Open Access
Translator Disclaimer
4 April 2020 Contrasting the suitability of shade coffee agriculture and native forest as overwinter habitat for Canada Warbler (Cardellina canadensis) in the Colombian Andes
Ana M. González, Scott Wilson, Nicholas J. Bayly, Keith A. Hobson
Author Affiliations +
Abstract

In the Neotropics, coffee production occurs on a large scale in some of the planet′s most biodiverse regions: tropical mountains. Coffee production systems involving shade trees are considered to have a lower impact on biodiversity than alternative sun coffee. To date, the majority of evidence for the value of shade coffee plantations has not taken into account the relative quality of this habitat compared to the native forests they replaced. We determined the suitability of shade coffee and forest as winter habitat for Canada Warbler (Cardellina canadensis) by comparing variation in the likelihood of capturing individuals, seasonal changes in body condition, and estimates of annual survival between the 2 habitats. We also determined the effect of the strong 2015–2016 El Niño event on survival. Males were relatively more likely to be captured in forest than females and this likelihood increased during drier years. Body condition change over the winter and apparent annual survival were similar for individuals that used forest and coffee. However, condition and survival decreased in both habitats during the El Niño year. Apparent survival was also lower for individuals carrying a radiotag or geolocator. Our findings suggest that shade coffee with high canopy cover and height offers similar benefits to forest in terms of body condition and survival. Landscape conservation approaches, promoting diverse matrices of structurally complex shade coffee and forest might best ensure long-term survival in Neotropical migrants like Canada Warbler.

INTRODUCTION

Migratory birds are declining globally due to threats associated with habitat loss, climate change, and human exploitation (Wilcove and Wikelski 2008). In the Western hemisphere, population declines in Nearctic–Neotropical migratory songbirds are particularly severe for species that overwinter in northern South America, including the Canada Warbler (Cardellina canadensis), Cerulean Warbler (Setophaga cerulea), Golden-winged Warbler (Vermivora chrysoptera), and Olive-sided Flycatcher (Contopus cooperi) (International Union for Conservation of Nature 2016, Sauer et al. 2017). These species depend on diverse montane habitats in the tropical Andes during the winter. However, extensive deforestation has occurred in this region with estimates suggesting that <10% of mid-elevation montane forest remains (Henderson et al. 1991). This loss of habitat is known to be driving numerous endemic species towards extinction (Rueda-Almonacid et al. 2004, Renjifo et al. 2016) and has recently been linked to declines in migratory species spending the winter in the Andes (González-Prieto et al. 2017, Kramer et al. 2018, Wilson et al. 2018).

With the extensive loss of native forests, shade coffee plantations, which include canopy trees, are one of the few remaining “habitats” with forest-like vegetation in many mid- to high-elevation mountain ranges in Latin America (Perfecto et al. 2005, González-Prieto 2018). The transformation of shade coffee to full-sun coffee plantations (i.e. those with no canopy trees) results in a much greater loss of biodiversity compared with the conversion of native forest into shade coffee (De Beenhouwer et al. 2013). This effect is particularly strong in Latin America compared with other coffee-producing regions of the world (De Beenhouwer et al. 2013). As such, conservation efforts for both resident fauna and overwintering migratory species are now focusing on shade coffee agroecosystems to address the widespread loss of natural habitats (Perfecto et al. 1996, Perfecto and Vandermeer 2008, Caudill et al. 2015). Several studies in the Caribbean and the Americas have shown that Nearctic–Neotropical migrants are equally or even more abundant in shade coffee compared with native forest (Wunderle Jr. and Latta 1996, Tejada-Cruz and Sutherland 2004, Bakermans et al. 2009), although with variation among species (McDermott and Rodewald 2014, Céspedes and Bayly 2019). However, the presence of individuals in a habitat alone does not necessarily indicate that the habitat is high quality (Van Horne 1983, Garshelis 2000) or contributes to the maintenance of populations. Assessing the effect of occupying shade coffee vs. native forest on the overwinter ecology and demographics of Neotropical migrants is critical if we are to identify the factors driving population declines or limiting population growth, and to predict how environmental changes will impact migratory populations.

The quality of winter habitat limits the maintenance and survival of Neotropical migratory songbirds during the winter (Sherry and Holmes 1996, Sherry et al. 2005, Studds and Marra 2005) and can produce residual effects that carry over to migration and breeding, influencing individual fitness and population dynamics (Marra et al. 1998, Norris et al. 2004, Wilson et al. 2011, Rushing et al. 2016). Habitat quality for Neotropical migrants is often assessed by measuring variables such as sex ratios, individual body condition, and survival (Johnson 2007). Higher proportions of dominant males are expected in the habitats of highest quality (Marra 2000), and this distribution pattern is expected to have demographic consequences. For example, American Redstarts (Setophaga ruticilla) occupying poor-quality female-biased habitats in Jamaica had a steeper decline in body condition over the winter and lower annual survival than individuals in high-quality male-biased habitats (Marra and Holmes 2001). The results of past studies on the overwinter condition of individuals in shade coffee are mixed. In the Venezuelan Andes, for example, Neotropical migrants occupying shade coffee during the winter increased their body condition through the season (Bakermans et al. 2009), whereas in the Caribbean, body condition of individuals in shade coffee was either constant or declined (Strong and Sherry 2000, Johnson et al. 2006). In the Colombian Andes, Neotropical migrants in shade coffee have been found to be in poor condition on average and condition through the winter improved only for some species (Colorado and Rodewald 2017). Fewer studies have examined the demographic consequences of shade coffee use by migratory birds. In Jamaica, overwinter and annual apparent survival of American Redstarts in shade coffee and natural habitats were comparable (Johnson et al. 2006). In the Dominican Republic, annual return rates for 3 Neotropical migrants were similar between shade coffee and natural forests (Wunderle and Latta 2000). To our knowledge no study has simultaneously estimated the survival of declining migrant birds in shade coffee and native forest in mainland areas of the Neotropics or in critical wintering regions of the tropical Andes.

One of the challenges in assessing the effects of occupying shade coffee vs. native forests during the winter is that individual condition and apparent survival can vary spatially and temporally due to a range of factors. In many regions of the Neotropics, for instance, climatic conditions related to phenomena such as the El Niño Southern Oscillation (ENSO) can have dramatic effects on moisture and food availability (Ropelewski and Halpert 1987, Jaksic 2001). In turn, these factors are important determinants of winter habitat quality for Neotropical migrant birds (Studds and Marra 2007, Smith et al. 2010). Because such effects vary over time and space, the best assessment of the habitat quality of shade coffee should include simultaneous measures in coffee relative to the local native forest from where those plantations were carved (Van Horne 1983, Vickery et al. 1992), while simultaneously testing for possible differential effects of climatic events such as ENSO.

