HIGH CONNECTIVITY and MINIMAL GENETIC STRUCTURE AMONG NORTH AMERICAN BOREAL OWL (AEGOLIUS FUNEREUS) POPULATIONS, REGARDLESS of HABITAT MATRIX Mюrni E

The Auk 124(2):690–704, 2007 © The American Ornithologists’ Union, 2007. Printed in USA.

HIGH CONNECTIVITY AND MINIMAL GENETIC STRUCTURE AMONG NORTH AMERICAN BOREAL OWL (AEGOLIUS FUNEREUS) POPULATIONS, REGARDLESS OF HABITAT MATRIX Mюrni E. Koopman,1 Gregory D. Hayward, and David B. McDonald Department of Zoology and Physiology, University of Wyoming, Laramie, Wyoming 82071, USA

Abstract.—Habitat connectivity and corridors are oĞen assumed to be critical for the persistence of patchily distributed populations, but empirical evidence for this assumption is scarce. We assessed the importance of connectivity among habitat patches for dispersal by a mature-forest obligate, the Boreal Owl (Aegolius funereus). Boreal Owls demonstrated a lack of genetic structure (T = 0.004 ± 0.002 [SE]) among subpopulations, regardless of matrix type and extent, which indicates that unforested matrix does not act as a barrier to dispersal for this vagile species. We found only slightly higher genetic distances (Cavalli-Sforzachord distances ranged from 0.015 to 0.025) among patchily distributed Rocky Mountain subpopulations as compared with largely contiguous boreal-forest subpopulations (0.013 to 0.019) and no evidence of a genetic split across theexpansive high plains of Wyoming. Even the most isolated subalpine patches are connected via gene ﬂow. Asnorthern boreal forests continuetoexperience intensive harvest of mature stands, geographic dispersion of Boreal Owl habitat may begin to more closely resemble that found in the Rocky Mountains. Wesuggest that decreased connectivity poses much less of athreat to continued abundance of this mature-forest obligate than overall loss of nesting and foraging habitat. Assessment of the importance of corridors and connectivity should be conducted on a species-by-species basis, given the variation in response of species to discontinuity of habitat, even among closely related taxaor guilds. Received 5 October 2005, accepted 22 June 2006.

Key words: Aegolius funereus, Boreal Owl, connectivity, corridors, dispersal, gene ﬂow, genetic structure, microsatellites.

Alta Conectividad y Estructura Genética Mínima entre Poblaciones Norteamericanas de Aegolius funereus, Independientemente de la Matriz del Hábitat

ResѢmen.—Frecuentemente, se supone que la conectividad del hábitat y los corredores son críticos para la persistencia de poblaciones distribuidas en parches, pero la evidencia empírica sobre esto es escasa. Evaluamos la importancia de la conectividad entre parches de hábitat para la dispersiónenAegolius funereus, una especie restringida a bosques maduros. Encontramos una ausencia de estructura genética entre subpoblaciones (Ό = 0.004 ± 0.002 [EE]), independientemente del tipo de matriz ydesu extensión, lo quesugiere que las matrices no boscosas no actúan como una barrera para la dispersión en esta especie de amplia movilidad. Sólo encontramos distancias genéticas ligeramente mayores (las distancias cuerda de Cavalli-Sforzaestuvieron entre 0.015 y 0.025) entre subpoblaciones de las Montañas Rocallosas distribuidas en parches en comparación con subpoblaciones

1Present address: Rocky Mountain Research Station, 240 West Prospect, Fort Collins, Colorado 80526, USA. E-mail: [email protected]

690 April 2007] High Connectivity among Boreal Owl Populations 691

de bosques boreales contiguos (0.013 a 0.019), y no observamos evidencia de una diferenciacióngenética a través de las amplias planicies altas de Wyoming. Incluso los parches subalpinos más aislados están conectados por fl ujogenético. A medida quelosbosques boreales del norte continúen siendo sometidos a extracción intensiva de rodales maduros, la dispersióngeográfica del hábitat de A. funereus en la regiónpodría comenzar a semejarse másaladel hábitat de las Montañas Rocallosas. Sugerimos que la conectividad reducida representa una amenazamucho menor sobre la abundancia de esta especie restringida a los bosques maduros quelapérdida general de hábitat de nidificacióny forrajeo. Las evaluaciones de la importancia de los corredores y la conectividad deben realizarse especie por especie, dada la variaciónenlarespuesta de las especies a la discontinuidad del hábitat, aún entre taxones estrechamente emparentados o pertenecientes al mismo gremio.

