Annual adult survival rates for four sympatric breeding swallow species: effects of environmental factors and density-dependence
Abstract
Swallow (Family: Hirundinidae) populations in the Canadian Maritimes have declined since the 1980s. Using mark–recapture data from 2012 to 2019, we determined apparent annual adult survival rates for Barn (Hirundo rustica Linnaeus, 1758), Tree (Tachycineta bicolor (Vieillot, 1808)), Bank (Riparia riparia (Linnaeus, 1758)), and Cliff (Petrochelidon pyrrhonota (Vieillot, 1817)) swallows. For two data-rich species (Barn and Tree swallows), we modelled the relationships between survival and weather (cold snaps, precipitation, temperature, and wind speed), climate (El Niño–Southern Oscillation (ENSO) and North Atlantic Oscillation (NAO)), Enhanced Vegetation Index (EVI) as a measure of primary productivity during the winter, number of active nests as a measure of site quality, and the Breeding Bird Survey (BBS) annual population index as density-dependent processes. Survival rates for all four species were typically higher (Barn and Tree) or similar to (Cliff and Bank) of estimates from populations that have not undergone severe, long-term declines. Across weather and climate variables, conditions that are typically favourable for high insect availability (e.g., higher precipitation, warmer temperatures, and lower wind speeds) resulted in higher survival. For female Barn and Tree swallows, survival was higher when EVI was lower, and for Barn Swallows, survival was also higher when the BBS index was higher. Collectively our results demonstrate that conditions throughout the annual cycle affect survival, and the relationships with weather and climate variables support the importance of high insect availability.
Résumé
Les populations d’hirondelles (famille : hirundinidés) dans les provinces maritimes canadiennes ont diminué depuis les années 1980. En utilisant des données de marquage–recapture pour la période de 2012 à 2019, nous déterminons les taux de survie annuels apparents des adultes pour l’hirondelle rustique (Hirundo rustica Linnaeus, 1758), l’hirondelle bicolore (Tachycineta bicolor (Vieillot, 1808)), l’hirondelle des rivages (Riparia riparia (Linnaeus, 1758)) et l’hirondelle à front blanc (Petrochelidon pyrrhonota (Vieillot, 1817)). Pour deux espèces pour lesquelles les données sont abondantes (rustique et bicolore), nous modélisons les relations entre la survie et la météo (vagues de froid, précipitations, température et vitesse du vent), le climat (El Niño–oscillation australe (ENSO) et oscillation nord-atlantique (NAO)), l’indice de végétation amélioré (EVI) comme mesure de la productivité primaire durant l’hiver, le nombre de nids actifs comme mesure de la qualité du site et l’indice démographique annuel du Relevé des oiseaux nicheurs (BBS) comme processus dépendant de la densité. Les taux de survie pour les quatre espèces sont typiquement plus élevés (rustique et bicolore) ou du même ordre (des rivages et à front blanc) que les valeurs estimées pour des populations ne présentant pas d’importants déclins sur le long terme. En ce qui concerne les variables météorologiques et climatiques, les conditions typiquement favorables à une grande disponibilité d’insectes (p. ex. précipitations abondantes, températures élevées et faibles vitesses des vents) se traduisent par une survie accrue. Pour les hirondelles rustiques et bicolores femelles, la survie est plus élevée quand l’EVI est plus faible, et pour les hirondelles rustiques, la survie est aussi plus grande quand l’indice BBS est plus élevé. Collectivement, nos résultats démontrent que les conditions durant tout le cycle annuel ont une incidence sur la survie, et les relations avec des variables météorologiques et climatiques soulignent l’importance d’une grande disponibilité d’insectes. [Traduit par la Rédaction]
Introduction
Globally, many recent studies have documented striking declines in different taxa driven by a diverse array of threats (Dulvy et al. 2014; Purcell et al. 2014; Paleczny et al. 2015). Birds, one of the most monitored taxa, are estimated to have lost 3 billion individuals in North America since the 1970s (Rosenberg et al. 2019). For conservation efforts to be successful in addressing and reversing population declines, it is important to target threats that have the greatest effect on the demographic rates that influence population declines (Rappole and McDonald 1994; Green 1999; Rushing et al. 2016). For migratory passerines or songbirds, population models often identify adult survival rates as the most influential demographic rate for declining species (e.g., Baillie and Peach 1992; Murphy 2001; Fletcher et al. 2006; Buehler et al. 2008; Kramer et al. 2017). Adult survival rates may be more important than other demographic rates, like reproductive success or juvenile survival, as lowered rates of survival remove breeding adults and their future young from the population. As a result, conservation efforts directed at increasing reproductive success may not offset the loss of mature individuals from the population (Buehler et al. 2008). Since survival may be influenced by limiting factors and threats throughout the annual cycle, it is important to identify and assess the potential contributions of these threats at different stages (Marra et al. 2015a).
One group of birds experiencing steep population declines is aerial insectivores (i.e., birds that feed mid-flight on flying insects) (Nebel et al. 2010; Smith et al. 2015; Rosenberg et al. 2019). The drivers of these population declines likely consist of multiple factors that affect populations at different stages of the annual cycle (Michel et al. 2016; Spiller and Dettmers 2019). Past studies have noted that adult survival rates, particularly for females, strongly influence population trends for North American populations of two aerial insectivores, Barn Swallow (Hirundo rustica Linnaeus, 1758) (Mann 2021; Zhao et al. 2022) and Tree Swallow (Tachycineta bicolor (Vieillot, 1808)) (Taylor et al. 2018; but see Cox et al. 2018).
