3 / The Wilson Journal ofOrnithology 118(1):36—41, 2006 2 A COMPARATIVE BEHAVIORAL STUDY OF THREE GREATER SAGE-GROUSE POPULATIONS SONJA E. TAYLOR1 AND JESSICA R. YOUNG — ABSTRACT. We compared male strut behavior of the genetically distinct Lyon, Nevada/Mono, California Greater Sage-Grouse (Centrocercus urophasianus) population with that oftwo proximal populations: Nye, Ne- vada, and Lassen, California. We measured strut rates and nine acoustic components ofthe strut display in all three populations. Male strut rates did not differ among populations. Acoustic components ofthe Lyon/Mono and Lassen populations were similar, whereas the Nye population was distinct. The genetically distinct Lyon Mono population was more similar behaviorally to the Nye population than the genetically similar Nye and Lassen populations were to each other. Overall, the Lyon/Mono populationdidnotexhibitdetectabledifferences in male strut behavior. Reproductive isolation through sexual selection does not appear to have occurred in the Lyon/Mono population. Received27 September2004, accepted 19 October2005. Two recent studies based on mitochondrial 1999) supported the morphological and be- gene sequence (Benedict et al. 2003, Oyler- havioral data and led to species designation McCance et al. 2005) and nuclear microsat- for the Gunnison Sage-Grouse (American Or- ellite markers (Oyler-McCance et al. 2005) re- nithologists’ Union 2000, Young et al. 2000). vealed a genetically distinct population of A similar approach would determine whether Greater Sage-Grouse (Centrocercus urophas- the genetic distinctiveness of the Lyon/Mono ianus) on the Nevada/California border(Lyon, population has been manifested morphologi- Nevada/Mono, California). Those studies in- cally and/orbehaviorally as it has in Gunnison dicated that the Lyon/Mono Greater Sage- Sage-Grouse. Ifso, it could potentially lead to Grouse population is more genetically distinct a taxonomic reclassification. from other Greater Sage-Grouse populations Male mating success and mate-choice cues than is the newly described (Young et al. (Gibson and Bradbury 1985), territoriality 2000) Gunnison Sage-Grouse (C. minimus) (Gibson and Bradbury 1987), components of species. Several factors, including the appar- female choice (Gibson et al. 1991), and male ent genetic and geographic isolation of Lyon/ strutting behavior (Young et al. 1994) have Mono sage-grouse from other populations, the been studied previously in the Mono sage- degradation and loss of sagebrush (Artemisia grouse population. However, with the excep- spp.) habitat, and an overall population de- tion of Young et al. (1994), there have been cline, have made this a population of interest no comparative studies among populations. from both evolutionary and conservation per- Young et al. (1994) compared secondary sex- spectives. ual characteristics from ma—le strut displays Morphological (Hupp and Braun 1991) and among three populations one Gunnison behavioral studies (Young et al. 1994) ofGun- Sage-Grouse population (Gunnison Basin, nison Sage-Grouse provided evidence that Colorado) and two Greater Sage-Grouse pop- sexual selection had driven speciation in the ulations (Mono, California, and Jackson, Col- isolated populations of sage-grouse in south- orado). The structure of the Gunnison male western Colorado and southeastern Utah. The strut display was strikingly different from that use of both mitochondrial (Kahn et al. 1999) of the other two populations. However, the and nuclear markers (Oyler-McCance et al. comparison of the similarly structured strut display between males from Mono and Jack- 1 Rocky Mountain CenterforConservationGenetics son indicated statistically significant differ- and Systematics, Dept, of Biological Sciences, Univ. ences in most of the acoustic measures. of Denver, Denver, CO 80208, USA. In light of the genetic distinctiveness of u8r1a22l3W1e,asntUdeSrAnE.nSvtiarteonCmoelnlteagle oSfciCeonlcoersa,do,GuDnenpits,ono,f NCatO- rLeysoulnt/sMoofnoYousangge-egtroalu.se(19a9n4d),twheebuenhdaevritooroakl 3Corresponding author; e-mail: a furtherexamination ofmale strut display be- sonja_taylor@comcast.net havior. We compared the Lyon/Mono popu- 36 Taylorand Young • GREATER SAGE-GROUSE