Divergent species richness and vocal behavior in avian migratory guilds along an elevational gradient Michael C. McGrann1,† and Brett J. Furnas2 1
Environmental Science Department, Division of Natural and Applied Sciences, William Jessup University, 2121 University Avenue, Rocklin, California 95765 USA 2 Wildlife Investigations Laboratory, California Department of Fish and Wildlife, 1701 Nimbus Road, Suite D, Rancho Cordova, C alifornia 95670 USA Citation: McGrann, M. C., and B. J. Furnas. 2016. Divergent species richness and vocal behavior in avian migratory guilds along an elevational gradient. Ecosphere 7(8):e01419. 10.1002/ecs2.1419
Abstract. Climate change is expected to disrupt the distribution and behavior of montane birds. Mon-
itoring these impacts will be essential because the ecological effects of climate change are likely to be complex. Hiking trails that traverse montane regions provide an opportunity to efficiently survey bird diversity along elevation and other ecological gradients, and these data can be used to model climate- related vulnerabilities of avian communities. In 2010, we surveyed a 697-km segment of the Pacific Crest Trail in northern California, USA. We conducted point counts of birds at 404 sites during the breeding season when birds were readily detected by song and other vocalizations. To bolster our sampling effort, we left automated recorders at approximately half of the sites to make recordings for later interpretation of bird vocalizations. Using a multispecies occupancy model, we investigated how relationships between richness and elevation and between vocal activity and daily temperature differed among three migratory guilds—residents, altitudinal migrants, and Neotropical migrants. We found that richness decreased with increasing elevation for residents and Neotropical migrants, whereas it increased for altitudinal migrants. As temperature increased, residents and altitudinal migrants curtailed their vocal activity, but Neotropical migrants did not reduce vocal activity even though this behavior is energetically expensive on hot days. We also found that total species within each of three elevation zones was greatest at middle elevations (1200–1900 m). Altogether, these findings suggest that as global temperature rises there may be greater competition among birds previously separated by elevation and that Neotropical migrants may be at greater risk of heat stress during the breeding season. Furthermore, the conservation of structurally complex, middle-elevation forests could provide birds a refugium to the impacts of climate change.
Key words: altitudinal migrants; California; detection probability; elevational diversity patterns; multispecies occupancy models; Neotropical migrants; Pacific Crest Trail; temperature relationships. Received 1 May 2016; accepted 13 May 2016. Corresponding Editor: D. P. C. Peters. Copyright: © 2016 McGrann and Furnas. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. † E-mail:
[email protected]
Introduction
mountain ranges within the same geographic region, bird species richness can display different associations with temperature, precipitation, and primary productivity (McGrann et al. 2014). The response of birds to climate change also varies, and over the past century, individual species across neighboring mountain ranges have altered their altitudinal ranges in divergent directions—both
Montane bird communities have complex species-diversity relationships with climate and other environmental drivers. On mountains around the globe, elevational patterns in avian species richness vary depending on the climate of a mountain (McCain 2009). Even among adjacent v www.esajournals.org
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upslope and downslope—depending on the climate niche of the species and the distinct climate of each mountain (Tingley et al. 2012). This regional heterogeneity in climate response underscores the challenges faced by decision makers in anticipating the impacts of climate change (Miller-Rushing et al. 2010), and large-scale studies on mountains can help to clarify the underlying climate factors that determine diversity patterns and inform conservation planning over the long term. Yet such efforts, particularly in remote mountain regions, remain rare. Breeding phenology is also sensitive to changes in climate because birds must match their reproductive cycles to climate-induced shifts in the peak availability of food resources on breeding grounds (Both et al. 2006, Møller et al. 2008). Furthermore, any changes in ambient temperature can have a direct influence on the metabolism of reproduction and timing of egg laying (Dunn and Winkler 2010). In general, birds have adapted to warming temperatures by advancing the timing of several reproductive behaviors, including vocal displays, to earlier dates in the spring (Dunn and Winkler 2010, Rubolini et al. 2010, Dunn and Møller 2014). However, depending on migratory status, species appear to differ in their ability to adjust this timing. For example, a study in central Europe found that year-round residents in temperate climates have advanced their song activity patterns more than long-distance migrants that winter in tropical climates but breed in temperate climates (Rubolini et al. 2010). This behavioral