The Auk 122(4):1261–1270, 2005 © The American Ornithologists’ Union, 2005. Printed in USA.

HABITAT AND SEX DIFFERENCES IN PHYSIOLOGICAL CONDITION OF BREEDING SOUTHWESTERN WILLOW FLYCATCHERS (EMPIDONAX TRAILLII EXTIMUS) J C. O,1,3 M K. S,1 M D. K2 1U.S. Geological Survey Southwest Biological Science Center, Colorado Plateau Research Station, Northern Arizona University, Flagstaff , Arizona 86001, USA; and 2Biology Department, College of Wooster, Wooster, Ohio 44691, USA

A.—The Southwestern Willow Flycatcher (Empidonax traillii extimus; here- a er “fl ycatcher”) is a federally listed endangered species that breeds in densely vegetated riparian habitats dominated by native and exotic plants, including intro- duced monotypic saltcedar (Tamarix ramosissima). Some workers have theorized that saltcedar is unsuitable habitat for the fl ycatcher, primarily because it generally supports a smaller and less diverse invertebrate community (the fl ycatcher’s food base) than native habitats (e.g. Salix spp.). However, diff erences in insect communi- ties between native and saltcedar habitats are not proof that saltcedar habitats are inferior. The only way to evaluate whether the habitats diff er in dietary or energetic quality is to document actual food limitation or its manifestations. Measurements of an individual’s body condition and metabolic state can serve as indicators of environmental stressors, such as food limitation and environmental extremes. We captured 130 fl ycatchers breeding in native and saltcedar habitats in Arizona and New Mexico and measured 12 variables of physiological condition. These variables included body mass, fat level, body condition index, hematocrit, plasma triglycer- ides, plasma free fa y acids and glycerol, plasma glucose and beta-hydroxybutyrate, plasma uric acid, total leukocyte count, and heterophil-to-lymphocyte ratio. We found substantial sex-based diff erences in the condition of male and female fl ycatch- ers. Ten of the 12 measures of physiological condition diff ered signifi cantly between the sexes. In all cases where male and female condition diff ered (except mass), the diff erences suggest that males were in poorer condition than females. We found few habitat-based diff erences in fl ycatcher condition. Only 3 of the 12 physiological con- dition indices diff ered signifi cantly between habitats. Our data show that, at least in some parts of the fl ycatcher’s range, there is no evidence that fl ycatchers breeding in saltcedar habitats exhibit poorer nutritional condition or are suff ering negative physiological aff ects. Received 8 April 2004, accepted 8 April 2005.

Key words: diet, Empidonax traillii extimus, physiology, saltcedar, Southwestern Willow Flycatcher, tamarisk.

Diferencias entre Hábitats y Sexos en la Condición Fisiológica de Individuos Reproductivos en Empidonax traillii extimus

Rzr.—Empidonax traillii extimus es un atrapamoscas que está incluido en la lista federal de especies amenazadas y se reproduce en ambientes riparios con vegetación densa dominada por plantas nativas y exóticas, incluyendo la especie introducida Tamarix ramosissima. Algunos investigadores han propuesto que los ambientes

3Present address: Department of Biological Sciences, University of Southern Mississippi, Ha iesburg, Mississippi 39406, USA. E-mail: [email protected]

1261 1262 O, S, K [Auk, Vol. 122

dominados por Tamarix son inadecuados para este atrapamoscas, principalmente porque por lo general albergan comunidades más pequeñas y menos diversas de invertebrados (la base de su dieta) que los ambientes nativos (e.g. los dominados por Salix spp.). Sin embargo, las diferencias en las comunidades de insectos entre los distintos hábitats no demuestran que los ambientes dominados por Tamarix son de inferior calidad. El único modo de evaluar si los ambientes difi eren en su calidad dietaria o energética es documentar la existencia de limitación de alimento o sus manifestaciones. Las medidas de la condición corporal de un individuo y su estado metabólico pueden servir como indicadoras de la presencia de agentes causantes de estrés en el ambiente, tales como limitación de alimento y condiciones ambientales extremas. En este estudio, capturamos 130 atrapamoscas