There are many factors that affect adult survival for swallows (e.g., habitat change, weather, competition, incidental loss, contaminants, insect availability, disease, and predation; reviewed in Imlay and Leonard 2019). Most research on the factors that affect survival has found relationships between different aspects of weather and climate during different stages of the annual cycle on survival. This includes relationships with prolonged periods of cold weather during the pre-breeding period, often called cold snaps (Brown and Bomberger Brown 1998, 1999; Hess et al. 2008; Custer et al. 2012), precipitation during the pre-breeding and breeding periods (Cowley and Siriwardena 2005; Weegman et al. 2017; Clark et al. 2018), wind during breeding (Møller 2013), and climate indices, like the El Niño-Southern Oscillation or ENSO during the winter (García-Pérez et al. 2014; Clark et al. 2018). In addition, other studies have noted relationships between adult survival rates and disease (Davidar and Morton 1993, 2006; but see Stutchbury et al. 2009), and density-dependent effects on survival (Norman and Peach 2013; Balbontín and Møller 2015; but see Paradis et al. 2002). However, these relationships are not always consistent between species (Imlay and Leonard 2019) and even within species, the factors that affect survival may be different for populations found throughout their geographic range (García-Pérez et al. 2014; Weegman et al. 2017). However, comparative studies on similar species at the same location can provide insight into the stages of the annual cycle that limit these populations and identify conservation actions that may benefit multiple species present in the same space and time.
The overarching goal of our research was to determine the apparent annual survival rates of four swallows species in a region that has experienced significant declines in breeding populations (Nebel et al. 2010; Smith et al. 2015; Michel et al. 2016). We predicted that if apparent annual survival rates were driven by factors during the stationary nonbreeding period, then variation in survival rates would be similar across the three species of long-distance migrants (Bank (Riparia riparia (Linnaeus, 1758)), Barn, and Cliff (Petrochelidon pyrrhonota (Vieillot, 1817)) swallows) that typically winter throughout southern Brazil, Paraguay, Uraguay, Bolivia, and northern Argentina (Hobson et al. 2015; Imlay et al. 2018) when compared to the short-distance migrant (Tree Swallow) which winters in southeastern USA and Cuba (Knight et al. 2018). Also, for the two species with the most data (Barn and Tree swallows), we determined if apparent annual adult survival rates are correlated with environmental conditions known to influence survival and behaviour for these and similar species (Imlay and Leonard 2019). For these species, we made several predictions. First, we predicted that inclement weather and climate conditions, and low primary productivity would be associated with lower survival; these factors would likely influence adult survival indirectly by lowering insect availability or, in severe weather events, like cold snaps, result in direct mortality (Brown and Bomberger Brown 1998, 1999; Hess et al. 2008; Custer et al. 2012; Møller 2013; García-Pérez et al. 2014; Clark et al. 2018). Second, we predicted that high rates of Avian Influenza and West Nile Virus on the breeding grounds would be associated with lower survival; swallows are often infected with both viruses and often with a high prevalence (Oesterle et al. 2009; Burns et al. 2012; Caron et al. 2014). Third, we predicted that we would not observe any density-dependent effects (i.e., lower survival with larger populations) given the substantial declines experienced by populations of both species (Nebel et al. 2010; Michel et al. 2016). Although both species nest in close proximity to conspecifics, these species are not known to benefit from relationships with conspecifics for most of known mechanisms (i.e., mate-finding, predator defence or satiation, cooperative foraging, dispersal or habitat modifications) involved in Allee effects (Kramer et al. 2009); therefore, we assumed Allee effects were unlikely but could be identified if there was a positive relationship between survival and population size.
Materials and methods
We captured adult Barn, Tree, and Cliff swallows at several sites in New Brunswick (NB) and Nova Scotia (NS), Canada, within 10 km of Petitcodiac, NB (45.94°N, 63.18°W), 15 km of Sackville, NB (45.90°N, 64.37°W), and 10 km of Shemogue (46.15°N, 64.19°W). We also captured Barn Swallows at one site within 10 km of Halifax, NS (44.64°N, 63.59°W). We captured Bank Swallows at several sites within 10 km of Sackville, NB and one site within 5 km of Shediac, NB (46.22°N, 64.53°W). We captured adult Barn and Tree swallows from 2012 to 2019, Bank Swallows from 2012 to 2018, and Cliff Swallows from 2013 to 2018 (Table 1). Within each year, we conducted one to five capture sessions at each breeding site throughout the active season; capture session dates varied by the breeding period of each species (mix–max capture dates in any year for each species — Barn: 5 June–9 August; Tree: 25 May–15 July; Bank: 21 June–29 July; Cliff: 30 May–3 August). We used mist nets placed in close proximity to nest sites to capture Barn, Bank, and Cliff swallows, and tube traps to capture Bank Swallows (Morris 1942). We captured Tree Swallows by hand in their nest box, and, in 2019, we trialed the use of remotely operated nest box traps at some of our sites (CHS Consulting Services, Canning, Nova Scotia, Canada). We banded all captured individuals with a uniquely numbered Canadian Wildlife Service aluminum band, and determined the sex of individuals by the presence of a brood patch or cloacal protuberance and plumage characteristics. From these data, we produced an annual capture history for each adult.
