J. Field Ornithol. 86(2):89–102, 2015

DOI: 10.1111/jofo.12093

Demography of Slate-throated Redstarts (Myioborus miniatus): a non-migratory Neotropical warbler Ronald L. Mumme Department of Biology, Allegheny College, 520 North Main Street, Meadville, Pennsylvania 16335, USA Received 28 October 2014; accepted 10 January 2015 ABSTRACT. Most wood-warblers (Parulidae) are non-migratory residents of the Neotropics and subtropics, and the demographic characteristics of these species are poorly known. I examined the annual survival, reproductive output, dispersal, age of first breeding, and other demographic characteristics of a permanently territorial nonmigratory tropical warbler, the Slate-throated Redstart (Myioborus miniatus), based on a 5-yr study of a color-banded population in Monteverde, Costa Rica. Territorial males showed strong site fidelity, but 26% of females engaged in short-distance between-year breeding dispersal. Estimated annual survival of territory holders, corrected for undetected female breeding dispersal, was 0.56 for males and 0.43 for females, values lower than expected and comparable to survival estimates for North American migrant warblers. The lower annual survival of females had two demographic consequences; unpaired territorial males were present in 3 of 5 yr, and some 1-yr-old males appeared to be floaters. Unpaired females or female floaters, however, were not observed. Mean natal dispersal distance was significantly greater for females (935 m) than males (485 m). Estimated first-year survival was 0.29, but this is almost certainly an underestimate because of undetected long-distance, female-biased natal dispersal. Annual fecundity (fledglings per female) was 1.8, less than that of temperate warblers and attributable to small mean clutch sizes and a low incidence of double brooding. Estimated population growth rate (␭) was <1 for both males and females, suggesting that the study population was a demographic sink, most likely due to lower-than-expected adult survival. RESUMEN. Demograf´ıa de Myioborus miniatus, un par´ ulido Neotropical no migratoria La mayor´ıa de los par´ulidos (Parulidae) son residentes no migratorias en zonas neotr´opicos y subtropicales, y las caracter´ısticas demogr´aficas de estas especies son poco conocidas. Examin´e la supervivencia anual, la tasa reproductiva, la dispersi´on, la edad cuando los par´ulidos comienzan a reproducir, y otras caracter´ısticas demogr´aficas de un par´ulido tropical, el Myioborus miniatus, que es un residente permanente, no migratoria, y mantiene un territorio. Las caracter´ısticas demogr´aficas fueron determinadas por un estudio de cinco a˜nos sobre una poblaci´on de par´ulidos que fueron anillados con colores en Monteverde, Costa Rica. Los machos territoriales mostraron fuerte fidelidad al sitio, pero el 26% de las hembras llevaron a cabo la dispersi´on reproductiva a distancia corta y entre a˜nos. La supervivencia anual fue estimada sobre los due˜nos del territorio, y se corrigi´o por dispersi´on de las hembras reproductoras que no fueron detectados. La supervivencia anual fue desde 0.56 para los machos y 0.43 para las hembra; los valores son inferiores de lo esperado y comparable a las estimaciones de supervivencia anual para par´ulidos migratorias de Norteam´erica. La supervivencia anual baja de las hembras tuvo dos consecuencias demogr´aficas. Machos territoriales no apareados estaban presentes en tres de los cinco a˜nos, y algunos machos de 1 a˜no de edad parec´ıan ser los flotadores (aparean con mas de un individuo). Sin embargo, no se observaron hembras no apareadas o hembras flotadoras. La distancia de dispersi´on natal fue significativamente mas alta en las hembras (935 m) que en los machos (485 m). Supervivencia del primer a˜no fue estimada a 0.29, pero esto es seguramente una subestimaci´on debido a que no fue detectada la dispersi´on natal de larga distancia, y que tambi´en tuvo un prejuicio sobre las hembras. La fecundidad anual (pollos por cada hembra) fue 1.8, que fue mas baja que la fecundidad anual de los par´ulidos templadas y atribuible a los peque˜nos tama˜nos de nidadas y una baja incidencia de nidadas dobles. La tasa de crecimiento estimada por la poblaci´on (␭) fue <1 para machos y hembras, lo que sugiere que la poblaci´on de estudio fue un sumidero demogr´afico, probablemente debido a la supervivencia de los adultos, lo cual fue mas baja de lo esperado. Key words: adult survival, breeding dispersal, first-year survival, floaters, natal dispersal, Parulidae, sex-biased dispersal, tropical birds

Wood-warblers (family Parulidae, Lovette et al. 2010) comprise 110 species of New World songbirds found from the Arctic through temperate regions of South America. In recent years, detailed population studies have increased

our understanding of the population biology and demography of migratory parulids that breed in North America, shedding light on important demographic processes such as pairing success, annual fecundity, breeding dispersal, adult survival, natal dispersal, and first-year survival (Chase et al. 1997, Bayne and Hobson

