183

Physiological Evidence That Anthropogenic Woodlots Can Substitute for Native Riparian Woodlands as Stopover Habitat for Migrant Birds* Ming Liu† David L. Swanson Department of Biology, University of South Dakota, Vermillion, South Dakota 57069

woodlots can, at least partially, substitute as stopover habitat for lost and degraded native riparian habitats for woodland birds.

Accepted 5/26/2013; Electronically Published 8/7/2013 Introduction ABSTRACT The ability to find sufficient high-quality stopover habitat is a crucial factor for successful migration for woodland migrant birds. Woodland habitats are scarce in the Northern Prairie region of North America, and natural woodlands have been greatly reduced concurrent with the appearance of small anthropogenic woodlands on the landscape. Landbird migrants use both natural and anthropogenic woodlands in this region as stopover habitats, but the relative quality of these two habitats is unknown. We assessed the relative habitat quality of the two habitats by comparing body mass (Mb) and plasma metabolites associated with fattening (triglycerides [TRIG]) or fat catabolism (b-hydroxybutyrate [BUTY], glycerol [GLYC]) in individual species, taxa, and foraging guilds of migrating woodland birds during both spring and fall migrations. The only significant difference in Mb between birds in the two habitats occurred for fall yellow-rumped warblers (Setophaga coronata), where Mb was 8% greater in corridors than in woodlots. No significant between-habitat differences occurred for plasma TRIG at either season. Significant between-habitat differences for plasma BUTY occurred only for ruby-crowned kinglets (Regulus calendula; 61% higher in corridors) in fall. Plasma GLYC differed significantly between habitats for a few groups, including vireos (190% higher in woodlots), warbling vireos (Vireo gilvus; 263% higher in woodlots), and Nashville warblers (Oreothlypis ruficapilla; 226% higher in woodlots) in fall. The few significant differences and absence of a consistent direction of variation in Mb and plasma metabolites suggests similar stopover habitat quality in these two habitat types. Thus, during migration through the Northern Prairie region anthropogenic * This paper was submitted in response to a call for papers for a Focused Issue on “Conservation Physiology.” † Corresponding author; e-mail: [email protected].

Physiological and Biochemical Zoology 87(1):183–195. 2014. 䉷 2013 by The University of Chicago. All rights reserved. 1522-2152/2014/8701-2145$15.00. DOI: 10.1086/671746

Woodland migrant birds are typically unable to complete migration in a single flight between breeding and wintering grounds. They need to stop over to refuel, as fat stores will be used as energy for the subsequent migratory flight (Zwarts et al. 1990; Moore et al. 1995; Smith and Moore 2003; Newton 2006). Consequently, stopover habitat quality may play a significant role in the population dynamics of migratory woodland birds (Rich et al. 2004; Berlanga et al. 2010; Faaborg et al. 2010a, 2010b). Land use changes and habitat alterations on breeding or wintering grounds can influence populations of woodland migrants, and the effects of such changes have received considerable research attention. Populations of woodland migrants may also be impacted by changes to available stopover habitat along the migratory route (e.g., Moore et al. 1995; Faaborg 2002; Mehlman et al. 2005; Packett and Dunning 2009; Faaborg et al. 2010a, 2010b). Unpredictable conditions encountered en route may result in migrants arriving at breeding or wintering grounds too late to obtain higher-quality resources (Moore et al. 1995). Climate change may exacerbate these unpredictable conditions and lead to mismatches in migratory timing and peak resource availability (Møller et al. 2008; Both et al. 2010). In addition, mortality during migration may be substantial, amounting to up to 85% of annual mortality (Sillett and Holmes 2002). Woodland habitats are scarce in the Northern Prairie region, amounting to less than 5% of total land cover, and historically consisted principally of riparian forests following river corridors (Castonguay 1982; Van Bruggen 1996). Such native riparian woodland habitats harbor the greatest abundance and diversity of bird species of any habitat in this region (Stauffer and Best 1980; Best et al. 1995; Peterson 1995; Bakker 2003). These native woodlands have been greatly reduced and degraded since the time of Euro-American settlement, thereby reducing available habitat for woodland birds for both breeding and migration (Johnson et al. 1976; Hesse 1996; Dixon et al. 2012). In addition, along the Missouri River, which forms the largest riparian corridor in this region, woodland composition has changed toward older successional stages with the completion

184 M. Liu and D. L. Swanson

Figure 1. Study sites in Clay County, South Dakota. The middle map shows the locations of study sites. Filled stars are the locations of corridor study sites, and open stars are the locations of woodlot study sites. The side aerial maps were generated with same scale. Asterisks on each study site represent the mist net locations. Study site areas: CO1 p 1.01 km2, CO2 p 1.59 km2, CO3 p 1.50 km2, WO1 p 0.17 km2, WO2 p 0.17 km2, WO3 p 0.20 km2. CO p corridors, WO p woodlots, Missouri p Missouri River. A color version of this figure is available online.