In this study, we determined the relative quality of adjacent shade coffee plantations and native forest as winter habitat for Canada Warbler in the Eastern Andes of Colombia. Canada Warbler is listed under Canada's Species at Risk Act and over 60% of the breeding population has been lost during the last 50 yr (Environment and Climate Change Canada 2017). Over 50% of the winter distribution of this species lies within the highly deforested and fragmented Andean forests of Colombia, where native forest and shade coffee plantations at mid-elevations are habitats widely used by the species (Céspedes and Bayly 2019). Canada Warbler shows longitudinal segregation across the Andes of Colombia, giving rise to moderate migratory connectivity between breeding and wintering populations (González-Prieto et al. 2017). Individuals spending the winter at our study sites were found to have likely origins mainly from steeply declining eastern breeding populations in North America (González-Prieto et al. 2017, Sauer et al. 2017, Wilson et al. 2018).

We assessed the relative quality of shade coffee as winter habitat by addressing 3 questions: (1) Is there variation in the likelihood of capturing individuals in shade coffee vs. forest? (2) Do individuals maintain body condition similarly over the winter in the 2 habitats? (3) Is apparent survival different for individuals occupying the 2 habitats during the winter? We hypothesized that the simplified vegetation composition and structure of shade coffee may be inappropriate to maintain overwinter energy demands. Therefore, we expected that individuals in shade coffee relative to native forest would (1) be predominantly females, (2) be in poorer body condition at the end of the winter, and (3) have lower apparent annual survival. We also determined the effect of the ENSO on the survival of birds occupying both habitats given the potential for climate to influence year-to-year patterns of individual condition and demography. The ENSO influences rainfall patterns in the study region with drier conditions during El Niño events (Ropelewski and Halpert 1987, Jaksic 2001). We expected drier than average conditions induced by El Niño to have a negative effect on apparent survival across habitats by lowering habitat quality. If our above 3 predictions about shade coffee being a poorer quality habitat are true, we also predicted that differences in condition and apparent survival for individuals in the 2 habitats would be accentuated during El Niño years.

METHODS

Study Sites

Fieldwork was carried out from December to March over 5 field seasons (2013–2014, 2014–2015, 2015–2016, 2016–2017, and 2017–2018) in 3 study sites located on the western slope of the Eastern Andes in Colombia (Figure 1): “Hacienda La Fragua” (shade coffee 1,400 meters above sea level [m.a.s.l.], forest 1,500 m.a.s.l.), “Los Vientos” (shade coffee and forest 1,350 m.a.s.l.), and “La Vuelta” (shade coffee 1,400 m.a.s.l., forest 1,700 m.a.s.l.). Sites were equidistant and separated by 5 km. In La Fragua, shade coffee and forest habitats were separated by 300 m, in Los Vientos by 500 m, and in la Vuelta by ∼1 km. Shade in coffee plantations was provided by native trees remaining from the original native forest cover. Native shade species included Inga ssp., Simarouba amara, Cordia alliodora, Trichanthera gigantean, Sebastiania commersoniana, Alfaroa colombiana, Anacardium excelsum, Senna spectabilis, and Hevea pauciflora. Across our study sites, the average canopy height in coffee plantations was mean ± standard deviation (SD) = 18.8 ± 3.6 m (n = 68) and the average shade cover was 44.5 ± 17.1% (n = 68) (Céspedes and Bayly 2019). Our sites did not include sun coffee plantations and hereafter we refer to shade coffee as “coffee”.

Individual Capture and Measurements

We carried out constant-effort mist netting at fixed banding stations from 1 December to 30 March during 8 days a month in each habitat. Weather permitting, 12–15 mist nets (30-mm mesh) were operated from 0600 to 1100 hours and from 1500 to 1730 hours. All captured birds were fitted with a U.S. Fish and Wildlife Service numbered aluminium band and processed and released at the capture site. We determined age and sex (Pyle 1997), and recorded body mass (±0.1 g, using an electronic balance) for each bird at first capture and for all birds recaptured. Individuals were aged as hatch year and after hatch-year during December, and as second year and after second-year after 31 December (Pyle 1997). We refer to hatch-year and second-year birds as immatures, and after hatch-year and after second-year as adults from herein.

Statistical Analysis

Likelihood of capturing individuals in forest vs. coffee. We used generalized linear models with habitat (coffee = 0, forest = 1) as a response variable to assess the likelihood of capturing a higher number of individuals in forest or coffee during the winter. We compared a set of 5 candidate models, including a null model, to test whether the likelihood of capturing individuals in each habitat varied by year, sex, the additive effect of sex on year, or the interaction of year and sex. We ranked candidate models by second-order Akaike's information criterion (AICc) and estimated the relative likelihood of each model with AICc weights (wi). Models within 2 units of the top model were considered to have equal support, except in cases where they differed by only one parameter and the more parameterized model had a higher AICc (Burnham and Anderson 2002). All analyses were performed in the statistical software program R (R Core Team 2019). Models were selected using package AICcmodavg in R (Mazerolle, 2017). We used the coefficients from the model with the highest support to obtain the odds, odds ratios, and converted odds ratios to percent change of the odds of being captured in forest. We checked model assumptions by visually examining deviations from uniformity.

FIGURE 1.

Location of study sites on the western slope of the Eastern Andes in Colombia: Hacienda La Fragua, Los Vientos, and La Vuelta. Study sites were separated by 5 km.

img-z4-4_01.jpg

Seasonal change in body condition. A Wilcoxon signed-ranks test indicated that males were structurally larger, having longer wings than females (W = 3,101, P < 0.001; males, mean ± SD = 63 ± 2.03 mm; females, 61 ± 1.59 mm). Mass and wing length in males (Pearson's correlation r = 0.39, n = 133, P < 0.001) and females (Pearson's correlation r = 0.33, n = 123, P < 0.001) were correlated. To assess seasonal changes in condition, we therefore used the residuals of the linear regression of mass on wing chord as an index of body condition to account for differences in structural size (Labocha and Hayes 2012). After pooling sites, we estimated seasonal body condition changes in the population based on all individuals measured at first capture during the winter. Day 1 was equal to December 1.

We conducted the analyses in a 2-stage process. We first assessed whether trends in seasonal condition were linear or nonlinear by running a linear model (I), a quadratic model (I + I2), and a polynomial model (I + I2 + I3), where “I” was capture day ( Supplementary Material Table S1). Model selection was carried out using AICc as described above. The model structure of the top ranked model ( Supplementary Material Table S1) was selected to be included in stage 2 (see below).