Email: [email protected]  C

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2001, Sillett and Holmes 2002, Hoover 2003, Faaborg et al. 2010, Bulluck et al. 2013, Cline et al. 2013, McKim-Louder et al. 2013). However, most parulids are non-migratory permanent residents of the tropics, subtropics, and south temperate zone (Curson et al. 1994, Winger et al. 2012), and data on the population biology and demography of these species are limited to a few studies of nesting success (Cox and Martin 2009, Mumme 2010, Ruggera and Martin 2010) and adult survival (Faaborg and Arendt 1995, Martin et al. 2000, 2015, Ghalambor and Martin 2001, Martin 2002). For nonmigratory parulids, virtually no data are available on other important demographic characteristics such as breeding dispersal, natal dispersal, firstyear survival, and age of first breeding. Additional data on the demography of nonmigratory tropical and subtropical parulids would be valuable for two reasons. First, 78% of the 23 species of parulids considered to be Vulnerable, Near Threatened, Endangered, or Critically Endangered by the International Union for Conservation of Nature are nonmigratory tropical or subtropical species with restricted ranges (IUCN 2014). Demographic data are an essential cornerstone of avian conservation efforts (Faaborg et al. 2010), providing insight into critical stages in the life cycle that influence population growth rates and long-term population viability (McDonald and Caswell 1993, Sæther and Bakke 2000, Cox et al. 2014). Even rudimentary data on basic demographic characteristics can greatly inform conservation efforts, providing a useful first step in the modeling of population dynamics and development of sound conservation plans (Heppell et al. 2000). Second, demographic data on tropical warblers can play an important role in the continuing development of avian life history theory. Because parulid warblers comprise a well-defined monophyletic group (Lovette et al. 2010) that spans a wide range of latitudes and habitats (Curson et al. 1994, Winger et al. 2012), comparisons of the demographic characteristics of tropical and temperate warblers can be especially valuable in advancing our understanding of avian life history evolution (Martin et al. 2000, in press). For example, rates of annual adult mortality and nest survival are known to be important predictors of a variety of avian life history traits, including clutch size, parental care, incubation temperatures, embryonic de-

J. Field Ornithol.

velopmental rates, and nestling growth rates (Martin et al. 2000, in press, Ghalambor and Martin 2001, Martin 2002, Robinson et al. 2010). Here I present data on the demographic characteristics of a non-migratory tropical warbler, the Slate-throated Redstart (Myioborus miniatus). The genus Myioborus includes 12 species of sexually monomorphic parulids found in montane forests throughout the American tropics and subtropics (Curson et al. 1994, P´erezEm´an 2005), including three species that are considered Near Threatened or Endangered (IUCN 2014). All members of the genus use animated displays of their contrasting blackand-white tails to startle potential insect prey that are then pursued and captured in flight (Jabło´nski 1999, Mumme 2002, Mumme et al. 2006). Slate-throated Redstarts are the most widely distributed member of the genus, ranging from the mountains of northern Mexico to the southern Andes of Bolivia (P´erezEm´an et al. 2010). They are non-migratory, socially monogamous, permanently territorial, and build domed nests on the ground in steep banks, frequently along roads and trails. Both sexes feed nestlings and fledglings, but females perform all nest building, incubation of eggs, and brooding of young (Skutch 1954, Shopland 1985, Mumme 2010, Ruggera and Martin 2010). In Costa Rica, Slate-throated Redstarts nest from March to June; clutch size is typically three eggs, with a 14-d incubation period and an 11-d nestling period. Although pairs regularly re-nest after failure of their initial nest, double brooding is rare (Mumme 2010). The data presented here, derived from a 5-yr study of a color-banded population of Slate-throated Redstarts in Monteverde, Costa Rica (Mumme 2002, 2010), provide the first complete demographic portrait of a non-migratory tropical parulid. METHODS Study area and general methods. I studied Slate-throated Redstarts during five consecutive breeding seasons (2000–2004) in Monteverde, Costa Rica (10.19°N, 84.48°W; Nadkarni and Wheelwright 2000). The 116ha study area was centered around the Estaci´on Biol´ogica Monteverde and the Cerro Amigos road (Fig. 1), encompassing an elevational range

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Fig. 1. Map of the 116-ha study area in Monteverde, Costa Rica. Free-form lines are roads serving the Estaci´on Biol´ogica Monteverde, the Cerro Amigos television towers, and the Monteverde Cloud Forest Reserve. Instances of natal dispersal by color-banded female (N = 5) and male (N = 13) Slate-throated Redstarts are also shown.