Table 1.
Environmental and density-dependent survival covariates
Based on the literature review by Imlay and Leonard (2019), we initially considered 13 potential covariates to represent environmental and density-dependent factors that may influence adult survival in swallows (Supplementary Table S1). To reduce the number of covariates included in our models, we examined multicollinearity among all covariates using variance inflation factor (VIF) tests and removed variables that had high (>2.5) VIF values. After these steps, we were left with nine covariates for Barn Swallow and seven covariates for Tree Swallow (for details see below). Note that different covariates were selected because we considered different time windows for some of these covariates for these two species. These time windows were selected based on the timing of different stages of the annual cycle, such as arrival on the breeding and wintering areas, that differed between the species.
Weather and climate variables
Different weather variables are associated with the survival of swallow species throughout different stages of their annual cycle (Imlay and Leonard 2019). Consecutive days of cold weather (i.e., cold snaps) during the pre-breeding period is associated with high mortality events for several swallow species (Brown and Bomberger Brown 1998, 1999; Hess et al. 2008; Custer et al. 2012). Similarly, high amounts of precipitation during the pre-breeding and breeding stages is associated with lower survival for adult swallows (Robinson et al. 2008; Clark et al. 2018). Both cold snaps and high precipitation likely lower survival by reducing insect availability and, for cold snaps, increase the risk of death by exposure. However, warm, dry conditions during the breeding season are also associated with lower survival and may also represent low insect availability (Weegman et al. 2017); reflecting the importance of local factors on these relationships. Finally, high breeding season wind speeds reduce food availability and are associated with lower survival for adult Barn Swallows (Møller 2013), potentially as a result of increased foraging effort when raising young.
We identified the closest Canadian weather station (https://climate.weather.gc.ca/index_e.html; accessed 13 February 2020) to each breeding site (mean ± SE distance: 21.0 ± 2.4 km) and compiled data on daily weather conditions, including maximum temperature, total precipitation, and mean wind speed. In some cases, the daily data were missing for one or more variables. To address these gaps, we predicted the daily data based on weather conditions on the preceding and subsequent days, by assuming that conditions on the days with missing data followed a linear relationship. For example, if the temperature on the preceding day was 10 °C and the following day was 9 °C, then the predicted temperature for the day missing data was 9.5 °C. Then, we calculated three covariates related to weather conditions on the breeding grounds. For cold-snap length, we used the daily temperature data to identify pre-breeding (Barn: 1–31 May; Tree: 1 April–31 May) cold snaps. Consistent with past studies (Brown and Bomberger Brown 1998, 1999), we defined cold snap as a period of four or more consecutive days with a maximum daily temperature of 11 °C or colder. Then, like García-Pérez et al. (2014), we summed the total number of days across all cold snaps in each year. For example, if there were two cold snaps of 4 and 5 days, respectively, the cold-snap length for that year was 9 days. For pre-breeding precipitation, we calculated the mean daily precipitation during the pre-breeding period when Barn and Tree swallows were arriving on the breeding grounds and starting to initiate nests (Barn: 1–31 May; Tree: 1 April–31 May). For breeding temperature, precipitation, and wind speed, we calculated mean daily temperatures, precipitation, and wind speeds during the breeding period when Barn and Tree swallows were raising young (Barn: 1 June–31 August; Tree: 1 June–31 July). After removing variables with a high VIF, we included cold-snap length, pre-breeding precipitation, breeding temperature, and breeding wind speed was included in the full model for Barn Swallows, and pre-breeding precipitation, breeding precipitation, and breeding temperature in the full model for Tree Swallows (Supplementary Table S1).
At the broader, climatic level, climate indices also provide an indication of weather patterns that may affect survival. The ENSO measures periods of warming and cooling in the Pacific Ocean that influences weather. In positive ENSO phases (i.e., El Niño), the southeastern USA and northern Mexico experience cool, wet weather conditions, whereas southern Mexico and northern Central America experience warm, dry weather conditions. The North Atlantic Oscillation (NAO) is related to temperature and precipitation in North America; in positive phases, it is associated with warm, wet conditions. Relationships between adult survival and ENSO or NAO conditions are mixed, but generally, warm, dry or warm, wet conditions, respectively, that support higher insect availability are associated with higher survival (García-Pérez et al. 2014; Clark et al. 2018).
To measure climate conditions during the winter, we compiled monthly values for the Bivariate ENSO Time Series (ENSO) and NAO from the National Oceanic and Atmospheric Administration (https://psl.noaa.gov/data/climateindices/; accessed 16 February 2020). For ENSO, we calculated the mean monthly value for each climate index over the period of time that individuals from our breeding populations were mostly at their stationary nonbreeding locations (Barn: November–February, Hobson et al. 2015; Tree: November–March, Gow et al. 2019). We predicted that ENSO and NAO may affect survival for Tree Swallows from the Maritimes that winter in southeastern USA and Cuba (Knight et al. 2018), but was less likely to affect survival for Barn Swallows from the Maritimes wintering in southern Brazil, Bolivia, Paraguay, Uruguay, and northern Argentina (Hobson et al. 2015; Imlay et al. 2018) (Supplementary Fig. S1) as these areas are less affected by this weather pattern. For NAO, we followed Clark et al. (2018) and calculated the mean monthly value from December to March. We predicted that NAO conditions would affect both species similarly on the breeding grounds. After removing variables with a high VIF, we included ENSO and NAO in the full model for Barn Swallows, and NAO in the full model for Tree Swallows (Supplementary Table S1).