BEHAVIOR 37 FIG. 1. Current Greater Sage-Grouse distribution in California and Nevada, and locations of three sample populations (modified from Schroeder et al. 2004). lation with two proximal populations of displays were taken at five leks. Greater Sage- Greater Sage-Grouse (Fig. 1). We tested the Grouse in Lyon County, Nevada, and Mono hypothesis that the Lyon/Mono population’s County, California, form a connected, inter- behavior is measurably different from that of breeding population (Lyon/Mono). Record- other Greater Sage-Grouse populations and ings were completed between 9 and 17 April may, in fact, be considered a separate taxon 2001 at three leks from the Lyon/Mono pop- given the genetic differences. Alternatively, ulation: Lyon County, Nevada (Desert Creek although the Lyon/Mono population appears 2 lek; 38°42' N, 1 19° 18' W; 1,603 m), south- genetically isolated, behaviorally it may not ern Mono County, California (Long Valley 1 be significantly different from other Greater lek; 37°42' N, 118°48' W; 2,124 m), and Sage-Grouse populations, indicating that sex- northern Mono County, California (Biedeman ual selection resulting in pre-mating isolating lek; 38° 12' N, 119°6'W; 2,447 m). Of the mechanisms has not occurred. three recorded Lyon/Mono leks, the Desert Creek and Biedeman leks are farthest apart METHODS (123 km). Lassen County, California (Eastside The three populations we studied are from lek; 40° 18' N, 120° 0'W; 1,490 m), is ap- the southwestern edge of the Greater Sage- proximately 250 km north and Nye County, Grouse range in Nevada and California (Fig. Nevada (Roadside lek; 38°42' N, 116°47' W; 1). Behavioral measurements of male strut 2,121 m), is approximately 215 km east ofthe n 38 THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 118, No. 1, March 2006 N X Airsacpops >s u c / aD> cr . Whistlepeak * a> k ^ Whistlpstart — * • « * ** ^1 jL-Whistleminimum Time (sec) FIG. 2. Typical sonagram ofa Greater Sage-Grouse male strut display. The two air sac pops, whistle start frequency, whistle peak, and whistle minimum are labeled. See Table 1 for all acoustic components (modified from Young et al. 1994). Lyon/Mono population; recordings at these for each component. An estimate of repeat- sites were completed between 3 and 1 1 April ability ([r = s2a/(s2 + s2a)]; Lessells and Boag 2002. The number of males sampled from 1987) was used to measure the proportion of each of the five leks was as follows: Desert within-individual variation within populations Creek 2 (n = 6), Long Valley 1 (n = 9), for each component. Repeatabilities range Biedeman (n — 9), Eastside ( = 11), and from 0 (low) to 1.0 (high). High repeatabilities = Roadside (n 14); therefore, the sample size indicate that the measured trait varies little for the Lyon/Mono population was n = 24. within individuals relative to the population Males perform a ritualized strut display in variation, suggesting that the trait could re- which they take a few steps forward and brush spond to sexual selection. their wings twice against their esophageal To calculate strut display rate, we timed be- pouch producing loud swishing noises (Fig. tween-strut intervals using Etholog 2.2, an 2). Following these wing movements, males ethological transcription tool (Ottoni 2000). compress air sacs and produce syringeal The display rate for each male was based on sounds to complete a single strut display 7—40 consecutive struts in which no more than (Hjorth 1970). Male strut displays were re- 30 sec had lapsed between struts. Females corded and compared using the methods of were present on all leks during strut-rate mea- Young et al. (1994) with the following mod- surements, but any male included in the strut- ifications. Only adult males were monitored, rate analyses had to have females within 20 m and these were distinguished fromjuveniles in of them during recording. This criterion the field by the presence ofaclearwhite upper lowered the sample sizes (number of males) breast on adults. Individual males were iden- for population strut-rate estimation (Fig. 3). tified by their tail patterns (Wiley 1973). At At the Lassen and Lyon leks, measurements least 15 struts per male were recorded using were taken as one female