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Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia: Influence of migratory distance, route, ENSO, age and body size

Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of... Anim. Migr. 2021; 8:27–39 Research Article Laura Cárdenas-Ortiz*, Nicholas J. Bayly, Keith A. Hobson Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia: Influence of migratory distance, route, ENSO, age and body size https://doi.org/10.1515/ami-2020-0105 Keywords: Bird migration, Deuterium, El Niño, fuel load, received May 11, 2020; accepted March 5, 2021 stable isotopes, vulnerability Abstract: Available energy stores determine stopover length, migration speed and likely survival in migrating birds. We measured energy stores by estimating fuel load in 11 species of Neotropical migrant songbirds in the Darién 1 Introduction of Colombia over five years. We evaluated 1) whether indi- viduals flying further from breeding origin arrived with As a group and throughout the World, long-distance smaller fuel loads, 2) if the ENSO (El Niño-Southern Oscil- migrant birds are declining at faster rates than short-dis- lation) cycle affected fuel load and 3) if species known to tance migrants and resident species [1, 2]. Why this group migrate mostly overwater arrived with less fuel relative to appears to be more vulnerable than other groups of those migrating overland. Breeding origin, inferred from birds is still open to speculation. Breeding origin is one feather δ H values, only had a significant positive effect factor that can influence survivorship [3, 4], with longer on fuel load in Swainson’s Thrush (Catharus ustulatus). migrations involving greater risks [5]. Other authors have Veery (Catharus fuscescens) and Swainson’s thrush had hypothesized that long-distance migrants are exposed to higher and lower fuel loads, respectively, in El Niño years. greater climatic variability, including tropical storms and Multi-species mixed-effects models revealed support for hurricanes [6]. For Neotropical migratory birds that cross larger fuel loads in larger-bodied species and in species the Gulf of Mexico and the Caribbean Sea, such factors are taking overwater routes, contrary to our prediction. also linked to the El Niño Southern Oscillation (ENSO)[7, Across species, we found no support for common effects 8]. Migratory success in songbirds has also been linked of breeding origin or ENSO on fuel loads, in contrast to to experience, with younger, more inexperienced birds community-wide effects of migration route and body-size. expected to have lower survival during migratory episodes In general, the variables considered here explained little [9]. of the variance in fuel loads, suggesting that inter-individ- To date, few studies have attempted to determine ual differences likely have a greater impact than broad- which factors might influence the success of long-distance scale factors in our study system. migration despite migration accounting for up to 80% of annual mortality in small migratory passerines [6, 10, 11]. Migratory birds are typically available for study before or after migration or at key stopover sites where they refuel *Corresponding author: Laura Cárdenas-Ortiz, University of Saskat- [3, 4, 12–20]. Birds from more northerly populations, or chewan. Department of Biology. 112 Science Place Saskatoon S7N those making over-water crossings, might be expected 5E2, Saskatchewan, Canada, Email: Laura.cardenas@usask.ca to arrive at stopover sites with relatively lower fuel loads Nicholas J. Bayly, SELVA: Investigación para la Conservación en el than those from southerly populations or those travel- Neotrópico. Diagonal 42A # 20-37, Bogotá D.C, Colombia ling overland where they are able to make more frequent Keith A. Hobson, University of Saskatchewan. Department of Biolo- stops [21]: particularly in a rapidly changing world where gy. 112 Science Place Saskatoon S7N 5E2, Saskatchewan, Canada Environment and Climate Change Canada. 11 Innovation Blvd., Sas- dependence on geographically restricted stopover habi- katoon, S7N 3H5, Saskatchewan, Canada Open Access. © 2021 Laura Cárdenas-Ortiz et al., published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 License. 28   Laura Cárdenas-Ortiz et al. tats can increase the chance of habitat availability becom- [32, 43, 44], but these differences are not always observed ing a limiting factor [22]. Longer migration distances and/ [45]. If juveniles remain less skilled foragers during migra- or more stopovers en route can also presumably expose tion, they may be able to compensate by increasing forag- individuals to more stochastic events influencing survi- ing time to achieve similar overall energy intake to adults vorship and predation [10, 16, 23, 24]. Finally, age or expe- or, alternatively, they may store larger energy reserves to rience, migration route and weather are factors known to compensate for errors generated through inexperience. affect survivorship of migrants. Several studies found refueling differences between juve- Body condition is a term used to describe the nutri- nile and adult passerines during stopover on fall migration ent and energy stores available to an individual to allocate [38, 40, 44, 46–49]; but for different findings see [50, 51]. towards life processes, with the assumption that condi- The El Niño Southern Oscillation Index (ENSO), the tion is positively related to health and fitness [25, 26]. As periodic variation in winds and sea-surface temperatures the absolute nutritional state of an individual is difficult over the tropical eastern Pacific Ocean, affects much of to obtain, body condition indices (BCIs) calculated using the tropics and subtropics [52]. The warming phase or El combinations of body morphometrics are often applied Niño results in reduced rainfall across much of Central as approximate measures of nutritional condition [27, 28]. and northern South America and reduces productivity, More direct, and non-invasive, approaches to quantifying while the cooling phase, La Niña, gives rise to increased body condition include the use of quantitative magnetic rainfall and is linked to increased productivity. How this resonance (QMR) [29] but that approach is typically dif- climatic variability affects bird migration remains poorly ficult at remote field sites. An alternative is to estimate understood, especially in the Neotropics [8]. The ENSO fuel load, a measure of the amount of energy stored by a cycle may affect the fuel load of Neotropical birds arriving bird during migration [3, 4] and therefore an appropriate at stopover sites by increasing or decreasing the availa- proxy for fuel loads in migrating birds [30]. Fuel load is bility of food resources necessary for the successful com- derived from the relationship linking a bird’s lean body pletion of migration [8]. Migrants that depend on insects mass (LBM) with some measure of physical size, such that for refueling during stopover may not be strongly affected positive values imply that an individual has fuel loads by El Niño because in the tropics, insects are generally above and beyond its LBM. When expressed as a percent- considered to be abundant year-round [53], although in age of LBM, fuel load is corrected for differences in size strongly seasonal tropical habitats this may not be true. between individuals/species, and can therefore be used to In contrast, migrants that depend on fruit resources for compare fuel reserves among species refueling may be affected by El Niño when fruit becomes Many species of Neotropical migrants undertake scarce due to dry conditions which inhibit fruiting in trop- long-distance migrations towards wintering sites located ical forests [8]. in South America but precise routes can vary greatly. To determine which factors most strongly influence Some species such as Veery (Catharus fuscescens), Black- fuel loads and therefore vulnerability during migration in poll Warbler (Setophaga striata) and Bobolink (Dolicho- Neotropical migratory landbirds, we evaluated the impact nyx oryzivorus) are known for making long over-water of several factors on arrival fuel loads in a group of 11 crossings [13, 23, 31, 32], while others such as Canada Neotropical migrants moving through a major stopover Warbler (Cardellina canadensis) and Mourning Warbler region [3, 14, 21], the Darién, in northwestern Colombia (Geothlypis philadelphia) tend to follow the Central Amer- on fall migration. This region concentrates populations ican landmass more closely [33]. If part of the risk of over- of migratory landbirds from across their North American water crossings is that birds exhaust energy reserves in breeding ranges and therefore provides a snapshot of the absence of feeding opportunities, then birds taking fuel loads from multiple breeding populations [20]. We such routes are expected to have a higher probability of aimed to determine: 1) whether individuals from northern exhausting their energy reserves relative to birds migrat- origins that travel further to reach the Darién, arrive with ing largely overland. smaller fuel loads than those from southern origins, 2) if As reviewed by McCabe and Guglielmo [34], juveniles migrants are affected by the ENSO cycle, whereby El Niño generally tend to experience poorer body condition com- years result in smaller fuel loads on arrival relative to la pared to adults during migration. This has been linked Niña years, and 3) if species known to migrate mostly over water arrived with lower fuel loads relative to those that to slower migration speed [35–37] and longer duration at migrate mostly overland. stopovers than adults [38–42]. Indeed, for some species, adults often arrive at stopover locations in better condi- tion, while juveniles may arrive lighter and with less fat Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia...    29 Figure 1: Location of study site in the Darién region of northwest Colombia: Tacarcuna Nature Reserve, Sapzurro, Chocó, Colombia. 