In the first stage, model selection suggested that the pattern of seasonal change in body condition was quadratic during most years and when years were pooled ( Supplementary Material Table S1). Therefore, in the second stage we modeled body condition as a quadratic function of capture day and included the variables habitat, age, sex, and year. Variables were entered as an interaction with capture day to ensure that we modeled the effect of these variables on the seasonal pattern of change in body condition and not as an additive effect. We entered capture time as an additive effect in each model to account for within-day changes in body condition. Results of individual years are presented in  Supplementary Material Table S2. We present and discuss the results of years combined (Table 1).

Annual apparent survival. There were a small number of cases where individuals switched habitats between years and, therefore, we modeled apparent survival using a multistate mark–recapture approach (Lebreton et al. 2009) in program MARK (White et al. 2006). A multistate framework provides an estimation of state-specific probabilities of apparent survival and recapture as well as the transition probabilities between states (i.e. habitats). With this framework, the encounter history for each individual at time t contained an “F” if it was in forest or a “C” if it was in coffee. As an example, we describe the probabilities for an individual i in forest at time t. This individual can either survive between the winters of t and t + 1 and return to the study area with probability (ϕF) or it can die or emigrate with probability (1 – ϕF). The individual's survival probability between years is thus conditional on the habitat it was in at the start of the interval. Also, note that we are estimating apparent survival in this analysis and cannot separate mortality from emigration outside of the study area in year t + 1. Thus, it remains possible that the habitat an individual is in at time t influences whether it returns to the study area in year t + 1. If the individual survives the interval and returns to the study area it may return to the same forest habitat with probability ψFF or move to coffee with probability ψFC = 1 – ψFF. Conditional on the individual surviving the interval and returning to the study area, it can then be recaptured at time t with probability pF in forest or pC in coffee.

TABLE 1.

Candidate model set for predicting body condition change during the winter in Canada Warbler in Colombia from December 1 to March 30 across 4 overwintering periods (2013–2014, 2014–2015, 2015–2016, and 2016–2017). D = Day, H = Habitat, Time = Capture time. k is the number of parameters; ΔAICc are the AICc differences; wi is the Akaike weight support for each model.

img-z5-6_01.gif

We began by modeling recapture probability as a function of age, sex, and habitat; the recapture probability model with the greatest support based on AICc was then used to examine which factors influenced apparent survival. Because so few individuals switched habitats between years, the probability of movement between habitats was only estimated as a single average value without covariates.

While accounting for recapture and movement probabilities, we then modeled apparent survival as a function of habitat (coffee, forest), age (immature, adult), sex (male, female), site (Los Vientos, La Fragua, La Vuelta), tag effects, time, and ENSO effects. Tag effects were tested because ∼33.3% of the individuals in the analysis had a coded very high frequency (VHF) radiotag (Model NTWB-2, 0.35 g) or a light-level geolocator (Model Intigeo-W30Z11-DIP, 0.32 g) during one year of the study, and research elsewhere has reported on the potential for negative effects of tracking technology on the apparent survival of migratory passerines (reviewed in Constantini and Møller 2013). We predicted that apparent survival would be lower for individuals in the year following application of the tag and this potential influence was included as an additive effect. A strong El Niño event occurred during the winter of 2015–2016 and we incorporated this event as a categorical variable in the model, allowing for differences in survival following the El Niño year vs. the other 3 years. We also included a time-dependent model, which allowed for a separate apparent survival estimate for each year.

Apparent survival probabilities for males and females in each habitat were obtained by model averaging using the same approach as for Marra et al. (2015). Because some models had annually variable survival due to covariate effects, model averaging yielded annual estimates of apparent survival. The average of these annual means is reported as the expected mean apparent survival probability for the group with standard errors obtained using the Delta Method (Powell 2007) in R (R Core Team 2019) with package emdbook (Bolker 2019). We did not use model averaging for the model coefficients because of the challenges in their interpretation (Cade 2015, Banner and Higgs 2017) and instead report the coefficient estimates and standard errors from the top model. We used a median ĉ test to examine model goodness-of-fit (GOF). Because it is not possible to test GOF with models that contain individual covariates in program MARK, we used the most parameterized model without individual covariates. We then corrected for overdispersion by adjusting AICc values to quasi-AICc if ĉ > 1.0 (Burnham and Anderson 2002).

RESULTS

Likelihood of Capturing Individuals in Forest vs. Coffee We assessed the likelihood of capturing a higher number of individuals in forest or coffee in 284 Canada Warblers captured with a banding effort of 45,085 mist net hr over 4 winters (one mist net hour = one 12-m net open during 1 hr). Banding effort was 0.2% and 17% higher in forest than coffee during 2013–2014 and 2014–2015, respectively, and 4% and 12% higher in coffee than forest during 2015–2016 and 2016–2017, respectively ( Supplementary Material Table S3).

The top ranked model had 61% of model weight and included an effect of year with the additive effect of sex ( Supplementary Material Table S4). Captured females were more likely to be in coffee than in forest in most years whereas males were more likely to be captured in coffee in 2013–2014 and 2014–2015 and in forest in 2015–2016 and 2016–2017. Confidence intervals for both sexes overlapped 1 in all years but 2014–2015 (Figure 2;  Supplementary Material Tables S4 and  S5). Visual inspection of residual plots indicated that the top ranked model complied with the assumptions.

FIGURE 2.

Annual and sex-specific variation in the likelihood of capturing Canada Warbler in shade coffee vs. forest during the winter on the western slope of the Eastern Andes of Colombia. Odds and 95% confidence intervals (CI) of capturing males and females in forest from winter 2013 (2013–2014), 2014 (2014–2015), 2015 (2015–2016), and 2016 (2016–2017). An El Niño event occurred during winter 2015.

img-z6-11_01.jpg

Seasonal Change in Body Condition

We modeled seasonal changes in body condition in 260 individuals captured over the 4 winters (2013–2014, n = 61; 2014–2015, n = 69; 2015–2016, n = 85; 2016–2017, n = 45). When years were combined, a quadratic model including a difference in seasonal gain in body condition between years received the greatest support (Table 1). A model including year and habitat was ranked below that containing just year, suggesting that habitat had no clear effect on the seasonal pattern of body condition change in Canada Warbler in our sample. However, when analyzing years individually, there was support for body condition being higher throughout the season in forest relative to coffee in 2013–2014 but not in other winters ( Supplementary Material Table S2). In general, body condition declined from early to mid-winter and increased at the end of the season. Birds showed the lowest condition during 2015–2016 (Figure 3).