que estaban criando en ambientes nativos y de Tamarix en Arizona y New Mexico, y medimos 12 variables relacionadas con su condición fi siológica. Estas variables incluyeron peso corporal, nivel de grasa, un índice de condición corporal, hematocrito, triglicéridos del plasma, ácidos grasos libres y glicerol en el plasma, glucosa e hidroxibutirato en el plasma, ácido úrico en el plasma, número total de leucocitos y el cociente entre heterófi los y linfocitos. Encontramos diferencias sustanciales con respecto al sexo: diez de las 12 medidas de la condición fi siológica difi rieron entre machos y hembras. En todos los casos en que hubo diferencias entre sexos (excepto en el peso), éstas sugieren que los machos estaban en peores condiciones que las hembras. Encontramos pocas diferencias con respecto al hábitat en la condición de los atrapamoscas. Sólo tres de las 12 medidas de la condición fi siológica difi rieron signifi cativamente entre hábitats. Nuestros datos muestran que al menos en algunas partes del rango de distribución de E. t. extimus, no existe evidencia de que los individuos que se reproducen en ambientes dominados por Tamarix se encuentran en peores condiciones nutricionales o sufren de efectos fi siológicos negativos.

T Sz W Flycatcher diversity and reliance on smaller prey items in (Empidonax traillii extimus; herea er “fl y- the saltcedar habitat. However, diff erences in catcher”) is a federally listed endangered species insect communities and fl ycatcher diet between (U.S. Fish and Wildlife Service 1995) that breeds native and saltcedar habitats are not, in them- in dense riparian habitats along rivers, streams, selves, evidence that saltcedar habitats are infer- lakes, and other wetlands. Flycatchers breed in ior or detrimental. The only way to determine a diverse array of riparian habitats (Sogge and whether the habitats diff er in terms of dietary Marshall 2000), including those dominated by or energetic quality is to document actual food introduced species such as saltcedar (Tamarix limitation or its manifestations. ramosissima) and Russian olive (Elaeagnus angus- One way to investigate manifestations of tifolia). Use of saltcedar is extensive; rangewide, food limitation is by measuring variables that 25% of fl ycatcher territories are found in habi- refl ect the physiological state of an individual. tats dominated by saltcedar (Sogge et al. 2003). Plasma metabolite levels depend strongly on Saltcedar has been implicated as a causative food intake, so diff erences in daily pa ern of factor in the decline of some southwestern bird food intake and changes in body mass (e.g. species and communities (e.g. Hunter et al. from diff erences in diet) may be refl ected in 1987). Furthermore, DeLoach et al. (2000) pro- concentrations of the diff erent metabolites in posed that saltcedar habitats are unsuitable for an individual bird (Jenni-Eiermann and Jenni breeding fl ycatchers because saltcedar plants 1994, 1998). In addition, plasma metabolites generally host fewer invertebrates than native may refl ect diff erences in the overall fa ening willows (Salix spp.) and thus do not provide rate of the population and, hence, the quality adequate food resources. In the fi rst study of a particular habitat (Guglielmo et al. 2002). of fl ycatcher diet, Drost et al. (1998) found Hematological variables, such as hematocrit and signifi cant diff erences among native and salt- leukocyte count, may provide additional infor- cedar habitats, with trends toward lower prey mation on the nutritional and immunological October 2005] Southwestern Willow Flycatcher Physiology 1263 health of an individual bird (Gross and Siegel Roosevelt Lake, the Lower San Pedro River, the 1983, Gershwin et al. 1985, Amand 1986). Other Gila River near the San Pedro River confl uence, traditional measures of condition, which do not and the middle Gila River in Arizona. require collecting blood, include body mass and The blood chemistry of a bird can vary with visual assessment of subcutaneous fat stores. Fat season and time of day. In females, a 10-fold is the primary form of energy storage in birds, increase in plasma triglycerides is associ- and energy stores fl uctuate in relation to dietary ated with