of dams in the 1950s and 1960s and the subsequent reduction in flooding events, and this has impacted the avian community (Hesse 1996; Swanson 1999; Dixon et al. 2012). However, simultaneous with this reduction in native riparian woodland habitats has been the appearance of anthropogenic woodland habitats, namely shelterbelts (narrow, linear woodland strips) and woodlots (larger, less linear woodlands typically planted around farmsteads; Bakker 2003; Swanson et al. 2005). Both natural and anthropogenic woodlands are used by migrating and breeding birds in the Northern Prairie region (Martin 1980; Dean 1999; Swanson et al. 2003, 2005; Gentry et al. 2006). Indeed, the abundance and species richness of woodland Neotropical migrant birds are similar between the two habitat types in this region (Skagen et al. 1998; Swanson et al. 2005; Packett and Dunning 2009). The similar abundance and species richness of migrants between the two habitats suggests that woodlots might, at least partially, substitute for lost and degraded corridor habitats in terms of providing suitable stopover habitat during migration. However, the simple presence of migrating birds does not distinguish whether these two habitats

provide similarly suitable stopover habitat for meeting the energetic demands of migration (Swanson et al. 2005; Cerasale and Guglielmo 2010). Rates of fat deposition during stopover depend on the quantity and quality of food intake (Schaub and Jenni 2001; Bairlein 2002). If habitat quality differences occur between stopover habitats, this can be detected through the measurement of several plasma metabolites (Jenni-Eiermann and Jenni 1994; Williams et al. 1999; Schaub and Jenni 2001; Guglielmo et al. 2002, 2005; Cerasale and Guglielmo 2006). Because some metabolites increase during fat deposition, such as plasma triglycerides (TRIG), whereas others increase during fat catabolism, such as plasma b-hydroxybutyrate (BUTY), these metabolites provide an instantaneous integrated measure of physiological state with regard to the bird’s refueling condition just before capture (Ramenofsky 1990; Jenni and Jenni-Eiermann 1992; Jenni-Eiermann and Jenni 1994; Landys et al. 2005; Cerasale and Guglielmo 2006). These measures are now routinely used to measure fattening rates of birds during migration (Schaub and Jenni 2001; Seaman et al. 2005; Cerasale and Guglielmo 2006, 2010).

Plasma Metabolites and Habitat Quality 185 Table 1: Foraging guild and taxon classification of migratory landbird species at our study sites Season Guild, taxa FGG VIR

WAR

GFG

THR

SPA

FLY

Spring

Fall Ruby-crowned kinglet (Regulus calendula) Bell’s vireo (Vireo bellii) Blue-headed vireo (Vireo solitarius) Red-eyed vireo (Vireo olivaceus) Warbling vireo (Vireo gilvus) Orange-crowned warbler (Oreothlypis celata) Nashville warbler (Oreothlypis ruficapilla) Magnolia warbler (Setophaga magnolia) Yellow-rumped warbler (Setophaga coronata) Black-and-white warbler (Mniotilta varia) Yellow warbler (Setophaga petechial) Morning warbler (Geothlypis philadelphia) Wilson’s warbler (Cardellina pusilla) Common yellowthroat (Geothlypis trichas) American redstart (Setophaga ruticilla) Gray catbird (Dumetella carolinensis) Ovenbird (Seiurus aurocapilla) Northern waterthrush (Parkesia noveboracensis) Indigo bunting (Passerina cyanea) Swainson’s thrush (Catharus ustulatus) Hermit thrush (Catharus guttatus)

Bell’s vireo (Vireo bellii) Red-eyed vireo (Vireo olivaceus) Warbling vireo (Vireo gilvus) Tennessee warbler (Oreothlypis peregrina) Orange-crowned warbler (Oreothlypis celata) Chestnut-sided warbler (Setophaga pensylvanica) Yellow-rumped warbler (Setophaga coronata) Black-and-white warbler (Mniotilta varia) Blackpoll warbler (Setohphaga striata) Yellow warbler (Setophaga petechia) Mourning warbler (Geothlypis philadelphia) Wilson’s warbler (Cardellina pusilla) Common yellowthroat (Geothlypis trichas) Gray catbird (Dumetella carolinensis) Ovenbird (Seiurus aurocapilla) Nothern waterthrush (Parkesia noveboracensis) Indigo bunting (Passerina cyanea) Gray-cheeked thrush (Catharus minumus) Swainson’s thrush (Catharus ustulatus) Hermit thrush (Catharus guttatus) Lincoln’s sparrow (Melospiza lincolnii) Harris’s sparrow (Zonotrichia querula) White-throated sparrow (Zonotrichia albicollis) Least flycatcher (Empidonax minimus) Traill’s flycatcher (Empidonax alnorum and traillii) Yellow-bellied flycatcher (Empidonax flaviventris)

Lincoln’s sparrow (Melospiza lincolnii) Harris’s sparrow (Zonotrichia querula) White-throated sparrow (Zonotrichia albicollis) Dark-eyed junco (Junco hyemalis) Least flycatcher (Empidonax minimus) Traill’s flycatcher (Empidonax alnorum and traillii)

Note. FGG p foliage-gleaning guild, GFG p ground-foraging guild, VIR p vireos, WAR p warblers, THR p thrushes, SPA p sparrows, FLY p flycatchers.