Primary productivity
Like the Normalized Difference Vegetation Index (NDVI), the Enhanced Vegetation Index (EVI) measures primary productivity by quantifying the greenness of vegetation which is associated with higher insect abundance (Wolda 1978; Pettorelli et al. 2011). However, unlike NDVI, EVI corrects for atmospheric conditions and canopy background. For swallows, relationships with NDVI have been used to understand movement ecology and population trends. For example, decreased primary productivity through the winter was associated within large-scale movements by Tree Swallows mostly to areas with higher productivity (Knight et al. 2019). Also, variability in population trends for Barn Swallows within the Afro-Palearctic system were most sensitive to primary productivity on the winter grounds and at a spring stopover site (Sicurella et al. 2016).
To examine primary productivity during the winter, we first determined the winter range of our breeding populations. For Barn Swallows, we obtained a map of the probable winter locations of individuals from the Maritime breeding population (Imlay et al. 2018). This map was based on probabilistic assignment of 
and 
stable isotopes in feathers molted during the winter. From the assignment surfaces for all individuals, we retained all pixels where at least one-quarter of the sampled individuals were assigned. Then, we obtained geolocator estimates of winter locations and their error for individuals that breed in New Brunswick (Hobson and Kardynal 2016). We overlaid the geolocator estimates with the probable winter areas from the stable isotope assignment. Then, we traced the maximum extent of these areas in ArcGIS Pro (Environmental Systems Research Institute) (Supplementary Fig. S1), excluding regions west of the Andes mountain range that were not used by geolocator tracked Barn Swallows (Hobson and Kardynal 2016). For Tree Swallows, we obtained geolocator point estimates of winter locations (with an error of ±90 km) for eastern breeding populations (Knight et al. 2019). With the geolocator estimates, we used the Minimum Bounding Geometry tool in ArcGIS Pro to create a convex hull polygon, adding a buffer of 90 km using the Buffer tool in ArcGIS Pro to account for the geolocator error (Supplementary Fig. S1).
and stable isotopes in feathers molted during the winter. From the assignment surfaces for all individuals, we retained all pixels where at least one-quarter of the sampled individuals were assigned. Then, we obtained geolocator estimates of winter locations and their error for individuals that breed in New Brunswick (Hobson and Kardynal 2016). We overlaid the geolocator estimates with the probable winter areas from the stable isotope assignment. Then, we traced the maximum extent of these areas in ArcGIS Pro (Environmental Systems Research Institute) (Supplementary Fig. S1), excluding regions west of the Andes mountain range that were not used by geolocator tracked Barn Swallows (Hobson and Kardynal 2016). For Tree Swallows, we obtained geolocator point estimates of winter locations (with an error of ±90 km) for eastern breeding populations (Knight et al. 2019). With the geolocator estimates, we used the Minimum Bounding Geometry tool in ArcGIS Pro to create a convex hull polygon, adding a buffer of 90 km using the Buffer tool in ArcGIS Pro to account for the geolocator error (Supplementary Fig. S1).To obtain the mean values of the EVI, we used the MOD13A2 MODIS/Terra Vegetation Indices 16-Day L3 Global 1 km SIN Grid V006 data set provided by NASA Earth Data (https://earthdata.nasa.gov; accessed 9 March 2021). This data set provides EVI measurements at a 1 km spatial resolution for a 16 day period. We extracted the data using AppEEARS (Application for Extracting and Exploring Analysis Ready Samples, https://lpdaacsvc.cr.usgs.gov/appeears/; accessed 9 March 2021) by creating an area sample extraction using the Barn and Tree swallow wintering range geometries. For both species, we calculated the mean EVI value within the winter range of each species for each nonbreeding period when the species were expected to be present (Hobson et al. 2015; Gow et al. 2019). The specific dates varied slightly from year to year with the 16 day windows that EVI was measured, but the period began around 1 November for both species, and ended around 6 March (Barn Swallows) or 21 March (Tree Swallows) (Gow et al. 2019). EVI was included in the full model for both species.
Disease risk
Swallows may become infected with a diverse range of infections across their geographic range (Oesterle et al. 2009; Burns et al. 2012; Stenkat et al. 2013; Caron et al. 2014; Von Ronn et al. 2015). Despite the often high prevalence of these infections, relationships between survival and disease prevalence are rare. For example, there was no relationship between apparent annual survival of adult Purple Martin (Progne subis (Linnaeus, 1758)) and the prevalence of West Nile Virus (Stutchbury et al. 2009). Regardless, these relationships have not previously been examined in our study species. Like Stutchbury et al. (2009), we calculated the prevalence of Avian Influenza and West Nile Virus in bird carcasses examined and tested in New Brunswick by the Canadian Cooperative Wildlife Health Centre during each year of the study (http://www.cwhc-rcsf.ca/disease_surveillance.php; accessed 13 February 2020). To determine prevalence, we determined the proportion of carcasses tested that were positive for each disease and summed these values. Therefore, the combined prevalence of positive tests provided an index of the annual disease risk. This variable was not included in full model for either species due to the high VIF.