moved throughout a Sony DCR TRV720 digital camcorder and the leks. The southern Mono, northern Mono, a Sennheiser MKH70-P48 microphone. and Nye leks all had multiple females visiting Sounds of individual struts were digitized at leks over the various days that measurements 22 kHz using Canary 1.2.4 sound analysis were taken. software (Cornell Laboratory of Ornithology, We used analysis of variance (ANOVA) to Ithaca, New York). assess differences among populations for each We measured nine acoustic components acoustic component and strut rate. We then (Table 1, Fig. 2) and calculated population used the GT2-method (Hochberg 1974) to means derived from individual male averages make unplanned comparisons among popula- n Taylorand Young • GREATER SAGE-GROUSE BEHAVIOR 39 TABLE 1. Nine measured acoustic components of male Greater Sage-Grouse strut display in three populations from Nevada and California. Males were recorded while strutting during spring 2001 and 2002. Lyon,Nevada/Mono, Lassen,California Nye,Nevada California( = 24) (n = 11) (n = 14) Acoustic Measuredvariable component Mean SE Mean SE Mean SE pa First pop to whistle peak (msec) 73.41 0.37 73.85 0.65 70.30 0.52 <0.001 1 Whistle peak to whistle minimum (msec) 2 40.21 0.28 39.81 0.32 41.69 0.61 0.012 Pop to pop (msec) 3 199.89 0.73 199.64 0.97 192.24 0.88 <0.001 Whistle start frequency (Hz) 4 861.17 7.61 861.65 10.97 930.19 20.19 <0.001 Whistle peak (Hz) 5 2,619.83 21.06 2,657.32 23.09 2,873.84 42.85 <0.001 Whistle minimum (Hz) 6 533.58 5.89 514.48 7.56 637.26 9.63 <0.001 Whistle start to peak difference (Hz) 7 1,771.61 20.69 1,795.22 23.94 1,944.72 35.09 <0.001 Whistle peak to minimum difference (Hz) 8 2,096.48 21.90 2,151.64 17.61 2,241.51 39.14 0.002 Whistle start to minimum difference (Hz) 9 333.90 11.33 353.70 13.99 290.38 16.80 0.020 aANOVA. tion means with unequal sample sizes for all P < 0.05; Table 1). The acoustic compo- acoustic components. This method uses the nents of the males’ displays were similar be- studentized maximum modulus distribution m tween Lyon/Mono and Lassen, whereas those to compute a minimum significant difference of Nye males’ displays were consistently dis- (MSD). The significance level for the tinct from those of the other two populations. ANOVA was set atP — 0.05 and forthe GT2- Nye differed from both Lyon/Mono and Las- method it was lowered from P = 0.05 to P = sen for acoustic components 1 and 3-7 (GT2- 0.017 using a Bonferroni correction (a" = a/ test, all P < 0.01). For component 8, Nye dif- k; Sokal and Rohlf 1995) for multiple tests. fered only from Lyon/Mono (GT2-test, P < We used a" = 0.01 when referring to the stu- 0.010). All other pairwise population compar- dentized maximum modulus m critical values isons for minimum significant differences table (GT2-method). were not significant (GT2-test, all P > 0.01). RESULTS Repeatability estimates ofthe acoustic components ranged from 0.41 to 0.84 in Lassen, All nine acoustic components of the strut 0.57 to 0.96 in Nye, and 0.35 to 0.91 in Lyon/ display differed among populations (ANOVA, Mono (Table 2). The highest repeatability estimate for all three populations was forwhistle 8.5 (ii) F2,31=3.97,P=0.029 peaSktru(tcormaptoesnen(tstr5u).ts/min) differed (F = jD^/5 8.0 tI 3.97, P = 0.029) among populations (Fi2g<3.1 3). 2, 7.5 (16) However, pairwise comparisons between pop- 0Q3) (7) ulations indicated that none were significant w| 7.0 f * (GT2-test, all P > 0.01). Lassen males had the highest strutting rate (7.84 struts/min), where- 6.5 as males from Nye had the lowest strutting rate (6.92 struts/min). Lyon/Mono males had 6.0 Lyon/Mono Lassen Nye an intermediate strutting rate (7.21 struts/min). FIG. 3. Means (with standard error bars) and DISCUSSION ANOVA Grouse frroemsultthrfeoerpsotpruutlartaitoenss:ofLymoanl,eNGerveaadtear/MSoangoe,- We measured behavioral traits and second- California; Lassen, California; andNye,Nevada. Sam- ary sexual characteristics that are related to ple sizes (number ofmales) are in parentheses. sexual selection in sage-grouse, which could 40 THE WILSON JOURNAL OL ORNITHOLOGY • Vol. 118, No. 1, March 2006 TABLE 2. Repeatability estimates ofstrutdisplay rather than a lack of genetic variation or in- acoustic components within individual males from accuracies in measurement (Boake 1989). Nye three Greater Sage-Grouse populations in California had the highest repeatability estimates forsev- and Nevada. Males were recorded while strutting dur- en of the nine acoustic components, suggesting spring 2001 and 2002. ing low variation in the acoustic measure- Lyon,Nevada/ Lassen, ments, despite samples being taken across cAocmopuosnteinct Monon,=Cal2i4fornia Canli=for1n1ia Nyen,=Ne1v4ada several days with multiple females being present. 