Plasma glycerol (GLYC) levels have also been used as an indicator of fat catabolism in birds (Jenni-Eiermann and Jenni 1991; Williams et al. 1999; Guglielmo et al. 2002), but they might be a less effective metric of refueling performance because levels may increase during high rates of both fat deposition and catabolism, producing a nonlinear U-shaped relationship with plasma TRIG levels (Guglielmo et al. 2005). Plasma metabolite profiling can be used to distinguish quality differences between stopover sites (Guglielmo et at. 2002, 2005; Seewagen et al. 2011). In this study, we assessed the relative habitat quality of natural riparian corridor woodlands and anthropogenic woodlots by comparing plasma metabolites associated with fattening (TRIG) or fat catabolism (BUTY, GLYC) in migrating woodland birds collected in southeastern South Dakota. We hypothesized that there would be higher levels of TRIG and lower levels of GLYC and BUTY (suggestive of higher habitat quality) in migrants from native riparian corridor woodlands because of their relatively larger size, more continuous nature, and higher vegetative di-

versity than woodlots (Swanson et al. 2003, 2005). Alternatively, if habitat quality is similar between natural riparian corridor woodlands and anthropogenic woodlots, then we would not expect to see a difference in plasma metabolite levels between birds in the two habitats. These data allow us to address the question of whether woodlots can substitute for lost and degraded native riparian corridor woodlands in meeting the energetic demands of migration for woodland migrant birds. Material and Methods Study Sites The Missouri River provides the largest riparian corridor in our study area, and the canopy of riparian woodlands at Missouri River study sites is mostly dominated by cottonwoods (Populus deltoides), with some later successional trees present, including green ash (Fraxinus pennsylvanica), elm (Ulmus spp.), and hackberry (Celtis occidentalis), among other tree species (Hesse 1996; Dixon et al. 2012). Understory shrub species at

14.1 Ⳳ .3 (13) 12.3 Ⳳ .3 (21) 36.7 Ⳳ .6 (28) 10.4 Ⳳ .4 (6) 13.0 Ⳳ .4 (11) 11.3 Ⳳ .3 (10)

14.6 Ⳳ .3 (27) 11.5 Ⳳ .3 (20)

35.9 Ⳳ .8 (22) 10.3 Ⳳ .2 (12)

14.8 Ⳳ .9 (5) 10.5 Ⳳ .3 (12)

TRFL LEFL WAVI RCKI SWTH OCWA NAWA MYWA YWAR 9.2 8.2 12.6 11.0

Ⳳ Ⳳ Ⳳ Ⳳ .1 .1 .2 .4

(32) (18) (28) (6)

13.8 Ⳳ .6 (6) 12.9 (1) 14.8 Ⳳ .2 (85) 6.3 Ⳳ .2 (13)

CO

8.9 8.3 11.7 10.2

13.7 10.5 14.6 6.3 Ⳳ Ⳳ Ⳳ Ⳳ

Ⳳ Ⳳ Ⳳ Ⳳ .1 .1 .2 .6

.5 .3 .4 .2

WO

(46) (30) (26) (6)

(9) (12) (19) (20) 9.1 Ⳳ .5 (13) 8.2 Ⳳ .1 (15) 11.9 Ⳳ .3 (7)

14.8 Ⳳ .2 (62)

CO

HY

Fall

9.1 Ⳳ .7 (23) 8.1 Ⳳ .1 (10) 11.8 Ⳳ .2 (16)

14.4 Ⳳ .4 (7)

WO

9.5 Ⳳ .3 (8) 8.2 Ⳳ .2 (3)

15.6 Ⳳ .6 (8)

CO

AHY

8.7 Ⳳ .2 (13) 7.9 Ⳳ .1 (5) 11.7 Ⳳ .3 (6)

15.0 Ⳳ .9 (2)

WO

Note. Significant differences are indicated by boldface type. CO p corridor, WO p woodlot, HY p hatch year, AHY p after hatch year, TRFL p complex of Empidonax alnorum and traillii, LEFL p least flycatcher (Empidonax minimus), WAVI p warbling vireo (Vireo gilvus), RCKI p ruby-crowned kinglet (Regulus calendula), SWTH p Swainson’s thrush (Catharus ustulatus), OCWA p orange-crowned warbler (Oreothlypis celata), NAWA p Nashville warbler (Oreothlypis ruficapilla), MYWA p yellow-rumped warbler (Setophaga coronata), YWAR p yellow warbler (Setophaga petechia).

WO

CO

Species

Spring

Table 2: Mean (ⳲSE) body mass (g) and sample sizes (in parentheses) of individual species by stopover habitat and age (fall only)

Plasma Metabolites and Habitat Quality 187 are scattered, isolated, and small (mostly less than 3 ha in area), rather than linear and relatively continuous like riparian woodlands, with woodlands usually in rectangular or L shapes (Swanson et al. 2003). Anthropogenic woodlands provide about 1% of the total landscape area in eastern South Dakota (Martin 1980; Castonguay 1982). The canopy of anthropogenic woodlot study sites were composed primarily of elm, mulberry (Morus alba), box elder (Acer negundo), hackberry, and green ash, with the understory sparser than at riparian sites and composed primarily of young canopy tree species (Swanson et al. 2003; Gentry et al. 2006). We sampled three representative study sites from both riparian corridor woodlands along the Missouri River (hereafter, “corridors”) and farmstead woodlot (hereafter, “woodlots”) habitat types in Clay County in southeastern South Dakota (fig. 1). We chose study sites from those sampled previously by Dean (1999), Swanson et al. (2003, 2005), and Gentry et al. (2006). Woodlot and corridor study sites were separated by at least 9.5 km. Blood Sample Collection Migrant birds were captured with 9-m, 36-mesh nylon mist nets. Each of the six study sites was sampled once per week, rotating through the sites with woodlot and corridor sites sampled on alternating days during spring (mid-April to early June 2010–2012) and fall (mid-August to mid-October 2010–2011) migration periods. Mist nets were operated for a few hours beginning at sunrise until noon under neutral weather conditions—no rain and relatively low wind speed (!40 km/h). We monitored nets continuously and removed birds from nets immediately after capture. Blood samples of 20–50 mL (depending on body mass; Voss et al. 2010) were obtained within 3 min of capture via venipuncture from the brachial vein on the underside of the wing with heparinized capillary tubes. After collection, blood samples were transferred into microcentrifuge tubes and stored on ice while in the field. On return to the laboratory, blood samples were centrifuged for 10 min at 3,000 g. The plasma was then removed, placed in new microtubes, and immediately stored at ⫺60⬚C until later measurement of plasma metabolites. Bird Banding and Morphological Measurements Figure 2. Least squares means (LSMEANS; ⳲSE) for plasma metabolites (mmol/L) for spring foraging guilds, taxonomic groups, and individual species by stopover habitat type. TRIG p triglycerides, BUTY p b-hydroxybutyrate, GLYC p glycerol, FGG p foliage-gleaning guild, GFG p ground-foraging guild, FLY p flycatchers, THR p thrushes, WAR p warblers, TRFL p complex of Empidonax alnorum and traillii, LEFL p least flycatcher (Empidonax minimus), SWTH p Swainson’s thrush (Catharus ustulatus).