of 1400–1800 m and a variety of habitats, including primary forest, old second growth, abandoned pastures with scattered trees, and low-density residential housing. Each year, 40 pairs of Slate-throated Redstarts bred on the study area. During May and June of each year, I captured adult Slate-throated Redstarts near nests in mist-nets and each was banded with a unique combination of color bands; nestlings were also color-banded prior to fledging (Mumme 2002, 2010). Sex of breeding adults was determined by the presence of a brood patch (females) or singing behavior (males). I resighted colorbanded birds during twice-weekly surveys of the study area conducted by walking trails and roads and mapping the locations of nests and colorbanded adults and fledglings. I defined breeding dispersal distance (observed only in females) as the distance between the approximate centers of an individual’s nesting territories in different years, and natal dispersal distance as the distance between a bird’s natal nest and the approximate center of its initial nesting territory. I estimated dispersal distances using high-resolution aerial

photos and mapping tools available in Google Earth. Survival of territory-holding adults. Estimates of annual survival for territory-holding males and females were based on resighting histories of 142 color-banded individuals (70 males and 72 females) banded from 2000 to 2003. To estimate apparent survival (ф) and resighting probability (p), I considered two separate Cormack-Jolly-Seber (CJS) models using program MARK (White and Burnham 1999): a four-parameter model where ф and p were sex-dependent (фS pS ) and a 10-parameter model where p was sex-dependent and apparent survival was sex- and year-dependent (фS *Y pS ). Because of sex differences in site fidelity (discussed below) and because resighting effort was consistent for all years of the study, I did not consider models that combined the sexes or included year-dependent values of p. I assessed goodness-of-fit of the year-dependent (global) model by estimating overdispersion using the median c-hat method implemented in program MARK, and relative strength of support for alternative models using Akaike’s information

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criterion for small samples (AICc ) and Akaike weight (wi ). Following Burnham and White (2002) and Moynihan et al. (2006), I constructed an intercept-only random-effect model to estimate process variance (total variance – sampling variance) and the proportion of total variance in annual survival that was not attributable to sampling variance. To correct for and estimate the magnitude of female breeding dispersal from the study area, I also modeled female survival with the spatially explicit CJS model of Schaub and Royle (2013). This model uses the observed distribution of dispersal movements in a study area to estimate dispersal off the study area and correct survival estimates accordingly. The model includes a spatially explicit Bayesian analytical module to estimate true survival (S) as well as a datasimulation module useful in estimating the magnitude of dispersal from the study area, given the observed distribution of known movements within the study area. First-year survival. Estimates of first-year survival (survival from fledging to the subsequent nesting season when birds were 1 yr old) were based on resightings of 133 individuals color-banded as nestlings that fledged from 2000 to 2003. Because some surviving individuals were not detected until they were 2–3 yr old, I used MARK models with four parameters, including ф1 (survival from fledging to the next nesting season), фA (survival in subsequent years), p1 (probability of resighting at age 1 yr), and pA (probability of resighting in subsequent years). Sex of nestlings and fledglings was unknown and therefore not included as a factor in the survival models. I used the same model to estimate ф1 in two different ways, using only birds resighted within the study area (N = 14) and using all resightings, including incidental encounters outside the study area (N = 18). To correct for undetected long-distance natal dispersal from the study area, particularly by females (see below), I used the spatial CJS model of Schaub and Royle (2013) to estimate true first-year survival. Unfortunately, their analytical model performs poorly when apparent survival is low and emigration is high (Schaub and Royle 2013), factors that characterized my dataset for juvenile redstarts. Instead, I estimated survival indirectly via the model’s data-simulation module. Using the observed distribution of

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natal dispersal distance, actual size and shape of the study area, and hypothetical values of true survival (S1 ) and true detection probability, I produced simulated data sets that yielded estimates of apparent first-year survival (ф1 ) and first-year detection probability (p1 ) that were identical to the CJS estimates in the actual dataset. Reproductive success and population growth rate (␭). I monitored nesting suc-