Apparent Survival

Estimates of apparent survival were based on 330 individuals marked between winter 2013–2014 and 2016–2017, including 228 immatures and 82 adults, 163 females and 167 males, and 197 individuals marked in coffee and 133 marked in forest. Of the 330 individuals, 93 had been fitted with a light-level geolocator or a radiotag in at least one year (see  Supplementary Material Table S6 for further details). Forty-two individuals were recaptured the year after they were marked, 33 in just one year and 9 individuals in 2 subsequent years. Average annual recapture probabilities varied by sex and habitat and were higher for females than males and higher for individuals in forest than coffee (Table 2). Recapture probabilities did not vary by age at first capture (Table 3,  Supplementary Material Table S7). Two of the 44 individuals that survived and returned to the study area switched habitat types with an estimated transition probability of 0.028 ± 0.019. One of these individuals was a female first marked in forest and recaptured in coffee the following year, while the other was a male marked in coffee and recaptured in forest 2 yr later. GOF tests with the median ĉ procedure showed no evidence of overdispersion (ĉ = 0.70).

FIGURE 3.

Seasonal body condition change in Canada Warbler captured in shade coffee plantations and forest on the western slope of the Eastern Andes of Colombia across 4 winters (December to March) 2013–2014, 2014–2015, 2015–2016, and 2016–2017. Lines are the predicted trajectory of the top ranked model Day:Year + Day2:Year + Time. Day 1 = December 1. Body condition = residuals of regressing mass on wing length. Time = capture time.

img-z7-4_01.jpg

We found evidence that individuals carrying radiotags or geolocators (i.e. tags) had lower average apparent survival than those without tags (^β = –1.19 ± 0.63). The coefficients from the top model in Table 3 predicted that the apparent survival for an individual tagged in year 1 would be 0.12 lower than an individual without a tag, due to higher mortality and/or emigration. Because of this influence, tag effects were included as an additive effect in all models. While including these tag effects, we found little support for our prediction that apparent annual survival would be lower for individuals occupying coffee during the winter than those occupying forest (Table 2). Model-averaged estimates of apparent annual survival were slightly higher (5%) for males in forest than males in coffee but were the same for females in the 2 habitats (Table 2). Males on average had a 4% higher annual apparent survival relative to females in coffee and 13% higher in forest but there was uncertainty in these estimates and models with sex had lower support than models without sex (Table 3).

While a fully time-dependent model had the greatest support, there was also strong evidence for a negative influence of El Niño year on apparent survival (^β = –1.69 ± 0.49, Table 3). The addition of ENSO led to a reduction in AICc of 11.95 units compared with the same model with only a constant time effect (Table 3). Apparent survival during the El Niño year was substantially lower than the other years, ranging from only 0.15 for females in coffee to 0.22 for males in forest (see  Supplementary Material Figure S1). We predicted that negative effects of El Niño event would also be greater for individuals in coffee than forest but found no evidence for this effect (AICc of the interaction model was 1.78 units higher than the additive model; Table 3).

TABLE 2.

Sex and habitat-specific apparent and survival recapture probabilities (mean ± SE) for Canada Warbler spending the winter on the western slope of the Eastern Andes of Colombia. Estimates were obtained by model averaging across the full candidate set in  Supplementary Material Table S7. See  Supplementary Material Figure S1 for annual estimates of apparent survival.

img-z8-4_01.gif

TABLE 3.

Summary of model selection results for the probabilities of annual apparent survival (ϕ) and recapture (p) of Canada Warblers at 3 sites in Colombia. Models are those with 95% of model support (see  Supplementary Material Table S7 for all candidate models tested). Variables include time = annual variation, ENSO = El Niño Southern Oscillation effect, tag = effect of radiotag or light-level geolocator, age = juvenile vs. adult, habitat = shade coffee vs. forest, and sex = male vs. female. Covariates were not included for movement among habitats between years (ψ). k is the number of parameters; ΔAICc, the change in Akaike′s Information Criterion; wi is the Akaike weight support for each model. The intercept only model for apparent survival with sex and habitat effects on recapture and no covariates for movement had a ΔAICc of 20.36.

img-z8-6_01.gif

DISCUSSION

We determined the suitability of shade coffee plantations and native forest as winter habitat for the declining Canada Warbler by comparing sex-specific variation in the likelihood of capturing individuals in each habitat, seasonal changes in condition, and annual survival between the 2 habitats. Males were slightly more likely to be captured in forest than females, and there was no strong effect of habitat on seasonal change in body condition or apparent annual survival. Apparent survival during the El Niño year was substantially lower than the other years. However, we found no evidence for a greater negative effect of El Niño event for individuals in coffee. Taken together, our measures of winter habitat quality suggest that, relative to native forest, shade coffee plantations with optimal conditions such as those at our study sites (high canopy height and cover) can be suitable winter habitats for Canada Warbler.

Sex-specific habitat segregation during the winter, in which males and females occur in different proportions in different habitats, has been reported in several Neotropical migrants (Lynch et al. 1985, Wunderle 1995, Marra 2000, Wunderle and Latta 2000, Latta and Faaborg 2002). One of the mechanisms underlying this habitat distribution pattern is behavioral dominance, where individuals of varying abilities compete for access to critical resources such as food, resulting in a greater proportion of dominant males in the highest quality habitats (Marra 2000). We found some support for our predictions that males may be more likely to be captured in forest than females. For instance, the mean likelihood of capturing a male in forest was higher than that of females and increased to a greater extent during the driest years (2015–2016 and 2016–2017). This result may suggest temporal variation in habitat quality linked to precipitation and its effects on food availability (Studds and Marra 2007, 2011). However, further studies estimating density in each habitat in relation to quality would be needed to evaluate whether annual winter conditions influence sex-specific habitat segregation.

Patterns of change in body condition and survival are consistent with previous research on the Caribbean islands showing that the amount and timing of precipitation during the winter has major effects on habitat quality and overwinter performance of Neotropical migrants in several habitats including shade-grown coffee plantations (Strong and Sherry 2000, Studds and Marra 2007, 2011). For instance, seasonal decline in body condition in both habitats across years was synchronized with the progression of the dry season from the beginning of December until the end of February before slightly increasing from late February to the end of March with the onset of the rainy season.