plasticity to climate change in residents may have evolved because these species complete their life cycles entirely within temperate climates that have highly variable weather throughout the year. Migrants, on the other hand, spend only a portion of their lives on temperate breeding grounds and have evolved more rigid behavioral responses to environmental cues (e.g., day length or changes in habitat quality) on tropical wintering grounds (Pulido and Widmer 2005, Lehikoinen and Sparks 2010, Rubolini et al. 2010, Knudsen et al. 2011). Therefore, residents are expected to be able to adjust their vocal activity more than migrants both in the short term, in response to daily temperature variation throughout the breeding season, and in the long term, in response to climate change. Given the heterogeneity observed in richness–elevation and breeding behavior–climate v www.esajournals.org
relationships, our aim was to compare these relationships among migratory guilds (residents, altitudinal migrants, and Neotropical migrants) of the montane bird community. We were interested in describing any divergence by these guilds in species diversity patterns along the elevation gradient. We expected that species belonging to different guilds will vary in their adaptations to climate and other environmental factors, and in their ability to compete for limited resources, and thus will be distributed along the elevation gradient differently. We employed a transect that follows the Pacific Crest National Scenic Trial (PCT) across the mountain ranges of northern California in the western United States. Hiking trails, like the PCT, can be effective tools to study montane biodiversity because they provide access to these remote ecosystems and span extensive climate–elevation gradients (McGrann and Thorne 2014, McGrann et al. 2014). We combined traditional point count methods with the use of automated recorders (Furnas and Callas 2015) to survey bird diversity and to facilitate the use of multispecies occupancy models (MSOMs) that account for imperfect species detection (Iknayan et al. 2014). Our objectives were to contrast species richness–elevation patterns across the three migratory guilds, describe the underlying differences in species composition at different elevations, and compare the response of vocal behavior to daily temperature changes among the three migratory guilds over the course of a single breeding season. We hypothesize that (1) birds will partition their occupancy of different elevations and show divergent richness– elevation patterns by migratory guild and that (2) birds that migrate shorter distances, or that do not migrate at all, will exhibit greater behavioral plasticity by vocalizing less on hotter days. We also explore the implications of our findings with respect to the resilience of avian communities to climate change.
Methods Study area
The PCT is a recreational hiking and equestrian trail that traverses the mountain ranges of the Pacific cordillera from Mexico to Canada in the western United States. In 2010, we completed bird and habitat surveys along a 698-km segment of
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PCT in northern California (39.85° N to 42.00° N). This transect began in the northern Sierra Nevada, crossed the Cascade Ranges and the Klamath Mountains, and ended at the Oregon border (Fig. 1). The ecoregions traversed by this route are predominantly forested and diverse in climate, geology, and vegetation composition (Schoenherr 1992). The lands throughout these ecoregions are a mix of public and private ownerships under diverse managements, ranging from timber harvest and cattle grazing to wilderness protection. However, the trail itself is mostly restricted to public lands with little recent timber harvest. Along this segment of trail that we surveyed, 404 survey sites were established at 10-min walking intervals (approximately 500–700 m) and ranged from 500 to 2307 m in elevation. Our protocols restricted surveys to morning hours, and observers completed surveys along the trail in an alternating pattern. Approximately 15 survey sites were completed in the morning each day along an 8- to 11-km trail segment. Observers then walked a trail segment of similar length each afternoon to reach the start of the next set of morning surveys. The PCT in northern California generally exhibits drier conditions in the east, where it lies within the rain shadow of the Cascade Range, and moister conditions in the Klamath Mountains in the west (McGrann et al. 2014). Habitats were predominantly composed of semiarid woodlands at lower elevations and more mesic, forested habitat types at middle to upper elevations (92% of sites surveyed were woodland or forest types). Shrub habitat types were also present but not common (8% of sites). Forested and shrub habitat types (Mayer and Laudenslayer 1988) included sagebrush (Artemisia tridentata), montane chaparral, blue oak–foothill pine woodlands (Quercus douglasii and Pinus sabiniana), juniper woodlands (Juniperus spp.), montane hardwood, montane hardwood conifer, Klamath mixed conifer, Sierran mixed conifer, Douglas fir (Pseudotsuga menziesii), white fir (Abies concolor), red fir (Abies magnifica), lodgepole pine (Pinus contorta), Jeffrey pine (Pinus jeffreyi), and subalpine conifer.