2 Methods ally constant among days and years. Nets were opened daily beginning at dawn and remained open for 4.5 h on average, and were checked every 30-40 min. Captured 2.1 Study site and data collection birds were banded with uniquely coded Porzana-made metal bands (band reporting website: www.aselva.co). We studied a group of 11 long-distance migrants: Red- For all species, we recorded date and time of capture, age eyed Vireo (Vireo olivaceus), Veery, Swainson’s Thrush, and sex, visible subcutaneous fat score (range 0 to 8), Gray-cheeked Thrush (Catharus minimus), Yellow Warbler pectoral muscle score (range 0-3), wing chord (± 1 mm), (Setophaga petechia), Northern Waterthrush (Parkesia and body mass (±0.1 g) using an electronic balance (Fast noveboracensis), Mourning Warbler, Canada Warbler (Car- Weigh digital pocket scale, model M-500). In addition, we dellina canadensis), Prothonotary Warbler (Protonotaria collected the first primary feather of a subset of individu- citrea), Scarlet Tanager (Piranga olivacea) and Summer als from each species to determine breeding origins based Tanager (Piranga rubra), at a constant-effort mist-net on stable hydrogen isotope (δ H ) analyses. See Table 1 for station in the Tacarcuna Nature Reserve, Chocó, Colom- sample sizes of captured birds and for the number of indi- bia (08 ° 39’41.53″N, 77 ° 22’06.74″W; ~100 m asl). The viduals for which a feather was collected. reserve lies within an important stopover region described We prepared feather samples in the Environment in previous publications [14, 21] for Neotropical migrants Canada stable isotope laboratory at the National Hydrol- and in a major migration corridor for raptors and aerial ogy Research Centre (NHRC) in Saskatoon, Canada. Each insectivores [54]. The station was located near the village feather sample was soaked for 5 h in 2:1 chloroform: of Sapzurro close to the border of Colombia and Panama methanol solution then rinsed and dried in a fume hood (Figure 1). Habitat consisted of seasonal tropical humid for 48 h [55]. The impact of exchangeable hydrogen on forest interspersed with small clearings for agriculture isotopic measurements was corrected using the compar- and houses. Fall migration was monitored between 2011 ative equilibration method [56]. Within analytical runs, to 2015 using 8 to 15 mist-nets (12 or 18 m long, 32-mm Environment Canada keratin reference standards CBS mesh) between mid-September and early November. Nets (caribou [Rangifer tarandus] hoof = -197‰) and KHS were positioned strategically to maximize captures and (kudu [Tragelaphus spp.] horn = -54.1‰) were used to the number of nets and their location were kept virtu- account for exchangeable H and to calibrate samples. H 30   Laura Cárdenas-Ortiz et al. isotopic measurements were performed on H gas derived 2.2 Fuel loads and lean body mass from high temperature (1350°C on glassy carbon) flash pyrolysis of 350 ±10 μg of distal-vane feather subsam- To describe fuel loads, we first generated a linear regres- ples in silver capsules. Resulting H gas was separated in sion equation describing lean body mass (LBM) in each a Eurovector 3000 (Milan, Italy) elemental analyzer and species, using body mass and wing length data from a introduced into an Isoprime (Crewe, UK) continuous-flow group of individuals with no visible fat deposits (fat score isotope-ratio mass spectrometer. All results are reported = 0). LBM represented the average body mass of a bird for non-exchangeable H expressed in the typical delta (δ) with no visible fat for a given wing length. Taking the notation, in units per mil (‰), and normalized on the LBM equation for each species, we calculated fuel load Vienna Standard Mean Ocean Water – Standard Light for each individual using the following equation that Antarctic Precipitation (VSMOW-SLAP) standard scale. expresses fuel reserves as a percentage of LBM [30]: Fuel Based on within-run replicate (N = 5) measurements of load = ((body mass-LBM)/LBM) * 100), where LBM was laboratory keratin standards, measurement precision was calculated for each individual based on its wing length. estimated to be ± 2‰. Expressing fuel load as a percentage of LBM allows for interspecies comparisons regardless of body size [57]. Figure 2. Fuel loads were not influenced by breeding origin in most species based on δ H values in feathers of 11 species of Neotropical mig - 2 f rants captured on fall migration (2011 – 2015) in the Tacarcuna Nature Reserve, Darién, Colombia. For one species, Swainson’s Thrush, fuel loads increased with shorter migratory distances (positive relation between fuel loads and δ H values, more positive (δ H ) values indicate 2 f 2 f more southerly origins). Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia...    31 2.3 Climate conditions-ENSO variables calculated using different groups of months (e.g. 12 months prior to and including October [peak month of For the years 2011–2015, average Southern Oscillation migration for most species] and 6 months prior to and index (SOI) values were derived from monthly index data including October) for each species and included the top available through the National Oceanic and Atmospheric ranked variable in subsequent analyses. Administration’s Climate Prediction Center [58]. The SOI was used to measure the strength of ENSO in Mexico and Central America (where stopover sites expected to be used 2.4 Modelling fuel load on arrival by most species including those that make oversea cross- ings prior to arriving in the Darien are located), as has To evaluate those factors influencing arrival fuel loads, been done in previous climate studies [59, 60]. A strong we created three model sets in which fuel load on arrival positive value indicates La Niña conditions (high precip- was the response variable. Modelling was carried out in itation), and a strong negative value indicates El Niño the program R version 3.3.3 [63] and model selection was conditions (low precipitation). Within the period of study, carried out using Akaike’s information criterion (AIC), there was both a strong La Niña event (2011) and a strong comparing Δi values, where Δi was the difference between El Niño event (2015; one of the strongest events in the pre- each model and the model with the lowest AIC (i.e. Δi = vious 65 years). We carried out a model selection process AIC – minimum AIC). using AIC values [61, 62] to determine the support for SOI Figure 3. A relationship between fuel loads and the El Niño Southern Oscillation was absent for most of the 11 species of Neotropical migrants captured on fall migration in the Tacarcuna Nature Reserve, Chocó, Colombia. When controlling for age and hour of capture, Veery had significantly lower fuel loads in wetter La Niña years, while Swainson’s Thrush showed the opposite pattern. The continuous variable fuel load includes negative values indicating that fuel loads have been exhausted, while positive values > 5 indicate adequate fuel loads for continuing migration. The SOI index includes negative values (< -0.5) representing El Niño conditions (low precipitation inducing drier conditions in the Caribbean basin), and positive values (> 0.5) representing La Niña conditions (high precipitation). 32   Laura Cárdenas-Ortiz et al. Table 1. Summary table of sample size by species and the coefficients for significant effects of breeding origin, age, and the ENSO cycle on the fuel loads of 11 migratory landbirds captured during fall migration in the Tacarcuna Nature Reserve, Chocó, Colombia over five years (2011-2015). Results and sample sizes come from two analyses, a first using only birds for which an analysis of stable hydrogen isotopes was carried out to infer breeding origin and a second for which all birds captured were included (results for Age, SOI, Year, Top model, R ). We report whether there was support for significant effects of year on fuel loads, regardless of whether these could be explained by the SOI index or not. Breeding Species N (isotopes) Age (HY) SOI index Year Top Model R (adj) Origin Veery 870 (218) - -1.715* -0.665* YES SOI+Age+Hour 0.019 Gray-cheeked Thrush 914 (152) - - - YES Hour 0.037 Swainson’s Thrush 2115 (306) 0.0539* - 1.344*** YES SOI+Hour 0.030 Red-eyed Vireo 1495 (170) - -1.5398** - - Age+Hour 0.020 Yellow Warbler 136 (105) - - - - Hour 0.008 Northern Waterthrush 135 (77) - - - - Hour 0.034 Prothonotary Warbler 288 (151) - - - - SOI+Hour 0.010 Mourning Warbler 304 (146) - - -0.532 YES SOI+Hour 0.014 Canada Warbler 158 (46) - - - - Hour 0.046 Summer Tanager 119 (34) - - - YES Hour 0.031 Scarlet Tanager 103 (61) - - - - Null - Significance of coefficients: *** P < 0.001, ** P < 0.01, * P < 0.05, italics