Breeding site population size and density dependence
The density of individuals at a breeding site may be a measure of habitat quality, such as insect availability or abundance of nesting sites. However, it can also be associated with density-dependent processes. Density-dependent effects have been observed in some swallow populations, with lower survival when population densities are high, and are mostly likely the result of competition for food resources (Norman and Peach 2013; Balbontín and Møller 2015).
During our study, breeding sites were clusters of nests in one or more buildings for Barn Swallows or nest boxes for Tree Swallows separated by a minimum of 2 km from the next closest site. To measure the role of breeding site population size on survival, we used the total number of nests monitored at each breeding site in each year. In most years, our nest monitoring efforts for Barn and Tree swallows included nest checks every 2–3 days to collect detailed data on breeding phenology and performance (for details see Imlay et al. 2017). However, in some years (2011–2013 and 2017), we had a reduced effort (∼1–2 nest checks/week), which made it difficult to determine when nests were active. As a result, we used total number of active nests during each year (i.e., those with at least one egg laid during that year) to provide an index of the numbers of adults and juveniles at each site. For Barn Swallows, we used the previous year’s nest monitoring data to identify nests with unhatched egg(s) from the previous year. For Tree Swallows, nest boxes were cleaned out annually in the spring. Therefore, we are confident that this represents actual nesting attempts during each year.
To measure potential density dependence at a regional level (i.e., within the Maritime provinces), we used the R package bbsBayes (Edwards and Smith 2020) in R version 4.0.3 (R Core Team 2021) to download Breeding Bird Survey (BBS) data (Pardieck et al. 2020) and model population trends using the approach described by Smith and Edwards (2021). Briefly, we downloaded data from 2012 to 2019 and stratified the data by provincial/territory/state boundaries and Bird Conservation Region. We ran a hierarchical Bayesian general additive model with year effects (“GAMYE”); the GAMYE model incorporates annual fluctuations into the population trend (Smith and Edwards 2021). Our model initially used three chains, 10 000 burn-in iterations, and a 1/10 thinning rate. Several parameters for the Barn Swallow model failed to converge, so we added an additional 30 000 iterations to the model for this species. Using this model, we generated an annual population index for both species that combined two strata: BCR 14 for New Brunswick and BCR 14 for Nova Scotia and Prince Edward Island.
Modelling apparent annual survival rates
To determine apparent survival rates, we used Cormack–Jolly–Seber models (Cormack 1964; Jolly 1965; Seber 1965). Model structures were different among species, mainly due to data availability across years for each species (Table 1), and, for Tree Swallows, a focus on capturing females in 2013–2017. As a result, we used two different approaches for modeling the relatively data-rich species and sexes (female and male Barn Swallows, and female Tree Swallows) compared to the data-poor species (Bank and Cliff swallows); we did not model survival for male Tree Swallows. Below we detail the model structure for the two approaches.
Barn and Tree swallows
For Barn Swallows, we assumed that site-, year-, and sex-specific apparent annual survival rates are functions of a series of covariates. Thus, we have logit (Sk,i,t) = αk + β1,k × x1,i,t + … + βm,k × xm,i,t + εk,i,t, in which Sk,i,t is apparent survival for sex k (male or female), sitei , and year t, αk is a sex-specific intercept, β1,k, …, βm,k are sex-specific slopes, and the error term εk,i,t follows a Normal distribution with mean 0 and standard deviation σk. For Tree Swallows, we used a similar model, except we focused solely on adult females. We assumed that site-, and year-specific apparent survival are functions of a series of covariates such that logit (Si,t) = α + β1 × x1,i,t + … + βm × xm,i,t + εi,t, in which Si,t is adult female apparent survival for site i and year t, α is the intercept, β1, …, βm are slopes, and the error term εi,t follows a Normal distribution with mean 0 and standard deviation σ.
To determine the effects of environmental factors and density dependence on apparent annual survival rates, we considered full models that include nine (cold snap length, pre-breeding precipitation, breeding temperature, breeding wind speed, ENSO, NAO, EVI, number of nests, and BBS index) covariates for female and male Barn Swallows and seven (pre-breeding precipitation, breeding temperature, breeding precipitation, NAO, EVI, number of nests, and BBS index) covariates for female Tree Swallows. To determine the relative importance of these covariates, we calculated tail probability (P-tail) statistics that were defined as the proportion of posterior samples (see below) that were smaller/larger than 0 when the posterior mean was positive/negative (Zhao et al. 2018). We then further considered the effect of a covariate “strong” when P-tail was less than 0.05, “moderate” when P-tail was between 0.05 and 0.20, and “little to no effect” when P-tail was greater than 0.20 (Zhao et al. 2022).
Bank and Cliff swallows
For Bank and Cliff swallows, we focused on estimating the spatiotemporal variation in apparent annual survival rates and comparing survival between the two sexes. Thus, their survival is assumed to be logit (Sk,i,t) = αk + εk,i,t, in which Sk,i,t is apparent survival for sex k (male or female), site i, and year t, αk is a sex-specific mean at the logit scale, and the error term εk,i,t follows a Normal distribution with mean 0 and standard deviation σk. We did not include additional covariates for these two species because of relatively short timeframe for data availability and larger credible intervals (CI) for apparent annual survival rates in some years (Fig. 1).