yolk production (Bacon et al. 1974, intake and metabolic demands (Blem 1990). Challenger et al. 2001, Vézina and Williams We measured plasma concentrations of tri- 2003). Therefore, we concentrated our capture glycerides, beta-hydroxybutyrate (BOHB), non- eff orts during the month a er females had fi n- esterifi ed fa y acids (NEFA), glycerol, glucose, ished egg laying and before the young fl edged. and uric acid to characterize individual physio- Dates of capture were from 5 June to 7 July in logical condition of fl ycatchers breeding in salt- 1999 and from 1 June to 30 June in 2000. In addi- cedar and native habitats in Arizona and New tion, triglyceride levels can rise sharply during Mexico. In addition, we measured hematocrit the early-morning feeding and then level off (packed red blood cell volume), total and dif- a er mid-morning (Jenni-Eiermann and Jenni ferential leukocyte (WBC) counts, and energetic 1997). In the same way, levels of BOHB are sig- condition. Few studies have investigated the nifi cantly lower in early morning as compared link between habitat quality and a bird’s physi- with other times of day. For this reason, we ology (but see Mazerolle and Hobson 2002). If began sampling birds 3 h a er sunrise, with saltcedar habitats present greater physiologi- daily capture times between 0800 and 1100 cal challenges (e.g. food or water limitations, hours. disease) than native habitats, birds breeding Birds were live-captured using a targeted in exotic habitats will have lower values for fat mist-ne ing technique (Sogge et al. 2001), in level, body condition index, hematocrit, uric which fl ycatcher songs and calls were broad- acid, and triglycerides. By contrast, WBC count, cast to lure territorial fl ycatchers into nets. heterophil-to-lymphocyte [H:L] ratio, NEFA, Flycatchers were removed from nets immedi- glycerol, and BOHB should be higher in poor- ately upon capture, and fi  ed with an alumi- quality patches. In addition, because sex-related num numbered federal band. We captured 130 diff erences have been documented for several of adult fl ycatchers at 11 diff erent breeding sites the indicators of physiological condition listed (Table 1). Fi y-fi ve individuals were captured above (Gave and Wakeley 1986, H¿rak et al. in exotic (saltcedar) habitats, and 75 in native 1998, Kern et al. 2001), we examined diff erences habitats. For each bird we collected the fol- between breeding males and females. lowing information: age, sex, subcutaneous fat (Helms and Drury 1960), wing chord, bill M width, culmen length, and mass to the nearest 0.1 g. For birds that we could not reliably sex by The study was conducted during the summers presence of brood patch or cloacal protuberance of 1999 and 2000 in south-central Arizona and (Pyle 1997), we sexed by genetic analysis, fol- southwestern New Mexico (Table 1). We cap- lowing Griffi ths et al. (1998). We quantifi ed the tured, measured, and took blood samples from amount of visible subcutaneous fat deposited in fl ycatchers breeding in both native and exotic the abdominal and furcular regions using a six- habitats. The dominant plant species within the point scale (Helms and Drury 1960). An addi- native breeding sites were willow, co onwood tional estimate of body condition was calculated (Populus spp.), and boxelder (Acer negundo). by generating size-specifi c, fat-free body mass Native sites had ≤10% saltcedar. The exotic sites for each individual (as described by Ellegren were dominated by saltcedar, with <10% native 1992, Yong and Moore 1997). Individuals were vegetation. Native sites were located at the grouped according to a common wing chord Salt River infl ow to Roosevelt Lake, the Lower (1-mm increments). For each wing chord, body San Pedro River, and the middle Gila River in mass was regressed on fat score. In each regres- Arizona, and in the Cliff –Gila valley in New sion, the b-intercept (equivalent to fat score = 0) Mexico. Exotic-dominated patches were found provided an estimate of fat-free mass for the at the Tonto Creek and Salt River infl ows to specifi c wing chord. Linear regressions were 1264 O, S, K [Auk, Vol. 122

T 1. Location, elevation, and number of Southwestern Willow Flycatchers captured and sampled.

