4 message from the editors
September 2008
Any remaining errors are the responsibility of the editors. The editors thank Christina Robinson-Swett for the beautiful illustration of a Loggerhead Shrike presented on the Volume 10 cover. We also kindly acknowledge all others who helped with the planning, production, and mailing of this issue, and in particular we thank Dana Hartley for providing his expertise in layout and printing.
Great Basin Birds10, 2008, pp.5-15 © 2008 by the Great Basin Bird Observatory
Dispersal and Population Genetic Structure of Migratory Red-naped Sapsuckers in a Naturally Fragmented Environment David P. Arsenault1, Mary M. Peacock2, Scott A. Fleury3, and J. Michael Reed4 1Sierra
Nevada Avian Center, PO Box 23 Quincy, CA 95971;
[email protected] 2Department of Biology, University of Nevada Reno, NV 89557 3Technology Associates, 9089 Clairemont Mesa Blvd, Ste 307 San Diego, CA 92123 4Department of Biology, Tufts University, Medford, MA 02155
INTRODUCTION Dispersal is an important life history character in the study of population and conservation biology, ecology, and evolution, but the patterns and process of dispersal in most vertebrates, including birds, is poorly known (Rockwell and Barrowclough 1987). Dispersal can be viewed as a continuum of movement with natal philopatry and adult site fidelity representing one end of the continuum, and unlimited dispersal capabilities the other (Reed 1993). The combination of data from molecular markers such as mini-satellites and movement data from mark-recapture methods has been shown to be an effective method to elucidate dispersal patterns (Arsenault et al. 2005, Peacock 1997). High levels of gene flow occur in many migratory species (Arguedas and Parker 2000), and populations throughout the range of migratory species can be highly inter-connected by dispersing individuals (Arsenault et al. 2005, Barrowclough 1980). Paradis et al. (1998) found that migratory species had significantly greater breeding dispersal than did residents since migrants may prospect for breeding sites during migration, and thus have a broader geographic range of potential future breeding sites to select from than do resident species (Johnson and Grier 1988, Reed et al. 1999, Spendelow et al. 1995). Studies have also shown that natal philopatry can be less common in migratory species than in residents (Weatherhead and Forbes 1994). Little is known about the dispersal patterns of woodpecker species, but most are thought to be short-distance dispersers (Dobbs et al. 1997, Koenig et al. 1996, Walters et al. 1988, Winkler et al. 1995). Red-naped Sapsuckers (Sphyrapicus nuchalis) are one of the few migratory woodpeckers, spending the winter in Mexico and the Southwest U.S., and breeding throughout the Rocky Mountains and the Great Basin of the western U.S. (Howell 1952). In the mountains of the Great Basin, Red-naped Sapsuckers nest primarily in riparian aspen forests (Dobkin et al. 1995, Ryser 1985), which are naturally fragmented because they are confined to mountain canyons (Dobkin and Wilcox 1986). The Toiyabe Mountain Range in the Great Basin, central Nevada, provided an excellent system in which to study the movements of sapsuckers between naturally fragmented patches of habitat. Furthermore, Red-naped Sapsuckers may have been extirpated from the Toiyabe Range prior to 1940 due to the 5
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cutting of aspen for mines (Dobkin and Wilcox 1986). Thus, we can apply our results to the probability of re-colonization of extirpated populations and illuminate possible re-colonization scenarios, the understanding of which may facilitate the conservation of this species in the Great Basin. Here we compare results from a mark-recapture study of dispersal in Red-naped Sapsuckers in central Nevada with estimates of gene flow using multi-locus mini-satellite data collected from the same individuals. Our aim was to understand the dispersal capabilities of this species in a fragmented habitat. We also tested for extra-pair copulation in nine families to determine if this species is genetically monogamous, as it is socially monogamous, because this is important in understanding woodpecker social systems. METHODS Study