Population biologists have become increas- their eĜcacy suěers from a lack of empirical ingly interested in the spatial ecology of popu- study (Simberloě et al. 1992, Rosenberg et al. lations, with particular focus on dispersal as 1997, Beier and Noss 1998, Berry et al. 2005), one of the fundamental processes infl uencing with theexception of a few well-documented population dynamics (Walters 2000). Because cases (Beier 1993, Dunning et al. 1995, Mech of discontinuity of suitable habitat, most spe- and HalleĴ 2001). When dispersal through the cies exist in a patchy geographic distribution in matrix is suĜciently high, increased habitat all or part of their range, with dispersal among connectivity may not increase population per- patches acting to connect thepopulation as a sistence or abundance (Hudgens and Haddad whole. Dispersal infl uences species ranges, the 2003), and limited conservation resources may synchrony of population fl uctuations (Huitu et be beĴer spent preserving or improving avail- al. 2003), and long-term persistence of popu- able habitat rather than improving or maintain- lations locally and range-wide (Levins 1969, ing connectivity. Additionally, some authors Stacey and Taper 1992, Martin et al. 2000). have suggested that habitat specialists are Populations may experience less variation in more sensitive to connectivity among habitat abundance and higher persistence because of patches than habitat generalists (Rosenberg et theexchange of individuals among patches al. 1997, Haddad 1999a), especially when large that vary in productivity (Lande 1988). The distances separate patches (Haddad 1999b). idea that movement among subpopulations Understanding commonalities among guilds or aěects the persistence and dynamics of the taxa, levels of connectivity among subpopula- broader population is central to theconceptof tions, and resulting relationships is critical to a metapopulations (Hanski 1999), but dispersal thorough understanding of population dynam- may be equally important in species that are not ics with implications for management and con- structured as a metapopulation. servation (Kareiva 1990). Models and theoretical understanding Here, we explore theeěects of habitat con- indicate that the nature of the matrix (i.e., nectivity on movement among subpopulations nonhabitat) between habitat patches can have of a mobile mature-forest obligate, the Boreal far-reaching eěects on populations (Gardner Owl (Aegolius funereus). Because of thegeo- et al. 1991). Lower matrix quality and increased graphic dispersion of suitable forest habitat, resistance may decrease thelikelihood of popu- Boreal Owls exhibit two distinctive distribu- lation persistence (Fahrig 2001, Vandermeer tion paĴerns, which makes them aĴractive for and Carvajal 2001). Increased theoretical investigating how connectivity aěects dispersal understanding of theeěects of patchy spatial rates. Innorthern boreal forests, Boreal Owls structure on such features as genetic diversity, occurthroughout highly connected habitat, dispersal rates, and extinction probabilities has butinsubalpine forest farther south, Boreal led to management that oĞen incorporates con- Owls exist in isolated high-elevation patches nectivity and corridors (Beier 1995, Dunning separated by variable expanses of unsuitable et al. 1995, Donnelly and Marzluě 2004), but matrix (Fig. 1; Hayward and Hayward 1993), 692 Koopman, Hayward, and McDonald [Auk, Vol. 124