riparian sites included dogwood (Cornus spp.), buckthorn (Rhamnus cathartica), and prickly ash (Zanthozylum americanum), among other species (Hesse 1996; Dean 1999; Gentry et al. 2006). Anthropogenic woodlots in eastern South Dakota

After blood samples were drawn, birds were banded with standard US Fish and Wildlife Service aluminum leg bands and aged (fall only) by skull ossification (Pyle 1997) as AHY (after hatch year) and HY (hatch year). The date and time at capture were recorded. We used a wing rule to measure unflattened wing chord to the nearest 0.5 mm and calipers to measure tarsus length to the nearest 0.1 mm. A portable electronic scale (model LS200; Ohaus, Parsippany, NJ) was used to measure body mass (Mb) to the nearest 0.1 g. Fat stores of each captured bird were measured on a 0–5 scale for both furcular and abdominal deposits (Helms and Drury 1960), after which birds were released. The fat scores were used to determine whether bird species breeding at our study sites were breeders or mi-

188 M. Liu and D. L. Swanson trophotometer. We conducted all assays in 1.5-mL polystyrene UV/Vis semimicro cuvettes (United Laboratory Plastics, St. Louis, MO) in accordance with the manufacturer’s instructions for each kit, using wavelengths of 540 nm for TRIG and GLYC and 405 nm for BUTY. All samples were run in duplicate, and average values were used in subsequent analyses. Plasma TRIG and GLYC were measured using a Sigma TR0100 kit (SigmaAldrich, St. Louis, MO), which is a sequential end point assay. Total plasma GLYC was measured following the measurement of free plasma GLYC, and plasma TRIG was calculated as the difference between the total plasma GLYC and free plasma GLYC. Plasma BUTY was measured with a kinetic assay using Wako Autokit 3-HB (Wako Diagnostics, Richmond, VA). If plasma volume was not sufficient for both TRIG and BUTY measurements, we diluted plasma samples with deionized water before metabolite assays and corrected final plasma metabolite values for dilution. Statistics

Figure 3. Least squares means (LSMEANS; ⳲSE) of plasma metabolites (mmol/L) for fall foraging guilds, taxomomic groups, and individual species by stopover habitat type. Asterisks indicate a significant difference between birds in corridors and woodlots. TRIG p triglycerides, BUTY p b-hydroxybutyrate, GLYC p glycerol, FGG p foliagegleaning guild, GFG p ground-foraging guild, VIR p vireos, WAR p warblers, SPA p sparrows, WAVI p warbling vireo (Vireo gilvus), RCKI p ruby-crowned kinglet (Regulus calendula), OCWA p orangecrowned warbler (Oreothlypis celata), NAWA p Nashville warbler (Oreothlypis ruficapilla), MYWA p yellow-rumped warbler (Setophaga coronata).

grants. We considered breeding bird species to be within the fall migratory period once we captured at least one individual with fat scores of 2 (common in migrants but not observed during the summer season) in both furcular and abdominal regions. Similarly, in spring we considered species to be within the migratory window as long as we continued to capture some individuals with fat scores of 2. Plasma Metabolite Assays Plasma metabolites were measured with commercially available spectrophotometric assay kits using a Beckman DU-7400 spec-

All statistical analyses were performed with SAS (ver. 9.3; SAS Institute, Cary, NC). Plasma metabolites were compared for individual species, taxonomic groups (species grouped by families, except that we excluded ovenbird [Seiurus aurocapilla] and nothern waterthrush [Parkesia noveboracensis] from warbler comparisons because of their different foraging habits), and foraging guilds (Simberloff and Dayan 1991; Martin and Finch 1995; table 1) with sample sizes 110 individuals in each habitat. Data were log10 transformed before analyses to meet normality and equal variance assumptions if the original data did not fit the assumptions. To adjust for individual differences in body size, principal components analysis (PCA) was used to incorporate structural measurements (wing and tarsus length) to produce a principal component describing body size (PCA1; Pedhazur 1997; Guglielmo et al. 2005; Seewagen et al. 2011). We used a backward stepwise multiple regression approach to generate predictors, with each metabolite as the dependent variable. Independent variables in the model included capture time, day of the year, year, and body size, with variables retained in the model at P ! 0.10 (Guglielmo et al. 2005; Thomas 2008). The variables retained after multiple regression were included as covariates in an ANCOVA to obtain least squares means to test for differences between habitat types and seasons. To control for possible individual species effects on plasma metabolite levels in analyses of foraging guilds and taxa, we included species and habitat type or season as categorical variables, along with species-habitat type and species-season interaction terms, in the general linear model ANCOVA. If no covariates were significant in multiple regressions, we tested for differences between birds from different stopover habitat types or seasons by ANOVA. We also applied ANCOVA to compare body size– adjusted Mb for individual species, including PCA1 as a covariate in the model, with habitat and ages (fall only) analyzed separately. Results are presented as means Ⳳ SE. For comparisons of relationships among the different plasma