During the winter, survival is the demographic measure most clearly linked to fitness, and therefore a robust indicator of winter habitat quality for population persistence (Johnson et al. 2006). Contrary to our expectations, we did not find differences in apparent annual survival between individuals that overwintered in coffee and those that overwintered in forest. Previous studies suggest that a decline in body condition during the winter is a strong predictor of annual survival probability in insectivorous birds overwintering in Jamaica (Marra and Holmes 2001, Johnson et al. 2006). While we found evidence for this effect in the influence of El Niño event, we did not observe this pattern among habitats, as in Jamaica (Johnson et al. 2006), which likely explains the similar apparent survival probabilities for individuals in forest and coffee. One possible explanation for the difference between our study and those in the Caribbean is the earlier initiation of the rainy season in Colombia (March) relative to the Caribbean (May), which allowed individuals to recover body condition during late winter in both habitats such that there were no subsequent consequences for apparent survival. Alternatively, it remains possible that within-winter apparent survival is lower for individuals in coffee compared with forest but that this effect is minimized across the other stages of the annual cycle after Canada Warblers have departed from the wintering grounds. Further studies comparing within- vs. between-winter survival would be useful to examine these possibilities.

A decrease in apparent survival in individuals carrying tags (i.e. radiotags or geolocators) is consistent with previous research reporting a negative effect of geolocators on birds (Constantini and Møller 2013) but contrasts with recent findings suggesting only slightly negative effects of geolocators on survival (Brlík et al. 2019). In our study, 28% of marked individuals carried a radiotag or geolocator in at least one year and of those that did, 63% carried a radiotag while 37% carried a geolocator. We did not separately examine the influence of each type as we were only attempting to control for the effects of tags that had been applied for other purposes over the course of this study. Further studies assessing the differential effects of geolocators vs. radiotags on small Neotropical migrant birds would allow us to better understand the impacts of this technology, including whether any observed decreases in apparent survival are due to an increase in mortality or a greater propensity to disperse elsewhere.

For Neotropical migratory songbirds, moisture and food availability are the main drivers of winter habitat quality (Sherry et al. 2005, Brown and Sherry 2006, Smith et al. 2010). In turn, these are some of the most important ecological factors limiting physical condition and survival of migrants during the winter (Sherry and Holmes 1996, Sherry et al. 2005, Studds and Marra 2005). We found evidence that drought conditions induced by the 2015–2016 El Niño event ( Supplementary Material Figure S2) amplified the negative effects of seasonal variation in rainfall on physical condition and annual survival. For instance, during the El Niño year, the decline in body condition and survival was steeper in both habitats. Within the coffee region, our study sites are characterized by drier than average conditions, with a median precipitation of 1,103 mm/year (Cenicafé 2011). Precipitation in our study sites follows a bimodal pattern with 2 rainy seasons (March to June and September to November) and 2 dry seasons (December to February and July to August) (Cenicafé 2011). The El Niño event induced drought conditions in our study sites; precipitation in December 2015 was only 0.7 mm compared with 108 mm in 2013, and ∼84 mm in both 2014 and 2016 (Cenicafé 2016a, 2016b, 2016c, 2017;  Supplementary Material Figure S2).

Severe drought induced by El Niño events has been shown to have lethal effects on Neotropical migrants spending the winter in primary forest by decreasing food availability and habitat quality (Sillett et al. 2000). We suggest that the steep decline in precipitation during the 2015–2016 El Niño event further challenged the response of individuals to seasonal drought (Strong and Sherry 2000, Latta and Faaborg 2002, Studds and Marra 2007, Smith et al. 2010), resulting in negative consequences for body condition and annual survival in both habitats. However, contrary to our expectations, we did not find evidence that the negative effects of the extreme El Niño event on apparent survival of individuals was stronger in coffee than forest, supporting our overall results that the 2 habitats offer similar quality. Further study is needed to determine whether this is true at a broader scale and whether within-season survival is impacted differentially among habitats.

Our results highlight the role of shade coffee in the conservation of Neotropical migrants. Demographic measures in both habitats were similar, particularly apparent survival, the parameter most closely linked to population change. It should be noted that the minimum amount of shade recommended in our study region is 29%, contrasting with other Andean regions with heavy cloud cover and high rainfall where 20% shade is recommended, and several regions have no shade (Farfán-Valencia and Jaramillo-Robledo 2009). Consequently, coffee plantations in our study sites have diverse floristic and structural attributes, and a complex and diverse vertical stratification, which increases habitat suitability for Canada Warbler and other Neotropical migrants (Bakermans et al. 2012, Céspedes and Bayly 2019). Indeed, shade coffee plantations at our study site were characterized by high canopies (mean 18.8 m) and an average canopy cover of 44.4%, and may not reflect “average conditions” across shade coffee plantations in the Andes. Therefore, we may have found clearer evidence for differences in habitat suitability in plantations with less favorable management practices such as less diverse shade trees or lower canopy cover and height; such practices are widespread across the Andes.

Traditionally, coffee has been produced in rustic systems where the native canopy was maintained across much of the Neotropical region (Moguel and Toledo 1999). Since the 1970s, coffee plantations have been more intensively managed and transformed into open-sun production systems (Perfecto et al. 1996, Moguel and Toledo 1999, Rice 1999). For instance, by 1990, almost 50% of the traditional shade coffee had been converted to sun coffee in Latin America, and this decrease continued between 1990 and 2010 across the globe (Jha et al. 2014). In Colombia alone, the share of coffee production under shade decreased from 23% of plantations in 1997 to 10% in 2013 (Perfecto et al. 1996, Escobar 2013).

The dramatic intensification of agricultural practices towards open-sun systems has resulted in a more severe loss of global biodiversity relative to the conversion of natural forest to agroforestry systems (De Beenhouwer et al. 2013), and undoubtedly in a decrease in winter habitat availability for Neotropical migrants. Despite the development of market-based conservation incentives to promote shade coffee retention, the remnants of this valuable agroecosystem are in danger of being lost across the Neotropics. Strategies aiming to conserve structurally complex shade coffee plantations from further intensification, and to diversify current open-sun systems, will enhance biodiversity and ecosystem services (Bakermans et al. 2012, De Beenhouwer et al. 2013) and habitat availability for Neotropical migrants such as the Canada Warbler. Recent models predict that reverting sun coffee to shade coffee maximizes farmers' income by increasing pest control services provided by birds and potential price premiums for higher quality coffee, while offsetting lower yields associated with shade coffee production (Hernandez-Aguilera et al. 2019). However, the effective implementation of such strategies depends, in part, on the development of financial and technical assistance programs to low-income smallholder farmers, and on the promotion of sustainable coffee among consumers (González-Prieto 2018, Hernandez-Aguilera et al. 2019).

The conservation value of shade coffee plantations is likely enhanced by the presence of forest in the landscape and, in addition, forest is expected to provide additional ecosystem services (Ricketts 2004, Ricketts et al. 2004, Karp et al. 2013). While shade coffee might be beneficial for Canada Warbler, this might not be true for resident non-migratory Neotropical forest specialists, which are severely affected by the global transformation of forest to agroecosystems and by management intensification (Tejada-Cruz and Sutherland 2004, De Beenhouwer et al. 2013). Landscape conservation approaches, promoting diverse matrices maintaining both habitats, might best ensure long-term survival in both Canada Warbler and resident species, while simultaneously creating resilience and satisfying the economic needs of local communities.