P < 0.1 2.4.1 Breeding origin average SOI values during 12 months of 6 months prior to and including October of the year of capture. To evaluate the effect of breeding origin on fuel load, we analyzed each species individually using only those individuals with a δ H value and a model set that also 2.4.3 Migration route and body size accounted for possible effects of year, age and hour of capture on fuel loads, where: Breeding origin – was the To examine the effect of migration route on fuel loads, continuous δ H value as a proxy for breeding latitude; we combined data across all species and created a third Age – a two-level factor, HY: hatch year <1 year old and model set (Table 2) including various combinations of the AHY: after hatch year >1 year old; Year – a five-level factor explanatory variables: Body Size – a continuous variable covering the years 2011 through 2015; Hour – capture hour taken as the mean LBM value by species, as an estimate of individuals converted into a continuous numeric varia- of body size; Migration Route – a two-level factor, over ble. Models included various combinations of the explan- land (migrating mostly by land) and over water (migrating atory variables through additive effects. mostly over water); Breeding Origin – the mean δ H value by species; ENSO – a continuous variable based on the SOI index; and Species – a categorical variable. Models 2.4.2 ENSO and age were run as mixed-effect models in the package lme4 [64] in Program R, including species as a random effect and To evaluate the effect of the ENSO cycle and age on fuel all other variables as fixed effects. We included the varia- load, we used the full capture dataset for each species ble lean body mass as a standard measure of body size in and ran a model set accounting for the possible effects of small passerines, as body size may influence the ability of capture hour on fuel loads. We also ran models with the birds to cope with adverse conditions such as wind, with five-level factor Year to determine whether significant vari- smaller, lighter birds being less able to counteract strong ation in fuel load existed that may or may not be accounted winds. Migration routes were based on a literature review for by the ENSO cycle. Models included various combina- of the most probable route of migration for the majority tions of the variables described above and the additional of individuals of each species during fall migration [4, 23, explanatory variable: SOI – a continuous value reflecting 65–67]. We assigned migration routes as follows: primar- Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia...    33 Table 2. Multi-species analysis using mixed effect models to determine how fuel load varies as a function of the variables: breeding origin (Origin), ENSO index, migration route (overland vs. overwater), species (S) and body size (mean lean body mass by species) on arrival at the Tacarcuna Nature Reserve, Chocó, Colombia during fall migration (years 2011- 2015). Models are ordered by the relative support they received from Akaike Information Criteria. The variable species (1|S), corresponds to a random effect. Model (Fuel load =) K AICc Delta_AICc AICcWt Migration Route + Body Size + ENSO + (1|S) 6 49539.63 0 0.35 Migration Route + Body Size + (1|S) 5 49540.15 0.52 0.27 Migration Route + Body Size + Origen + (1|S) 6 49541.88 2.25 0.12 Migration Route + ENSO + (1|S) 5 49543.47 3.84 0.05 Body Size + (1|S) 4 49543.54 3.91 0.05 Migration Route + (1|S) 4 49543.94 4.31 0.04 Origin + Body Size + ENSO + (1|S) 6 49543.98 4.34 0.04 Origin + Body Size + (1|S) 5 49544.39 4.76 0.03 Migration Route + Origin + (1|S) 5 49545.86 6.23 0.02 ENSO + (1|S) 4 49546.73 7.1 0.01 Null + (1|S) 3 49547.17 7.54 0.01 Migration Route: ENSO + (1|S) 5 49547.79 8.15 0.01 Origen 4 49548.40 8.77 0 ily overland species - Canada Warbler, Mourning Warbler, migrant), and Northern Waterthrush (a trans-Gulf, cir- Scarlet Tanager, Summer Tanager, Yellow Warbler; pri- cum-Gulf, and trans-Caribbean migrant). marily over water - Red-eyed Vireo (a trans-Gulf migrant), Veery, Swainson’s Thrush, Gray-cheeked Thrush, Protho- notary Warbler (a trans-Gulf migrant and trans-Caribbean 3 Results 6637 individuals of eleven study species were considered for analysis, of which 1466 individuals were sampled for stable isotopes in order to infer breeding origin (see Table 1 for sample sizes by species). There was considerable variation in arrival fuel load both within and between species, with values ranging from -20% LBM to 45% LBM. Averaged across species, 38% of individuals arrived at the study site with a body mass below our lean body mass estimates and typically had no visible fat reserves. The following sections summarize which of the factors pre- dicted to affect fuel loads influenced the eleven species examined in this study. 3.1 Breeding origin (surrogate for migratory Figure 4: Arrival fuel loads of 11 species of Neotropical migrants distance) grouped by their primary migratory route: over land via Mexico and Central America or trans-Gulf/trans-Caribbean before arrival at the We found support for an effect of breeding origin (as Tacarcuna Nature Reserve, Chocó, Colombia during fall migration (years 2011- 2015). Fuel loads were larger in species traveling inferred from δ H values, with more positive values indi- overwater and in birds of larger body size e.g. Swainson’s Thrush cating shorter distances [20]) in just one species, the (SWTH) and Veery (VEER). Boxplots describe the inter-quartile Swainson’s Thrush (Table 3). Swainson’s Thrush showed range, whiskers the 97.5% quartiles and individual points represent outliers. 34   Laura Cárdenas-Ortiz et al. increasing fuel loads as migratory distance decreased in Table 3. Model coefficients (SE) from the top mixed effects model describing the variation in fuel loads across 11 Neotropical migrant line with more likely southern origins. songbirds captured on fall migration in the Tacarcuna Nature Reserve, Chocó, Colombia, between 2011 and 2015. 3.2 ENSO cycle Dependent variable: Fuel load There was support for an effect of the SOI variable on Migration Route (Overwater) 3.809** fuel load in Veery and Swainson’s Thrush, with the 95% (1.431) confidence intervals for coefficients excluding zero in Body Size (LBM) 0.254** both species. In Swainson’s Thrush the coefficient was positive, indicating that individuals migrating during El (0.091) Niño years arrived with lower fuel loads than individuals ENSO (SOI12) 0.136 migrating during La Niña years (Table 3) (Figure 3). The (0.086) opposite trend was true for Veery, with birds arriving with Constant -0.412 larger fuel loads in El Niño years. In a third species, the (1.82) Mourning Warbler, there was support for an effect of SOI, Observations however, the 95% confidence intervals for the coefficient Log Likelihood -24763.81 marginally overlapped with zero. Like Veery, the coeffi- Akaike Inf. Crit. cient was negative in Mourning Warblers. 49539.62 Bayesian Inf. Crit. 49580.42 Significance of coefficients: *p<0.05; **p<0.01; ***p<0.001 3.3 Age that fuel loads at a migratory stopover in the Darién There was support for age effects in Red-eyed Vireo and region of Colombia were affected by several factors. These Veery (Table 2), with hatch-year (HY) individuals gener- included migration distance, climatic events like the El ally arriving with lower fuel loads than AHY individuals. Niño–Southern Oscillation (ENSO), age, body size and migration route. However, the influence of these factors varied considerably among species and, in general, 3.4 Effect of migration route & body size migration distance and ENSO effects on fuel loads were not as strong as we predicted for most species. Further, Among the mixed effects models including all eleven the direction of likely relationships varied among species, species there were two top models (Table 2), which as was the case for ENSO for example, implying poten- included the variables Migration Route, Body Size and tially species-dependant responses to these variables. In ENSO. However, only the 95% confidence intervals for contrast, strong support for body size being a determinant migration route and body size excluded zero, both having of fuel loads for the suite of migratory species examined, a positive effect on fuel load, such that fuel loads were suggests that physical processes may have greater influ- larger in species with overwater routes and in larger ence than either migration distance or climatic variation bodied species (Table 3). There was no support for a com- [34]. Migration route also influenced fuel load, with birds munity wide influence of breeding origin in these models. taking over water routes arriving in better condition than The effect of body size was such that for each 10 g increase those traveling primarily overland, contrary to our predic- in lean body mass, fuel load was predicted to increase by tion. Age was only significant in a few species, suggesting 2.5%, while fuel loads in species using overwater routes that there are not universal patterns among age classes were predicted to be 3.8% higher than species using over- affecting all species either. Taken together, our study land routes on average. points to the complexity of the multiple factors affecting avian migration and stopover ecology and underlines the