Fig. 1. The North American range of Boreal Owls, based on the distribution of boreal and subalpine forest. Sample sizes and expected and observed heterozygosities are listed for each sampling locality. Despite a potential metapopulation structure based on patchily distributed habitat in the Rocky Mountains of the United States, long-distance dispersal limits genetic differentiation among subpopulations. including lower-elevation forest, prairie, desert, For example, the Northern SpoĴed Owl (Strix and urban development. occidentalis caurina) requires corridors of mature In addition to the contrasting paĴerns of dis- forest to facilitate dispersal from one habitat persion, Boreal Owls in northern boreal forests patch to another (Miller 1989, Forsman et al. and subalpine forests diěer in ecology, behav- 2002). If Boreal Owls, which are also mature- ior, and even basic life-history traits (Hayward forest obligates (Hayward 1997), required such 1997). Given their long dispersal distances and dispersal corridors, we would expect a negative irruptive behavior in northern boreal forests relationship between theextent of unforested (Löfgren et al. 1986, Korpimäkietal. 1987, matrix and gene flow. Sonerudetal. 1988), Boreal Owls can be consid- Although dispersal is crucial for a variety of ered highly vagile. However, Boreal Owls have ecological functions, thediĜculty associated a Holarctic distribution (Hayward and Hayward with estimation of dispersal rates has contrib- 1993), and data on dispersal come from north- uted to poor understanding of this vital compo- ern boreal forests in Fennoscandia. Subalpine nent of population ecology (Koenig et al. 1996, populations in the Rocky Mountains of the Walters 2000). We used microsatellite DNA United States are patchy, and barriers could markers to address the question of how matrix prevent significant exchange among patches. composition, including both type and extent, April 2007] High Connectivity among Boreal Owl Populations 693 aěects movement among habitat patches. In separated by inhospitable matrix and seem- contrast to direct methods such as radiotelem- ingly independent population dynamics. One etry or satellite telemetry, genetic markers allow assumption of the original metapopulation investigation into movement paĴerns of small concept (Levins 1969) is that “theexchange animals at a continental scale. Furthermore, rate of individuals among local populations is genetic approaches facilitate detection of so low that migration has no real eěect on local relatively low movement rates that may not be dynamics in theexisting populations” (Hanski detected by radiotelemetry or banding eěorts. and Simberloě 1997:9). Given theextensive tree- Molecular methods are not only becoming more less matrix separating Rocky Mountain subpop- economical than traditional field methods, ulations, it seemed likely that dispersal (gene they also may provide more informative data flow) would be limited, allowing subpopulation on dispersal, because only successful dispers- diěerentiation. Because much of metapopula- ers incorporate their genetic signature into the tion theory has developed with liĴle empirical population (Koenig et al. 1996). With a variety support from vertebrate studies, the potential to of new statistical methods available to assess test metapopulation theory in such a system is dispersal rates and paĴerns using molecular very aĴractive, especially given that connected markers (Paetkau et al. 1995, Cornuet et al. 1999, subpopulations in northern boreal forests allow Pritchard et al. 2000, Beerli and Felsenstein 2001, for comparison to a baseline level of gene flow Goudet et al. 2002), biologists are discovering across largely continuoussuitable breeding paĴerns of dispersal that were unexpected on habitat. the basis of field data alone (Scribner et al. 2001, Kerth et al. 2002, Korfanta et al. 2005). Methods Westudied gene flow among subpopulations of Boreal Owls separated by a spectrumof Sample collection and molecular genetic matrix extent and type to determine the limits methods.—We sampled Boreal Owls in sub- to dispersal by a vagile mature-forest obligate. populations separated by a spectrumof dis- Specifically, we hypothesized that patchysub- tances and matrix types (Table 1). By sampling populations in the Rocky Mountains, though the range of connectivity available to North geographically proximate, would show more American Boreal Owls, we were able to assess genetic structure (higher FST values and genetic how matrix composition aěects gene flow distances) than northern boreal-forest sub- among subpopulations. We sampled birds at populations that are geographically distant but sites separated by habitat (boreal or subalpine highly connected. Because dispersal is a func- forest), and by unsuitable matrix, including tion of theextent and resistance of the matrix lower-elevation forest (e.g., ponderosa pine or as well as the vagility of a species, we expected Douglas fir), urban development, and treeless to find that forested matrix allowed more gene expanse (e.g., prairie, desert, shrublands). Here, flow than unforested matrix. We hypothesized we use the term “subpopulation” loosely, to that the large expanse of high plains across refer to an area where we sampled Boreal Owls, Wyoming would act as a barrier to dispersal for rather than to a biological subpopulation. Boreal Owls, as it has for a number of species Boreal Owls were captured primarily at nest of montane mammals (Findley and Anderson boxes along logging roads on several national 1956). The genetic signature of such a barrier forests where an extensive system of nest boxes would appear as a departure from thenull was established beginning in 1987 (Hayward model of isolation-by-distance (genetic distance et al. 1992). More than 2,000 nest boxes were among subpopulations increasing linearly with checked each year, from 1998 to 2002. Samples geographic distance), resulting in a dramatic from Idaho were collected between 1995 and increase in genetic distance in the presence of 2002. On average, nest box use by Boreal Owls inhospitable matrix (Paetkau et al. 1997). was only ~1%. Adult females were trapped while We also expected that subpopulations of brooding or incubating, and males were trapped Boreal Owls in the Rocky Mountains would as they brought food to thechicks. We collected exhibit classical metapopulation structure. They blood samples from all individuals captured. If fit many assumptions of the metapopulation we were unable to trap adults at a nest, we col- concept, including discrete local populations lected a blood sample from one of the nestlings. 694 Koopman, Hayward, and McDonald [Auk, Vol. 124

Table 1. Pairwise comparisons of subpopulations of Boreal Owls in the boreal forest and in the Rocky Mountains showing the range of matrix types and geographic distances between subpopulations. We sampled subpopulations with varying types of dominant matrix between them, including suitable breeding habitat (boreal forest), montane forest (largely connected lower-elevation forest), patchy forest (disconnected subalpine and lower-elevation forest with interspersed grasslands), high plains, and urban development. Sample locations are shown in Figure 1.

Distance between Subpopulations subpopulations being compared (km) Dominant matrix types W. CO / S. CO 166.6 Patchy forest ID / MT 175.9 Montane forest WY / W. CO 207.0 Patchy forest, urban development WY / S. CO 368.6 Patchy forest, urban development FAIR /ANCH 415.2 Boreal forest MT / WY 781.6 High plains, patchy forest MT / W. CO 881.3 High plains, patchy forest ID / WY 893.7 High plains, patchy forest ID / W. CO 961.8 High plains, patchy forest MT / S. CO 1,020.2 High plains, patchy forest ID / S. CO 1,083.8 High plains, patchy forest FAIR / CAN 3,338.4 Boreal forest ANCH / CAN 3,407.9 Boreal forest