Plasma Metabolites and Habitat Quality 189 Table 3: Mean (ⳲSE) plasma metabolite concentrations (mmol/L) and sample sizes (in parentheses) of individual species by stopover habitat and age (fall only) HY Species, site WAVI: CO WO OCWA: CO WO NAWA: CO WO MYWA: CO WO

TRIG

BUTY

AHY GLYC

TRIG

BUTY

.99 Ⳳ .05 (60) 1.07 Ⳳ .19 (63) .57 Ⳳ .07 (60) 1.86 Ⳳ .12 (8) 1.00 Ⳳ .19 (7) 1.21 Ⳳ .18 (7) .78 Ⳳ .12 (7) 1.32 Ⳳ .70 (7) 2.11 Ⳳ 1.23 (2) .70 Ⳳ .43 (2)

GLYC .53 Ⳳ .13 (8) .47 Ⳳ .23 (2)

2.01 Ⳳ .30 (13) 1.59 Ⳳ .40 (12) .98 Ⳳ .14 (13) 1.86 Ⳳ .30 (8) 1.82 Ⳳ .15 (23) 2.03 Ⳳ .35 (23) 1.21 Ⳳ .37 (23) .99 Ⳳ .21 (13)

.23 Ⳳ .27 (8) .38 Ⳳ .08 (8) .23 Ⳳ .33 (13) 1.04 Ⳳ .32 (13)

1.19 Ⳳ .23 (15) 1.03 Ⳳ .18 (15) .35 Ⳳ .11 (15) 1.58 Ⳳ .25 (3) 1.04 Ⳳ .24 (10) 1.25 Ⳳ .35 (10) 1.84 Ⳳ .73 (10) 1.59 Ⳳ .35 (5)

.87 Ⳳ .42 (3) .41 Ⳳ .36 (3) 1.77 Ⳳ 1.04 (5) 2.08 Ⳳ 1.50 (5)

.70 Ⳳ .20 (7) 1.30 Ⳳ .77 (7) 1.14 Ⳳ .19 (16) 1.13 Ⳳ .20 (16)

.29 Ⳳ .07 (7) .55 Ⳳ .14 (16) 1.74 Ⳳ .26 (6)

.73 Ⳳ .16 (6)

.76 Ⳳ .63 (6)

Note. Significant differences are indicated by boldface type. CO p corridor, WO p woodlot, HY p hatch year, AHY p after hatch year, TRIG p triglycerides, BUTY p b-hydroxybutyrate, GLYC p glycerol, WAVI p warbling vireo (Vireo gilvus), OCWA p orange-crowned warbler (Oreothlypis celata), NAWA p Nashville warbler (Oreothlypis ruficapilla), MYWA p yellow-rumped warbler (Setophaga coronata).

metabolites, we normalized data for individual birds to species averages (for species with n 1 10 ) so that we could include data from individual birds in our comparisons. To normalize the plasma metabolite data for each individual bird, the individual values for plasma GLYC, TRIG, or BUTY levels were divided by the mean value for that species. These normalized data from individual birds were then used for correlation and nonlinear regression analyses of GLYC versus TRIG and BUTY versus TRIG. Results Body Mass (Mb) No species showed significant differences in body size–adjusted Mb between corridors and woodlots for either spring or fall migration except for yellow-rumped warblers during fall migration. The Mb of fall yellow-rumped warblers from corridors (12.6 Ⳳ 0.2 g) was significantly higher (F1, 52 p 11.22, P ! 0.001) than that from woodlots (11.7 Ⳳ 0.2 g; table 2). For fall juveniles, we obtained sufficient sample sizes for comparisons for only orange-crowned and Nashville warblers, and Mb was statistically similar between habitats for both species. In addition, Mb of orange-crowned warblers (adults and juveniles pooled) during fall migration showed a nonsignificant trend (F1, 75 p 3.30, P p 0.07) toward higher Mb (3% increase) in corridors than in woodlots (table 2). Fat Deposition: TRIG Plasma TRIG concentrations were statistically similar between corridors and woodlots for all foraging guilds, taxa, and individual species in both spring and fall (figs. 2, 3). Plasma TRIG concentrations did not differ significantly between adults and juveniles for warbling vireos and orange-crowned warblers in fall. Within juveniles, fall plasma TRIG concentrations were

also statistically similar for orange-crowned and Nashville warblers in corridors and woodlots (table 3). We did not obtain sufficient sample sizes for between-habitat comparisons of adult birds for any individual species.