Area and Field Methods. The Toiyabe Range is approximately 122 km long and has a north-to-south orientation, with peaks ranging in elevation from 2,100 to 3,600 m. Much of the suitable breeding habitat for Red-naped Sapsuckers occurs in aspen woodlands in seven large drainages within an 85-km stretch on the west slope, at elevations of 2,100 to 2,900 m (Dobkin and Wilcox 1986, Fleury 2000). This breeding habitat is naturally fragmented within and among drainages, and is 50 m wide on average. Other major riparian plant communities occurring in these drainages are dominated by cottonwood (Populus spp.), willow (Salix spp.), or birch (Betula occidentalis) trees, or by meadow plant communities with species including Carex, Juncus, and Poa (Fleury 2000). Our study area included well-developed aspen riparian habitat in five canyons on the west slope of the Toiyabe Range: Washington, Cottonwood, San Juan, North Clear, and Clear. The study sites comprised approximately 6-km segments in each canyon with a cumulative length of 29 km for the study sites combined. Canyons were 1.5 km to 29 km apart. Fleury (2000) provides more detail on study sites. For our mark-recapture analysis, we captured and uniquely color-banded a total of 375 adults and nestlings in five canyons from 1994 to 1996 and re-sighted birds from 1995 to 1997. Birds were re-sighted during all visits to study sites, including surveys specifically for re-sighting birds, as well as during nest finding and nest checking visits. The locations of re-sighted individuals were recorded with a GPS unit and on U.S. Geological Survey (USGS) 7.5-minute topographic maps. For our genetic and parentage analysis, we sampled blood from adults (N = 31; 16 males, 15 females) and nestlings (N = 27) from 17 nests in 1997. A total of 9 families (both adults and all nestlings) were used for our parentage analysis. Nestlings were removed from nest cavities by making an inverted wedge-shaped opening cut below the cavity entrance, which was replaced using nails. We captured adult birds as they exited the nest cavity using a mist net on a long pole with a hoop at the top. Adults were captured after eggs hatched to preclude nest abandonment. For the 58 birds sampled, up to 250 μL of blood was taken from the wing using heparinized hematocrit tubes, which was immediately mixed with lysis buffer and stored in a field cooler during transport to the University of Nevada, Reno.
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DNA Fingerprinting. DNA was extracted from blood samples using a standard phenol-chloroform extraction method. Extracted DNA was cut with Hae III restriction enzyme and loaded onto 1% agarose gels with sizing standards every 5 lanes. Family groups were run in adjacent lanes for parentage analysis. Separated DNA fragments were transferred to neutral charge nylon membrane, which was then incubated in blocking solution, hybridized to two alkalinephosphate labeled oligonucleotides (i.e. mini-satellite probes, Jeffrey’s 33.15 and 33.6), washed, and incubated in assay buffer. CDP-star substrate was applied, which enabled visualization of the banding pattern (i.e. DNA fingerprint) when the membrane was exposed to medical X-ray film. Two individuals scored all gels (N = 4) independently. For population analysis, DNA fragments detected by each mini-satellite probe and size standard fragments were drawn on acetate overlays using a light board, which was scanned and digitized in Arcview GIS to obtain spatial x and y coordinates. The size of each DNA fingerprint fragment was determined by comparison to the nearest size standard lane, and band sizes were estimated by regressing the known length (in base pairs) of size standard bands against their x and y coordinates. Control individuals were used to estimate error intervals to determine which fragments were homologous. Banding patterns were visually compared between putative parents and offspring for parentage analysis. Band-sharing estimates between parents and offspring, the male and female of each pair, siblings, unrelated adults in each canyon, and adults with juveniles not from that adult’s nest (presumably unrelated) were calculated as twice the number of shared bands divided by the sum of the number