Fig. 1. Route of the Pacific Crest Trail (gray line) through California, Oregon, and Washington in the western United States and the 698-km transect (black line) in northern California where bird surveys were completed from 16 May to 22 July 2010.
for fixed-radius point counts (Blondel et al. 1970, Ralph et al. 1995). Observers completed 5-min counts at each site and counted all birds seen or heard on fixed-radius (50 m) circular plots. Only adults were counted and fledglings were excluded from point count observations. Human activity was light throughout this section of the PCT and point counts were rarely interrupted by other trail users, but when this did occur, the observers restarted the point count when the trail users left the area. Two observers separately
Bird surveys
We completed bird surveys from 16 May to 22 July 2010 and followed standard methodology v www.esajournals.org
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completed a point count on different dates. Automated devices for recording bird vocalizations were deployed at a random subset of 173 of the 404 sites. The first observer completed the first point count and deployed the automated recorder. The second observer followed 3 d later, completed a second point count, and retrieved the recorder. We followed protocols described by Furnas and Callas (2015) using a lightweight digital voice recorder with factory provided stereo microphones (DS-40; Olympus Corporation, Center Valley, Pennsylvania, USA). We placed the digital voice recorder inside a protective container on the ground and off the trail about 5–10 m from the center of the plot, while being careful not to place the recorder directly adjacent to sound attenuating obstructions (large tree bole, large rock, shrub, etc.) but out of sight of trail users. The recorders were programmed to record for 5 min, three times each day, for three consecutive days at 30 min before local sunrise, sunrise, and 30 min after sunrise, generating a total of 1557 recordings across all the sites. A biologist (MCM) experienced in California bird identification listened to and viewed the spectrogram of each recording using Raven Pro software (version 1.4; Cornell Lab of Ornithology, Ithaca, New York, USA), and all species were identified by song, call, or other aural cue (woodpecker drumming).
the relative differences among grid cells in the 800-m data for May, June, or July, depending on which month in 2010 the surveys occurred. The values of these points were computed as their daily value from the 4-km gird plus their difference from the mean value of pooled points from the 800-m grid. By following this procedure, we obtained estimates of daily maximum temperature at 800-m resolution for each observation site.
Data analysis
Furnas and Callas (2015) found that the effective distance for detecting species using recording devices of the design we employed was about 40–50 m, similar to the 50-m fixed distance used in our point counts. They also found that occupancy estimates from points counts were comparable to those from automated recorder surveys after controlling for differences in detection probability. Therefore, we combined data from the two point counts and the nine recordings, producing 11 temporal replicates at sites where both methods were used and two replicates at the other sites. Multiple visits at each site allowed us to construct a detection history for use in occupancy estimation techniques (MacKenzie et al. 2006, Iknayan et al. 2014). To compare differences among migratory guilds, we categorized species as residents, if they are sedentary and remain in the same climate year-round, altitudinal migrants, if they winter at low-elevation climates and breed Temperature data Temperature data were extracted from spatial in high-elevation climates in California, and grids at two spatial (800-m and 4-km) and Neotropical migrants, if they winter in the neotemporal resolutions (daily maximum tempera- tropics (Mexico, Central America, and South ture and 30-yr monthly maximum temperature) America) and breed in California. We classified derived from the Parameter-elevation Relation species into these guilds based upon natural hisships on Independent Slopes Model (http://prism. tory data found in Birds of North America online oregonstate.edu; Daly et al. 2008). From the 4-km species accounts (Cornell Lab of Ornithology; grids, we extracted daily maximum temperature http://bna.birds.cornell.edu). We limited modvalues for each day that surveys were conducted eled species to membership in Galliformes, at every site in ArcGIS (version 10; Environmental Columbiformes, Piciformes, and Passeriformes, Systems Research Institute, Redlands, California, which comprised the bulk of the data set (96% of USA). Using the same process, we extracted detections). monthly maximum temperatures for May, June, Occupancy represents the proportion of a and July for each site during a 30-yr period span- study area in which a particular species occurs ning 1981–2010. We used spatial differences in or the probability that a given location is occupredicted temperature from the 800-m grid to pied by the species (MacKenzie et al. 2006). adjust the daily temperature values from the Occupancy modeling allows simultaneous esti4-km grid. We did this by pooling all survey mation of detection and occupancy probabilities points for a given day occurring in the same 4-km using temporally replicated surveys occurring grid cell and adjusting their values according to over a time period for which occupancy is v www.esajournals.org