cess and annual reproductive performance of breeding pairs using methods described previously (Mumme 2010). I documented annual reproductive success (number of young fledged per year) for 146 breeding pairs, including 87 pairs where both breeders were color-banded and 47 pairs where one member of the pair was banded. Because all resident adult females were part of a territorial breeding pair, mean annual female reproductive success was calculated using these 146 pairs. For males, however, I included an additional 10 unpaired territorial males in the estimate of mean annual male reproductive success; annual reproductive success for these unpaired males was assumed to be 0. I estimated sex-specific population growth rates (␭) and elasticities from Leslie projection matrices (McDonald and Caswell 1993) using matrix manipulation methods described by Stevens (2009) for program R (version 3.02; R Core Team 2013). I estimated ␭ for females and males separately and assumed a 1:1 sex ratio of offspring at fledging. Because all surviving females appeared to become territory-holding breeders when one year old, I modeled female demography with a 2 × 2 matrix that included values of survival and reproductive success for two age classes: juveniles and females one year old or older. Males established territories and bred initially either when one year old (N = 6) or two years old (N = 6), so I modeled male demography with a 3 × 3 matrix and three age classes; juveniles, 1-yr-olds, and males  2 yr old. Because I could not directly estimate either the proportion of one-year-old males that were non-territorial floaters or their survival from age 1 yr to age 2 yr, estimating mean annual survival and reproductive success for all 1-yr-old males is problematic. I therefore assumed that annual reproductive output of one-year-old males was 50% that of older males, and that annual survival of males from age 1 yr to age 2 yr was the same as annual survival for older males. Values

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Table 1. Comparison of two models of apparent survival in breeding male and female Slate-throated Redstarts, with number of parameters (K), change from the model with the lowest Akaike’s Information Criterion adjusted for small samples (AICc), and Akaike model weight (wi ) shown. The model that included sex- and year-dependent effects on annual survival (фS *Y pS ) received stronger support than the model that included only sex-dependent effects (фS pS ). Model фS *Y pS фS pS a

K 10 4

AICc 0.0a 2.2

wi 0.75 0.25

AICc = 336.1.

are presented as means ± SE, unless otherwise noted. RESULTS Territory fidelity and estimated survival of territory-holding adults. Once estab-

lished on a territory, adult males showed high site fidelity. Of 34 territorial males detected in two or more years, none changed territory location from one year to the next (N = 53 male-years). Territory-holding breeding females, in contrast, showed less site fidelity. In seven cases (26% of 27 different females, 18% of 39 femaleyears), females dispersed a short distance (mean = 166 ± 50 [SD] m, range = 90–240 m) from their initial breeding territory, usually (57% of seven cases) by pairing with a neighboring male following the disappearance and presumed death of their original mate. Of the two MARK models considered, the model that included year- and sex-dependent effects on apparent survival received stronger support (Table 1) and showed good fit to the data (c-hat = 1.22). Estimates of ф suggested important effects of both sex and year, with males showing higher apparent survival than females and both sexes, but particularly females, showing markedly lower apparent survival during 2003 and 2004 (Fig. 2A). Process variance (0.016) represented 75% of total variance (0.021), suggesting that only 25% of the variance in observed survival was due to sampling variance. Estimates of mean resighting probabilities (p) were high for both males (0.83 ± 0.08) and females (0.92 ± 0.07).

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Mean annual apparent survival (ф) was 0.56 ± 0.06 for males and 0.39 ± 0.05 for females (Fig. 2B). Because I observed no instances of breeding dispersal by males, the estimate of ф for males is unlikely to be confounded with significant undetected dispersal from the study area. In contrast, the calculated value of apparent survival in females is almost certainly a biased underestimate of true survival, as some females that disappeared are likely to have changed territories and dispersed from the main study area rather than died. To correct for and estimate the magnitude of breeding female dispersal from the study area, I modeled female survival with the spatially explicit CJS model of Schaub and Royle (2013). Estimated true female survival (S) was 0.43 (95% credible interval 0.32–0.55), 0.04 higher than the estimate of apparent survival (ф). This modest correction is consistent with the observed low frequency and short distance of female breeding dispersal in the study area; generation of simulated data sets using the spatial CJS model suggested that each year 3% of all breeding females (5% of females that disappeared) may have dispersed from the study area and escaped subsequent detection. Natal dispersal and estimated first-year survival. Of 133 banded nestling redstarts

that fledged from 2000 to 2003, 18 (14%; 13 males, 5 females) were later detected as territoryholding breeders, either on the primary study area (12 males, 2 females) or via incidental encounters outside the study area (1 male, 3 females; Fig. 1). Observed mean natal dispersal distance for females was 935 ± 298 m (range = 340–1960 m), significantly greater than that for males (485 ± 75, range = 260–1250 m; onetailed t16 = 1.9, P = 0.04, log-transformed data; Fig. 3). The two females that bred on the study area both became paired territory-holders at age 1 yr. However, of the 12 males that established territories on the study area, six became territory holders when one year old, whereas the other six were not observed defending a territory until they were two years old. MARK-derived CJS estimate of apparent first-year survival (ф1 ) was 0.20 ± 0.07 (c-hat = 1.28) for the subset of data limited to birds resighted in the study area, and 0.27 ± 0.09 (chat = 1.38) when all resightings were included (Table 2). However, because of undetected longdistance natal dispersal from the study area, the

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Fig. 2. Cormack-Jolly-Seber (CJS) estimates of annual survival for breeding territorial male and female Slatethroated Redstarts in Monteverde, Costa Rica. (A) Annual variation in apparent survival, ф. (B) Estimates of mean annual survival, including the CJS mean of apparent survival (ф) and the estimate of true survival (S) derived from the spatially explicit CJS model of Schaub and Royle (2013). Error bars reflect the SE except for the spatial CJS mean for females, where they reflect the Bayesian 50% credible interval.