Boreal Owls were tagged with a federal band so others assess diěerences (or similarities) among that we could recognize family members and individuals, thereby allowing for identification recaptures. Tissue samples obtained from Boreal of subpopulations based on genetic substruc- Owl specimens from Manitoba and Minnesota ture (assignment tests, allele-sharing distances, consisted of heart or muscle tissue. Additional model-based clustering method of the Bayesian tissue samples collected near Fairbanks, Alaska, program STRUCTURE). were obtained from the University of Alaska Wetested for departure from Hardy- museum. Blood was stored in Longmire’s Weinberg equilibrium, within and among Solution (Longmire et al. 1988), and most tissue each pair of loci, using GENEPOP, version 3.3 was stored in 100% ethanol. (Raymond and Rousset 1995) and, for genotypic To isolate DNA from samples, we used a linkage disequilibrium, FSTAT, version 2.9.3.2 Sigma GenElute mammalian DNA extraction kit (Goudet 1995). We used sequential Bonferroni (Sigma-Aldrich, St. Louis, Missouri). We geno- procedures to adjust for multiple comparisons typed 275 unrelated individuals using seven (overall D = 0.05). polymorphic microsatellite loci, following the We estimated genetic diěerentiation among protocol described by Koopman et al. (2004). subpopulations, T (equivalent to FST) using the Genetic structure.—We assessed genetic struc- measure of Weir and Cockerham (1984), which ture of subpopulations of Boreal Owls in North is weighted by sample size, in FSTAT. Ninety- America. Because microsatellite mutation pro- five percent confidence intervals around Weir cesses are not fully understood at this time and and Cockerham’s FST (hereaĞer referred to there is no consensusonthe most appropriate simply as FST) were estimated with 10,000 boot- measurements to use (Goldstein and Pollock 1994, strap replicates. In GENEPOP, we ran a G-like Ruzzante 1998, Foulley and Hill 1999, Kalinowski exact test (Goudet et al. 1996) to assess diěer- 2002), the use of a variety of measurements, with ences among subpopulations in overall allelic diěerent underlying assumptions, can increase distributions. confidence in the results, especially if they agree Toevaluate the appropriate geographic scale (Neigel 2002). Some tests or measures assess dif- for population-diěerentiation analysis, we ferences among user-defined “subpopulations” used hierarchical F statistics (Weir 1996), which (FST, measures of genetic distance), whereas involve grouping of individual subpopulations, April 2007] High Connectivity among Boreal Owl Populations 695 on the basis of geographic proximity, until overall geographic distance using a Mantel test (Mantel genetic diěerentiation is maximized. Using the 1967) and 5,000 permutations in MCMANTEL grouping with highest genetic structure (great- (McDonald et al. 1999). We calculated straight- est FST), we tested for genetic subdivision on a line distances between subpopulations in regional scale usingalikelihood-based assign- ARCVIEW (ESRI, Redlands, California), using ment test (Paetkau et al. 1995) in DOH (see the center of the area where themost Boreal Acknowledgments) and a Bayesian assignment Owls were captured as the end points of each test (Cornuet et al. 1999) in GENECLASS (see line connecting two subpopulations. Because Acknowledgments). When populations show suf- most individuals were captured near Winnipeg ficient genetic diěerentiation (FST > 0.05; Cornuet for our samples from Canada, we used Winnipeg et al. 1999), this procedure allows identification as the endpoint for our Canadian comparisons. of individuals that may have dispersed between We hypothesized that, if matrix type regu- populations (Rannala and Mountain 1997). We lates gene flow among subpopulations, we also assessed structure among subpopulations should see a departure from the linear isolation- or geographic regions using STRUCTURE (see by-distance model (Paetkau et al. 1997), such Acknowledgments), which determines whether that subpopulations separated by inhospitable sampled genotypes are substructured into mul- matrix would have higher genetic distance than tiple (K > 1) clusters or whether they constitute a expected from geographic distance alone. single genetically homogeneouspopulation (K = We used three diěerent pairwise measures 1) in Hardy-Weinberg equilibrium. Wetested for of genetic distance. First, we calculated pair- one to eight separate subpopulations without wise Cavalli-Sforza and Edwards (1967) chord prior information on capture location of individu- distance because of its superior performance als (Pritchard et al. 2000). Burn-in and replication in phylogenetic tree-building (Takezaki and values were set at 25,000 and 1,025,000. Nei 1996) and its linear nature over large dis- Phylogenetic trees.—We calculated pairwise tances, and because it makes no assumptions Cavalli-Sforzachord distances (Cavalli-Sforza aboutmutation models. We also calculated and Edwards 1967) among subpopulations the ratio FST/(1 – FST) (Rousset 1997) and Nei’s and generated a rooted neighbor-joining tree standard distance (Nei 1972), both of which in the NEIGHBOR subroutine of PHYLIP (see have been shown to accurately reflect isolation- Acknowledgments), with Norwegian Teng- by-distance (Takezaki and Nei 1996, Paetkau malm’s Owls (A. f. funereus) as an outgroup. et al. 1997, Rousset 1997), though FST/(1 – FST) Under microsatellite locus and sample number may be accurate only over small geographic conditions similar to ours, chord distances show distances (Rousset 1997). We decided not to use greater success in generating the correct tree microsatellite-specific measurements because topology than other distance measurements of departures from a strict stepwise mutation (Takezaki and Nei 1996). One-thousand boot- model (SMM) apparent in some of our loci and strap replications were performed to calculate because other studies have found that the high percentage of support for individual nodes. A variance associated with these measurements maximum-likelihood (ML) tree was also con- obscures paĴerns (Paetkau et al. 1997), espe- structed using the ML subroutine (CONTML) cially with high levels of gene flow (Balloux and in PHYLIP and bootstrapped 1,000 times, with Goudet 2002). Tengmalm’s Owls as an outgroup. We calculated allele-sharing distances Results (Bowcock et al. 1994) using the MS TOOLS add- in for EXCEL (see Acknowledgments). Pairwise The 275 genotyped individuals were from allele-sharing distances are calculated as one eightsubpopulations (Fig. 1). Thenumber of minus half the average number of shared alleles alleles per locus ranged from 3 to 11 among per locus. Finally, we constructed a neighbor- seven microsatellite loci. We found evidence for joining tree (Saitou and Nei 1987) in PHYLIP, heterozygote deficiency at one locusinthesub- using unrelated North American individuals as population from Canada (P < 0.001). Otherwise, the operational taxonomic units. all subpopulations were in Hardy-Weinberg Isolation-by-distance.—We compared matri- equilibrium for all loci. We found no evidence ces of pairwise genetic distance and pairwise for genotypic disequilibrium among paired loci 696 Koopman, Hayward, and McDonald [Auk, Vol. 124