1 0.51 0.78 0.65 Although strut rates did differ among pop- 2 0.35 0.44 0.62 3 0.64 0.74 0.65 ulations, pairwise comparisons of strut rate 4 0.57 0.67 0.79 did not differ statistically between popula- 5 0.91 0.84 0.96 tions. This result agrees with the observations 6 0.57 0.68 0.79 of Young et al. (1994), who found that strut 7 0.53 0.80 0.88 rates did not differb—etween two Greater Sage- 8 0.74 0.49 0.87 Grouse populations Mono, California, and 9 0.41 0.41 0.57 Jackson, Colorado. Strut rates may vary with time of day, time of season, and proximity of females (R. M. Gibson pers. comm.); there- therefore lead to divergence. Based on behav- fore, variation in strut rate within and between ioral differences in male strut displays, our males may outweigh differences in strut rates study did not support the idea that the genet- among populations except in strong cases of ically distinct Lyon/Mono population should population divergence. be considered for separate taxonomic status. Our results suggest that the Lyon/Mono The Lyon/Mono and Lassen populations were population does not exhibit any appreciable similar to each other, while the Nye popula- behavioral differences in male mating displays tion was the most unique across nine acoustic from other Greater Sage-Grouse populations. components of male mating displays. How- The Lyon/Mono population is significantly ever, across six components (1-4, 6, 9), the different genetically from the Lassen popula- Nye versus Lassen populations were either tion (Benedict et al. 2003, Oyler-McCance et more different or as different as Nye versus al. 2005), yet behaviorally, the Lyon/Mono Lyon/Mono populations (Table 1). Even and Lassen populations have similar acoustic though the Lyon/Mono population is geneti- strut components and strut rates. The impli- cally distinct, male mating behaviors are more cations ofthe slight behavioral differences ob- similar to those of the Nye population than served in the Nye population on female mate those of the genetically similar Nye and Las- choice may be determined upon further be- sen populations are to each other (Table 1). havioral observations that include additional The repeatability estimates generally varied leks, years, and populations. It is possible that widely across populations. However, three there are measurable differences in acoustic acoustic components (3, 5, and 9) were rela- components ofthe strut display between most tively comparable among the three popula- populations, but these differences are gener- tions. The high repeatability estimates for ally minimized by gene flow. components 3 (pop to pop) and 5 (whistle The Lyon/Mono population is genetically peak) indicate that these traits vary little with- more diverse and distinct than the Gunnison in individual males relative to the variation Sage-Grouse species (Kahn et al. 1999, Oyler- within populations and could potentially re- McCance et al. 1999, Benedict et al. 2003, spond to selection. Young et al. (1994) also Oyler-McCance et al. 2005). Using mitochon- DNA found high repeatability estimates for whistle drial sequence, Benedict et al. (2003) peak, which has been shown to be related to estimated that the Lyon/Mono population has female mate choice (Gibson and Bradbury been isolated from other Greater Sage-Grouse 1985, but see Gibson et al. 1991). A low re- populations for tens of thousands of years. peatability for component 9 (whistle start to Yet, neither local adaptation to ecological or minimum difference) is most likely the result environmental factors, nor genetic drift, nor ofhigh levels of variability within individuals sexual selection has led to detectable pheno- Taylorand Young • GREATER SAGE-GROUSE BEHAVIOR 41 typic (behavioral) differences in this popula- dae, with special reference to males. Viltrevy 7: tion. Reproductive isolation does not appear 183-596. to have occurred through sexual selection in Hochberg, Y. 1974. Some generalizations of the T- methodinsimultaneousinference.JournalofMul- the Lyon/Mono population as it has in the tivariate Analysis 4:224-234. Gunnison Sage-Grouse species. Hupp, J. W. and C. E. Braun. 