Fat Catabolism: BUTY and GLYC Plasma BUTY and GLYC concentrations did not differ significantly between birds in the two stopover habitats for any foraging guild, taxon, or individual species in spring (fig. 2). During fall migration, plasma BUTY concentrations were also similar between habitat types for all bird groups and individual species except ruby-crowned kinglets, which showed significantly higher BUTY (60% increase) in corridors relative to woodlots (F1, 23 p 4.94, P p 0.04; fig. 3). Plasma GLYC concentrations differed significantly between birds in the two habitats only for fall vireos (F1, 126 p 3.89, P p 0.049, 190% higher in woodlots), warbling vireos (F1, 99 p 7.25, P p 0.008, 263% higher in woodlots), and Nashville warblers (F1, 41 p 12.79, P ! 0.001, 226% higher in woodlots; fig. 3). Concentrations of plasma BUTY and GLYC were statistically similar between adults and juveniles for warbling vireos and orange-crowned warblers in fall (table 3). Within juveniles during fall migration, plasma BUTY levels did not differ significantly by stopover habitat for either orange-crowned or Nashville warblers (table 3). A significant between-habitat difference in plasma GLYC occurred for juvenile Nashville warblers (F1, 22 p 12.70, P p 0.002, 426% higher in woodlots; table 3). Significant species effects on plasma metabolite levels within guilds or taxa occurred only for plasma BUTY in the foliagegleaning guild (F14, 329 p 4.70, P ! 0.001), the ground-foraging guild (F9, 101 p 2.93, P ! 0.001), and warblers (F9, 180 p 2.10, P p 0.01) in fall and for plasma GLYC in the ground-foraging guild (F9, 93 p 2.39, P p 0.01) in spring. The interaction be-

190 M. Liu and D. L. Swanson P p 0.002) and nearly significantly so for spring (F1, 255 p 2.80, r p 0.27, P p 0.09; fig. 4). Plasma TRIG and GLYC showed a significant nonlinear U-shaped relationship for spring migrants (y p 0.58 ⫺ 1.71x ⫹ 1.80x 2; F2, 223 p 44.61, r p 0.53, P ! 0.001; fig. 4). Plasma TRIG and GLYC showed significant linear (F1, 481 p 11.17, r p 0.15, P ! 0.001) and nonlinear (y p 0.47 ⫺ 0.72x ⫹ 0.73x 2; F2, 480 p 30.13, r p 0.33, P ! 0.001) relationships for fall migrants, but the nonlinear model fit the data better (fig. 4). Effects of Covariates on Plasma Metabolites The effects of covariates on plasma metabolites showed different relationships for the different metabolites (table 4). We found that capture time was significantly positively associated with plasma TRIG for all bird groups except flycatchers and Traill’s flycatchers in spring and the ground-foraging guild, flycatchers, and yellow-rumped warblers in fall. Capture time was significantly negatively related to plasma BUTY for flycatchers, Traill’s flycatchers, and warblers in spring and for the foliage-gleaning guild, warblers, and Nashville warblers in fall. Capture time was also significantly negatively associated with plasma GLYC for the ground-foraging guild, thrushes, and Swainson’s thrush in spring and the foliage-gleaning and ground-foraging guilds, warblers, sparrows, and orangecrowned and Nashville warblers in fall. Body size (described by PCA1) did not significantly influence plasma metabolites in most bird groups. Moreover, the few significant body size effects on plasma metabolites that did occur lacked a consistent direction. Capture date and year had significant effects on plasma metabolites in some bird groups, but these effects also lacked a consistent direction (table 4). Between-Season Comparisons

tween species and habitat type for comparisons of plasma metabolites was not significant except for the fall ground-foraging guild (F9, 101 p 2.83, P p 0.01). After accounting for species effects and interactions, the between-habitat difference in plasma metabolites for all of these groups remained nonsignificant.

Significant differences in plasma TRIG and BUTY levels between seasons occurred for the foliage-gleaning guild (TRIG: F1, 461 p 4.32, P p 0.04, 33% higher in spring; BUTY: F1, 450 p 4.41, P p 0.02, 17% lower in spring), the ground-foraging guild (TRIG: F1, 178 p 4.70, P p 0.03, 79% higher in spring; BUTY: F1, 189 p 3.23, P p 0.01, 30% lower in spring), and warblers (TRIG: F1, 294 p 4.20, P p 0.03, 59% higher in spring; BUTY: F1, 286 p 5.30, P p 0.04, 33% lower in spring; fig. 5). Sparrows showed nonsignificant trends toward higher plasma TRIG (F1, 101 p 2.93, P p 0.09, 29% higher) and lower plasma BUTY (F1, 105 p 2.91, P p 0.07, 45% lower) in spring relative to fall. Flycatchers also showed 48% higher plasma TRIG in spring, a difference that approached significance (F1, 103 p 2.16, P p 0.06; fig. 5). The only significant difference between seasons for plasma GLYC levels occurred for sparrows (F1, 102 p 11.51, P p 0.001, 54% higher in spring; fig. 5).

Relationships among Plasma Metabolites

Discussion

Plasma levels of TRIG and BUTY were negatively correlated in both seasons, significantly so for fall (F1, 439 p 10.36, r p 0.23,

In general, our Mb and plasma metabolite data suggest that migrating woodland birds are capable of adding mass during

Figure 4. Relationship between plasma triglycerides (TRIG) and glycerol (GLYC) and between TRIG and b-hydroxybutyrate (BUTY) in spring and fall migrant birds. In the bottom panel, the dashed line represents fall migrants, and the solid line represents spring migrants.