of bands in both individuals (Lynch 1991). We tested for genetic differentiation among canyons (Lynch 1991) by calculating within and between canyon band-sharing (Piper and Rabenold 1992), and using the Kruskal-Wallis and Mann-Whitney U nonparametric tests with SYSTAT 7.0. We calculated population (i.e. canyon) subdivision (Fst), which is the probability of drawing two alleles at random from two populations that are identical by descent and is a measure of genetic differentiation among populations (Lynch 1991, Wright 1969). We used Lynch’s (1991) equation developed for multi-locus mini-satellite data that corrects for the non-independence inherent in band-sharing data. Band-sharing scores between mated pairs and average heterozygosity within canyons were calculated to determine the extent of genetic isolation and potential breeding between first-order relatives within canyons (Stephens et al. 1992). Exclusion analysis of putative parents and offspring was based on band-sharing and novel fragments. Novel fragments were those detected in juveniles, but not in either of the adults to which they were compared. We considered an adult to be the parent of a juvenile at their nest if the band-sharing value was greater than 0.38 and there were no more than two novel fragments. Mutation to new length variants in mini-satellite regions occurs at a high rate, thus some novel fragments can be expected between juveniles and their biological parents within a population (Jeffreys et al. 1988). We scored all resolvable bands between approximately 23 and 2 kb for 58 individuals. Mean number of bands scored for the Jeffrey’s 33.15 and 33.6 probes were 16.14 (± 4.38) and 15.63 (± 5.03) respectively. Means are reported ± SD.
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RESULTS Twenty-one percent (77 of 375) of Red-naped Sapsuckers banded from 1994 to 1996 were re-sighted from 1995 to 1997, including 46% of males, 39% of females, and 3% of juveniles (Table 1). Seven cases of natal dispersal were detected: 2 males moved an average of 2,292 m and 5 females moved an average of 1,746 m between birth site and first breeding site (Table 1). Breeding dispersal was observed 67 times; males dispersed an average of 229 m between years and females an average of 246 m (Table 1). A total of 45 males and 49 females immigrated into the banded population from 1995 to 1997 (Table 1). Although a large proportion of the sapsuckers in the five canyons were banded, only one banded pair was observed dispersing between canyons, and they moved 2,685 m between successive nest sites (Table 2). Thus, long-distance dispersal Table 1. Return rate, immigration rate, and dispersal distances of Red-naped Sapsuckers in the Toiyabe Range, central Nevada. Dispersal distances are in m (± SE). Return Ratea
Immigrantsb
Natal Dispersalc (n)
Breeding Dispersald (n)
Male 39/84 (46%) 45 2,292 ± 837 (2) 229 ± 86 (36) Female 32/83 (39%) 49 1,746 ± 364 (5) 246 ± 94 (31) Nestling 7/208 (3%) NA NA NA a Number of sapsuckers re-sighted divided by the total number of sapsuckers banded. b The number of unbanded sapsuckers that immigrated into the marked population from 1995-1997. c The dispersal distance (m) of sapsuckers banded as nestlings that returned to breed in the study area. d The dispersal distance (m) of sapsuckers banded as adults that returned to breed in the study area.
Vol. 10 Arsenault, peacock, fleury, and reed Table 3. Results of DNA fingerprinting analysis of population differentiation for 31 adult and parentage for 27 nestling Red-naped Sapsuckers from 9 nests in 5 canyons in the Toiyabe Range, central Nevada.
na Mean ± SD Min. Max. Band-sharing among breeding adults within canyons 82 0.31 ± 0.11 0.10 0.60 Band-sharing among breeding adults between canyons 204 0.28 ± 0.11 0.06 0.53 Band-sharing between paired male and female 34 0.33 ± 0.10 0.17 0.50 Sibling band-sharing 89 0.62 ± 0.11 0.38 0.88 Band-sharing between parents and offspring 170 0.61 ± 0.10b 0.39 0.83 Band-sharing between juveniles and unrelated adultsc 108 0.27 ± 0.13 0.07 0.56 a Number of pairwise comparisons. b Lower 95% CI= 0.59. The upper 95% CI was 0.30 for band-sharing comparisons between all breeding adults. c Juveniles and unrelated adults within the same canyon.