1991. Geographic var- ACKNOWLEDGMENTS iation among Sage Grouse in Colorado. Wilson Bulletin 103:255-261. Funding and support for this project was provided Kahn, N. W., C. E. Braun, J. R. Young, S. Wood, D. by theCaliforniaDepartmentofFishandGame, Quail R. Mata, andT. W. Quinn. 1999. Molecularanal- Unlimited, the National Fish and Wildlife Foundation, ysis ofgenetic variation among large- and small- Western State College ofColorado, and the Bureau of bodied Sage Grouse using mitochondrial control Land Management. We are grateful to D. S. Blanken- region sequences. Auk 116:819-824. Rsh.ipM,.F.GiAb.soHnal,l,W.T.F.L.MaRnudsesiv,ilJl.e,Faatnoodh,T.SS.laLt.auNseklisofno,r Lesserlelpesa,taCb.iliMt.iesa:nadcP.omT.moBnoamgi.st1a9k8e7..AUunkre1p0e4a:t1a1b6le- logisticalandfieldsupport.WeappreciateM. K. Bollig 121. and M. D. Kascak for their assistance with graphics. Ottoni, E. B. 2000. EthoLog 2.2: a tool for the tran- We thank C. E. Braun, J. W. Connelly, R. M. Gibson, scription and timing ofbehavior observation ses- hS.elJp.fuOlylceorm-mMecnCtasncoen,thKe.mPa.nuRsecersiep,t.anFdinJa.llSyt,.wJeohtnhafnokr s&ionCso.mpBuethearvsio3r2:R4e4s6e-a4r4c9h.Methods, Instruments, S. L. Thode and R. D. Taylorforpatienceandsupport. OyleCr.-ME.cCBarnacuen,, Sa.ndJ.,T.N.W.W.QuKianhnn.,1K9.99P.. BAurponphualma,- LITERATURE CITED tion genetic comparison of large- and small-bodied Sage Grouse in Colorado using microsatellite American Ornithologists’ Union. 2000. Forty-sec- and mitochondrial markers. MolecularEcology 8: ond supplement to the American Ornithologists’ 1457-1465. Union check-list of North American birds. Auk Oyler-McCance, S. J., S. E. Taylor, and T. W. 117:847-858. Quinn. 2005. Amultilocuspopulationgeneticsur- Benedict, N. G., S.J. Oyler-McCance, S. E.Taylor, vey of Greater Sage-Grouse across their range. C. E. Braun, and T. W. Quinn. 2003. Evaluation Molecular Ecology 14:1293-1310. of the eastern (Centrocercus urophasianus uro- Schroeder, M. J., C. A. Aldridge, A. D. Apa, J. R. phasianus) and western (Centrocercus urophasi- Bohne, C. E. Braun, S. D. Bunnell, J. W. Con- anusphaios) subspecies ofsage-grouse using mi- nelly, et al. 2004. Distribution of Sage Grouse tochondrial control-region sequence data. Conser- in North America. Condor 106:363-376. vation Genetics 4:301-310. Sokal, R. R. and F. J. Rohlf. 1995. Biometry: the Boake, C. R. B. 1989. Repeatability: its role in evo- principles and practice of statistics in biological lutionary studies of mating behaviour. Evolution- research. W. H. Freeman and Company, New ary Ecology 3:173-182. York. Gibson, R. M. and J. W. Bradbury. 1985. Sexual se- Wiley, R. H. 1973. Territorialityandnon-randommat- lection in lekking Sage Grouse: phenotypic cor- ing in Sage Grouse, Centrocercus urophasianus. relates of male mating success. Behavioral Ecol- Animal Behavior Monographs 6:85-169. ogy and Sociobiology 18:117-123. Young, J. R., C. E. Braun, S. J. Oyler-McCance, J. Gibson, R. M. and J. W. Bradbury. 1987. Lek orga- W. Hupp, and T. W. Quinn. 2000. A new species nization in Sage Grouse: variations on aterritorial ofSage-Grouse (Phasianidae: Centrocercus from ) theme. Auk 104:77-84. southwestern Colorado. Wilson Bulletin 112:445- Gibson, R. M., J. W. Bradbury, and S. L. Vehren- 453. camp. 1991. Mate choice in lekking Sage Grouse Young, J. R., J. W. Hupp, J. W. Bradbury, and C. E. revisited: the roles of vocal display, female site Braun. 1994. Phenotypic divergence of second- fidelity, and copying. Behavioral Ecology 2:165- ary sexual traits among Sage Grouse, Centrocer- 180. cus urophasianus populations. Animal Behaviour , Hjorth, I. 1970. Reproductive behavior in Tetraoni- 47:1353-1362.

A COMPARATIVE BEHAVIORAL STUDY OF THREE GREATER SAGE-GROUSE POPULATIONS

Similar A COMPARATIVE BEHAVIORAL STUDY OF THREE GREATER SAGE-GROUSE POPULATIONS