Elevation 1999 2000 Total Latitude, longitude (m) (n) (n) (n) Exotic (saltcedar) sites Gila–Lower San Pedro River Confl uence, Arizona 32.8°N, 110.7°W 600 5 8 13 Roosevelt Lake–Salt River Infl ow, Arizona 33.6°N, 110.9°W 640 14 5 19 Roosevelt Lake–Tonto Creek Infl ow, Arizona 33.8°N, 111.2°W 640 6 0 6 Middle Gila River, Arizona 33.1°N, 110.0°W 770 0 17 17 Total 25 30 55 Native sites Lower San Pedro River, Arizona 32.9°N, 110.7°W 660 11 15 26 Roosevelt Lake–Salt River Infl ow, Arizona 33.7°N, 111.0°W 640 0 14 14 Middle Gila River, Arizona 33.1°N, 110.0°W 770 0 11 11 Cliff –Gila, New Mexico 32.9°N, 108.6°W 1,370 0 24 24 Total 11 64 75 performed for all wing chord lengths, and a the system by a nonetiological process, such as second regression model was then produced by severe malnutrition (Gershwin et al. 1985) or regressing fat-free mass on corresponding wing strenuous exercise (Mackinnon 1992). chord lengths. Using the equation generated For diff erential counts (i.e. heterophil:lym- by the second regression model, we calculated phocyte [H:L] ratio), 100 WBCs were counted size-specifi c fat-free mass for each individual. and the relative proportion of each blood cell We then subtracted fat-free body mass from type estimated. H:L ratio is used to assess stress body mass at capture to produce an estimate of in birds (Gross and Siegel 1983, Vleck 2001). stored fat (in grams). Studies show that the H:L ratio increases in Immediately following capture, a blood response to a variety of stressors, including sample (50–125 µL) was taken via the brachial food or water deprivation, malnutrition, and vein (26-gauge needle) and collected into hepa- injury (Gross and Siegel 1986, Tripathi and ranized capillary tubes. Capillary tubes were Bhati 1997, Vleck et al. 2000). stored on ice. A drop of blood was placed on a Within 6 h of blood collection, we spun the glass slide and a thin smear was made using a capillary tubes in a clinical centrifuge for 9 beveled slide. Blood smears were air-dried, fi xed min at 14,000 rpm. Using digital calipers, we with 100% methanol, and air-dried again. For determined hematocrit by measuring height identifi cation of white blood cells, slides were of RBC layer and dividing by height of total stained with combination Wright and Giemsa blood sample. Hematocrit is frequently used to stains. Absolute counts include all white blood assess a bird’s nutritional state (Amand 1986), cells (i.e. lymphocytes, monocytes, heterophils, but interpretation of values is diffi cult. A low eosinophils, and basophils) per 100 fi elds of hematocrit can indicate anemia or other mineral view, using oil immersion (Campbell and Dein defi ciencies, or bacterial and parasite infections 1984). Total WBC count is expressed as the num- (Campbell and Dein 1984). However, dehydra- ber of WBCs per 10,000 red blood cells (RBC). tion or elevated oxygen consumption may cause Changes in leukocyte number, whether leuko- a high hematocrit (Carpenter 1975). Hematocrit cytosis (elevated leukocyte count) or leukope- may also refl ect the reproductive activity of nia (depressed leukocyte count), refl ect ongoing birds, being higher in breeding males because disease processes of bacterial, parasitic, or viral of increased testosterone levels (Sturkie 1986). origin. Leukopenia may also indicate stress on Blood plasma was separated from RBCs, October 2005] Southwestern Willow Flycatcher Physiology 1265 stored frozen, and then shipped to The Ohio Rz State University Department of Animal Sciences for plasma constituent analysis under the direc- We conducted preliminary analyses to deter- tion of W. Bacon. Plasma metabolites were mine whether the condition indices diff ered assayed using standard reagent kits that require with year, date (day within breeding season), small amounts of blood, ranging from 3 to and time of sampling. NEFA was the only vari- 12 µL. Glucose, uric acid, BOHB, glycerol, and able to vary between years (F = 190.60, df = 