0.80 to 0.96 (Table 5). Band-sharing in Washington Canyon was significantly higher than in Cottonwood Canyon (Mann-Whitney U test, P = 0.043; Table 4) when pair-wise comparisons were made independently. Other betweenpopulation comparisons were not significantly different (Mann-Whitney U test, P > 0.60; Table 4) and there were no significant differences when all pair-wise comparisons were evaluated simultaneously (Kruskal-Wallis test, P = 0.39; Table 4). Table 4. Average band-sharing values (number of pair-wise comparisons in parentheses) of comparisons between Red-naped Sapsuckers breeding in five canyons located in the Toiyabe Range, central Nevada. Band-sharing values between canyons were not significantly different when all pairwise comparisons were evaluated simultaneously (Kruskal-Wallis test, P = 0.39). C1
by breeding adults was observed infrequently, and natal dispersal distance was greater than breeding dispersal distance. Average band-sharing among adults within canyons was 0.31 ± 0.11 and between canyons was 0.28 ± 0.11 (Table 3). Therefore, between-canyon comparisons had lower mean band-sharing values than were found between adults within canyons as well as between mated pairs (Table 3). Furthermore, the distribution of band-sharing scores between 13 mated pairs overlapped completely with the distribution of band-sharing scores among adults within canyons (Table 3), indicating that breeding pairs were a random mix of adults from, the ,entire population and no breeding between first-order relatives occurred. Average band-sharing values for comparisons of adults within and among canyons ranged from 0.25 to 0.34 (Table 4). Population (i.e. canyon) subdivision (Fst) was moderately low, ranging from 0.02 to 0.08, and heterozygosity estimates were relatively high, ranging from Table 2. Breeding dispersal distances and fidelity to the nest tree, breeding area, and canyon for Rednaped Sapsuckers in the Toiyabe Range, central Nevada. Dispersal distances are in m (± SE).
Site Fidelity Type Nest Tree (male) Nest Tree (female) Breeding Area (male) Breeding Area (female) Canyon (male) Canyon (female)
Dispersal Distance
Number of Individuals
Faithful 0 0 7 (± 4) 9 (± 5) 159 (± 51) 166 (± 49)
Faithful 13 (36%) 10 (32%) 16 (44%) 13 (42%) 35 (98%) 20 (97%)
Dispersed 359 (±128) 363 (±131) 408 (±144) 417 (±149) 2685 (±0) 2685 (±0)
Dispersed 23 (64%) 21 (68%) 20 (56%) 18 (58%) 1 (2%) 1 (3%)
9
C1a 0.34 (32)
C2
C2 0.26 (27)b
C3
C4
C5
0.30 (36)
0.28 (33)
0.29 (45)
0.25 (24)
0.29 (10)
0.28 (42)
0.25 (22)
0.31 (21)
0.28 (30)
C3 C4
C5 0.30 (26) a C1= Washington, C2 = Cottonwood, C3 = San Juan, C4 = North Clear, and C5 = Clear. b Band-sharing values between canyons were significantly different when evaluated independently (Mann-Whitney U test, P = 0.04).
The average band-sharing value among siblings was 0.62 ± 0.11 (Table 3). The average band-sharing value among juveniles and presumably unrelated adults within canyons was 0.27 ± 0.13 (Table 3). Juvenile Red-naped Sapsuckers had an average of 5.68 ± 3.22 and 5.64 ± 2.11 paternal- and maternal-specific bands respectively, corresponding to a probability of 6.9 x 10-4 for assigning Table 5. Heterozygosity values (italics), and between-canyon subdivision (Fst) values for Red-naped Sapsuckers in five canyons of the Toiyabe Range, central Nevada. C1a
C2
C3
C4
C5
C1 0.89 0.08 C2 0.96 0.02 0.02 0.07 C3 0.85 0.03 0.06 C4 0.87 0.05 C5 0.80 a C1= Washington, C2 = Cottonwood, C3 = San Juan, C4 = North Clear, and C5 = Clear.