Fig. 1.
Model implementation and post-modeling analysis
We used MCMC computing in Jags software (Plummer 2003), called from R version 4.0.3 (R Core Team 2021) using the package “jagsUI” (Kellner 2015). We used three chains, each of which has 100 000 iterations including 50 000 burn-in without thinning, resulting in 150 000 posterior samples for each parameter. We checked convergence of the model using trace-plot and Rhat statistics. All chains are well mixed and stable, with all Rhat values less than 1.02, indicating convergence of the model.
Ethics approval
All bird handling and monitoring was done under protocols approved by Animal Use committees at Acadia University (06-18), Dalhousie University (14-025, 15-103, 18-043), and Environment and Climate Change Canada (12MC01, 13MC01, 13MC02). Additionally, bird banding was conducted under federal banding permits (10619 and 10407) from Environment and Climate Change Canada.
Results
Annual and sex-specific variation in survival
There were differences in apparent annual survival rates for all four species, and sometimes between sexes (Fig. 1). For Barn Swallows, mean annual apparent survival rates were lower for females (52.2%, 95% CI: 32.7%–71.6%) compared to males (68.3%, 95% CI: 51.2%–85.5%). For Bank and Cliff swallows, apparent survival rates were similar for females (46.2%, 95% CI: 36.1%–56.2% and 34.9%, 95% CI: 32.9%–36.9%, respectively) and males (47.0%, 95% CI: 36.9%–57.1% and 39.4%, 95% CI: 33.5%–45.8%, respectively). The mean annual apparent survival of female Tree Swallows was 59.8% (95% CI: 48.0%–71.5%).
There was considerable annual variation in annual apparent survival rates for Barn Swallows (Fig. 1). While there was less annual variation in survival rates for Tree, Bank, and Cliff swallows, there were also large CI around those survival rates in some years (i.e., less precision in apparent survival rates). For Barn Swallows, the difference between the lowest and highest years was 54.0% and 55.0% for females and males, respectively, for female Tree Swallows, this was 38.8%, and for Bank Swallows, this difference was 24.8% and 25.8% for females and males, respectively. In contrast, for Cliff Swallows, the maximum difference in mean annual survival rates was 3.4% and 11.7%, respectively. Therefore we focused on Barn, Tree, and Bank swallows to identify years with consistently high or low survival rates across species and sexes. Mean apparent annual survival rates for were similarly high (i.e., at or above the mean value) in 2012 for Barn Swallows, and female Tree Swallows, and male Bank Swallows; 2013 for Barn, Tree, and Bank swallows; and 2018 for Barn and Tree swallows. Also, survival rates were similarly low in 2015 and 2016 for Barn Swallows, and female Tree and Bank swallows; and 2017 for all three species.
Environmental and density-dependent effects
We found strong relationships between several weather variables and the apparent annual survival of Barn and Tree swallows. During the pre-breeding period, there was a moderate, negative relationship between cold-snap length and the survival of female and male Barn Swallows, with higher survival in years with fewer cold-snap days (P-tail = 0.14 and 0.05, respectively; Table 2). There was also a moderate, positive relationship between pre-breeding precipitation and the survival of female Tree Swallows, with higher survival in years with more precipitation (P-tail = 0.20). There was a positive relationship between breeding temperature and survival for both species, with higher survival in years with warmer temperatures. This relationship was strong for female Barn Swallows (P-tail = 0.01; Fig. 2), and moderate for male Barn Swallows (P-tail = 0.06; Fig. 2) and female Tree Swallows (P-tail = 0.11). There was a moderate, positive relationship between summer precipitation and survival for female Tree Swallows, with higher survival in years with warmer temperatures (P-tail = 0.11). There was a negative relationship between breeding wind speeds and survival for Barn Swallows, with higher survival in years with lower wind speeds. This relationship was strong for female Barn Swallows (P-tail = 0.04) and moderate for male Barn Swallows (P-tail = 0.09) (Fig. 2).
Table 2.
Fig. 2.
We found a relationship between NAO and the apparent annual survival of female Barn and Tree swallows. For females of both species, this was a moderate, negative relationship, indicating higher survival in years with cool, dry conditions (P-tail = 0.06 and 0.06, respectively; Table 2).
We also found a relationship between EVI primary productivity and the apparent annual survival of female Barn and Tree swallows. For females of both species, this was a moderate, negative relationship, indicating higher survival in years when primary productivity was lower (P-tail = 0.19 and 0.15, respectively; Table 2).
Finally, we found a relationship between the BBS population index and the apparent annual survival of Barn Swallows. This moderate, negative relationship indicates that the survival of females and males was higher in years with a lower regional population (P-tail = 0.09 and 0.20, respectively; Table 2).
Discussion
The goal of our study was to assess patterns in variability in apparent annual survival across four swallow species, and determine what factors across breeding, wintering, and pre-breeding stages affect survival rates in two species: Barn and Tree swallows. We observed annual variability in apparent survival rates for all four species, although this was greatest for Barn, female Tree, and Bank swallows. Also, female Barn Swallows had lower survival when compared to males. For Barn and Tree swallows, apparent annual survival was related to several factors during stationary periods of their annual cycle. There were strong and moderate effects of several weather (i.e., cold-snap length, pre-breeding precipitation, breeding precipitation, breeding temperature, and breeding wind speed depending on the species) and climate (i.e., NAO) factors on both species. These results were generally consistent with past work demonstrating that weather conditions that are associated with poor food availability had negative effects on survival. We also found survival was higher in years with lower primary productivity (i.e., EVI) during the winter for female Barn and Tree swallows, and that for Barn Swallows, survival was higher in years when the regional population was smaller.