1 triglyceride levels were determined by quantita- and 130, P < 0.0001). For all subsequent analy- tive enzymatic tests (Sigma Chemical, St. Louis, ses, NEFA was separated by year. We found a Missouri) and NEFA (Wako Chemicals USA, signifi cant time-of-sampling eff ect on male tri- Richmond, Virginia). Intra-assay coeffi cients glyceride levels (r2 = 0.12, F = 11.51, df = 1 and 85, of variation ranged from 0.2% (triglycerides) P = 0.001), such that triglyceride levels increased to 3.7% (glycerol) for the various assays. Inter- throughout the morning, with highest values assay coeffi cients of variation ranged from 1.1% observed later in the morning (Jenni-Eiermann (glycerol) to 7.0% (uric acid). Birds gaining mass and Jenni 1997). To control for the time eff ect, may exhibit higher levels of plasma triglycer- we regressed triglyceride level on time, saved ides and glucose, though the la er is generally residuals, and used residuals for subsequent kept within narrow limits (Jenni-Eiermann analyses. Otherwise, no other condition vari- and Jenni 1994, 1997). On the other hand, lev- ables were signifi cantly related to time or date els of plasma glycerol, NEFA, and BOHB will of sampling. decrease in response to lipid catabolism (Jenni- Overall, 50 females were sampled, most of Eiermann and Jenni 1994, 1998). Uric acid lev- which (n = 36) had fully vascularized brood els must be interpreted with caution, because patches, indicating that they were incubating high levels have been linked to a high-protein eggs. The remaining females (n = 14) had either diet (Hochleithner 1994) and to short-term a smooth or no brood patch and no evidence of food stress (Jenni-Eiermann and Jenni 1994). an egg in the oviduct, an indication that they Therefore, understanding the meaning of uric were in the nest-building or prelaying stage. We acid pa erns requires consideration of the other found no statistical diff erences in the variables measures of physiological condition. of physiological condition between these two Statistical analysis.—To obtain plasma levels groups of females. Therefore, all females were of true triglycerides, we subtracted free glyc- combined for subsequent analyses. erol from total triglycerides. The process of egg Plasma metabolites.—There were signifi cant production causes exceptionally high levels of diff erences between habitats for triglycerides, triglycerides. Therefore, females with triglycer- glycerol, and uric acid, but not for BOHB, NEFA, ide levels of ≥800 mg dL–1 were excluded from or glucose (Table 2). Specifi cally, we found that analysis. Not all variables were measured for all triglyceride and uric acid levels were higher, individuals (primarily owing to diff erences in and glycerol was lower, in fl ycatchers sampled the amount of blood taken per individual) and in saltcedar habitats compared with those cap- therefore, sample sizes vary among variables tured at native sites. We ran additional analysis (Table 2). on habitat diff erences in male triglyceride levels We tested for the eff ect of habitat type and a ributable to the signifi cant time eff ect. Using sex on variation in physiological condition of residuals computed by regressing triglyceride fl ycatchers with analysis-of-variance (ANOVA) level on time of sample, the habitat diff erence in models, using type III sums of squares. triglyceride levels was still signifi cant (F = 4.28, Statistical signifi cance was set at α = 0.05. All df = 1 and 70, P = 0.042). We found signifi cant signifi cance levels refer to two-tailed tests. diff erences by sex for all plasma metabolites White blood cell count and heterophil:lym- except NEFA (Table 2). Females had higher levels phocyte ratio did not meet the assumptions of of glucose, triglyceride, and uric acid, and lower normality. However, while log-transforming the levels of BOHB than males. Glucose showed a variables created normality, it did not aff ect the signifi cant interaction eff ect between sex and results of the analysis. Therefore, we present all habitat (Table 2), in that males in saltcedar had nontransformed data for clarity. We performed lower glucose levels than those in native habitats, all analyses using SPSS 12.0. whereas females showed the opposite trend. 