CJS estimates of ф1 are likely biased underestimates of true first-year survival. Generation of simulated data sets by the spatially explicit model of Schaub and Royle (2013) suggested a corrected estimate of first-year survival of 0.29 (Table 2); an estimated 17 juveniles (13% of 133 fledglings) survived, but dispersed from the study area. Because three of the four longdistance natal dispersers I detected were females, and because 12 of 14 (86%) juveniles that dispersed within the study area were males, it is likely that most undetected cases of natal dispersal from the study area were by females. Annual reproductive success and population growth rate (␭). On average, 70%

of 146 breeding pairs fledged young during a given nesting season, producing a mean of 2.6 ± 0.7 (SD) fledglings for successful pairs and 1.8 ± 1.3 (SD) for all pairs. Although all females age 1 yr or older were part of a breeding territorial pair, 10 territorial males were unpaired and unsuccessful during a given nesting season, making mean annual reproductive success for all territorial males 1.7 ± 1.3 (SD; N = 156). Using the values of survival and reproduction shown in sex-specific life cycle graphs (Fig. 4), the estimated population growth rates (␭) for

females and males were 0.77 and 0.82, respectively. Elasticity analysis for females suggested that first-year survival, subsequent survival, and annual reproductive success all had similar effects on ␭ (elasticities = 0.31, 0.38, and 0.31, respectively). For males, however, adult annual survival had stronger effects on ␭ (elasticity = 0.56) than either first-year survival or annual reproductive success (elasticities = 0.22 and 0.22, respectively).

DISCUSSION Comparison with other parulids. My results, which include estimates of breeding dispersal, natal dispersal, age of first breeding, annual survival, and annual fecundity, provide a critical first step in establishing a basic understanding of the population dynamics of non-migratory tropical warblers, a group that includes many threatened and endangered species (IUCN 2014). My results also add to the growing literature comparing reproductive strategies and demographic characteristics of temperate and tropical birds, comparisons that have contributed significantly to recent advances in avian life history theory (Martin et al. 2000,

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Fig. 3. Sex bias in the frequency distribution of natal dispersal distance by female and male Slate-throated Redstarts. Table 2. Parameter estimates (mean ± SE) of firstyear survival (ф1 ), subsequent survival (фA ) and resighting probabilities (p1 and pA ) of fledgling Slatethroated Redstarts in Monteverde, Costa Rica, based on resightings of 133 color-banded nestlings that fledged from 2000 to 2003. Standard CJS estimates

Parameter ф1 фA p1 pA

Resightings within study area 0.20 ± 0.07 0.47 ± 0.13 0.30 ± 0.13 1.00 ± 0.00

All resightings 0.27 ± 0.09 0.65 ± 0.18 0.22 ± 0.09 0.67 ± 0.17

Spatial CJS estimatesa 0.29 0.59

a

Estimated indirectly from simulations of Schaub and Royle (2013); SE cannot be determined.

2015, Ghalambor and Martin 2001, Martin 2002, Robinson et al. 2010). Costa Rican Slate-throated Redstarts in my study shared many basic demographic similarities with migratory warblers that breed in the north temperate zone. I found that breeding male Slate-throated Redstarts have higher

between-year territory fidelity than females, reflecting a pattern of sex-biased breeding dispersal that is well documented for migratory temperate-breeding warblers (Cilimburg et al. 2002, Hoover 2003, Howlett and Stutchbury 2003, Cline et al. 2013). However, the overall magnitude of breeding dispersal by Slatethroated Redstarts was relatively modest, involving only 26% of females making relatively short dispersal movements (90–240 m); breeding dispersal in migratory parulids, in contrast, typically involves both sexes and a greater range of dispersal distances (Cilimburg et al. 2002, Hoover 2003, Howlett and Stutchbury 2003, Cline et al. 2013). I also documented sex differences in the annual survival of Costa Rican Slate-throated Redstarts, with females having lower estimated survival than males (Fig. 2). Similar femalebiased mortality occurs in many migratory temperate zone warblers (Table 3), a pattern often attributed at least partially to the low breeding site fidelity of females and undetected dispersal from study areas (e.g., Cilimburg et al. 2002, Sillett and Holmes 2002, Howlett and Stutchbury 2003, Cline et al. 2013). In my