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assumed to remain constant. We pooled the survey data from numerous species to fit a Bayesian MSOM wherein differences among species were modeled with hyperparameters varying as random effects about mean values for a group of species (Dorazio and Royle 2005, Zipkin et al. 2009). To address differences among migratory guilds, we fit separate hyperparameters for each of the three guilds such that parameter means were for guilds and not the entire set of modeled species. To provide unbiased estimates of alpha and gamma diversity (species richness either at a single site or the total for a group of sites), our model included data augmentation to include the effects of rare and cryptic species that were present but never observed (Iknayan et al. 2014). This method is analogous to extrapolation of a species accumulation curve (Colwell and Coddington 1994). It is important to address potential biases in occupancy and species richness measurement so that our conclusions are not confounded by factors affecting the observation process. We modeled whether a species i drawn from the augmented data set occurred in our avian community: wi ~ Bernoulli (Ω); whether this species occurred at site j: zi,j ~ Bernoulli (wi × Ψi,j); and whether it was detected in survey k: yi,j,k ~ Bernoulli (zi,j × pi,j,k). Covariates on occupancy (Ψ) and detection probability (P) were modeled via logistic regression. Hyperparameters were placed on all covariates. Data augmentation consisted of 90 additional unnamed species (30 for each migratory guild) added to the detection history (y) used in the models. The occurrence state (w) of species at sites in the augmented data was linked to the occurrence state (z) of observed species governed by the parameter Ω. We fit a single MSOM including covariates representing our a priori beliefs about the important factors likely to affect occupancy and detection probabilities of birds along the PCT in northern California. To address differences in the phenology of vocal behaviors that could vary by species and affect detectability (McClure et al. 2011, Furnas and Callas 2015), we included survey start date and its quadratic term in the detection component model. The inclusion of the survey date covariate was also important to assure that any findings about the effects of daily temperature on detection probability were not confounded by seasonal changes in vocal activity. Based on the findings of v www.esajournals.org
Furnas and Callas (2015), the detection component included an intercept representing either one of the three recorder survey times (30 min before sunrise, sunrise, 30 min after sunrise) or a point count. We included a covariate on detection probability to address potential differences among the two point count surveyors. This was not necessary for the automated recordings which were reviewed by a single individual. We addressed remaining potential autocorrelation among sites and survey occasions through inclusion of a covariate on detection probability calculated as the total number of species detected in a 5-min survey. Finally, after controlling for the factors mentioned above, we evaluated the effect of temperature on vocal behavior, and how this varied by migratory guild, by including daily maximum temperature as a covariate on detection probability. Whether song or other calls, most of the birds we modeled are more active vocally during the breeding season as males seek to attract mates and defend territories (Catchpole and Slater 2008). We assumed that detection probably in our data was a direct measure of vocal activity at each site. We believe this is a reasonable because the vast majority of detections were based on the aural identification of birds. All of the detections based on interpreting the recordings were aural. For point counts in the field, observers indicated whether each detection was aural only, both aural and visual, or visual only. After combining the recorder and point counts data (n = 7318 detections), 93% of the detections were aural only, 6% were both aural and visual, and just 1% were visual only. As hypothesized earlier, we expected occupancy to vary with elevation. We also expected differences in canopy cover to reflect variation in habitat and to be associated with differences in bird species composition (Beedy 1981, Siegel and Desante 2003, Furnas and Callas 2015). To address spatial differences in species occurrences, we included elevation, tree canopy cover, and their quadratic terms in the occupancy component of the model. The inclusion of hyperparameters and quadratic terms in the model allowed the shapes of these associations (positive or negative slope vs. unimodal) to vary by species. We extracted elevations at each site from the National Elevation Dataset (10-m resolution; U.S. Geological Survey, http://ned.usgs.gov). Average canopy cover within a 200-m radius surrounding each survey site was 5