SUPPLEMENTARY MATERIAL

Supplementary material is available at The Condor: Ornithological Applications online.

ACKNOWLEDGMENTS

We are thankful to the owners of Hacienda La Fragua, and the farms Villa Gloria, El Diamante, Puerto Lopez, and El Quininí, who allowed us access to their properties and provided logistic support. We are grateful for the hard work of our field assistants, Jeyson Sanabria, Angela Caguazango, Ana M. Díaz, Daniel Giesbrecht, Nestor Espejo, Catalina González, Alejandro Suarez, Diego Cueva, Dominic Cormier, Tom Squires, Sergio Gómez, Pilar Caicedo, and many others. We thank Jorge Botero and the Comité de Cafeteros of Cundinamarca for helping us locate our study sites. Anonymous reviewers provided helpful comments on the manuscript.

Funding statement: Fieldwork was funded by an operating grant to K.A.H. from Environment and Climate Change Canada and a Natural Sciences and Engineering Research Council of Canada grant (NSERC, Discovery grant #2017–04430). A.M.G. also received funding from an Industrial Natural Sciences and Engineering Research Council of Canada grant (ID#468866) sponsored by Bird Canada. Support was also received from BirdLife International, The Neotropical Migratory Bird Conservation Act (NMBCA), Swarovski Optic, and the University of Saskatchewan.

Ethics statement: All applicable institutional and national guidelines for the care and use of animals were followed. We captured and marked birds following Animal Use Protocol #20100084 approved by the University of Saskatchewan Animal Research Ethics Board. Research permits were issued by Agencia Nacional de Licencias Ambientales (Res. 0597).

Author contributions: A.M.G. conceived the idea. A.M.G., N.J.B., and K.A.H. designed the study. A.M.G. carried out the study and collected data. A.M.G. and S.W. analyzed data. A.M.G. wrote the manuscript with contributions and feedback from all co-authors.

Data depository: The datasets generated and analyzed during the current study can be found at González et al. (2020).

LITERATURE CITED

1.

Bakermans, M. H., A. D. Rodewald, A. C. Vitz, and C. Rengifo (2012). Migratory bird use of shade coffee: The role of structural and floristic features. Agroforestry Systems 85:85–94. Google Scholar

2.

Bakermans, M. H., A. C. Vitz, A. D. Rodewald, and C. G. Rengifo (2009). Migratory songbird use of shade coffee in the Venezuelan Andes with implications for conservation of Cerulean Warbler. Biological Conservation 142:2476–2483. Google Scholar

3.

Banner, K. M., and M. D. Higgs (2017). Considerations for assessing model averaging of regression coefficients. Ecological Applications 27:78–93. Google Scholar

4.

Bolker, B. (2019). emdbook: Ecological Models and Data in R. Princeton University Press, Princeton, NJ, USA. Google Scholar

5.

Brlík, V., J. Koleček, M. Burgess, S. Hahn, D. Humple, M. Krist, J. Ouwehand, E. L. Weiser, P. Adamík, J. A. Alves, et al. (2019). Weak effects of geolocators on small birds: A meta-analysis controlled for phylogeny and publication bias. Journal of Animal Ecology 89:207–220. Google Scholar

6.

Brown, D. R., and T. W. Sherry (2006). Food supply controls the body condition of a migrant bird wintering in the tropics. Oecologia 149:22–32. Google Scholar

7.

Burnham, K. P., and D. R. Anderson (2002). Multimodel Selection and Multimodel Inference: A Practical Information Theoretic Approach. Springer-Verlag, New York, NY, USA. Google Scholar

8.

Cade, B. S. (2015). Model averaging and muddled multimodel inferences. Ecology 96:2370–2382. Google Scholar

9.

Caudill, S. A., F. J. A. DeClerck, and T. P. Husband (2015). Connecting sustainable agriculture and wildlife conservation: Does shade coffee provide habitat for mammals? Agriculture, Ecosystems and Environment 199:85–93. Google Scholar

10.

Cenicafé. Federación nacional de cafeteros de Colombia. Centro Nacional de investigaciones de café (2011). Patrones de distribución de la lluvia en la zona cafetera. Google Scholar

11.

Cenicafé. Federación nacional de cafeteros de Colombia. Centro Nacional de investigaciones de café (2016a). Anuario meteorológico cafetero 2015. Google Scholar

12.

Cenicafé. Federación nacional de cafeteros de Colombia. Centro Nacional de investigaciones de café (2016b). Anuario meteorológico cafetero 2013. Google Scholar

13.

Cenicafé. Federación nacional de cafeteros de Colombia. Centro Nacional de investigaciones de café (2016c). Anuario meteorológico 2014. Google Scholar

14.

Cenicafé. Federación nacional de cafeteros de Colombia. Centro Nacional de investigaciones de café (2017). Anuario meteorológico cafetero 2016. Google Scholar

15.

Céspedes, L. N., and N. J. Bayly (2019). Over-winter ecology and relative density of Canada Warbler Cardellina canadensis in Colombia: The basis for defining conservation priorities for a sharply declining long-distance migrant. Bird Conservation International 29:232–248. Google Scholar

16.

Colorado, G. J., and A. D. Rodewald (2017). Patterns of change in body condition in wintering Neotropical-nearctic migratory birds in shaded plantations in the Andes. Agroforestry Systems 91:1129–1137. Google Scholar

17.

Constantini, D., and A. P. Møller (2013). A meta-analysis of the effects of geolocator application on birds. Current Zoology 59:697–706. Google Scholar

18.

De Beenhouwer, M., R. Aerts, and O. Honnay (2013). A global meta-analysis of the biodiversity and ecosystem service benefits of coffee and cacao agroforestry. Agriculture, Ecosystems and Environment 175:1–13. Google Scholar

19.

Environment and Climate Change Canada (2017). North American breeding bird survey - Canadian trends website, Data-version 2015. Google Scholar

20.

Escobar, D. (2013). Evolución de la caficultura en Colombia. Misión estudios competitividad caficultura en Colombia. Universidad del Rosario, Bogotá, Colombia. Google Scholar

21.

Farfán-Valencia, F., and A. Jaramillo-Robledo (2009). Sombrío para el cultivo de café según la nubosidad de la región. Federación nacional de cafeteros de Colombia. Cenicafé, Centro Nacional de investigaciones de café. Avances técnicos 379. Google Scholar

22.