1266 O, S, K [Auk, Vol. 122 F Habitat Sex Habitat * Sex * Habitat Habitat Sex n Saltcedar n = heterophil:lymphocyte ratio, WBC y acids, BOHB = beta-hydroxybutyrate, H:L ed fa ed Native Native n ect of habitat type and sex on variables of physiological condition of Southwestern Willow Willow of physiological condition Southwestern ect of habitat type and sex on variables NEFA = non-esterifi NEFA

Saltcedar n < 0.001; abbreviations: P < 0.01, *** = P < 0.05, ** = P Flycatchers captured in Arizona and New Mexico during the breeding season of 1999 2000. Flycatchers captured in * = Male Female Native Native T 2. Descriptive statistics (means ± SD) and eff 2. Descriptive T Triglycerides Triglycerides BOHB 65.32 ± 16.54 40 Uric acid Glycerol 78.22 ± 25.32 Glucose 32 20.42 ± 7.18 16.84 ± 6.32 (1999) NEFA 107.30 ± 60.37 35 41 (2000) 26 43.58 ± 10.7 NEFA 329.40 ± 47.13 3.52 ± 0.08 40 WBC count 124.22 ± 63.40 41 19.70 ± 7.37 20.16 ± 6.65 15 2.98 ± 0.19 ratio H:L 6 16 32 313.54 ± 49.82 35 41.10 ± 10.91 12.39 ± 13.56 Hematocrit 32 33 37 Stored fat (g) 11.91 ± 5.86 19.36 ± 7.64 6.59** 332.08 ± 67.8 3.45 ± 0.19 39.44 ± 16.68 2.98 ± 0.16 Mass (g) 18 28 0.49 ± 0.58 10.16 ± 5.90 15 0.51 ± 0.02 24 27 0.12 ± 0.77 17 Fat score 34 27 39 23.83*** 327.89 ± 53.41 39 14.57 ± 6.98 26.00 ± 7.85 31.74 ± 10.71 13 3.49 ± 0.17 15 14 25.68 ± 23.48 2.94 ± 0.16 12.16 ± 0.79 5 0.91 ± 1.97 26 0.50 ± 0.02 5 41 0.61 ± 0.83 19 2.37 0.67 ± 0.58 20 26 1.22 12.12*** 29 29.49 ± 15.35 39 4.19* 12 0.23 12.37 ± 0.76 3.54 ± 0.27 3.12 ± 0.20 0.42 ± 0.35 0.48 ± 0.03 31 1.68 ± 0.97 9.83** 7 8 25 0.59 ± 0.61 27 27 7.55** 7.38** 0.13 11.97 ± 0.85 34 11.23** 0.31 ± 0.16 27 0.48 ± 0.03 0.02 1.84 ± 0.88 3.92 1.04 11 1.80 ± 0.77 13 13 12.13 ± 0.70 21.08*** 1.10 1.10 28 0.68 13 0.74 0.34 0.60 1.23 1.41 ± 0.99 3.08 0.30 16 0.71 18.17*** 2.07 57.10*** 1.18 3.82 1.79 1.36 0.18 1.04 51.64*** 1.09 0.02 0.96 count = white blood cell (leukocyte)/10,000 red cells. October 2005] Southwestern Willow Flycatcher Physiology 1267

Leukocyte counts.—We found no habitat dif- fl ycatchers in saltcedar may be (1) consuming ferences in WBC or H:L ratio (Table 2). WBC a higher-protein diet (Hochleithner 1994) or (2) count diff ered signifi cantly by sex (Table 2); experiencing food stress and metabolizing body females had higher WBC counts in both native protein (Anthony et al. 1990). The former inter- and saltcedar habitats. H:L ratio did not diff er pretation is more consistent with our observed between sexes for either habitat type. pa erns in fat levels, mass, condition indices, Hematocrit.—We found no habitat-related and other plasma metabolites. diff erences in hematocrit, but there was a sig- Our results may not be intuitive, given stud- nifi cant main eff ect diff erence between sexes ies documenting lower arthropod diversity and (Table 2). Females had lower hematocrits in abundance in saltcedar habitats (see DeLoach et both native and saltcedar habitats. al. 2000). One possible explanation is that earlier Body condition indices.—Although mass, fat studies did not specifi cally investigate the rela- score, and stored fat did not diff er signifi cantly tionship between saltcedar, associated arthro- by habitat, there were signifi cant main eff ect pods, and fl ycatcher diet. Flycatchers consume diff erences between the sexes for fat and stored a relatively diverse array of invertebrates (Drost fat (Table 2). In both habitat types, females had et al. 1998, 2003), and the simple fact that fl y- higher fat scores and stored fat than males. catcher diet diff ers in diff erent habitats does not mean that one habitat is inferior to another from Dz the perspective of food availability. Although the greater variety of prey