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Fig. 4. Sex-specific life cycle graphs for female (A) and male (B) Slate-throated Redstarts in Monteverde, Costa Rica. Plain text numbers indicate estimated annual transition probabilities from one stage to the next. Numbers in italics indicate estimated annual sex-specific production of fledged young, assuming a 1:1 sex ratio at fledging.

study, however, I used a spatially explicit CJS model (Schaub and Royle 2013) that employs information about known breeding dispersal movements within the study area to correct for undetected breeding dispersal from the study area (Fig. 2B). Thus, for Slate-throated Redstarts, the observed sex differences in estimated survival likely reflect sex differences in true survival, not just sex differences in breeding dispersal. Increased female exposure to predators during the nesting season, when females incubate eggs and brood developing nestlings, probably contributes to the higher annual mortality of females (e.g., Reidy et al. 2009). For Slate-throated Redstarts, however, that cannot be the entire explanation; during 2003–2004, for example, when the female mortality rate was especially high (Fig. 2A), nearly all female mortality occurred outside of the nesting season. The relatively low annual survival of female Slate-throated Redstarts contributes to another demographic characteristic that the species shares with many temperate-breeding migratory warblers: the presence of unpaired males and male floaters. Of 12 males banded as nestlings that eventually settled on my study area as

territory holders, six did not do so until they were two year old. The absence of these males as territory holders when one year old cannot be explained entirely by failure to detect them; four (67%) of the 2-yr-olds settled on territories that had been unambiguously either unoccupied or occupied by another male in the previous year. It is likely therefore that at least some 1yr-old males do not defend territories, but are floaters, a phenomenon well established in both temperate zone warblers (Marra and Holmes 1997, Bayne and Hobson 2001) and tropical passerines (Smith 1978, Fedy and Stutchbury 2004). The existence of male floaters in Slatethroated Redstarts is also supported by two cases where banded paired territorial males disappeared during the nesting season and both were immediately replaced by unbanded immigrant males. However, my results also suggest that few or no 1-yr-old females are floaters. Only two females banded as nestlings later bred on the study area, but both nested initially when one year old. In addition, in three of five years of my study, unmated males were present in the study population, including three in 2000, none in 2001 and 2002, one in 2003, and six in 2004. In 2004, following a year of exceptionally

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Table 3. Demographic characteristics of migratory temperate and non-migratory tropical wood-warblers (Parulidae). Annual adult survival

Connecticut

0.47

Tennessee

0.43

0.62

3.0

Bulluck et al. 2013

Ontario

0.48

0.62

2.7

Tennessee

0.47

0.53

3.9

Bulluck et al. 2013 Petit 1999

Location

Ovenbird (Seiurus aurocapilla) Worm-eating Warbler (Helmitheros vermivorum) Golden-winged Warbler (Vermivora chrysoptera) Golden-winged Warbler Prothonotary Warbler (Protonotaria citrea) Prothonotary Warbler Hooded Warbler (Setophaga citrina) Cerulean Warbler (Setophaga cerulea) Cerulean Warbler Black-throated Blue Warbler (Setophaga caerulescens) Golden-cheeked Warbler (Setophaga chrysoparia) Wilson’s Warbler (Cardellina pusilla)

Missouri

Females

Illinois Pennsylvania

0.11 0.43

Ontario Michigan New Hampshire

0.40

Texas California

Mean ± SD N

a

Annual

Males survival fecunditya Sources Migratory temperate warblers 0.62 2.1 Porneluzi and Faaborg 1999 0.73 2.2 Vitz et al. 2013

Species

Slate-throated Redstart (Myioborus miniatus)

First-year

0.45

0.52

3.2

0.54

2.2

0.59 0.51

4.3

0.46

2.2

0.52

McKim-Louder et al. 2013 Chiver et al. 2011 Jones et al. 2004 Rogers 2013 Holmes et al. 2005 Ladd and Gass 1999 Chase et al. 1997, Ammon and Gilbert 1999

0.45 ± 0.03 0.57 ± 0.08 0.11 2.9 ± 0.8 7 11 1 9 Non-migratory tropical warblers Costa Rica

0.43

0.56

0.29

1.8

This study

Fledged young per female.

high female mortality (Fig. 2A), unmated males constituted 17% of the territorial males in the population. The presence of these unmated males suggests that a surplus of unpaired females was not normally present in the study popula-

tion. Studies of migratory temperate-breeding warblers have also documented the frequent presence of unpaired males (Probst and Hayes 1987, Porneluzi and Faaborg 1999, Bayne and Hobson 2001).