need for long-term monitoring of avian migration, espe- 4 Discussion cially in the tropics [68]. Our analysis of five-years of data from long-distance Neo- tropical migrant songbirds during fall migration revealed Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia...    35 4.1 Effect of migration distance (breeding able effect of the ENSO cycle on two species, Veery and Swainson’s Thrush, and it is notable that the direction origin) on fuel loads of the effect differed between the two. In Veery, individ- We only found evidence for an effect of breeding origin uals arrived with lower fuel loads during La Niña condi- (as revealed by estimates of breeding latitude provided by tions, contrary to our expectation for a largely frugivorous feather δ H analysis) on fuel loads in Swainson’s Thrush. species [21]. Meanwhile, the Swainson’s Thrush, also a As predicted, Swainson’s Thrush with likely southern largely frugivorous species showed higher fuel loads in origins arrived in better condition to our site than birds (wetter) La Niña years. from more northern origins. Although breeding origin Other frugivorous species (on fall migration) in this appeared among the top models (within 2 AIC values) for study, such as Gray-cheeked Thrush, Scarlet Tanager and six of eleven species (including Swainson’s Thrush), it Red-eyed Vireo, also failed to follow the expected pattern, was often ranked below the null model, indicating a very although in the Gray-cheeked Thrush there were signifi- weak effect if it was present at all. Sample sizes varied cant differences in fuel loads between years. Such var- from 34 to 306 among species for the breeding origin anal- iation among ecologically similar species suggests that ysis and it was only in the species with the largest sample other factors may be at play and these are likely related to size that there was support for an effect. This suggests that differences in migration routes and the location of stopo- increased sample sizes could help to determine the preva- ver sites, which expose species to different conditions. It is lence of migration distance effects on fuel loads but given notable that in Costa Rica, Swainson’s Thrushes on spring the lack of support for an effect in species with samples migration showed the opposite pattern [8] to that recorded sizes >100, it is likely that migration distance does not in fall birds in the Darién. have a strong influence on fuel loads in migratory land- Five of eleven species in this study showed significant birds arriving at a stopover site. Indeed, given the number differences in fuel loads between years (Table 1), however, of species examined, that one species would show a sig- in two species the ENSO cycle did not explain this varia- nificant relationship with breeding origin is to be expected tion and in two of the remaining three, the SOI index we by chance alone. used only explained part of the variation (as evidenced by The lack of relationship between fuel loads and breed- stronger support for models with the categorical variable ing origin may also arise because of the method we used to Year versus the continuous variable SOI). These results calculate lean body mass, in which we used wing length as imply that even where inter-annual variation exists, the a measure of body size. If wing length but not overall body ENSO cycle can only explain part of it and likely other size increases with migration distance, as observed in factors such as the presence of tropical storms in the certain species [69], then we may have underestimated the Caribbean basin or conditions at distant stopover sites fuel loads of birds with more northerly origins. However, influence arrival fuel loads in our study region during fall we found no evidence for a negative relationship between migration. Finally, we cannot rule out that effects were wing length and δ H values among the 11 study species, as masked by the high inter-individual variation in our data would be expected if the above is true. and the limited number of years available. Generating more years of data under differing ENSO conditions may help to clarify this point. 4.2 Effect of the ENSO cycle on fuel loads Few studies have evaluated the direct effects of El Niño 4.3 Effect of age on fuel loads events in tropical forest animals [8, 70] but variable com- munity-level fruit production has been found to induce Fuel loads were influenced by age in Red-eyed Vireo and fluctuations in the abundance of species of frugivorous Veery. HY individuals of Veery and Red-eyed Vireo arrived mammals in Panama [70]. In Costa Rica, the fuel loads in the Darién with lower fuel loads than AHY birds, as we of insectivorous Eastern Wood-Pewees improved during had predicted based on the expectation that younger birds spring migrations coinciding with El Niño, whereas are less experienced [49, 71] and require more time to gain frugivorous Swainson’s Thrushes and Traill’s Flycatch- migratory fuel, migrate with lower fuel loads, stay longer ers experienced reduced condition during El Niño years at stopover sites, and take longer to complete their jour- [8]. However, it is unclear how general these patterns are neys [34, 71]. Further, AHY birds are expected to be more and particularly how the ENSO cycle might affect different efficient when foraging, not only due to their greater expe- species during the migration period. We found a discern- rience, but also because they may be socially dominant 36   Laura Cárdenas-Ortiz et al. over HY birds throughout the non-breeding season [72, 5 Conclusions 73]. Our study is the first attempt to understand how a suite of factors may affect fuel loads in a diverse group of migra- 4.4 Effect of migration route and body size tory landbirds at a migratory bottleneck that have com- pleted a significant proportion of their migration. Aside on fuel loads from body size and migration route, no one factor was Contrary to our prediction, species with primarily overwa- found to be common to all eleven of our study species and ter routes did not have lower fuel loads than those migrat- more importantly, the direction of effects often differed ing primarily overland. Indeed, the opposite pattern was among species. The relatively weak signal when using fuel true, with species using overwater routes having 3.8% loads as an indicator of condition suggests that high indi- larger fuel loads on average. We can only speculate as to vidual variation in fuel load may be hiding more general why this might be the case and a number of factors may patterns. It also suggests that we did not include all the explain the larger fuel loads such as the need for a greater sources of variation in our models and future studies buffer in energy reserves when migrating overwater. Alter- should examine ways to incorporate adverse weather con- natively, those species migrating overwater may migrate ditions such as tropical storms and headwinds, as well in longer flight stages and therefore generally carry more as estimating the distance that birds must cover to reach reserves than those travelling overland – this is relevant their final destination [4], for example. Importantly, the if some individuals had already refuelled to the north of lack of clear patterns implies that the factors that directly our study site following overwater flights. Interpretation impact migratory condition through body mass are of this result is further complicated by the fact that actual species dependent and cannot be summarized in general routes adopted by the different species that pass through relationships. This has important implications for under- the Darién have not been well documented. Nonetheless, standing which species are most vulnerable to events or among the Catharus thrushes for which geolocators have changes during migration. While we can conclude that, in described the migration routes of disparate populations general, smaller bodied species will likely be more vulner- [23, 74, 75], Veery and Swainson’s Thrush [21] showed no able to shifting wind patterns or loss of stopover habitat, clear difference in condition, despite the trans-Caribbean few other factors were as clear cut. route adopted by Veery and the trans-Gulf/Central Ameri- It was surprising to find opposite responses to predic- can route used by most Swainson’s Thrushes. tions regarding the ENSO cycle among species and while In addition to migration route, body size also had a this may in part be due to high variation between indi- significant effect on fuel load in our multi-species model. vidual strategies that could hide more general patterns, Our results showed that larger species (e.g. Veery, Gray- it suggests that the impacts of climate change [5], for cheeked Thrush, Swainson’s Thrush) arrived in better example, will not be unidirectional but instead depend on condition than smaller individuals/species (e.g. North- the location of individual species/population’s stopover ern Waterthrush, Mourning Warbler, Yellow Warbler, sites. Another important finding from this study, is that and Canada Warbler). In terms of flight efficiency, bigger increasing migration distance does not necessarily make birds have higher aspect ratios than smaller birds, which individuals more vulnerable to the rigors of migration or promote greater flight efficiency [76]. In general, smaller at least when fuel loads are considered an indicator of vul- birds have lower lift to drag ratios than larger ones, as well nerability to starvation or other lethal events. Alternative as having higher basal metabolism [76], both of which explanations for the steeper declines observed in long-dis- translate into a higher energy expenditure in order to tance migrants include a higher potential for phenologi- cover a given distance. Reduced lift [76] also means that cal mismatch at more distant points on the globe [77] or a smaller birds may be less able to counteract unfavorable lower cumulative survival probability in birds that migrate wind directions, making them more vulnerable to storms farther as they typically spend more days on migration over water and daily survival probability is generally lower during migration [10]. Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia...    37 [10] Sillett T.S., Holmes R.T., Variation in survivorship of a Acknowledgments migratory songbird throughout its annual cycle, J. Anim. Ecol., 2002, 71, 296–308 This research was funded by an operating grant to KAH [11] Calvert A.M., Walde S.J., Taylor P.D., Nonbreeding-Season Drivers of Population Dynamics in seasonal migrants : from Environment and Climate Change Canada and a Conservation parallels across taxa, Avian Conserv. Ecol., grant to NJB from the Rufford Small Grants Foundation. 2009, 4 Fieldwork and exportation of feathers was conducted [12] Bayly N.J., Gomez C., Comparison of autumn and spring under permits issued by the Autoridad Nacional de Licen- migration strategies of Neotropical migratory landbirds in cias Ambientales (ANLA) to SELVA in Colombia. We are northeast Belize, J. F. Ornithol., 2011, 82, 117–131 most grateful to F. Jimenez and M. Rubio for supporting [13] Bayly N.J., Gómez C., Hobson K.A., González A.M., Rosenberg K. V., Fall migration of the Veery (Catharus fuscescens) in this research and allowing us to work in the Tacarcuna northern Colombia: determining the importance of a stopover Nature Reserve in Sapzurro, Darién. We also thank our site, Auk, 2012, 129, 449–459 field researchers, including C. Gomez, J. Sanabria, M. [14] Bayly N.J., Gómez C., Hobson K.A., Rosenberg K. V, Rubio, V. Gomez, H. 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Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia: Influence of migratory distance, route, ENSO, age and body size

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Anim. Migr. 2021; 8:27–39 Research Article Laura Cárdenas-Ortiz*, Nicholas J. Bayly, Keith A. Hobson Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia: Influence of migratory distance, route, ENSO, age and body size https://doi.org/10.1515/ami-2020-0105 Keywords: Bird migration, Deuterium, El Niño, fuel load, received May 11, 2020; accepted March 5, 2021 stable isotopes, vulnerability Abstract: Available energy stores determine stopover length, migration speed and likely survival in migrating birds. We measured energy stores by estimating fuel load in 11 species of Neotropical migrant songbirds in the Darién 1 Introduction of Colombia over five years. We evaluated 1) whether indi- viduals flying further from breeding origin arrived with As a group and throughout the World, long-distance smaller fuel loads, 2) if the ENSO (El Niño-Southern Oscil- migrant birds are declining at faster rates than short-dis- lation) cycle affected fuel load and 3) if species known to tance migrants and resident species [1, 2]. Why this group migrate mostly overwater arrived with less fuel relative to appears to be more vulnerable than other groups of those migrating overland. Breeding origin, inferred from birds is still open to speculation. Breeding origin is one feather δ H values, only had a significant positive effect factor that can influence survivorship [3, 4], with longer on fuel load in Swainson’s Thrush (Catharus ustulatus). migrations involving greater risks [5]. Other authors have Veery (Catharus fuscescens) and Swainson’s thrush had hypothesized that long-distance migrants are exposed to higher and lower fuel loads, respectively, in El Niño years. greater climatic variability, including tropical storms and Multi-species mixed-effects models revealed support for hurricanes [6]. For Neotropical migratory birds that cross larger fuel loads in larger-bodied species and in species the Gulf of Mexico and the Caribbean Sea, such factors are taking overwater routes, contrary to our prediction. also linked to the El Niño Southern Oscillation (ENSO)[7, Across species, we found no support for common effects 8]. Migratory success in songbirds has also been linked of breeding origin or ENSO on fuel loads, in contrast to to experience, with younger, more inexperienced birds community-wide effects of migration route and body-size. expected to have lower survival during migratory episodes In general, the variables considered here explained little [9]. of the variance in fuel loads, suggesting that inter-individ- To date, few studies have attempted to determine ual differences likely have a greater impact than broad- which factors might influence the success of long-distance scale factors in our study system. migration despite migration accounting for up to 80% of annual mortality in small migratory passerines [6, 10, 11]. Migratory birds are typically available for study before or after migration or at key stopover sites where they refuel *Corresponding author: Laura Cárdenas-Ortiz, University of Saskat- [3, 4, 12–20]. Birds from more northerly populations, or chewan. Department of Biology. 112 Science Place Saskatoon S7N those making over-water crossings, might be expected 5E2, Saskatchewan, Canada, Email: Laura.cardenas@usask.ca to arrive at stopover sites with relatively lower fuel loads Nicholas J. Bayly, SELVA: Investigación para la Conservación en el than those from southerly populations or those travel- Neotrópico. Diagonal 42A # 20-37, Bogotá D.C, Colombia ling overland where they are able to make more frequent Keith A. Hobson, University of Saskatchewan. Department of Biolo- stops [21]: particularly in a rapidly changing world where gy. 112 Science Place Saskatoon S7N 5E2, Saskatchewan, Canada Environment and Climate Change Canada. 11 Innovation Blvd., Sas- dependence on geographically restricted stopover habi- katoon, S7N 3H5, Saskatchewan, Canada Open Access. © 2021 Laura Cárdenas-Ortiz et al., published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 License. 28   Laura Cárdenas-Ortiz et al. tats can increase the chance of habitat availability becom- [32, 43, 44], but these differences are not always observed ing a limiting factor [22]. Longer migration distances and/ [45]. If juveniles remain less skilled foragers during migra- or more stopovers en route can also presumably expose tion, they may be able to compensate by increasing forag- individuals to more stochastic events influencing survi- ing time to achieve similar overall energy intake to adults vorship and predation [10, 16, 23, 24]. Finally, age or expe- or, alternatively, they may store larger energy reserves to rience, migration route and weather are factors known to compensate for errors generated through inexperience. affect survivorship of migrants. Several studies found refueling differences between juve- Body condition is a term used to describe the nutri- nile and adult passerines during stopover on fall migration ent and energy stores available to an individual to allocate [38, 40, 44, 46–49]; but for different findings see [50, 51]. towards life processes, with the assumption that condi- The El Niño Southern Oscillation Index (ENSO), the tion is positively related to health and fitness [25, 26]. As periodic variation in winds and sea-surface temperatures the absolute nutritional state of an individual is difficult over the tropical eastern Pacific Ocean, affects much of to obtain, body condition indices (BCIs) calculated using the tropics and subtropics [52]. The warming phase or El combinations of body morphometrics are often applied Niño results in reduced rainfall across much of Central as approximate measures of nutritional condition [27, 28]. and northern South America and reduces productivity, More direct, and non-invasive, approaches to quantifying while the cooling phase, La Niña, gives rise to increased body condition include the use of quantitative magnetic rainfall and is linked to increased productivity. How this resonance (QMR) [29] but that approach is typically dif- climatic variability affects bird migration remains poorly ficult at remote field sites. An alternative is to estimate understood, especially in the Neotropics [8]. The ENSO fuel load, a measure of the amount of energy stored by a cycle may affect the fuel load of Neotropical birds arriving bird during migration [3, 4] and therefore an appropriate at stopover sites by increasing or decreasing the availa- proxy for fuel loads in migrating birds [30]. Fuel load is bility of food resources necessary for the successful com- derived from the relationship linking a bird’s lean body pletion of migration [8]. Migrants that depend on insects mass (LBM) with some measure of physical size, such that for refueling during stopover may not be strongly affected positive values imply that an individual has fuel loads by El Niño because in the tropics, insects