(P values ranged from 0.01 to 0.96; adjusted 5% nominal level for multiple comparisons = 0.0025). Genetic structure.—Genetic diěerentiation among subpopulations of Boreal Owls throughout North America was extremely small, as demonstrated by estimates of global FST (T = 0.004 ± 0.002 [SE]; 95% CI: 0.000 to 0.008). We found no significant overall diěerence in allelic distribution among subpopulations (G-like test, P = 0.794, df = 14). Using STRUCTURE, we consistently found a higher log likelihood of one subpopulation (–3,801.3) rather than two to eightsubpopulations (–4,004.2 to –6,699.1), which indicates that, throughoutthe North American range, Boreal Owls occurasasingle genetically homogeneouspopulation. When we grouped all northern (Alaska and Canada) and southern (Colorado and Wyoming) subpopulations while excluding central subpopulations (Montana and Idaho), Fig. 2. Assignment likelihoods for 206 individ- slightly more genetic structure was apparent. uals captured in northern (Alaska and Canada) The magnitude of this structure, however, was and southern (Colorado and Wyoming) sub- still very small (T = 0.012 ± 0.003 [SE]; 95% CI: populations of Boreal Owls. If genotype were a 0.007 to 0.017). Weconducted the assignment good indicator of origin, most individuals from test by reclassifying our samples into two thenorth would have fallen well above the line, groups: north and south, excluding Idaho and whereas those from thesouth would have fallen Montana. However, regardless of assignment well below the line. Theobvious lack of pattern algorithm, few individuals were correctly and proximity to the line of equal likelihood both assigned to their origin of capture, because of suggest a lack of clear genetic differentiation. low levels of genetic diěerentiation between northern and southern subpopulations (Fig. 2). Isolation-by-distance.—Cavalli-Sforzachord When we used the assignment test of Paetkau distances were extremely small, ranging from et al. (1995), only 65% of individuals (133 of 0.013 to 0.019 among boreal forest subpopula- 206) were correctly assigned to their sampled tions and 0.015 to 0.025 among Rocky Mountain subpopulation. Onthe basis of chance alone, subpopulations. Similarly, Nei’s standard one would expect 50% of individuals to be cor- distances ranged from 0.006 to 0.020 among rectly assigned. Under the Bayesian method of boreal forest subpopulations and from 0.006 to Cornuet et al. (1999), only one individual of 206 0.030 among Rocky Mountain subpopulations. had a significantly higher likelihood of having Pairwise comparisons of geographic distance originated in thesubpopulation from which it among all subpopulations were significantly was sampled than in theother subpopulation. correlated with Cavalli-Sforzachord distances Phylogenetic trees.—A phylogenetic tree for (R = 0.559, P = 0.001), but not with FST/(1 – FST) the eight North American subpopulations (R = 0.143, P = 0.238) or Nei’s standard distance recovered the geographic split between north- (R = 0.116, P = 0.280). By contrast, all three ern and southern subpopulations of Boreal genetic distances were significantly correlated Owls (Fig. 3), but bootstrap support for most with geographic distances when we assessed clades was extremely low. Rocky Mountain only the Rocky Mountain subpopulations (R subdivisions had higher bootstrap support than ranged from 0.752 to 0.847; P < 0.008; Fig. 5). other clades. Results from the ML tree corrobo- Nei’s standard genetic distance had thebestfit, rated those from the neighbor-joining tree. Our butthe relationship was confounded by the fact neighbor-joining tree of allele-sharing distances that larger distances between subpopulations in between individuals showed no clustering the Rockies were correlated with treeless matrix based on capture location (Fig. 4). (Fig. 5). April 2007] High Connectivity among Boreal Owl Populations 697