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Slate-throated Redstarts differ markedly from temperate-breeding warblers in fecundity. Estimated annual fecundity of the Monteverde population was 1.8 fledglings per female, considerably lower than that of migratory warblers that breed in North America (Table 3). This difference in fecundity, typical in comparisons of tropical and temperate birds (e.g., Martin et al. 2000), reflects the small mean clutch size (2.9), low nest success (40%), and low incidence of double brooding (<1%) that characterize the Monteverde study population (Mumme 2010) and other tropical parulids (Cox and Martin 2009, Ruggera and Martin 2010). Thus, even though tropical warblers live year-round in environments with relatively little seasonality in temperatures, they are highly seasonal breeders with a low frequency of double brooding and lower annual fecundity than their temperatebreeding relatives. Surprisingly, even though Slate-throated Redstarts in Monteverde are non-migratory and not subject to the mortality risks associated with long-distance migration, estimated values of female and male annual survival were virtually identical to the means of values reported for migratory warblers that breed in North America (Table 3). Few comparative data are available for non-migratory parulids. Annual survival of Slate-throated Redstarts in Costa Rica is roughly comparable to that reported for Adelaide’s Warblers (Setophaga adelaidae) in Puerto Rico (0.55; Faaborg and Arendt 1995), but much lower than the mean annual adult survival reported for Slate-throated Redstarts (0.79) and Threestriped Warblers (Basileuterus tristriatus, 0.76) in Venezuela (Martin et al. 2015) and nonmigratory Two-banded Warblers (Myiothlypis bivittata, 0.83) and Pale-legged Warblers (M. signata, 0.87; Ghalambor and Martin 2001, Martin 2002) in subtropical Argentina. Comparative analyses that relate adult mortality to clutch size and incubation period (Ghalambor and Martin 2001, Martin 2002) also suggest that the observed annual adult survival of Slatethroated Redstarts in Monteverde is considerably lower than expected. Given their mean clutch size (2.9) and incubation period (14.2 d; Mumme 2010), expected mean annual survival for adult Slate-throated Redstarts in Monteverde would be in the range of 0.65–0.75 (Fig. 1C in Ghalambor and Martin 2001, Fig. 6B in Martin 2002).

J. Field Ornithol.

Estimated first-year survival for fledgling Slate-throated Redstarts in Monteverde was 0.29, which is likely a significant underestimate due to undetected long-distance natal dispersal from the study area, particularly by females. Unfortunately, little relevant data from other warblers, either temperate or tropical, is available for comparison (Table 3). In virtually all previous studies of migratory warblers, high apparent natal dispersal has meant that return of birds banded as nestlings occurs too rarely to provide a reliable estimate of first-year survival (e.g., Holmes et al. 2005). The only robust estimate, ф1 = 0.11 (Table 3), is surprisingly low and derived from a large-scale study of juvenile survival and natal dispersal in cavitynesting Prothonotary Warblers (Protonotaria citrea) in Illinois (McKim-Louder et al. 2013). However, even this estimate, based on exhaustive efforts to detect all dispersers within 30 km of the primary study area, could be a significant underestimate of true first-year survival if the distribution of natal dispersal distance in Prothonotary Warblers includes a tail of undetected long-distance dispersal events (Koenig et al. 1996). Additional work is needed to determine if estimates of first-year survival for Prothonotary Warblers and Slate-throated Redstarts are representative of other temperate and tropical warblers. I also found evidence of female-biased natal dispersal by Slate-throated Redstarts (Fig. 1, 3), a pattern typical of birds (Greenwood 1980, Dale 2001, Mabry et al. 2013, Dobson 2013). Unfortunately, the low natal return and recruitment rates of migratory parulids means that few comparative data on natal dispersal distance are available for other warblers. The only exception comes from the study of Prothonotary Warblers in Illinois, where males and females had similar natal dispersal distances (McKim-Louder et al. 2013). Nonetheless, female-biased natal dispersal likely occurs in at least some other parulids. For example, of 108 nestlings banded in a study of Swainson’s Warblers (Limnothlypis swainsonii) in Arkansas, the nine individuals that returned to the study area as breeders were all males (Anich et al. 2010). Estimated population growth rate (␭) and uncertainty in estimates. Because es-

timated population growth rate (␭) was <1 for both females and males in my study population, the demographic parameter estimates presented

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Fig. 5. Values of first-year and adult annual survival required for an intrinsic population growth rate (␭) = 1 for male and female Slate-throated Redstarts, assuming reproductive parameters as shown in Fig. 4.