Plasma Metabolites and Habitat Quality 191 Table 4: Variables retained in multiple regression models following backward stepwise regression at the P ! 0.10 level for foraging guilds, taxonomic groups, and individual species for the different plasma metabolites Spring Guild/species FGG GFG FLY VIR THR WAR SPA TRFL LEFL WAVI RCKI SWTH OCWA NAWA MYWA

TRIG

Fall

BUTY

GLYC

T⫹, Y, D⫹ T⫹, P⫹ Y

D⫹, Y P⫺ T⫺

N T⫺ N

T⫹ T⫹, Y

N D⫹, T⫺

T⫺ N

D⫹ T⫹, Y

T⫺ P⫺

N N

T⫹

N

TRIG

BUTY

GLYC

T⫹, D⫺, Y Y, P⫺

T⫺ D⫹

D⫺, T⫺ D⫺, T⫺

T⫹, D⫺

N

Y, D⫺

D⫺, T⫹, Y Y, T⫹

Y, D⫹, T⫺ Y, D⫹

Y, T⫺, D⫹ D⫺, T⫺

D⫺, T⫹ D⫺, T⫹

Y N

D⫺, Y D⫺

Y, T⫹ T⫹, D⫺ P⫹

N T⫺ N

Y, T⫺ T⫺ D⫺

T⫺

Note. Positive or negative symbols indicate the direction of the effect, where applicable. TRIG p triglycerides, BUTY p b-hydroxybutyrate, GLYC p glycerol, Y p year, D p date of the year, T p capture time, P p principal component of body size, N p no covariate, FGG p foliagegleaning guild, GFG p ground-foraging guild, FLY p flycatchers, VIR p vireos, THR p thrushes, WAR p warblers, SPA p sparrows, TRFL p complex of Empidonax alnorum and traillii, LEFL p least flycatcher (Empidonax minimus), WAVI p warbling vireo (Vireo gilvus), RCKI p rubycrowned kinglet (Regulus calendula), SWTH p Swainson’s thrush (Catharus ustulatus), OCWA p orange-crowned warbler (Oreothlypis celata), NAWA p Nashville warbler (Oreothlypis ruficapilla), MYWA p yellow-rumped warbler (Setophaga coronata).

stopover for both spring and fall migrations in both corridors and woodlots. Mb did not vary significantly between habitats for most species in this study, and the few differences that did occur lacked a consistent direction of variation between habitats (table 2). In addition, significant between-habitat differences in plasma metabolites were limited for birds in this study. No significant between-habitat differences in plasma TRIG levels occurred for any foraging guilds, taxa, or individual species at either season, and between-habitat differences in plasma BUTY were detected only for ruby-crowned kinglets during fall migration (figs. 2, 3). The few significant differences in Mb and plasma metabolites between the two habitats and the absence of a consistent direction of variation suggest generally similar stopover habitat quality for corridors and woodlots in the Northern Prairie region for the landbird migrant community as a whole. Plasma levels of TRIG and BUTY are considered the best metabolites to use for plasma metabolite profiling and for assessing stopover habitat quality in birds (Guglielmo et al. 2002, 2005; Smith and McWilliams 2010; Seewagen et al. 2011). In this study, plasma TRIG and BUTY were negatively correlated for birds during both spring and fall migration (fig. 4), which is in accord with their roles in fat deposition and fat catabolism, respectively (Guglielmo et al. 2002, 2005). Plasma levels of TRIG and GLYC showed a nonlinear U-shaped relationship in both spring and fall, similar to that documented by Guglielmo et al. (2005). These relationships are not consistent with opposing roles for TRIG and GLYC in fat metabolism. These data reinforce the idea that plasma GLYC is a less effective metric

than plasma TRIG for assessing relative rates of fattening in birds and, therefore, provide a less effective measure of stopover habitat quality. Thus, our results support the use of plasma TRIG and BUTY as the best metrics for plasma metabolite profiling and for assessing relative habitat quality during migratory stopover. Most covariates were not consistently correlated with plasma metabolites at either season across the landbird migrant community (table 4). However, capture time was retained as a covariate in multiple regression models for most bird groups and individual species and was uniformly positively related to plasma TRIG and negatively related to plasma BUTY and GLYC. This suggests that birds at our study sites are generally capable of depositing fat throughout the day (Jenni and JenniEiermann 1996; Guglielmo et al. 2005; Swanson and Thomas 2007), which is consistent with the idea that both corridors and woodlots provide suitable stopover habitat. Refueling performance of adult migrating landbirds is generally better than for juvenile migrants (e.g., Swanson et al. 1999; Guglielmo et al. 2002; Thomas 2008). In this study, however, Mb and plasma metabolite concentrations for individual species generally did not differ significantly by age (tables 2, 3). This suggests that both juvenile and adult birds were capable of meeting the energetic demands of migration at our study sites. One possible explanation for this pattern is that both habitat types in our study provide sufficiently high-quality stopover habitat so that juveniles are as capable as adults of meeting the energetic demands of migration. Another possibility is a trade-off between competition and food availability (Moore

192 M. Liu and D. L. Swanson

Figure 5. Least squares means (LSMEANS; ⳲSE) of plasma metabolites (mmol/L) for foraging guilds and taxomomic groups by season. Asterisks indicate a significant difference between birds in spring and fall. TRIG p triglycerides, BUTY p b-hydroxybutyrate, GLYC p glycerol, FGG p foliage-gleaning guild, GFG p ground-foraging guild, FLY p flycatchers, WAR p warblers, SPA p sparrows.