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the male parent incorrectly and 7.4 x 10-4 for assigning the female parent incorrectly (Bruford et al. 1992). Therefore, the probability of false inclusion of extra-pair young was low. The average band-sharing value of parent to offspring comparisons was 0.61 ± 0.10 (Table 3) and band-sharing values were never lower than 0.38 (our cutoff value) for all parent to offspring comparisons. We detected an average of 0.61 (± 0.95) novel bands in parent to offspring comparisons. For eight of the nine families we analyzed, there were no more than two novel bands present in parent to offspring comparisons. Based on these results, we did not exclude any of the social parents as the genetic parents of their putative offspring. DISCUSSION Band-sharing values of comparisons between breeding adult Red-naped Sapsuckers in the Toiyabe Range were similar to estimates (using DNA fingerprinting) for purportedly outbred populations of birds around the world (mean = 0.28 ± 0.05 for 6 species) (Dickinson and Akre 1998, Fleischer et al. 1994, Haydock et al. 2001, Pereira and Wajntal 2001, Piper and Rabenold 1992). Heterozygosity values were reported in studies of the Flammulated Owl (Otus flammeolus), Western Bluebird (Sialia mexicana) and Bare-faced Curassow (Crax fasciolata) and averaged 0.82 ± 0.07 SD (Arsenault et al. 2005, Dickinson and Akre 1998, Pereira and Wajntal 2001), similar to those we calculated for Red-naped Sapsucker. In comparison, Paxinos et al. (2002) found that Hawaiian Goose (Branta sandvicensis) populations suffered bottlenecks in both historic and prehistoric times, resulting in current populations with an average band-sharing value of 0.69 (Rave 1995). Thus, the Red-naped Sapsuckers we studied appeared to be “outbred” with sufficient mixing among unrelated individuals and no founder effect from extinction-colonization events. Furthermore, the average band-sharing value among siblings and between parents and offspring was similar to that reported in the literature for first-order relatives in other bird and mammal species, as assessed by DNA fingerprinting (Arsenault et al. 2002, Dickinson and Akre 1998, Peacock 1997, Piper and Rabenold 1992). Thus, there appeared to be no breeding among first order relatives (i.e. inbreeding) in the Red-naped Sapsucker. Currently, Red-naped Sapsuckers are common and widespread in aspen groves throughout Nevada’s mountains (Floyd et al. 2007). However, in the 1930s, Jean Linsdale noted that aspen trees in the Toiyabe Range were harvested for mining operations (Dobkin and Wilcox 1986) and Red-naped Sapsuckers were not detected anywhere in the Toiyabe Range during surveys conducted there from 1930 to 1933 (Linsdale 1938). Therefore, it is presumed that sapsuckers were extirpated from the entire range (Dobkin and Wilcox 1986) and only two woodpeckers, Northern Flicker (Colaptes auratus) and Hairy Woodpecker (Picoides villosus), persisted at low densities (Linsdale 1938). We found that some adults and juveniles dispersed between canyons in our study area and a large number of birds immigrated into the banded population each year (94 sapsuckers from 1995-1997). It is unknown where the immigrants came from, but the high numbers suggest that some dispersed long distances. Furthermore, the low Fst and moderate band-sharing values suggests there is
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little isolation among canyons within the Toiyabe Range and perhaps from other sapsucker populations outside of this mountain range, as we might expect for a migratory species (Arguedas and Parker 2000). These results suggest that, at the spatial and temporal scale studied here, fragmentation does not pose a substantial barrier to Red-naped Sapsucker dispersal. These results also indicate that sapsuckers were able to re-colonize areas from which they were extirpated soon after suitable habitat regenerated and that re-colonization was by new