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calculated in ArcGIS using data representing vertically projected percent cover of the live tree canopy layer for 30-m grid cells (Toney et al. 2009). To the address potential effect of seasonality on occupancy due to seasonal variation in abundance and behavior, we included survey date as a covariate in the occupancy component of the model. The inclusion of this covariate was important to assure that any findings about the effects of elevation on species richness by migratory guild were not confounded by seasonal changes in occupancy. Posterior distributions of derived quantities can be readily computed in Bayesian models. We computed average occupancies of species within subsets of sites representing low ( 1900 m) elevations. These breakpoints were somewhat arbitrary corresponding to a desire to maintain balanced sample sizes among elevation zones, but they generally correspond to differences between low-elevation foothill-transitional forests, middle-elevation mixed-conifer forests, and high-elevation red fir and subalpine forests (Mayer and Laudenslayer 1988). As the MSOM can pull estimates of rarely detected species toward the community mean through “shrinkage” (Link et al. 2002), we focused on reporting species-specific occupancies > 0.2 for species that occurred at > 10% of sites surveyed within an elevation zone because these species had enough data for us to consider their estimates robust. We also calculated gamma diversity (total number of species) and the expected alpha diversity (average number of species at a site) in each elevation zone. Finally, we computed site-level partial species richness values within each migratory guild (i.e., total number of species from a guild that occur at each site). After fitting the model, we used ordinary least squares regression to illustrate associations between elevation and the richness of species in migratory guilds. This was necessary as an additional step because covariates in the MSOM were on occupancy not species richness. We also estimated the elevation at which richness for the three guilds was most similar (the elevation at which the SD of the predicted regression values for the guilds was minimized). We report 90% credible and confidence intervals following recommendations for avian monitoring programs (Bart et al. 2004). The MSOM was solved through a Markov chain Monte Carlo (MCMC) algorithm (Link et al. v www.esajournals.org
2002) implemented in WinBUGS (version 1.4; www.mrc-bsu.cam.ac.uk/bugs) accessed via R statistical software (version 3.1.3; www.r-project. org) with the R2WinBUGS package (Sturtz et al. 2005). Uninformative priors were assumed for all parameters. Three independent chains each of 10,000 samples were run with a burn-in period of 5000 and a thinning rate of three. Effective mixing of these chains was assessed visually and by means of the Gelman–Rubin convergence statistic ( 10% of survey sites in at least one of the three elevation zones and had estimated occupancies > 0.2. We considered these species to represent the common birds in each elevation zone (Table 1). Average site-level species richness (alpha diversity) was 13.5 (90% CI: 13.1–14.0) compared to a naïve value of 7.4 based on a simple tally of species without consideration of detection probability. Correlations between site-level partial richness and elevation differed by migratory guild (Fig. 2). We found that richness decreased with increasing elevation for residents and Neotropical migrants, whereas it increased with increasing elevation for altitudinal migrants. Richness among the three guilds was most similar at 1240 m. These species richness findings complement the results from our examination of species composition and dominance (Ψ > 0.6) across the three elevation zones (Fig. 3). At lower elevations ( 1900 m), altitudinal migrants were dominant. Black- headed grosbeak (Pheucticus melanocephalus) and western tanager (Piranga ludoviciana) are examples of Neotropical migrants that were dominant at lower elevations, whereas red-breasted nuthatch (Sitta canadensis) and dark-eyed junco 6
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McGRANN AND FURNAS Table 1. Common birds surveyed along the along the Pacific Crest Trail in northern California (ΨMSOM† > 0.2 and Ψ naïve > 0.1). AOU code‡
MOUQ NOFL OSFL WEWP DUFL PSFL CAVI HUVI STJA CLNU MOCH CBCH BUSH RBNU BRCR GCKI TOSO HETH AMRO NAWA YRWA BTYW HEWA MGWA GTTO SPTO FOSP DEJU BHGR BHCO CAFI PISI LEGO EVGR LAZB WETA