are generally above and beyond its LBM. When expressed as a percent- considered to be abundant year-round [53], although in age of LBM, fuel load is corrected for differences in size strongly seasonal tropical habitats this may not be true. between individuals/species, and can therefore be used to In contrast, migrants that depend on fruit resources for compare fuel reserves among species refueling may be affected by El Niño when fruit becomes Many species of Neotropical migrants undertake scarce due to dry conditions which inhibit fruiting in trop- long-distance migrations towards wintering sites located ical forests [8]. in South America but precise routes can vary greatly. To determine which factors most strongly influence Some species such as Veery (Catharus fuscescens), Black- fuel loads and therefore vulnerability during migration in poll Warbler (Setophaga striata) and Bobolink (Dolicho- Neotropical migratory landbirds, we evaluated the impact nyx oryzivorus) are known for making long over-water of several factors on arrival fuel loads in a group of 11 crossings [13, 23, 31, 32], while others such as Canada Neotropical migrants moving through a major stopover Warbler (Cardellina canadensis) and Mourning Warbler region [3, 14, 21], the Darién, in northwestern Colombia (Geothlypis philadelphia) tend to follow the Central Amer- on fall migration. This region concentrates populations ican landmass more closely [33]. If part of the risk of over- of migratory landbirds from across their North American water crossings is that birds exhaust energy reserves in breeding ranges and therefore provides a snapshot of the absence of feeding opportunities, then birds taking fuel loads from multiple breeding populations [20]. We such routes are expected to have a higher probability of aimed to determine: 1) whether individuals from northern exhausting their energy reserves relative to birds migrat- origins that travel further to reach the Darién, arrive with ing largely overland. smaller fuel loads than those from southern origins, 2) if As reviewed by McCabe and Guglielmo [34], juveniles migrants are affected by the ENSO cycle, whereby El Niño generally tend to experience poorer body condition com- years result in smaller fuel loads on arrival relative to la pared to adults during migration. This has been linked Niña years, and 3) if species known to migrate mostly over water arrived with lower fuel loads relative to those that to slower migration speed [35–37] and longer duration at migrate mostly overland. stopovers than adults [38–42]. Indeed, for some species, adults often arrive at stopover locations in better condi- tion, while juveniles may arrive lighter and with less fat Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia...    29 Figure 1: Location of study site in the Darién region of northwest Colombia: Tacarcuna Nature Reserve, Sapzurro, Chocó, Colombia. 2 Methods ally constant among days and years. Nets were opened daily beginning at dawn and remained open for 4.5 h on average, and were checked every 30-40 min. Captured 2.1 Study site and data collection birds were banded with uniquely coded Porzana-made metal bands (band reporting website: www.aselva.co). We studied a group of 11 long-distance migrants: Red- For all species, we recorded date and time of capture, age eyed Vireo (Vireo olivaceus), Veery, Swainson’s Thrush, and sex, visible subcutaneous fat score (range 0 to 8), Gray-cheeked Thrush (Catharus minimus), Yellow Warbler pectoral muscle score (range 0-3), wing chord (± 1 mm), (Setophaga petechia), Northern Waterthrush (Parkesia and body mass (±0.1 g) using an electronic balance (Fast noveboracensis), Mourning Warbler, Canada Warbler (Car- Weigh digital pocket scale, model M-500). In addition, we dellina canadensis), Prothonotary Warbler (Protonotaria collected the first primary feather of a subset of individu- citrea), Scarlet Tanager (Piranga olivacea) and Summer als from each species to determine breeding origins based Tanager (Piranga rubra), at a constant-effort mist-net on stable hydrogen isotope (δ H ) analyses. See Table 1 for station in the Tacarcuna Nature Reserve, Chocó, Colom- sample sizes of captured birds and for the number of indi- bia (08 ° 39’41.53″N, 77 ° 22’06.74″W; ~100 m asl). The viduals for which a feather was collected. reserve lies within an important stopover region described We prepared feather samples in the Environment in previous publications [14, 21] for Neotropical migrants Canada stable isotope laboratory at the National Hydrol- and in a major migration corridor for raptors and aerial ogy Research Centre (NHRC) in Saskatoon, Canada. Each insectivores [54]. The station was located near the village feather sample was soaked for 5 h in 2:1 chloroform: of Sapzurro close to the border of Colombia and Panama methanol solution then rinsed and dried in a fume hood (Figure 1). Habitat consisted of seasonal tropical humid for 48 h [55]. The impact of exchangeable hydrogen on forest interspersed with small clearings for agriculture isotopic measurements was corrected using the compar- and houses. Fall migration was monitored between 2011 ative equilibration method [56]. Within analytical runs, to 2015 using 8 to 15 mist-nets (12 or 18 m long, 32-mm Environment Canada keratin reference standards CBS mesh) between mid-September and early November. Nets (caribou [Rangifer tarandus] hoof = -197‰) and KHS were positioned strategically to maximize captures and (kudu [Tragelaphus spp.] horn = -54.1‰) were used to the number of nets and their location were kept virtu- account for exchangeable H and to calibrate samples. H 30   Laura Cárdenas-Ortiz et al. isotopic measurements were performed on H gas derived 2.2 Fuel loads and lean body mass from high temperature (1350°C on glassy carbon) flash pyrolysis of 350 ±10 μg of distal-vane feather subsam- To describe fuel loads, we first generated a linear regres- ples in silver capsules. Resulting H gas was separated in sion equation describing lean body mass (LBM) in each a Eurovector 3000 (Milan, Italy) elemental analyzer and species, using body mass and wing length data from a introduced into an Isoprime (Crewe, UK) continuous-flow group of individuals with no visible fat deposits (fat score isotope-ratio mass spectrometer. All results are reported = 0). LBM represented the average body mass of a bird for non-exchangeable H expressed in the typical delta (δ) with no visible fat for a given wing length. Taking the notation, in units per mil (‰), and normalized on the LBM equation for each species, we calculated fuel load Vienna Standard Mean Ocean Water – Standard Light for each individual using the following equation that Antarctic Precipitation (VSMOW-SLAP) standard scale. expresses fuel reserves as a percentage of LBM [30]: Fuel Based on within-run replicate (N = 5) measurements of load = ((body mass-LBM)/LBM) * 100), where LBM was laboratory keratin standards, measurement precision was calculated for each individual based on its wing length. estimated to be ± 2‰. Expressing fuel load as a percentage of LBM allows for interspecies comparisons regardless of body size [57]. Figure 2. Fuel loads were not influenced by breeding origin in most species based on δ H values in feathers of 11 species of Neotropical mig - 2 f rants captured on fall migration (2011 – 2015) in the Tacarcuna Nature Reserve, Darién, Colombia. For one species, Swainson’s Thrush, fuel loads increased with shorter migratory distances (positive relation between fuel loads and δ H values, more positive (δ H ) values indicate 2 f 2 f more southerly origins). Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia...    31 2.3 Climate conditions-ENSO variables calculated using different groups of months (e.g. 12 months prior to and including October [peak month of For the years 2011–2015, average Southern Oscillation migration for most species] and 6 months prior to and index (SOI) values were derived from monthly index data including October) for each species and included the top available through the National Oceanic and Atmospheric ranked variable in subsequent analyses. Administration’s Climate Prediction Center [58]. The SOI was used to measure the strength of ENSO in Mexico and Central America (where stopover sites expected to be used 2.4 Modelling fuel load on arrival by most species including those that make oversea cross- ings prior to arriving in the Darien are located), as has To evaluate those factors influencing arrival fuel loads, been done in previous climate studies [59, 60]. A strong we created three model sets in which fuel load on arrival positive value indicates La Niña conditions (high precip- was the response variable. Modelling was carried out in itation), and a strong negative value indicates El Niño the program R version 3.3.3 [63] and model selection was conditions (low precipitation). Within the period of study, carried out using Akaike’s information criterion (AIC), there was both a strong La Niña event (2011) and a strong comparing Δi values, where Δi was the difference between El Niño event (2015; one of the strongest events in the pre- each model and the model with the lowest AIC (i.e. Δi = vious 65 years). We carried out a model selection process AIC – minimum AIC). using AIC values [61, 62] to determine the support for SOI Figure 3. A relationship between fuel loads and the El Niño Southern Oscillation was absent for most of the 11 species of Neotropical migrants captured on fall migration in the Tacarcuna Nature Reserve, Chocó, Colombia. When controlling for age and hour of capture, Veery had significantly lower fuel loads in wetter La Niña years, while Swainson’s Thrush showed the opposite pattern. The continuous variable fuel load includes negative values indicating that fuel loads have been exhausted, while positive values > 5 indicate adequate fuel loads for continuing migration. The SOI index includes negative values (< -0.5) representing El Niño conditions (low precipitation inducing drier conditions in the Caribbean basin), and positive values (> 0.5) representing La Niña conditions (high precipitation). 