. Migration counts indicate decreasing American kestrel numbers from 1973 to 1986, but an increasing trend from 1934 to 1986.

Book chapter

Saker falcon research and conservation efforts in Mongolia, 1997

This past summer. our small field team followed a 4000 km route through central and eastern Mongolia. Even though there was a population crash underway for picas (Ochotona sp.) and voles (Microtus sp.). we found 38 new saker nests and visited 60 eyries found in previous years. Many of the former eyries were unoccupied. Others were occupied but without young. Productivity was good at eyries with large young. and southeastern Mongolia seemed unaffected by food shortages. The main goal for 1997 was to create new eyries and enlarge. stabilise. or otherwise alter marginal eyries. \Ve created 65 eyries as follows: 8 on wooden powerlines or telephone supports, 8 on metal power line towers, 3 in trees, 3 on boulders, 11 on cliffs, 17 on abandoned buildings, 9 on metal geological survey towers, and 6 on miscellaneous structures. \Ve also enlarged or repaired three establishedeyries and did minor repairs on several others. Lesser accomplishments include what may be the first observation of siblicide for the saker falcon (please contact us immediately if you have other records of sakerchicks attacking or killing their nest mates) and the description of a new saker flight display. We also documented an unusual golden eagle eyrie containing the remains of nearly 30 foxes, several predatory birds, and a number of gazelle. In 1998. we plan to return to Mongolia to see how many of our 'fake eyries' attracted falcons. Our work in 1997 was supported by Mr. Howell. another philanthropist (anonymous) and the Institute of Raptor Studies.

Falco

The austral peregrine falcon: Color variation, productivity, and pesticides

The austral peregrine falcon (Falco peregrinus cassini) was studied in the Andean foot- hills and across the Patagonian steppe from November to December 1981. The birds under study (18 pairs) were reproducing at or near normal (pre-DDT) levels for other races. Pesticide residues, while elevated, were well below the values associated with reproductive failure in other populations. With one exception, eggshells were not abnormally thin. The peregrine falcon in Patagonia exhibits extreme color variation. Pallid birds are nearly pure white below (light cream as juveniles), whereas normally pigmented birds are black-crowned and conspicuously barred with black ventrally. Rare individuals of the Normal Phase display black heads, broad black ventral barring, and warm reddish-brown ventral background coloration.

National Geographic Research

Peregrine falcon predation of endangered Laysan teal and Laysan Finches on remote Hawaiian atolls

We report the first records of Peregrine falcon ( Falco peregrinus ) predation on endangered Laysan teal (or duck; Anas laysanensis ) and predation on endangered Laysan finches ( Telespiza cantans ). At Midway Atoll, vagrant Peregrine falcons killed &ge;4% of a newly translocated Laysan teal population in 2006 and &ge;2% in 2008. On Laysan Island during 2008&ndash;2009, remains of >76 Laysan finches (<1% of the population) were found at peregrine perches. On Midway Atoll, all depredated Laysan teal and other seabirds were recovered at kill sites on tarmac (runways). If the frequency or duration of vagrant raptors visitation increases at small atolls, this could pose a mortality risk to consider, especially during proposed translocations of endangered species. Vegetation restoration of abandoned runways near wetlands at Midway Atoll would provide cover and may help reduce mortality of endangered species due to vagrant raptors.

Laysan Island, Midway atoll

Organochlorine contaminants in passeriformes and other avian prey of the peregrine falcon in the western United States

About 1,150 individuals of 38 species of Passeriformes and other small birds were collected in 1980 at 36 locations in eight western U.S. states for organochlorine (OC) chemical analysis. The bird carcasses (less beak, tarsi, gastrointestinal tract, and feathers) were combined by species and location (4 to 15 specimens per sample) into 124 composited samples for analysis. Also analyzed were 77 single specimens of four species, to assess variation in residue concentrations in individual birds. The chemicals detected (greater than 0.05 ppm) were the following (in order of frequency): DDE, polychlorinated biphenyls (PCBs), hexachlorocyclohexane (HCH), heptachlor epoxide, oxychlordane, dieldrin and toxaphene. DDE accounted for 72% of total OC concentrations (ppm DDE/ppm total OCs) overall and PCBs accounted for 3%. DDE mean (geometric) residues were highest in tree swallows ( Tachycineta bicolor Vieillot), 12.0 ppm; killdeer ( Charadrius vociferus L.), 5.9 ppm; and Brewer's blackbirds ( Euphagus cyanocephalus Wagler), 2.7 ppm. Eight migratory species showed mean DDE residues 13 times higher than those in four resident species (1.3 vs. 0.1 ppm, p < 0.05), but PCB residues were similar (0.03 vs. 0.02 ppm). Insectivorous species showed higher DDE, PCB and total OC residues than did either omnivores or granivores ( p < 0.05). Males of some species showed higher residues of DDE, PCBs and total OCs than did females ( p < 0.05). DDE residues, but not PCBs, in killdeer, Brewer's blackbirds and violet-green swallows ( Tachycineta thalassina Swainson) were significantly related (0.01 < p < 0.08) to latitude and longitude of origin. Concentrations of DDE in the carcass fat of some individual tree swallows and killdeer would be in the lethal range if 15 to 20% of the stored DDE were rapidly mobilized to the brain. Samples of 13 species contained DDE concentrations (greater than 3 ppm) considered sufficient to inhibit the normal reproduction of avian predators feeding on them. The evidence suggests that potentially harmful OC concentrations are present in certain western migrants and pose an even greater hazard to avian predators such as the peregrine falcon ( Falco peregrinus Tunstall).