Common name§
Scientific name§
Guild membership¶
Total sites where detected
Mountain Quail Northern Flicker Olive-sided Flycatcher Western Wood-Pewee Dusky Flycatcher Pacific-slope Flycatcher Cassin’s Vireo Hutton’s Vireo Steller’s Jay Clark’s Nutcracker Mountain Chickadee Chestnut-backed Chickadee Bushtit Red-breasted Nuthatch Brown Creeper Golden-crowned Kinglet Townsend’s Solitaire Hermit Thrush American Robin Nashville Warbler Yellow-rumped Warbler Black-throated Gray Warbler Hermit Warbler MacGillivray’s Warbler Green-tailed Towhee Spotted Towhee Fox Sparrow Dark-eyed Junco Black-headed Grosbeak Brown-headed Cowbird Cassin’s Finch Pine Siskin Lesser Goldfinch Evening Grosbeak Lazuli Bunting Western Tanager
Oreortyx pictus Colaptes auratus Contopus cooperi Contopus sordidulus Empidonax oberholseri Empidonax difficilis Vireo cassinii Vireo huttoni Cyanocitta stelleri Nucifraga columbiana Poecile gambeli Poecile rufescens Psaltriparus minimus Sitta canadensis Certhia americana Regulus satrapa Myadestes townsendi Catharus guttatus Turdus migratorius Oreothlypis ruficapilla Setophaga coronata Setophaga nigrescens Setophaga occidentalis Geothlypis tolmiei Pipilo chlorurus Pipilo maculatus Passerella iliaca Junco hyemalis Pheucticus melanocephalus Molothrus ater Haemorhous cassinii Spinus pinus Spinus psaltria Coccothraustes vespertinus Passerina amoena Piranga ludoviciana
A R N N N N N R R R R R R A R A A A A N A N N N N A A A N A A A A A N N
64 63 32 36 135 15 37 14 130 16 167 18 12 199 58 75 66 68 96 71 206 33 50 29 94 65 97 204 83 18 48 53 12 39 40 111
† Birds shown here are those for which we had sufficient data to report robust species-specific results. Our threshold for this determination was species with modeled occupancies (Ψ) > 0.2 and naive frequencies of sites at which a species was detected > 0.1. ‡ Four-letter codes as defined by the Institute for Bird Populations based on nomenclature in the 56th Supplement to the American Ornithologists’ Union Check-list of North American Birds. § Nomenclature and taxonomy according to the 56th Supplement to the American Ornithologists’ Union Check-list of North American Birds. ¶ R = resident; A = altitudinal migrant; N = Neotropical migrant.
(Junco hyemalis) are altitudinal migrants that were dominant at higher elevations. Mountain chickadee (Poecile gambeli) and Steller’s jay (Cyanocitta stelleri) are examples of resident species that were dominant in middle and/or high elevations notwithstanding the general pattern of increased occurrence at lower elevations for species within v www.esajournals.org
this guild. Although alpha diversity varied little by elevation, gamma diversity was greatest at middle elevations (1200–1900 m) and then dropped by 40% at higher elevations. Although detection probability varied by species, survey method, observer, date, time of day, and forest density, the average detection 7
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Fig. 2. Elevational trends in site-level species richness for (A) residents, (B) altitudinal migrants, and (C) Neotropical migrants along the Pacific Crest Trail in northern California, USA. Points represent the occupancy model predicted values of partial species richness within migratory guilds at each bird survey site. Lines represent patterns of fit (and 90% confidence intervals) from ordinary least squares regression of the model predicted values. The latter step was necessary because we modeled covariate associations with occupancy not species richness.
probability for a single 5-min survey was 0.182 (SD = 0.082). Associations between detection probability and maximum daily temperature varied by migratory guild, even after controlling for the start date of surveys (Fig. 4). For Neotropical migrants, we did not find evidence of a temperature effect (credible intervals overlapped zero). In contrast, the odds of detection of residents v www.esajournals.org
and altitudinal migrants, if present, declined as temperature increased, with residents showing a sharper decline than altitudinal migrants. For every increase of 1°C daily maximum temperature, the average odds of detecting a resident species declined by 3.7% vs. 1.9% for altitudinal migrants. Complete model results are provided in Table 2 and as Supporting Information (Data S1). 8
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Fig. 3. Estimates of average occupancy of birds along the Pacific Crest Trail in northern California, USA. Results are shown separately for (A) lower elevations, (B) middle elevations, and (C) higher elevations for all species with naïve frequencies of detection > 10% of survey sites in a zone and estimated occupancies > 0.2. Average site-level species richness (α) and total species richness (γ) for each elevation zones are also included. We highlight the dominant species (occupancy > 0.6) in each elevation zone. See Table 1 for details of the American Ornithologists’ Union species codes used.