Garshelis, D. L. (2000). Delusions in habitat evaluation: Measuring use, selection, and importance. InResearch Techniques in Animal Ecology, Controversies and Consequences ( M. C. Pearl, L. Boitani, and T. K. Fuller, Editors). Columbia University Press, New York, NY, USA. pp. 111–114. Google Scholar

23.

González-Prieto, A. M. (2018). Conservation of Neotropical migrants: The coffee connection revisited. Avian Conservation and Ecology 13:19. Google Scholar

24.

González-Prieto, A. M., N. J. Bayly, G. J. Colorado, and K. A. Hobson (2017). Topography of the Andes mountains shapes the wintering distribution of a migratory bird. Diversity and Distributions 23:118–129. Google Scholar

25.

González, A. M., S. Wilson, N. J. Bayly, and K. A. Hobson (2020). Data from: Contrasting the suitability of shade coffee agriculture and native forest as overwinter habitat for Canada Warbler (Cardellina canadensis) in the Colombian Andes. The Condor: Ornithological Applications 122:1–12. https://doi.org/10.5061/ dryad.7sqv9s4pkGoogle Scholar

26.

Henderson, A., S. P. Churchill, and J. L. Luteyn (1991). Neotropical plant diversity. Nature 351:21–22. Google Scholar

27.

Hernandez-Aguilera, J. N., J. M. Conrad, M. I. Gómez, and A. D. Rodewald (2019). The economics and ecology of shade-grown coffee: A model to incentivize shade and bird conservation. Ecological Economics 159:110–121. Google Scholar

28.

International Union for Conservation of Nature (2016). The IUCN Red List of Threatened Species.  http://www.iucnredlist.orgGoogle Scholar

29.

Jaksic, F. M. (2001). Ecological effects of El Niño in terrestrial ecosystems of Western South America. Ecography 24:241–250. Google Scholar

30.

Jha, S., C. M. Bacon, S. M. Philpott, V. E. MÉndez, P. LÄderach, and R. A. Rice (2014). Shade coffee: Update on a disappearing refuge for biodiversity. BioScience 64:416–428. Google Scholar

31.

Johnson, M. D. (2006). Effects of shade-tree species and crop structure on the winter arthropod and bird communities in a Jamaican shade coffee plantation. Biotropica 32:133–145. Google Scholar

32.

Johnson, M. D. (2007). Measuring habitat quality: A review. The Condor 109:489–504. Google Scholar

33.

Johnson, M. D., T. W. Sherry, T. H. Richard, and P. P. Marra (2006). Assessing habitat quality for a migratory songbird wintering in natural and agricultural habitats. Conservation Biology 20:1433–1444. Google Scholar

34.

Karp, D. S., C. D. Mendenhall, R. F. Sandi, N. Chaumont, P. R. Ehrlich, E. A. Hadly, and G. C. Daily (2013). Forest bolsters bird abundance, pest control and coffee yield. Ecology Letters 16:1339–1347. Google Scholar

35.

Kramer, G.R., D.E. Andersen, D.A. Buehler, P.B. Wood, S.M. Peterson, J. A. Lehman, K. R. Aldinger, L. P. Bulluck, S. Harding, J. A. Jones, et al. (2018). Population trends in Vermivora warblers are linked to strong migratory connectivity. Proceedings of the National Academy of Sciences USA 115:E3192–E3200. Google Scholar

36.

Labocha, M. K., and J. P. Hayes (2012). Morphometric indices of body condition in birds: A review. Journal of Ornithology 153:1–22. Google Scholar

37.

Latta, S. C., and J. Faaborg (2002). Demographic and population responses of Cape May Warblers wintering in multiple habitats. Ecology 83:2502–2515. Google Scholar

38.

Lebreton, J. D., J. D. Nichols, R. J. Barker, R. Pradel, and J. A. Spendelow (2009). Modeling individual animal histories with multistate capture-recapture models. Advances in Ecological Research 41:87–173. Google Scholar

39.

Lynch, J. F., E. S. Morton, and M. E. der Voort (1985). Habitat segregation between the sexes of wintering Hooded Warblers (Wilsonia citrina). The American Naturalist 102:714–721. Google Scholar

40.

Marra, P. P. (2000). The role of behavioral dominance in structuring patterns of habitat occupancy in a migrant during the nonbreeding season. Behavioral Ecology 11:299–308. Google Scholar

41.

Marra, P. P., K. A. Hobson, and R. T. Holmes (1998). Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282:1884–1886. Google Scholar

42.

Marra, P. P., and R. T. Holmes (2001). Consequences of dominance-mediated habitat segregation in American Redstarts during the nonbreeding season. The Auk 118:92–104. Google Scholar

43.

Marra, P. P., C. E. Studds, S. Wilson, T. Scott Sillett, T. W. Sherry, and R. T. Holmes (2015). Nonbreeding season habitat quality mediates the strength of density dependence for a migratory bird. Proceedings of the Royal Society B: Biological Sciences 282:1–8. Google Scholar

44.

Mazerolle, M. J. (2017). AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c).  https://cran.rproject.org/web/packages/AICcmodavg/index.htmlGoogle Scholar

45.

McDermott, M. E., and A. D. Rodewald (2014). Conservation value of silvopastures to Neotropical migrants in Andean forest flocks. Biological Conservation 175:140–147. Google Scholar

46.

Moguel, P., and V. M. Toledo (1999). Biodiversity conservation in traditional coffee systems of Mexico. Conservation Biology 13:11–21. Google Scholar

47.

Norris, D. R., P. P. Marra, T. K. Kyser, T. W. Sherry, and L. M. Ratcliffe (2004). Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird. Proceedings of the Royal Society of London Series B 271:59–64. Google Scholar

48.

Perfecto, I., R. A. Rice, R. Greenberg, and M. E. der Voort (1996). Shade coffee: A disappearing refuge for biodiversity. BioScience 46:598–608. Google Scholar

49.

Perfecto, I., and J. Vandermeer (2008). Biodiversity conservation in tropical agroecosystems: A new conservation paradigm. Annals of the New York Academy of Sciences 1134:173–200. Google Scholar

50.

Perfecto, I., J. Vandermeer, A. Mas, and L. S. Pinto (2005). Biodiversity, yield, and shade coffee certification. Ecological Economics 54:435–446. Google Scholar

51.

Powell, L. A. (2007). Approximating variance of demographic parameters using the delta method: A reference for avian biologists. The Condor 109:948–954. Google Scholar

52.

Pyle, P. (1997). Identification Guide to North American Birds, Part I: Columbidae to Ploceidae. Slate Creek Press, Bolinas, CA, USA. Google Scholar

53.

R Core Team (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.  https://www.R-project.org/Google Scholar

54.