Environmental Toxicology and Chemistry

Summer diet of the Peregrine Falcon in faunistically rich and poor zones of Arizona analyzed with capture-recapture modeling

We collected prey remains from 25 Peregrine Falcon ( Falco peregrinus ) territories across Arizona from 1977 to 1988 yielding 58 eyrie-years of data. Along with 793 individual birds (107 species and six additional genera), we found seven mammals and nine insects. In addition, two nestling peregrines were consumed. We found a larger dependence upon White-throated Swifts ( Aeronautes saxatalis ) and birds on migration in northern Arizona, while in southeastern and central Arizona average prey mass was greater and columbiforms formed the largest dietary component. In northern, central, and southeastern Arizona, 74, 66, and 56 avian prey taxa, respectively, were recorded. We used capture-recapture modeling to estimate totals of 111 ± 9.5, 113 ± 10.5, and 86 ± 7.9 (SE) avian taxa taken in these same three areas. These values are counterintuitive inasmuch as the southeast has the richest avifauna. For the entire study area, 156 ± 9.3 avian taxa were estimated to be taken by peregrines.

Arizona

Territory occupancy and breeding success of Peregrine Falcons Falco peregrinus at various stages of population recovery

Organochlorine pesticides disrupted reproduction and killed many raptorial birds, and contributed to population declines during the 1940s to 1970s. We sought to discern whether and to what extent territory occupancy and breeding success changed from the pesticide era to recent years in a resident population of Peregrine Falcons Falco peregrinus in southern Scotland using long-term (1964–2015) field data and multi-state, multi-season occupancy models. Peregrine territories that were occupied with successful reproduction in one year were much more likely to be occupied and experience reproductive success in the following year, compared with those that were unoccupied or occupied by unsuccessful breeders in the previous year. Probability of territory occupancy differed between territories in the eastern and western parts of the study area, and varied over time. The probability of occupancy of territories that were unoccupied and those that were occupied with successful reproduction during the previous breeding season generally increased over time, whereas the probability of occupancy of territories that were occupied after failed reproduction decreased. The probability of reproductive success (conditional on occupancy) in territories that were occupied during the previous breeding season increased over time. Specifically, for territories that had been successful in the previous year, the probability of occupancy as well as reproductive success increased steadily over time; these probabilities were substantially higher in recent years than earlier, when the population was still exposed to direct or residual effects of organochlorine pesticides. These results are consistent with the hypothesis that progressive reduction, followed by a complete ban, in the use of organochlorine pesticides improved reproductive success of Peregrines in southern Scotland. Differences in the temporal pattern of probability of reproductive success between south-eastern and south-western Scotland suggest that the effect of organochlorine pesticides on Peregrine reproductive success and/or the recovery from pesticide effects varied geographically and was possibly affected by other factors such as persecution.

Ibis

Environmental implications of Ptolemaic Period rodents and shrews from the Sacred Falcon Necropolis at Quesna, Egypt (Mammalia: Muridae and Soricidae)

Background Assemblages of mummified and preserved animals in necropoleis of Ptolemaic Period Egypt (ca. 332–30 BC) document some aspects of the ceremonial and religious practices of the ancient Egyptians, but study of these animal remains can also provide insight into the local environments in which the animals and humans lived. Results Excavations of the Sacred Falcon Necropolis at Quesna in the Nile Delta have yielded many thousands of animal remains, mostly of raptors, but also of a lesser number of small, wild mammals. Among the latter, we identified four species of murid rodents (Rodentia: Muridae) and five species of shrews (Eulipotyphla: Soricidae). The soricids are of particular interest because they represent a more diverse assemblage of species than occurs in the delta today. They include one species, Crocidura gueldenstaedtii (Pallas, 1811), that no longer occurs in the delta and another, C. fulvastra (Sundevall, 1843), that is now extirpated from Egypt. Conclusions The coexistence of this diverse small mammal community suggests that a greater availability and variety of mesic habitats were present during the Ptolemaic Period than occur there now. The local mammal faunas recovered at Quesna and other well-studied ancient Egyptian sites together provide evidence of a richer, more complex regional environment along the Nile Valley. They also provide important insight regarding the biogeography of the individual species comprising the faunas and about the extent of faunal turnover since the Ptolemaic Period.