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continental-scale divergence in abundance patterns along latitudinal gradients between migrants and resident species and have suggested additional ecological mechanisms (O’Connor 1990, Mönkkönen and Forsman 2005), including the competitive interactions between resident and migrant species for food resources and nest sites, the differences in the metabolic requirements of residents and migrants, and the differences in reproductive strategies of residents (K-selected) and migrants (r-selected). The richness patterns observed in this study, along an altitudinal gradient, are potentially driven by a combination of all these mechanisms and require further study to disentangle. The abrupt decline in richness that we observed for Neotropical migrants across high-elevation sites suggests that fewer species are able to tolerate the colder temperatures, lower productivity, and shorter breeding season of subalpine habitats Fig. 4. Change in odds of detection probability for (McCain 2009). In contrast, altitudinal migrants every 1°C increase in daily maximum temperature for attained maximum richness in these same habitats. residents, altitudinal migrants, and Neotropical migr Many of these birds may prefer to breed in habitats ants. See “Daily maximum temperature” parameters in where there is reduced competition with residents and Neotropical migrants and where there are Table 2. reduced rates of nest predation (O’Connor 1990). Residents and Neotropical migrants were most Discussion diverse at low- to mid-elevation sites, where winter temperatures are warmer, where the breeding Our results show that groups of migratory and season is longer, and where habitats are generally nonmigratory birds partitioned their use of dif- more productive. Neotropical migrants, in particferent elevational zones in northern California ular, may select these habitats to meet the energetic summer range habitats. We also demonstrated demands of breeding and to build fat reserves differences in how these groups adjusted their for the return trip to wintering grounds (Bairlein vocal activity in response to higher temperatures. 1990). Taken in context with previous research, our Evolutionary history, including adaptations findings suggest that as global temperature rises from past climate and past species interactions, there may be greater competition among birds likely influenced the present-day richness patterns previously separated by elevation and that and species distributions that we observed along Neotropical migrants may be at greater risk of the PCT. This richness–elevation structure has heat stress during the breeding season. the potential to be disrupted by the rapid climate We found divergent elevational trends in rich- change forecasted for California; temperatures ness for each of the three migratory guilds— are expected to increase by 2°C to 5°C throughout residents, altitudinal migrants, and Neotropical the state by the end of the 21st century (Snyder migrants—across the mountain ranges of northern et al. 2002, Cayan et al. 2012). In response, many California on the PCT (Fig. 2). Many underlying species may independently adjust their range mechanisms potentially drive species diversity margins (Tingley et al. 2012) and this reshuffling patterns on mountains, including species inter- of species distributions into new assemblages actions, habitat complexity, evolutionary history, could create novel species interactions. As a conclimate, and energy-related factors, such as pro- sequence, species interactions may arise that do ductivity and temperature (McCain 2009, Sanders not occur today, or did not occur in more recent and Rahbek 2012). Other studies have observed evolutionary history. Many montane species may v www.esajournals.org
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McGRANN AND FURNAS Table 2. Multispecies occupancy model results. Group mean† Parameter
Resident
Altitudinal
Neotropical
*−4.540 *−2.986 *−2.627 *−2.186 *−0.321 *0.756 0.053 −0.063 *−0.227
*−2.064 *−1.774 *−1.821 *−1.851 −0.107 *0.853 *0.306 −0.012 −0.115
*−1.508 *−0.967 *−1.029 *−0.777 −0.052 *0.724 *−0.333 *−0.564 0.085
*−7.723 *−0.840 −0.378 −0.580 *−0.764 *−0.812
*−4.694 0.513 *−0.474 −0.316 *−0.242 *−0.550
*−4.806 *−1.155 *−0.743 −0.210 *−0.403 −0.302
*0.872
*0.709
*0.671
Detection Model Parameters Automated recorder before sunrise (intercept) Automated recorder at sunrise (intercept) Automated recorder after sunrise (intercept) Point count (intercept) Point count (difference of second surveyor) Total number of species detected in 5-min survey‡ Start date Start date2 Daily maximum temperature Occupancy Model Parameters Intercept Elevation Elevation2 Tree canopy cover Tree canopy cover2 Start date Data Augmentation Proportion of species predicted to occur
Notes: Data are from bird surveys along the Pacific Crest Trail in northern California, USA. Survey methods included point counts and the use of automated recorders. † Model hyperparameters were fit as random effects centered on separate means for each migratory guild and covariate data were standardized. The symbol * represents nonzero effects based on the 90% credible interval (Bayesian P value). ‡ This autocovariate was included to address residual heterogeneity in detection probability not addressed by other covariates in the model.