Apparent annual survival among the four swallow species ranged from 34.9% to 68.3%, and was lowest in Bank and Cliff swallows and highest for male Barn Swallows and female Tree Swallows. Our estimates were higher (Barn and Tree swallows) or similar to (Cliff and Bank swallows) estimates from populations that have not experienced long-term declines as great as in the Maritime provinces (MacBriar and Stevenson 1976; Freer 1977; Stahura 1982; Sikes and Arnold 1984; Safran 2004; Custer et al. 2007; Hallinger et al. 2011; Roche et al. 2013; García-Pérez et al. 2014; Brown et al. 2016; Cox et al. 2018; Brown and Brown 2020). However, we studied the swallows during a time period where population declines have slowed or growth stabilized in all species across the Maritimes, and throughout their Canadian range (Smith and Edwards 2021). As such, our relatively high estimates may be reflective of healthier populations than observed in the other studies examining other time periods, and other regions.
In all but one year (2014), there was some evidence that apparent annual survival rates varied in a consistent manner across species and sexes. Therefore, it is likely that conditions on the breeding grounds during these years may have influenced the similar survival rates across species. This is supported by the results of survival models for Barn and Tree swallows that identify a number of breeding ground covariates that are strongly or moderately correlated with survival. However, we do recognize that most of the covariates in our models are related to conditions on the breeding grounds. Female Barn and Cliff swallows had lower survival rates than males of the same species. These differences may be driven by investment in parental care, predation risk, and physiology, resulting in female swallows being more vulnerable to pressures that impact their survival. Differences in survival rates between female and male birds is a pattern often observed in many passerine species (e.g., Ovenbirds (Seiurus aurocapilla (Linnaeus, 1766)): Bayne and Hobson 2002; American Redstarts (Setophaga ruticilla (Linnaeus, 1758)): Marra et al. 2015b). To further investigate the sex- and species-specific patterns we observed in apparent annual survival rates, we considered the factors that affect survival.
Annual apparent survival rates for Barn and Tree swallows were related to a large number of weather variables during the pre-breeding and breeding seasons. Inclement weather conditions, such as long periods of cold snaps (Barn), high pre-breeding and breeding precipitation (Tree), low breeding temperatures (Barn and Tree), and strong breeding wind speeds (Barn), were all related to lower apparent annual survival rates. These types of inclement weather conditions can create suboptimal foraging conditions and reduce insect abundance (Bryant 1975; Grüebler et al. 2008; Winkler et al. 2013). Further, these conditions are linked to reduced survival in adult Tree Swallows (e.g., Custer et al. 2012; Clark et al. 2018) and mass mortality events in Cliff and Tree swallows (Brown and Bomberger Brown 1996, 1998; Hess et al. 2008). Also, we found that female Barn and Tree swallow survival was highest during negative phases of NAO which are typically associated with cool, dry conditions during the breeding season. At this time, we do not understand why the relationships with regional weather conditions would differ from site-level conditions. Further, the relationship between NAO and annual survival are not consistent with previous findings for Barn Swallows in North America (García-Pérez et al. 2014) and only some populations of Tree Swallows (Clark et al. 2018). However, these studies cover wide geographic areas and it is unsurprising to see regional variation in the results (Weegman et al. 2017). Within the Maritime populations, we anticipated that Tree Swallow survival would be more strongly affected by weather conditions as they arrive on the breeding grounds earlier in the spring and are exposed to more inclement conditions than Barn Swallows. However, we found stronger relationships between inclement weather and survival for the latter species. As a short-distance migrant, Tree Swallows may arrive on the breeding grounds with a greater capability to withstand harsh weather either due to a less demanding migration or a stronger ability to respond to irregular weather events (La Sorte et al. 2016). This is consistent with other passerine species, where early arriving, short distance migrants do not experience the higher costs to survival that long distance migrants experience (Lerche-Jørgensen et al. 2018). In addition to these factors, it is possible that the cold snaps observed during the years of our study were not sufficient to have the severe effects on survival observed in other populations (Hess et al. 2008; Custer et al. 2012).
Conditions during the winter were also related to apparent survival rates and these conditions varied between species. For Barn Swallows, we did not find a relationship between ENSO, but this is consistent with García-Pérez et al. (2014) survival analysis of adult Barn Swallows that breed in Ontario. The Maritimes and Ontario Barn Swallow populations both overwinter in areas of southeastern South America (e.g., Brazil, Bolivia, Paraguay, Uraguay, and Argentina; Hobson et al. 2015; Hobson and Kardynal 2016; Imlay et al. 2018) not typically affected by ENSO. For female Barn and Tree swallows, survival was moderately related to EVI, with higher survival in years with lower primary productivity. This was a surprising result, and more research is needed to understand the link between survival and primary productivity through the winter, especially given the propensity of some swallows to undertaken intratropical migration during the winter which may help to mitigate the effects of poor conditions (Stutchbury et al. 2016; Imlay et al. 2018; Knight et al. 2019).