Fig. 3. Neighbor-joining tree of Cavalli-Sforzachord distances among subpopulations of North American Boreal Owls, with the Norwegian subspecies includedasanoutgroup. Percentage of support for each node was calculated from 1,000 trees built from bootstrapped data. Nodes with >50% support (marked with an asterisk) include thenode joining Canada, Anchorage, and Fairbanks (54% support); that joining western Colorado, southern Colorado, and Wyoming (66%); and that joining western Colorado and Wyoming (69%). Higher bootstrap support for southern Rocky Mountain clades may indicate slightly less gene flow because of patchy habitat.

Fig. 5. Pairwise comparisons of genetic distance and geographic distance. Although genetic distances were very small, we found a slight linear increase in genetic distance with geographic distance among Rocky Mountain subpopulations (filled symbols) but no increase among subpopulations separated by boreal- Fig. 4. Unrooted neighbor-joining tree of forest habitat (open squares). Although the allele-sharing distances among 250 unrelated slope of the line appears to be quite steep, the Boreal Owls captured in North America. If total change in genetic distance is only 0.03; for subpopulations were genetically well differenti- other published studies, Nei’s distances may be ated, individuals sampled from the same locality an order of magnitude higher (McDonald et would cluster together. Theobvious lack of clus- al. 1999). The relationship between geographic tering indicates a lack of genetic structure among distance and genetic distance was confounded Boreal Owl subpopulations in North America. By by matrix type in the Rocky Mountains, where contrast, including Old World subpopulations treeless matrix was associated with longer dis- produces nearly total reciprocal monophyly tances; but even across treeless matrix, genetic among Old World and New World populations, distances were very small. even when using individuals as the operational taxonomic units (Koopman et al. 2005). 698 Koopman, Hayward, and McDonald [Auk, Vol. 124