in native habitat may Body mass, fat levels, and plasma metabolites off er some buff er against a temporary shortage depend strongly on food intake; therefore, dif- of any particular prey species, the large number ferences in daily pa erns of food intake (caused of pollinator species a racted to fl owering salt- by weather, diff erences in diet, etc.) may cause cedar appears to provide a very good source of diff erences in daily pa erns of these indica- prey in this habitat (Drost et al. 1998). Given that tors of condition (Jenni-Eiermann and Jenni saltcedar fl owers during much of the fl ycatcher 1994). Hematological variables (e.g. WBC, breeding season at our study sites, abundance H:L ratio) may refl ect acute or chronic stress- of large prey items (e.g. pollinators) may more ors, such as food or water limitations, injuries, than compensate for reduced diversity of avail- or disease processes (Campbell and Dein 1984, able prey types. Gershwin et al. 1985, Maxwell 1993, Vleck 2001). Recently, Durst (2004) reported on the diet Therefore, the variables of physiological condi- and potential arthropod prey base of fl ycatch- tion we measured should provide insights into ers at Roosevelt Lake, Arizona. Flycatcher environmental stressors that might be associ- diet diff ered between habitats. Birds in salt- ated with breeding in saltcedar habitats as cedar consumed more Homoptera, and less compared with native habitats, and between the Lepidoptera and Ananeae, than those in native energetic–physiological stressors on breeding habitats. Further, biomass of several inverte- males and females. brate taxa diff ered signifi cantly between habi- Habitat diff erences.—The indicators we mea- tats. However, total arthropod biomass was not sured showed no evidence that the physiologi- diff erent, and Durst (2004) concluded that there cal condition of fl ycatchers is lower in saltcedar were no diff erences in relative quality of food habitats. Only 3 of the 12 variables diff ered resources between native and exotics habitats. between habitats (Table 2), and the pa erns in 2 This conclusion is consistent with our physiol- of these 3 variables suggested that saltcedar pro- ogy results, both at Roosevelt Lake and at the vided be er energetic–dietary conditions than other sites we sampled. native habitats. Higher triglyceride and lower Our fi nding that fl ycatchers breeding in glycerol levels indicated that the fl ycatchers in saltcedar habitats do not suff er negative physi- saltcedar had deposited fat more recently (e.g. ological consequences does not mean that all producing and storing more fat) than those in saltcedar-dominated riparian areas would pro- native habitat (Jenni-Eiermann and Jenni 1994, vide suitable breeding habitat. Although our Schaub and Jenni 2001). The signifi cantly higher samples came from sites that support most of uric acid levels (Table 2) for fl ycatchers nesting the fl ycatchers breeding in Arizona and New in saltcedar could be interpreted in two ways: Mexico, these sites were located in an elevational 1268 O, S, K [Auk, Vol. 122 range of 560–1,370 m and typically within 200 m the diff erent activity pa erns of males and of surface water or moist soil. Furthermore, the females. During the breeding season, male riparian habitats at our study sites were usu- fl ycatchers are strongly territorial (Sogge 2000) ally embedded within a local matrix of desert and active, spending much of their time singing shrub uplands (o en dominated by mesquite and defending against conspecifi cs’ intrusions. [Prosopis spp.]) or irrigated croplands. These By contrast, female fl ycatchers (during the early adjacent habitats may have provided a source nesting period that we sampled) are relatively for many strong-fl ying invertebrates (e.g. bees, inactive, periodically foraging and singing but wasps) that are a racted to fl owering saltcedar spending most of the day incubating (M. K. (Drost et al. 2003). Many of the earlier