Lastly, while we did not find a relationship between breeding site population size (i.e., number of nests), at a broader regional scale, we observed effects of density dependence for Barn Swallows. Despite large declines in the Maritime Barn Swallow population (Nebel et al. 2010; Smith et al. 2015; Michel et al. 2016), the BBS population index in the spring was negatively related to apparent annual survival rates in the subsequent year, resulting in higher adult survival in years when the regional population was lower. This is consistent with what would be expected due to density-dependent effects, and would suggest that even with the presently small population relative to historical population, there are density-related limiting factors for Barn Swallow survival. The driver of this density-dependent effect is unknown. We speculate that competition for resources, such as high quality nest sites or nonbreeding roost sites, during some period of the annual cycle may contribute to this effect. Furthermore, the lack of a relationship for female Tree Swallows could reflect species-related differences in resource availability at some point during the annual cycle. For example, differences in the timing of migration for Barn and Tree swallows (Gow et al. 2019; Imlay et al. 2021) could lead differences in the temporal occupancy of migratory roost sites and differences in the quality of these sites at different times during the season. Therefore, a large Barn Swallow population could increase competition in a resource-poor environment, however, that level of competition would not be the same for a large Tree Swallow population in a resource-rich environment.
Certainly, our analysis does not capture all the potential factors that influence survival. For example, disease risk and hurricane days were not included in our analysis due to high VIF. In the case of the former variable, we were unable to examine the relationships between the prevalence of West Nile Virus and Avian Influenza on apparent annual survival rates; one of the three predictions for our study. Additionally, we were often constrained at measuring some variables at a relatively coarse level. For example, during the winter, our survival models may have been hampered by the relatively large scale at which we measured conditions. For example, for Barn Swallows, we averaged values of the EVI across approximately 805 million ha. Another constraint is that due to the short time series, we were unable to model variables that included relatively rare events. These types of severe weather events almost certainly affect survival in the populations that we studied due to the coastal location of the breeding sites and fall migration routes (Knight et al. 2018; Imlay et al. 2020, 2021); however, their relative rarity requires a longer time series to compare their effects to the other parameters that we considered.
Conclusions
We have shown that apparent annual survival in swallows is variable across time, and responds to factors differently across species. These differences between species are likely due, at least in part, to differences as short- and long-distance migrants, either as a result of migration distance or the specific stationary nonbreeding sites used by each group. There are effects of environmental conditions throughout the annual cycle, including weather during the pre-breeding and breeding periods and measures of primary productivity on nonbreeding grounds. Furthermore, for Barn Swallows, the regional population size has a negative effect on survival and may result in density-dependent limitation of population growth. In particular, apparent annual survival rates were often related to weather and climate (e.g., cold snaps, temperature, precipitation, and NAO) which are also related to population trajectories in aerial insectivores, particularly swallows (Michel et al. 2021). These adverse conditions often have strong links to insect availability; therefore, insects will continue to be an important consideration in the context of aerial insectivore conservation. Finally, to best inform conservation measures in the context of survival in the future, it would be important to assess the factors affecting survival during their migration (i.e., habitat availability and quality, weather), which is a key period for mortality. Continuing to use comparative studies will help answer important questions for hard to study animals, and help to guide actions in the future.
Acknowledgements
We thank all the field staff involved in bird monitoring and banding efforts, L. Achenbach for compiling some of the raw environmental covariate data, and P.D. Taylor and two anonymous reviewers for comments on an earlier version of this manuscript. We are also grateful to the landowners who provided access to their properties for monitoring swallow populations throughout this project.
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Published In
Canadian Journal of Zoology
Volume 100 • Number 10 • October 2022
Pages: 647 - 659
History
Received: 10 November 2021
Accepted: 26 April 2022
Accepted manuscript online: 15 July 2022
Version of record online: 23 September 2022
Notes
This paper is part of a Special collection entitled “Ecology and conservation of avian aerial insectivores”.
Copyright
© 2022 The Author(s). This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
Data Availability Statement
The data sets generated during and (or) analysed during the current study are available from the corresponding author on reasonable request.
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Author Contributions
Conceptualization: TLI
Data curation: TLI, HARM, ACD
Formal analysis: QZ
Funding acquisition: TLI, HARM, PT, RMW, MLL
Investigation: TLI, HARM
Methodology: TLI, HARM, ACD, QZ
Project administration: TLI, HARM, PT, RMW
Resources: TLI, HARM
Supervision: TLI, PT, RMW, MLL
Visualization: TLI, ACD, QZ
Writing — original draft: TLI, HARM, ACD, QZ
Writing — review & editing: TLI, HARM, ACD, PT, RMW, MLL, QZ
Competing Interests
The authors declare that there are no competing interests.
Funding Information
Funding for this project was provided by Environment and Climate Change Canada, New Brunswick Wildlife Trust Fund, Nova Scotia Habitat Conservation Fund, and Wildlife Preservation Canada.
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Tara L. Imlay, Hilary A.R. Mann, Andrew C. Ding, Peter Thomas, Rebecca M. Whittam, Marty L. Leonard, and Qing Zhao. 2022. Annual adult survival rates for four sympatric breeding swallow species: effects of environmental factors and density-dependence. Canadian Journal of Zoology.
100(10): 647-659. https://doi.org/10.1139/cjz-2021-0207
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