Discussion frequently disperses long distances over inhospitable habitat, even >200 kmacrossthe high Many species exhibit naturally patchy distri- plains of Wyoming. Wecaution against apply- butions, and even more are becoming patchily ing the term “metapopulation” on the basis of distributed because of habitat loss. Resource physical patchiness of habitat only (Major et al. managers require improved understanding of 1999, Martin et al. 2000, Sweanor et al. 2000). dispersal, resulting spatial paĴerns, and relation- Boreal Owls have extremely large home ships to population persistence and demography. ranges for birds their size (Hayward et al. 1993), Empirical evidence for theeĜcacy of connectiv- and in boreal forest, they are known to move ity and corridors is scarce, buta few cases clearly great distances during natal dispersal and win- demonstrate the importance of connectivity and ter irruptions (Löfgren et al. 1986, Korpimäkiet favorable matrix in facilitating dispersal among al. 1987). In addition, females find new mates habitat patches (Beier 1993, Dunning et al. 1995, each year, sometimes in new home ranges Berry et al. 2005). Boreal Owls, on theother hand, (Hayward et al. 1993). Over their lifetimes, total exhibit only a modest increase in genetic struc- area traversed may span hundreds to thousands ture when habitat patches are more isolated (Fig. of square kilometers. 3). Dispersal rates are high even when patches are Habitat connectivity and Boreal Owls.— Genetic separated by inhospitable matrix, long distances, distances among sites with forested and treeless or both. Given their dependence on mature for- matrix diěered minimally, leading ustocon- est for foraging and nesting (Hayward 1997), we clude that dispersal rates are high, regardless of expected that Boreal Owls would require conti- matrix type and extent. Inthe Rocky Mountains, nuity of forested habitat to traverse the matrix. all three measures of genetic distance increased Our results reveal that generalizations about linearly, if slightly, with geographic distance, movement rates based on closely related taxa as expected under the island model with no (e.g., SpoĴed Owls) or guilds (e.g., mature-forest barriers to dispersal (Fig. 5). However, greater obligates) are not reliable, and that assessment of distances between Rocky Mountain subpopula- the benefits of connectivity needs to be done on a tions were correlated with treeless matrix, mak- species-by-species basis. If dispersal rates among ing it diĜcult to determine whether matrix type subpopulations are high, managing matrix com- or distance was the primary factor involved position for connectivity among subpopulations in the significant relationship. In either case, may waste scarce conservation resources. gene flow was suĜciently high, even between Are Boreal Owls a metapopulation?—With an the most distant and disconnected patches, to FST of 0.004, Boreal Owls in North America are homogenizesubpopulations genetically. For not partitioned into distinct subpopulations. example, the assignment test failed to assign Despite thepatchy distribution of spruce–fir individuals to their population of origin, forest throughoutthe Rocky Mountains and STRUCTURE indicated that Boreal Owls con- despite strong dependence of Boreal Owls on stitute a single population, and the individual- mature forest, our genetic analysis indicates that based neighbor-joining tree (Fig. 4) showed Boreal Owl subpopulations do not constitute a total lack of clustering of individuals sampled metapopulation. High rates of gene flow among at the same locale. subpopulations of Boreal Owls makeit unlikely Our results demonstrate that Boreal Owls that local populations exhibit independent pop- disperse across large areas of unsuitable habi- ulation dynamics or that recruitment is almost tat and that no North American subpopulation invariably local, some of the fundamental tenets is genetically isolated from theothers. These of classical metapopulation theory (Harrison high rates of gene flow makeit unlikely that and Taylor 1997). Various measurements (both subpopulations are demographically indepen- classic ones, such as FST and Nei’s standard dent. High dispersal rates likely act to dampen distance, as well as more recently developed population fl uctuations and boost breeding Bayesian and likelihood-based measurements) success in population sinks (the “rescueeěect”; painted similar pictures of lack of distinct Brown and Kodric-Brown 1977), synchronize genetic structure among subpopulations. A demographic paĴerns among subpopulations lack of genetic structure among subpopulations (Huitu et al. 2003), and overwhelm adapta- indicates that this resident but highly vagile owl tions to local conditions. Some subpopulations April 2007] High Connectivity among Boreal Owl Populations 699 in the Rocky Mountains are less productive forest (Koopman et al. 2005). By contrast, Old than others (M. E. Koopman unpubl. data) and World and New World populations showed a may depend on high levels of immigration for high degree of diěerentiation (T = 0.37; Koopman long-term persistence. Nevertheless, thetime- et al. 2005), demonstrating thatathreshold level scale of genetic homogenization (on the order exists, at least at intercontinental scales. of several to many generations) may overlook Genetic diě erentiation.—The level of genetic demographic paĴerns that occuronamuch diěerentiation in ourstudy (T = 0.004) was shorter scale of a few years. Although genetic lower than that found, using microsatellite substructuring clearly suggests demographic markers, among subpopulations of other independence among subpopulations, a lack of avian species (0.027 for Greater Sage-Grouse genetic structure does not necessarily preclude [Centrocercus urophasianus], Oyler-McCance et a degree of demographic independence. Thus, al. 1999; 0.014 for Yellow Warbler [Dendroica the relationship between gene flow and demo- petechia], Gibbs et al. 2000; 0.014 for Burrowing graphic paĴerns invites further investigation. Owl [Athene cunicularia], Korfanta 2001; 0.02 Boreal vs. subalpine subpopulations.