the rate of evaporative water loss (Ward et al. 2003, Ward and Slater 2005). Residents and altitudinal migrants complete their life cycles entirely within the same temperate climate region and have evolved adaptive behaviors for the highly variable weather occurring in these regions throughout the year (Rubolini et al. 2010). In contrast, our results showed for Neotropical migrants no relationship in behavior with temperature. These species complete their life cycles in both temperate and tropical climates and therefore must adapt to the conditions found in wintering areas, breeding areas, and in transit. Thus, Neotropical migrants may be limited in their evolutionary response to environmental change on breeding territories because there is strong selection for the maintenance of migratory traits over traits that are adaptive to local conditions (Pulido and Widmer 2005). Migrants must complete their breeding cycles and store up fat reserves in the brief period between the completion of the breeding season and the fall migration (Bairlein 1990). Our results also support findings from Europe, including an analysis of a long-term data set (1977–2006) on the singing activity patterns of
suffer rapid declines or extinction because adaptations to these newly formed competitive interactions will be slow to evolve (Stralberg et al. 2009). An important future research direction, therefore, is to understand how species interactions and climate have caused the present partitioning of the elevation gradient among migratory guilds and to further investigate the potential for future and novel competitive interactions. Our observations were consistent with the hypothesis that residents and altitudinal migrants exhibit greater plasticity in vocal behavior than Neotropical migrants when responding to daily variation in temperature (Fig. 4). Although the intensity and frequency of vocal displays are mainly controlled internally by the production of testosterone, which is triggered by changes in day length (Catchpole and Slater 2008), birds can also make daily adjustments in vocal behavior in response to local weather conditions (Garson and Hunter 1979, Strain and Mumme 1988). We found that residents and altitudinal migrants reduced vocal activity as daily maximum temperatures increased. These reductions in vocal activity may serve to lower energy expenditure by reducing v www.esajournals.org
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birds throughout northern Germany (Rubolini et al. 2010). Temperatures increased throughout the region during this period and residents advanced their first singing date more than sub- Saharan migrants. Thus, it appears that there is some commonality in the pattern, across different temporal and spatial scales, with our findings for northern California. If this lack of plasticity is indeed a general pattern for long-distance migrants, then it presents significant conservation concerns, including potential mismatches in the timing of breading events with peak abundances of food resources (Both et al. 2006, Møller et al. 2008) and the increase in the physiological stress of completing reproduction in hotter ambient temperatures (Dunn and Winkler 2010). Although our results demonstrate divergence in the distribution and behavior of birds in montane environments, we also found some patterns of convergence. Gamma diversity and the overlap of migratory and resident species were greatest in middle-elevation forests (Fig. 3). Interestingly, these findings are consistent with those of Tingley and Beissinger (2013) who found that turnover of avian species over the past 100 yr has been greatest at the lowest and highest elevations in California forests, but that species from middle elevations were not expanding their ranges to fill these gaps. Middle-elevation forests in California are generally characterized by higher productivity and a more mixed tree species composition than forests at lower or higher elevations (Schoenherr 1992). Variable geology and frequent fire promote complex structure in these forests. However, fire suppression and the logging of large-diameter trees over the past century have reduced some of this complexity (Stephens et al. 2009, McIntyre et al. 2015). Nevertheless, avian diversity is still high in mixed-conifer forests due to niche partitioning of foraging habitats (Beedy 1981). For these reasons, the conservation and restoration of structurally complex, middle-elevation, montane, mixed- conifer forests is likely to provide birds a critical refugium in California.
Conclusions To our knowledge, this study represents the first comparison of elevational species richness and vocal activity patterns between migratory guilds of a montane bird community. We further v www.esajournals.org
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accounted for heterogeneity in detection probability that could bias results if not addressed (Iknayan et al. 2014). In our case, occupancy modeling nearly doubled our estimate of average site-level species richness (alpha diversity). Furthermore, we approached detectability as more than a nuisance variable in occupancy estimation by using it as a measure of vocal behavior that we expected would be affected by temperature. Montane bird communities have already experienced declines in richness over the past century of human land use and climate change (Tingley and Beissinger 2013). Predictions of the future community response will be crucial in making adaptive conservation decisions, and our results suggest that such predictions must take into account the heterogeneity in richness patterns and the behavioral responses to temperature among species employing different migration strategies. This potential for climate-induced change in the bird community and breeding phenology highlights the complexity of interacting mechanisms (species interactions, climate, habitat, and evolution) and the need to closely monitor population and diversity trends into the future.
Acknowledgments We thank R. Landers, who assisted with fieldwork, and A. McGrann, who provided logistical support in the field. J. Thorne and two anonymous reviewers provided useful comments on earlier versions of the manuscript. The California Department of Fish and Wildlife and the U.S. Fish and Wildlife Service jointly funded this research through State Wildlife Grants F08AF00126 and F12AF00829.
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Supporting Information Additional Supporting Information may be found online at: http://onlinelibrary.wiley.com/doi/10.1002/ ecs2.1419/supinfo
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