BMC Ecology and Evolution

DDE decreases in plasma of spring migrant peregrine falcons, 1978-94

Mean p,p'-DDE (DDE) residues in plasma of combined adult and subadult female peregrine falcons (Falco peregrinus) decreased significantly in spring migrants captured at Padre Island, Texas, between 1978 and 1979 (1.00 μg /g wet wt), 1980 (0.57), 1984 (0.50), and 1994 (0.34). No other organochlorine pesticides were detected (detection limit, 0.02 μ g/g) in 1994. Mirex, oxychlordane, dieldrin, heptachlor epoxide, and the parent material DDT were routinely found in plasma samples in earlier years. Polychlorinated biphenyls (PCBs) were found in 75% of the adult females in 1994, but PCB data collected in 1984 were not comparable. The decrease in organochlorine pesticide residues was associated with peregrine population increases in the Arctic and elsewhere in North America. The arctic peregrine ( F. p. tundrius ) was removed from the list of Threatened and Endangered Species by the U.S. Fish and Wildlife Service in 1994. Satellite telemetry and plasma sampling provide new insight into continuing sources of DDE and PCBs. Chemicals that replaced organochlorine pesticides require additional investigation in North and South America.

Texas

The effects of management practices on grassland birds—Prairie Falcon ( Falco mexicanus )

Keys to Prairie Falcon ( Falco mexicanus ) management include maintaining cliffs with suitable recesses for use as nest sites (that is, the substrate that supports the nest or the specific location of the nest on the landscape), protecting nest sites from human disturbance by designating buffer zones, and maintaining open landscapes and habitats that support populations of ground squirrels ( Urocitellus species) and small birds.

Professional Paper

Organochlorine pesticides in plasma of migrating peregrine falcons at Padre Island, Texas, Spring 1978-80 vs. Spring 1984

A spring concentration of migrating Peregrine Falcons (Falco peregrinus) was first discovered at Padre Island, Texas, in April 1978. The birds were first captured and blood-sampled for monitoring residue burdens and trends in the late 1970' s. Only 29 Peregrines were sampled in 1978 and 1979, but 111 were sampled in 1980. The initial investigation showed that DDE in the plasma of spring migrants returning from Latin America for the first time declined significantly during the study (through 1980). In the spring of 1984, 48 Peregrines were captured at Padre Island with blood samples again collected. This report will compare plasma residue data from the earlier study with residues obtained in 1984.

Book chapter

Alaska peregrine falcon productivity in 1984 and the role of organochlorine residues

Twenty Peregrine Falcon (Falco peregrinus) eggs (one per eyrie) were collected at random in Alaska in 1984 for organochlorine residue analysis. Prior to this study we had obtained only addled eggs which were possibly not representative of the egg-laying population if addled eggs contained different levels of organochlorines than viable eggs that hatched. Ten eggs were collected from the American (anatum) population (8 upper Yukon River, 2 Tanana River) and 10 eggs from the Arctic (tundrius) popUlation were later collected in the study area. Productivity at specific eyries and eggshell thickness were evaluated in relation to residue burdens in sample eggs collected. Residue levels and residue profiles for the two subspecies were compared. The tentative 'critical' residue level in Peregrine eggs of 15-20 ppm DDE (wet weight) was compared to results obtained from this study. We also present some data on residue levels in prey species from the study area.

Book chapter

Productivity, pesticides, and management of the Peregrine Falcon in Arizona

In the decade since research commenced with the Peregrine in Arizona, over 60 sites have been identified which historically or presently are occupied by breeding pairs. Productivity was determined for about 120 breeding attempts from 1975-85. Almost all sites, for which productivity information is available for two or more years, have hatched young. Average values for fledging success were ca. 1.4 young/attempt for all active sites and ca. 2.3 young/attempt for successful sites. Eggshell thickness values were highly varied, but few samples reflect thinning sufficient to cause reproductive failure, and the population appears to be increasing slightly. Management practices which can further benefit the falcon include: controlling pesticide use, habitat protection, and information management.

Book chapter

Peregrine falcon

Since 1975, 101 peregrine falcon breeding sites have been documented in Arizona, New Mexico and western Texas. Eyries were found in either riverine or montane canyons, habitats which supported dense and diverse avian prey and provided structural characteristics that may increase prey vulnerability. Approximately 85% of the sites visited each year were occupied. Egg-laying (mid-February to mid-May) typically occurred first in the south and at lower elevations, and later in the north and at higher elevations. Mean productivity of adult pairs (mean =1.55 young/year) was comparable to rates reported for healthy populations. Poor productivity and decreased territorial occupancy in western Texas and southeastern New Mexico occurred in the presence of high levels of environmental DDE. Estimates of the breeding population (141-187 occupied territories) are twice the U.S. Fish and Wildlife Service (USFWS) recovery goal for the region; however, the population is not considered recovered. The discrepancy of these assessments stems from the suitable-habitat approach used by the authors vs. the narrower eyrie-based USFWS recovery plan. Recommendations include reevaluation of recovery goals to ensure adequate habitat protection, elimination of regional sources of organochlorine pesticides, delineation of suitable habitat, formulation of habitat management prescriptions, winter habitat studies,continued monitoring of territorial occupancy and productivity, and accountability for sensitive information.

Book chapter