— for Song Sparrow [Melospiza melodia], Chan Diěerences in climate, habitat structure, prey and Arcese 2002), especially considering cycles, and prey composition between northern that ourstudy was conducted over a larger boreal forests and more southerly subalpine spatial extent than most of theothers. Even forests appear to drive behavioral and ecologi- though genetic distances were small, we cal diěerences between northern and southern found evidence of limited genetic subdivision subpopulations of Boreal Owls (Hayward 1997). in the neighbor-joining and ML trees, which Judging from these diěerences in broad-scale revealed two clades among North American dynamics, we expected high connectivity in the Boreal Owls. Thesouthern clade showed >50% north and classical metapopulation structure support for subdivisions in Colorado and in thesouthern parts of the range. We found Wyoming. Hierarchical F statistics lent support slightly lower values of genetic distance among to thenorth versussouth split, with Montana widely separated boreal-forest subpopulations and Idaho acting as middle ground between than among proximate Rocky Mountain sub- the two clades. The fact that slight genetic subpopulations (Fig. 5), which indicates that patch- division is apparent only at a continent-wide iness of habitat may slow movement. Similarly, scale does not support our hypothesis that we found higher bootstrap support for subdivi- the treeless sagebrush steppe of the Wyoming sions among Rocky Mountain subpopulations Basin acts as a physical barrier to dispersal for than for subdivisions among northern subpop- Boreal Owls. By contrast, many mammalian ulations in our neighbor-joining and ML trees. spruce–fir forest obligates have distinct north- Thediěerences in genetic distance were slight, ern and southeastern subspecies or are limited however, and were overshadowed by a consis- in their range by the Wyoming Basin (Findley tent lack of genetic structure under global FST, and Anderson 1956). assignment tests, a G-liketest, STRUCTURE, Boreal-forest subpopulations of Boreal Owls and allele-sharing distances. undergo irruptions, or mass southward move- Our boreal-forest samples were from two ments of individuals, during extreme condi- breeding subpopulations in Alaska, plus irruptions (Hayward and Hayward 1993). Subalpine tive individuals in northern Minnesota and subpopulations in the Rocky Mountains do southern Manitoba (labeled “CAN” in Fig. 1). not, possibly explaining their slightly greater Our samples from Canada represented indi- genetic diěerentiation. Winter irruptions may viduals that moved south from a wider breed- drive waves of immigrants from northern boreal ing range farther north because of severe winter forests into southern subalpine forests, thereby conditions. No genetic diěerentiation existed largely overwhelming any local adaptations or between our samples from Alaska and Canada, genetic structuring. and we feel confident that this is representative Implications for Boreal Owl management in sub- across the boreal forest of North America. alpine and boreal forests.—Breeding populations Similarly, no genetic diěerentiation existed of Boreal Owls throughout inland mountain among Boreal Owls sampled in far eastern and ranges of the western United States were not far western locations in the Eurasian boreal detected until the mid- to late 1980s (Hayward 700 Koopman, Hayward, and McDonald [Auk, Vol. 124 et al. 1987). Since then, Boreal Owls have been and predators (BriĴingham and Temple 1983, regarded as isolated mountain-top dwellers Wilcove 1985, Burke and Nol 1998, Brown and that are rarely heard or seen. Subpopulations Sullivan 2005) can act to degrade remaining are oĞen managed at the geographic scale of habitat patches and negatively aěect mature- individual national forests, and local subpopu- forest obligates such as Boreal Owls. Although lations likely remain undiscovered in certain Boreal Owls are currently numerousacross regions. The response of Boreal Owls to forest- much of their range, and their ability to disperse management practices and large-scale habitat across inhospitable matrix increases their prob- alterations is, therefore, virtually unknown. ability of persistence, their close ties to a quickly In lightof earlier understanding, the pres- vanishing habitat type continues to represent a ent study provides managers with amore significant threat to the future abundance of this optimistic scenario for long-term persis- species. tence of Boreal Owls, especially in the Rocky Mountains, where individual subpopulations Acјnowledgments are smaller and potentially more vulnerable to extinction. Because Boreal Owls appear to be More U.S. Forest Service (USFS) biologists structured not as a metapopulation, but instead than we can name here provided logistical sup- as a well-connected yet patchily distributed port in the field—thanks to all of them, especially population, consideration of connectivity and F. Gordon, C. Hescock, S. Jacobson, J. Ormiston, matrix composition is not as critical for man- and R. Skorkowsky. We are gratefulto T. agement as it would be under a classic meta- Bodreaux, B. DiĴrick, T. Holland, L. Moorehead, population structure. Additionally, temporary T. Swem, E. Taylor, and especially C. Schultz, for extinctions of local populations resulting from generously sending samples from Boreal Owls. large-scale natural disturbances and extensive Additional Boreal Owl genetic samples were timber harvest, both of which we have observed provided by the Bell Museum, the Agricultural (M. E. Koopman et al. unpubl. data), are likely University of Norway, Manitoba Conservation, to be followed by recolonization when mature University of Alaska Museum, and the Burke spruce–fir habitat is restored, even when the Museum. We had excellent field assistance by nearest extant subpopulation is distant or sepa- many dedicated biologists, including L. Ayers, rated by treeless matrix. With this knowledge, J. Bassinger, J. BenneĴ , J. Carpenedo, S. Dubay, managers can focus conservation resources on T. Hampton, the Hayward family, T. Heekin, other aspects of Boreal Owl life history, such K. Keěer, S. Koopman, S. Mullins, K. OĴ , M. as managing large tracts of mature spruce–fir Suedkamp, and P. Sutherland. J. BenneĴ provided forest habitat to sustain foraging and nesting GIS support. This project was funded by Global requirements (Hayward 1997). Forest (GF-18-2000-132), USFS Rocky Mountain We have referred to thenorthern boreal forest Research Station, the Nansen Endowment as a large swath of connected habitat hospitable (grant to G. A. Sonerud), and awards from the to Boreal Owls. Indeed, Boreal Owls are quite American Museumof Natural History, Sigma Xi, numerousthroughoutthe region. Because of and the Department of Zoology and Physiology intensive logging pressure in the boreal forest, and the Institute of Environment and Natural however, Boreal Owls in this region may begin Resources at the University of Wyoming. Insight to more closely resemble Rocky Mountain sub- and ideas provided by S. Jackson, J. Lovvorn, populations as large tracts of habitat are lost and S. Anderson are greatly appreciated. The and remaining tracts become disconnected. On comments of G. A. Sonerud and an anonymous a positive note, discontinuity of boreal forest reviewer greatly enhanced this manuscript. The may not significantly increase extinction proba- DOH assignment test calculator is available at bilities because of high rates of dispersal among www2.biology.ualberta.ca/jbrzusto/Doh.php, suitable habitat patches, as long as suĜcient GENECLASS at www.montpellier.inra.fr/ tracts of mature forest continue to persist on URLB/geneclass/geneclass.html, PHYLIP at the landscape. Weacknowledge, however, that evolution.genetics.washington.edu/phylip.html, a decrease in connectivity is only one of many the MS TOOLS add-in for EXCEL at deleterious eěects of habitat fragmentation. animalgenomics.ucd.ie/sdepark/ms-toolkit/, and Infl ux of invasive species, disease, competitors, STRUCTURE at pritch.bsd.uchicago.edu/. April 2007] High Connectivity among Boreal Owl Populations 701

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