Renjifo, L. M., M. F. Gomez, J. Velásquez-Tibatá, Á. M. Amaya-Villarreal, G. H. Kattan, J. D. Amaya-Espinel, and J. Burbano-Girón (2016). Libro rojo de aves de Colombia, Volumen II: bosques húmedos de los Andes y la costa Pacífica. Editorial Pontificia Universidad Javeriana e Instituto Alexander von Humboldt, Bogotá DC, Colombia. Google Scholar

55.

Rice, R. A. (1999). A place unbecoming: The coffee farm of northern Latin America. The Geographical Review 89:554–579. Google Scholar

56.

Ricketts, T. H. (2004). Tropical forest fragments enhance pollinator activity in nearby coffee crops. Conservation Biology 18:1262–1271. Google Scholar

57.

Ricketts, T. H., G. C. Daily, P. R. Ehrlich, and C. D. Michener (2004). Economic value of tropical forest to coffee production. Proceedings of the National Academy of Sciences USA 101:12579–12582. Google Scholar

58.

Ropelewski, C. F., and M. S. Halpert (1987). Global and regional scale precipitation patterns associated with the El Nino/Southern Oscillation. Monthly Weather Review 115:1606–1626. Google Scholar

59.

Rueda-Almonacid, J. V., J. D. Lynch, and A. Amézquita (2004). Libro rojo de los Anfibios de Colombia. InICN-Universidad Nacional de Colombia, Ministerio del Medio Ambiente. Conservación Internacional Colombia, Bogotá DC, Colombia. Google Scholar

60.

Rushing, C. S., P. P. Marra, and M. R. Dudash (2016). Winter habitat quality but not long-distance dispersal influences apparent reproductive success in a migratory bird. Ecology 97:1218–1227. Google Scholar

61.

Sauer, J. R., D. K. Niven, J. E. Hines, D. J. Ziolkowski, Jr , K. L. Pardieck, J. E. Fallon, and W. A. Link (2017). The North American Breeding Bird Survey, Results and Analysis 1966–2015, version 2.07.2017. USGS Patuxent Wildlife Research Center, Laurel, MD, USA. Google Scholar

62.

Sherry, T. W., and R. T. Holmes (1996). Winter habitat quality, population limitation, and conservation of Neotropical–Nearctic migrant birds. Ecology 77:36–48. Google Scholar

63.

Sherry, T. W., M. D. Johnson, and A. M. Strong (2005). Does winter food limit populations of migratory birds? InBirds of Two Worlds: The Ecology and Evolution of Migration ( R. R. Greenberg and P. P. Marra, Editors). The Johns Hopkins University Press, Baltimore, MD, USA. pp. 414–425. Google Scholar

64.

Sillett, T. S., R. T. Holmes, and T. W. Sherry (2000). Impacts of a global climate cycle on population dynamics of a migratory songbird. Science 288:2040–2042. Google Scholar

65.

Smith, J. A. M., L. R. Reitsma, and P. P. Marra (2010). Moisture as a determinant of habitat quality for a nonbreeding Neotropical migratory songbird. Ecology 91:2874–2882. Google Scholar

66.

Strong, A. M., and T. W. Sherry (2000). Habitat-specific effects of food abundance on the condition of Ovenbirds wintering in Jamaica. Journal of Animal Ecology 69:863–895. Google Scholar

67.

Studds, C. E., and P. P. Marra (2005). Nonbreeding habitat occupancy and population processes: An upgrade experiment with a migratory bird. Ecology 86:2380–2385. Google Scholar

68.

Studds, C. E., and P. P. Marra (2007). Linking fluctuations in rainfall to nonbreeding season performance in a long-distance migratory bird, Septophaga ruticilla. Climate Research 35:115–122. Google Scholar

69.

Studds, C. E., and P. P. Marra (2011). Rainfall-induced changes in food availability modify the spring departure programme of a migratory bird. Proceedings of the Royal Society of London Series B 278:3437–3443. Google Scholar

70.

Tejada-Cruz, C., and W. J. Sutherland (2004). Bird responses to shade coffee production. Animal Conservation 7:169–179. Google Scholar

71.

Van Horne, B. (1983). Density as a misleading indicator of habitat quality. The Journal of Wildlife Management 47:893–901. Google Scholar

72.

Vickery, P. D., M. L. Hunter, and J. V. Wells (1992). Is density an indicator of breeding success? The Auk 109:706–710. Google Scholar

73.

White, G. C., W. L. Kendall, and R. J. Barker (2006). Multistate survival models and their extensions in program MARK. The Journal of Wildlife Management 70:1521–1529. Google Scholar

74.

Wilcove, D. S., and M. Wikelski (2008). Going, going, gone: Is animal migration disappearing? PLoS Biology 6:1361–1364. Google Scholar

75.

Wilson, S., S. L. Ladeau, A. P. Toøttrup, and P. P. Marra (2011). Range-wide effects of breeding- and nonbreeding-season climate on the abundance of a Neotropical migrant songbird. Ecology 92:1789–1798. Google Scholar

76.

Wilson, S., J. F. Saracco, R. Krikun, D. T. T. Flockhart, C. Godwin, and K. R. Foster (2018). Drivers of demographic decline across the annual cycle of a threatened migratory bird. Scientific Reports 8. https://doi.org/10.1038/s41598-018-25633-zGoogle Scholar

77.

Wunderle, J. M. (1995). Population characteristics of Blackthroated Blue Warblers wintering in three sites on Puerto Rico. The Auk 112:931–946. Google Scholar

78.

Wunderle, J. M., and S. C. Latta (2000). Winter site fidelity of Nearctic migrants in shade coffee plantations of different sizes in the Dominican Republic. The Auk 117:596–614. Google Scholar

79.

Wunderle, J. M., Jr., and S. C. Latta (1996). Avian abundance in sun and shade coffee plantations and remnant pine forest in the cordillera Central, Dominican Republic. Ornitología Neotropical 7:19–34. Google Scholar
© The Author(s) 2020. Published by Oxford University Press for the American Ornithological Society. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/),which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
Ana M. González, Scott Wilson, Nicholas J. Bayly, and Keith A. Hobson "Contrasting the suitability of shade coffee agriculture and native forest as overwinter habitat for Canada Warbler (Cardellina canadensis) in the Colombian Andes," The Condor 122(2), 1-12, (4 April 2020). https://doi.org/10.1093/condor/duaa011
Received: 20 August 2019; Accepted: 9 February 2020; Published: 4 April 2020
JOURNAL ARTICLE
12 PAGES


Share
SHARE
KEYWORDS
El Niño Southern Oscillation
forest
habitat quality
neotropical migrants
shade coffee
RIGHTS & PERMISSIONS
Get copyright permission
Back to Top