studies Sogge unpubl. data). The higher activity level of saltcedar, its invertebrate communities, and of males entails higher energy demands, with its reduced value to wildlife were conducted subsequent heightened physiological stress. at sites that were lower in elevation, ho er, and Our comparison of the eff ects of breeding drier than those included in Durst (2004) and the in saltcedar versus native habitats was con- present study. Indeed, in many of the extensive ducted within a specifi c geographic region and monotypic saltcedar stands along the lower stage within the breeding season. The pa erns Colorado River and elsewhere in the deserts of that we found may diff er in other parts of the the Southwest, high temperatures, dry condi- fl ycatcher’s range. Also, there are other ways in tions, or lack of invertebrate prey may preclude which diff erences in habitat suitability may be breeding by fl ycatchers. These potential regional manifested, including diff erences in clutch size, and site-specifi c diff erences in suitability under- productivity (number of young fl edged per score the reality that not all saltcedar habitats are female per season), adult or juvenile mortality equal with regard to habitat quality. and survival, site fi delity, and breeding popula- Sex diff erences.—We found substantial sex- tion age and density. None of this information based diff erences in the condition of male and is available, and additional studies and data female Southwestern Willow Flycatchers; 10 of analyses are needed to determine whether such the 12 physiological condition indices diff ered diff erences exist at our study sites and else- signifi cantly between the sexes (Table 2). In all where in the Southwest. However, our results cases where male and female condition diff ered, show that there is no evidence that fl ycatchers the diff erences suggested that males experi- breeding in saltcedar habitats are suff ering enced higher stress or lower food intake and negative physiological eff ects and reinforce were in poorer condition than females, regard- the fact that such negative eff ects should not be less of habitat type. In both native and exotic assumed a priori. habitats, higher levels of fat, body condition, glucose, and triglyceride indicated that females Ar were gaining more mass than males, and lower levels of BOHB and glycerol demonstrated that This work was partially funded by federal females were catabolyzing their fat reserves assistance from the U.S. Bureau of Reclamation to a lesser degree than males (Jenni-Eiermann and the U.S. Geological Survey (USGS); funding and Jenni 1994, 1997). Judging from these pat- was also provided by the Arizona Department terns, the higher uric acid levels in females of Transportation. We thank the following mem- probably refl ected a higher-protein diet. The bers of the USGS banding crew for their hard higher hematocrit in males may be a ributable work and dedication: R. Emerson, H. English, to dehydration or to higher energy demands. K. Kenwood, T. Koronkiewicz, S. Langridge, J. (Carpenter 1975, Work et al. 1999), which is Luff , R. Ne er, E. Paxton, and J. D. Semones. consistent with our plasma metabolite results. We are grateful to the U.S. Forest Service Rocky Our fi ndings agree with other studies that Mountain Research Station (Albuquerque, New found sex-related diff erences in hematocrit and Mexico) and the U-Bar Ranch for access to immunological variables (Gave and Wakeley and assistance while at the Cliff –Gila site. Our 1986, H¿rak et al. 1998, Ots et al. 1998). thanks to P. Keim and E. Paxton for assistance Male fl ycatchers appear to be more ener- with genetic sexing of blood samples. W. Bacon getically challenged than females during the at The Ohio State University conducted the nesting season. One probable explanation is plasma metabolite analyses. October 2005] Southwestern Willow Flycatcher Physiology 1269

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