and Yong 1991; Yong et al. 1998; Kelly et al. 2002). Dean et al. (2004) found that the proportion of juveniles was significantly greater in woodlots than in corridors within our study area. We also caught more juvenile migrants from woodlots (82% juveniles) than from corridors (58% juveniles) in this study (M. Liu and D. L. Swanson, personal observation). The numerical dominance of juveniles at our study sites may allow

juveniles to largely avoid competition with adults. If juvenile birds preferentially occur in woodlots, they might be largely released from competition with adult birds in corridor habitats and thus improve relative refueling rates compared with adult birds. Confirmation of such a pattern of differential habitat use and relative refueling performance for different age groups will require further research. We found higher plasma TRIG and lower plasma BUTY for several bird groups in spring relative to fall (fig. 5). This suggests that refueling conditions for migrants might be better in spring than in fall at our study sites or that spring migrants might forage with greater intensity than fall migrants. Spring migration is potentially more urgent than fall migration, as early arrival on the breeding grounds is generally positively correlated with fitness (e.g., Smith and Moore 2005; Cooper et al. 2011; Gargallo et al. 2011; Gienapp and Bregnballe 2012). Spring migrants typically migrate at a faster pace than fall migrants (Pearson and Lack 1992; Ellegren 1993; Fransson 1995; Kemp et al. 2010), which may be reflected in differences in their physiological capacities (Swanson 1995; Swanson and Dean 1999). The increased pace of migration in spring may require spring migrants to invest greater effort in refueling and thereby show better refueling performance (Schaub and Moore 1996; Dunn 2002). Indeed, Seewagen et al. (2013) also found higher rates of refueling in spring than in fall migrants for four of five species tested and suggested that these differences in refueling performance might drive the faster pace of migration in spring. The suggestion of better refueling performance in spring than in fall in this study contrasts with results from Swanson et al. (2005) for a woodlot study site in this area, where higher mass gains for recaptured woodland migrants occurred in fall compared with spring. Dunn (2002) also documented better refueling performance in fall than in spring migrants. One possible explanation for the seasonal differences in plasma metabolites documented in this study is that food availability is higher in spring than in fall (Schaub and Jenni 2001; Guglielmo et al. 2002, 2005). However, this was not supported by prey-availability data, which were collected concurrently with blood sampling in this study and showed that arthropod dry mass per sampling unit was higher in fall than in spring at our study sites (M. Liu and D. L. Swanson, unpublished data). We have no obvious explanation for why patterns of seasonal differences in refueling performance in our current study differ from those of previous studies. Taken together, our data suggest similar stopover habitat quality for migrating woodland birds in riparian corridors and farmstead woodlot habitat types in the Northern Prairie region. This contrasts with our initial expectations based on the larger areas, more contiguous nature, and higher vegetative diversity in riparian habitats in this region (Gentry et al. 2006). The similar stopover habitat quality could be because of the roughly similar vegetation structure and the similar adjacent habitats (e.g., agricultural fields) and overall landscape patterns for both corridor and woodlot habitat types (Swanson et al. 2003; Gentry et al. 2006). Our physiological results from this study, which suggest similar stopover habitat quality between corridors and woodlots,

Plasma Metabolites and Habitat Quality 193 are consistent with survey data, which reveal similar abundances and species richness of woodland migrants in the two habitats (Dean 1999; Swanson et al. 2003, 2005; Packett and Dunning 2009). This conclusion of similar stopover habitat quality between corridors and woodlots is also consistent with analyses of plasma corticosterone from birds at our study sites (M. Liu and D. L. Swanson, unpublished data). These data suggest that anthropogenic woodlots can, at least partially, substitute for lost and degraded native riparian habitats during migration stopover for landbird migrants in the Northern Prairie region. Donovan et al. (2002) suggested that one research priority regarding migrant birds is the identification of high-quality stopover habitat. Similarly, Mehlman et al. (2005) listed the Great Plains region as one region specifically in need of further research efforts directed at identifying important woodland stopover habitat and urged that migration stopover sites for migratory woodland birds should be included in comprehensive biodiversity planning. Partners in Flight (Rich et al. 2004; Berlanga et al. 2010) recommend restoring riparian woodland corridors, floodplain forests, and streamside buffers within the Prairie Avifaunal biome. Similarly, the South Dakota Comprehensive Wildlife Conservation Plan (South Dakota Department of Game, Fish and Parks 2005) recommends preserving an appropriate level of ecosystem diversity throughout the state, including riparian woodland habitats, especially along the Missouri River. Identification of appropriate habitats for preservation requires not just a description of the composition and structure of these sites but also a knowledge of the quality of habitat as it relates to functional processes, so that high-quality habitats are the primary targets of conservation efforts. Geographically isolated human-planted shelterbelts and woodlots in the Northern Prairie region are viewed largely in a negative light for their detrimental effects on grassland birds (Bakker 2003; Rich et al. 2004). However, most of these woodlots in southeastern South Dakota exist in a matrix composed mainly of agricultural landscapes dominated by row crops, which are not productive habitats for grassland birds (Best et al. 1995). Thus, the potential benefits of these isolated woodland habitats to resident and migratory woodland birds (Swanson et al. 2003, 2005; Gentry et al. 2006) should be considered in conservation plans for the region. The data in this study suggest that the conservation of even small woodland parcels, such as the isolated woodlot sites in this study, will benefit woodland birds by providing suitable stopover habitat during migration and thereby positively impact populations of these birds.

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