here should be viewed with some caution. First, the calculated value of first-year survival (0.29) is almost certainly an underestimate because of undetected long-distance natal dispersal. Although I attempted to correct for dispersal off of the study area using the spatial CJS model of Schaub and Royle (2013), the correction was based on the observed variance in natal dispersal distance. The strong sex bias in observed natal dispersal distance (Fig. 3) suggests that I failed to detect many instances of long-distance dispersal by females and have underestimated true variance in natal dispersal. Underestimation bias due to undetected dispersal is also possible for adult survival, but less likely. I observed no instances of breeding dispersal by males and only infrequent short-distance breeding dispersal by females, which was incorporated into a corrected estimate of female survival (Fig. 2B). Second, given that ␭ < 1 for both females and males, the Monteverde study population may be a demographic sink that is sustained as a stable population only by immigration from more productive source populations. This hypothesis is plausible given that much of the study area is bisected by roads and trails and

altered by human influence, including older agricultural development and more recent residential development. Habitat modifications and other human influences may have contributed to the surprisingly low adult annual survival, resulting in ␭ < 1. Human activities may have also depressed annual fecundity, but this is less likely. Nests in human-modified habitats (on road and trail banks) had similar success rates as nests on natural slopes (Mumme 2010). In addition, nesting success of Slate-throated Redstarts in Monteverde (40%; Mumme 2010) was considerably higher than that of Slate-throated Redstarts (15%, Ruggera and Martin 2010) and Three-striped Warblers (22%, Cox and Martin 2009) in Venezuela. The quantitative effects of uncertainty in survival estimates on population growth rate (␭) can be visualized in Figure 5, which shows the combinations of values of first-year and adult survival that would produce a stable population, assuming fecundity parameters as shown in Figure 4. For example, if true first-year survival were 0.45 instead of 0.29, a plausible scenario given the underestimation bias associated with this estimate, a stable population (␭ = 1)

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would be achieved if annual survival of females and males were 0.59 and 0.68, respectively (Fig. 5), values that are 21% and 37% higher than the actual estimates (Fig. 2B), but more consistent with predictions from comparative analyses relating annual survival to clutch size and incubation period (Ghalambor and Martin 2001, Martin 2002).

CONCLUSION

Despite questions surrounding the quantitative estimates of first-year and adult survival, my results provide the first complete demographic portrait and population model of a nonmigratory tropical parulid. They characterize Slate-throated Redstarts as a species with high male territory fidelity, female-biased dispersal, female-biased annual mortality, and a surplus of non-breeding males existing as either unpaired territory holders or 1-yr-old floaters. My results also suggest that Slate-throated Redstarts are strongly seasonal breeders with small clutch sizes, a low incidence of double-brooding, and low annual fecundity compared to temperatebreeding warblers. This demographic characterization provides a starting point for the development of population models and conservation plans for non-migratory tropical and subtropical parulid warblers (Heppell et al. 2000, Sæther and Bakke 2000, Faaborg et al. 2010, Cox et al. 2014), many of which are of conservation concern (IUCN 2014). Elasticity analysis of the demographic model (Fig. 4) indicates that the growth rate (␭) of the Monteverde population of Slate-throated Redstarts is more sensitive to changes in annual survival than changes in fecundity, a result typical for birds (Sæther and Bakke 2000). I also found evidence of high annual variation in adult survival (Fig. 2A) and estimated that 75% of the variance in adult survival appears to be attributable to ecological factors (process variance) and only 25% to sampling variance. The presence of significant annual variation in a critical demographic parameter has important implications for population viability analysis and the design of monitoring programs for populations of tropical warblers (Sæther and Bakke 2000), suggesting that multi-year studies will be necessary to capture the range of natural variation in key demographic processes.

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ACKNOWLEDGMENTS

I am grateful to M. Hidalgo of the Estaci´on Biol´ogica Monteverde (EBM) for allowing me to work on EBM properties. Many other Monteverde landowners, including C. Echeverr´ıa, J. Forrest, W. Haber, S. and B. Kendall, S. Kinsman, A. and K. Masters, J. and P. Richards, B. Young, and W. Zuchowski provided me with access to their land. I thank P. Cygan, M. Galatowitsch, P. Jabło´nski, L. Petell, S. Sargent, T. Stawarczyk, U. Valdez, and S. Wissinger for field assistance, and P. Tanimoto for alerting me to the presence of banded redstarts outside my study area. A. Mora and F. Campos of the San Jos´e office of the Organization for Tropical Studies offered helpful assistance with permits, and M. Schaub provided generous advice regarding survival analyses. I also thank J. Faaborg, T. Martin, and two anonymous reviewers for very constructive criticisms of an early draft of the manuscript. Financial support was provided by grant 7194–02 from the Committee for Research and Exploration of the National Geographic Society, and by the Allegheny College Academic Support Committee.

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