32   Laura Cárdenas-Ortiz et al. Table 1. Summary table of sample size by species and the coefficients for significant effects of breeding origin, age, and the ENSO cycle on the fuel loads of 11 migratory landbirds captured during fall migration in the Tacarcuna Nature Reserve, Chocó, Colombia over five years (2011-2015). Results and sample sizes come from two analyses, a first using only birds for which an analysis of stable hydrogen isotopes was carried out to infer breeding origin and a second for which all birds captured were included (results for Age, SOI, Year, Top model, R ). We report whether there was support for significant effects of year on fuel loads, regardless of whether these could be explained by the SOI index or not. Breeding Species N (isotopes) Age (HY) SOI index Year Top Model R (adj) Origin Veery 870 (218) - -1.715* -0.665* YES SOI+Age+Hour 0.019 Gray-cheeked Thrush 914 (152) - - - YES Hour 0.037 Swainson’s Thrush 2115 (306) 0.0539* - 1.344*** YES SOI+Hour 0.030 Red-eyed Vireo 1495 (170) - -1.5398** - - Age+Hour 0.020 Yellow Warbler 136 (105) - - - - Hour 0.008 Northern Waterthrush 135 (77) - - - - Hour 0.034 Prothonotary Warbler 288 (151) - - - - SOI+Hour 0.010 Mourning Warbler 304 (146) - - -0.532 YES SOI+Hour 0.014 Canada Warbler 158 (46) - - - - Hour 0.046 Summer Tanager 119 (34) - - - YES Hour 0.031 Scarlet Tanager 103 (61) - - - - Null - Significance of coefficients: *** P < 0.001, ** P < 0.01, * P < 0.05, italics P < 0.1 2.4.1 Breeding origin average SOI values during 12 months of 6 months prior to and including October of the year of capture. To evaluate the effect of breeding origin on fuel load, we analyzed each species individually using only those individuals with a δ H value and a model set that also 2.4.3 Migration route and body size accounted for possible effects of year, age and hour of capture on fuel loads, where: Breeding origin – was the To examine the effect of migration route on fuel loads, continuous δ H value as a proxy for breeding latitude; we combined data across all species and created a third Age – a two-level factor, HY: hatch year <1 year old and model set (Table 2) including various combinations of the AHY: after hatch year >1 year old; Year – a five-level factor explanatory variables: Body Size – a continuous variable covering the years 2011 through 2015; Hour – capture hour taken as the mean LBM value by species, as an estimate of individuals converted into a continuous numeric varia- of body size; Migration Route – a two-level factor, over ble. Models included various combinations of the explan- land (migrating mostly by land) and over water (migrating atory variables through additive effects. mostly over water); Breeding Origin – the mean δ H value by species; ENSO – a continuous variable based on the SOI index; and Species – a categorical variable. Models 2.4.2 ENSO and age were run as mixed-effect models in the package lme4 [64] in Program R, including species as a random effect and To evaluate the effect of the ENSO cycle and age on fuel all other variables as fixed effects. We included the varia- load, we used the full capture dataset for each species ble lean body mass as a standard measure of body size in and ran a model set accounting for the possible effects of small passerines, as body size may influence the ability of capture hour on fuel loads. We also ran models with the birds to cope with adverse conditions such as wind, with five-level factor Year to determine whether significant vari- smaller, lighter birds being less able to counteract strong ation in fuel load existed that may or may not be accounted winds. Migration routes were based on a literature review for by the ENSO cycle. Models included various combina- of the most probable route of migration for the majority tions of the variables described above and the additional of individuals of each species during fall migration [4, 23, explanatory variable: SOI – a continuous value reflecting 65–67]. We assigned migration routes as follows: primar- Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia...    33 Table 2. Multi-species analysis using mixed effect models to determine how fuel load varies as a function of the variables: breeding origin (Origin), ENSO index, migration route (overland vs. overwater), species (S) and body size (mean lean body mass by species) on arrival at the Tacarcuna Nature Reserve, Chocó, Colombia during fall migration (years 2011- 2015). Models are ordered by the relative support they received from Akaike Information Criteria. The variable species (1|S), corresponds to a random effect. Model (Fuel load =) K AICc Delta_AICc AICcWt Migration Route + Body Size + ENSO + (1|S) 6 49539.63 0 0.35 Migration Route + Body Size + (1|S) 5 49540.15 0.52 0.27 Migration Route + Body Size + Origen + (1|S) 6 49541.88 2.25 0.12 Migration Route + ENSO + (1|S) 5 49543.47 3.84 0.05 Body Size + (1|S) 4 49543.54 3.91 0.05 Migration Route + (1|S) 4 49543.94 4.31 0.04 Origin + Body Size + ENSO + (1|S) 6 49543.98 4.34 0.04 Origin + Body Size + (1|S) 5 49544.39 4.76 0.03 Migration Route + Origin + (1|S) 5 49545.86 6.23 0.02 ENSO + (1|S) 4 49546.73 7.1 0.01 Null + (1|S) 3 49547.17 7.54 0.01 Migration Route: ENSO + (1|S) 5 49547.79 8.15 0.01 Origen 4 49548.40 8.77 0 ily overland species - Canada Warbler, Mourning Warbler, migrant), and Northern Waterthrush (a trans-Gulf, cir- Scarlet Tanager, Summer Tanager, Yellow Warbler; pri- cum-Gulf, and trans-Caribbean migrant). marily over water - Red-eyed Vireo (a trans-Gulf migrant), Veery, Swainson’s Thrush, Gray-cheeked Thrush, Protho- notary Warbler (a trans-Gulf migrant and trans-Caribbean 3 Results 6637 individuals of eleven study species were considered for analysis, of which 1466 individuals were sampled for stable isotopes in order to infer breeding origin (see Table 1 for sample sizes by species). There was considerable variation in arrival fuel load both within and between species, with values ranging from -20% LBM to 45% LBM. Averaged across species, 38% of individuals arrived at the study site with a body mass below our lean body mass estimates and typically had no visible fat reserves. The following sections summarize which of the factors pre- dicted to affect fuel loads influenced the eleven species examined in this study. 3.1 Breeding origin (surrogate for migratory Figure 4: Arrival fuel loads of 11 species of Neotropical migrants distance) grouped by their primary migratory route: over land via Mexico and Central America or trans-Gulf/trans-Caribbean before arrival at the We found support for an effect of breeding origin (as Tacarcuna Nature Reserve, Chocó, Colombia during fall migration (years 2011- 2015). Fuel loads were larger in species traveling inferred from δ H values, with more positive values indi- overwater and in birds of larger body size e.g. Swainson’s Thrush cating shorter distances [20]) in just one species, the (SWTH) and Veery (VEER). Boxplots describe the inter-quartile Swainson’s Thrush (Table 3). Swainson’s Thrush showed range, whiskers the 97.5% quartiles and individual points represent outliers. 34   Laura Cárdenas-Ortiz et al. increasing fuel loads as migratory distance decreased in Table 3. Model coefficients (SE) from the top mixed effects model describing the variation in fuel loads across 11 Neotropical migrant line with more likely southern origins. songbirds captured on fall migration in the Tacarcuna Nature Reserve, Chocó, Colombia, between 2011 and 2015. 3.2 ENSO cycle Dependent variable: Fuel load There was support for an effect of the SOI variable on Migration Route (Overwater) 3.809** fuel load in Veery and Swainson’s Thrush, with the 95% (1.431) confidence intervals for coefficients excluding zero in Body Size (LBM) 0.254** both species. In Swainson’s Thrush the coefficient was positive, indicating that individuals migrating during El (0.091) Niño years arrived with lower fuel loads than individuals ENSO (SOI12) 0.136 migrating during La Niña years (Table 3) (Figure 3). The (0.086) opposite trend was true for Veery, with birds arriving with Constant -0.412 larger fuel loads in El Niño years. In a third species, the (1.82) Mourning Warbler, there was support for an effect of SOI, Observations however, the 95% confidence intervals for the coefficient Log Likelihood -24763.81 marginally overlapped with zero. Like Veery, the coeffi- Akaike Inf. Crit. cient was negative in Mourning Warblers. 