individuals year after year, rather than by one or a few founders during extraordinary dispersal events. Although the focus of our study was to use mark-recapture and DNA fingerprinting to elucidate dispersal capabilities of the Red-naped Sapsucker, we also used our DNA fingerprinting data to determine parentage for 9 families. Our results indicated that in the Red-naped Sapsuckers we studied, males did not successfully fertilize females other than their social mate. Our sample size of families was small (N = 9), but our results indicate that extra-pair fertilization is not a common mating strategy in this species. However, extra-pair mating may occur in this species, but at a rate lower than we were able to detect (less than approximately 10%). In two cooperatively breeding woodpeckers, the Red-cockaded Woodpecker (Picoides borealis) and Acorn Woodpecker (Melanerpes formicivorus), breeding groups vary from monogamous pairs to groups including multiple breeding adults and non-reproductive helpers (Dickinson et al. 1995, Haig et al. 1994, Mumme et al. 1985). In both species, socially monogamous pairs are usually genetically monogamous, but larger social groups often have shared parentage (Dickinson et al. 1995, Haig et al. 1994, Haydock et al. 2001). In the Red-cockaded Woodpecker, 1.3% of offspring were from extra-pair mating (Haig et al. 1994). Unfortunately, genetic parentage has not been determined for strictly socially monogamous woodpeckers. However, polyandry has been reported once in the typically monogamous Northern Flicker (Wiebe 2002) so some generally monogamous woodpeckers may sometimes exhibit alternative mating strategies. ACKNOWLEDGMENTS Field assistance was provided by J. Long, S. Parsons, B. Trussell, H. Woodward, and L. Butcher. We thank M. Lyons-Weiler and Dr. J. Ellsworth for lab help and K. Kopec for running gels and scoring fingerprints. This research was funded by the U.S. Forest Service (USFS), the Center for Conservation Biology of Stanford University, the Wells Family Foundation, and the Biological Resources Research Center of the University of Nevada, Reno. Monetary support was facilitated and coordinated by L. Hillerman (UNR), C. Boggs (Stanford University), and by G. Grevsted and M. Schwalbach (USFS). Thanks also to UNR’s Laboratory of Ecological and Evolutionary Genetics, the Yomba Shoshone Tribal Council, staff from the Austin Ranger District office of the USFS, and the people of Austin NV for their assistance and cooperation.
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Fleury, S.A. 2000. Population and Community Dynamics in Western Riparian Avifauna: the Role of the Red-Naped Sapsucker (Sphyrapicus nuchalis). PhD thesis, University of Nevada, Reno, NV. Floyd, T., C.S. Elphick, G. Chisholm, K. Mack, R.G. Elston, E.M. Ammon, and J.D. Boone. 2007. Atlas of the Breeding Birds of Nevada. University of Nevada Press. 608 pp. Haig, S.M., J.R. Walters, and J.H. Plissner. 1994. Genetic evidence for monogamy in the cooperatively breeding Red-cockaded Woodpecker Behavioral Ecology and Sociobiology 34:295-303. Haydock, J., W.D. Koenig, and M.T. Stanback. 2001. Shared parentage and incest avoidance in the cooperatively breeding Acorn Woodpecker. Molecular Ecology 10:1515-1525. Howell, T.R. 1952. Natural history and differentiation in the Yellow-bellied sapsucker. Condor 54:237-282. Jeffreys, A.J., N.J. Royle, V. Wilson, and Z. Wong. 1988. Spontaneous mutation rates to new length alleles at tandem-repetitive hypervariable loci in human DNA. Nature 332:278-281. Johnson, D.H., and J.W. Grier. 1988. Determinants of breeding distributions of ducks. Wildlife Monographs 100:1-37. Koenig, W.D., D. Van Vuren, and P.N. Hooge. 1996. Detectability, philopatry, and the distribution of dispersal distances in vertebrates. TREE 11:514-517. Linsdale, J.M. 1938. Environmental responses of vertebrates in the Great Basin. American Midland Naturalist 19:1-206.
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