49539.62 Bayesian Inf. Crit. 49580.42 Significance of coefficients: *p<0.05; **p<0.01; ***p<0.001 3.3 Age that fuel loads at a migratory stopover in the Darién There was support for age effects in Red-eyed Vireo and region of Colombia were affected by several factors. These Veery (Table 2), with hatch-year (HY) individuals gener- included migration distance, climatic events like the El ally arriving with lower fuel loads than AHY individuals. Niño–Southern Oscillation (ENSO), age, body size and migration route. However, the influence of these factors varied considerably among species and, in general, 3.4 Effect of migration route & body size migration distance and ENSO effects on fuel loads were not as strong as we predicted for most species. Further, Among the mixed effects models including all eleven the direction of likely relationships varied among species, species there were two top models (Table 2), which as was the case for ENSO for example, implying poten- included the variables Migration Route, Body Size and tially species-dependant responses to these variables. In ENSO. However, only the 95% confidence intervals for contrast, strong support for body size being a determinant migration route and body size excluded zero, both having of fuel loads for the suite of migratory species examined, a positive effect on fuel load, such that fuel loads were suggests that physical processes may have greater influ- larger in species with overwater routes and in larger ence than either migration distance or climatic variation bodied species (Table 3). There was no support for a com- [34]. Migration route also influenced fuel load, with birds munity wide influence of breeding origin in these models. taking over water routes arriving in better condition than The effect of body size was such that for each 10 g increase those traveling primarily overland, contrary to our predic- in lean body mass, fuel load was predicted to increase by tion. Age was only significant in a few species, suggesting 2.5%, while fuel loads in species using overwater routes that there are not universal patterns among age classes were predicted to be 3.8% higher than species using over- affecting all species either. Taken together, our study land routes on average. points to the complexity of the multiple factors affecting avian migration and stopover ecology and underlines the need for long-term monitoring of avian migration, espe- 4 Discussion cially in the tropics [68]. Our analysis of five-years of data from long-distance Neo- tropical migrant songbirds during fall migration revealed Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia...    35 4.1 Effect of migration distance (breeding able effect of the ENSO cycle on two species, Veery and Swainson’s Thrush, and it is notable that the direction origin) on fuel loads of the effect differed between the two. In Veery, individ- We only found evidence for an effect of breeding origin uals arrived with lower fuel loads during La Niña condi- (as revealed by estimates of breeding latitude provided by tions, contrary to our expectation for a largely frugivorous feather δ H analysis) on fuel loads in Swainson’s Thrush. species [21]. Meanwhile, the Swainson’s Thrush, also a As predicted, Swainson’s Thrush with likely southern largely frugivorous species showed higher fuel loads in origins arrived in better condition to our site than birds (wetter) La Niña years. from more northern origins. Although breeding origin Other frugivorous species (on fall migration) in this appeared among the top models (within 2 AIC values) for study, such as Gray-cheeked Thrush, Scarlet Tanager and six of eleven species (including Swainson’s Thrush), it Red-eyed Vireo, also failed to follow the expected pattern, was often ranked below the null model, indicating a very although in the Gray-cheeked Thrush there were signifi- weak effect if it was present at all. Sample sizes varied cant differences in fuel loads between years. Such var- from 34 to 306 among species for the breeding origin anal- iation among ecologically similar species suggests that ysis and it was only in the species with the largest sample other factors may be at play and these are likely related to size that there was support for an effect. This suggests that differences in migration routes and the location of stopo- increased sample sizes could help to determine the preva- ver sites, which expose species to different conditions. It is lence of migration distance effects on fuel loads but given notable that in Costa Rica, Swainson’s Thrushes on spring the lack of support for an effect in species with samples migration showed the opposite pattern [8] to that recorded sizes >100, it is likely that migration distance does not in fall birds in the Darién. have a strong influence on fuel loads in migratory land- Five of eleven species in this study showed significant birds arriving at a stopover site. Indeed, given the number differences in fuel loads between years (Table 1), however, of species examined, that one species would show a sig- in two species the ENSO cycle did not explain this varia- nificant relationship with breeding origin is to be expected tion and in two of the remaining three, the SOI index we by chance alone. used only explained part of the variation (as evidenced by The lack of relationship between fuel loads and breed- stronger support for models with the categorical variable ing origin may also arise because of the method we used to Year versus the continuous variable SOI). These results calculate lean body mass, in which we used wing length as imply that even where inter-annual variation exists, the a measure of body size. If wing length but not overall body ENSO cycle can only explain part of it and likely other size increases with migration distance, as observed in factors such as the presence of tropical storms in the certain species [69], then we may have underestimated the Caribbean basin or conditions at distant stopover sites fuel loads of birds with more northerly origins. However, influence arrival fuel loads in our study region during fall we found no evidence for a negative relationship between migration. Finally, we cannot rule out that effects were wing length and δ H values among the 11 study species, as masked by the high inter-individual variation in our data would be expected if the above is true. and the limited number of years available. Generating more years of data under differing ENSO conditions may help to clarify this point. 4.2 Effect of the ENSO cycle on fuel loads Few studies have evaluated the direct effects of El Niño 4.3 Effect of age on fuel loads events in tropical forest animals [8, 70] but variable com- munity-level fruit production has been found to induce Fuel loads were influenced by age in Red-eyed Vireo and fluctuations in the abundance of species of frugivorous Veery. HY individuals of Veery and Red-eyed Vireo arrived mammals in Panama [70]. In Costa Rica, the fuel loads in the Darién with lower fuel loads than AHY birds, as we of insectivorous Eastern Wood-Pewees improved during had predicted based on the expectation that younger birds spring migrations coinciding with El Niño, whereas are less experienced [49, 71] and require more time to gain frugivorous Swainson’s Thrushes and Traill’s Flycatch- migratory fuel, migrate with lower fuel loads, stay longer ers experienced reduced condition during El Niño years at stopover sites, and take longer to complete their jour- [8]. However, it is unclear how general these patterns are neys [34, 71]. Further, AHY birds are expected to be more and particularly how the ENSO cycle might affect different efficient when foraging, not only due to their greater expe- species during the migration period. We found a discern- rience, but also because they may be socially dominant 36   Laura Cárdenas-Ortiz et al. over HY birds throughout the non-breeding season [72, 5 Conclusions 73]. Our study is the first attempt to understand how a suite of factors may affect fuel loads in a diverse group of migra- 4.4 Effect of migration route and body size tory landbirds at a migratory bottleneck that have com- pleted a significant proportion of their migration. Aside on fuel loads from body size and migration route, no one factor was Contrary to our prediction, species with primarily overwa- found to be common to all eleven of our study species and ter routes did not have lower fuel loads than those migrat- more importantly, the direction of effects often differed ing primarily overland. Indeed, the opposite pattern was among species. The relatively weak signal when using fuel true, with species using overwater routes having 3.8% loads as an indicator of condition suggests that high indi- larger fuel loads on average. We can only speculate as to vidual variation in fuel load may be hiding more general why this might be the case and a number of factors may patterns. It also suggests that we did not include all the explain the larger fuel loads such as the need for a greater sources of variation in our models and future studies buffer in energy reserves when migrating overwater. Alter- should examine ways to incorporate adverse weather con- natively, those species migrating overwater may migrate ditions such as tropical storms and headwinds, as well in longer flight stages and therefore generally carry more as estimating the distance that birds must cover to reach reserves than those travelling overland – this is relevant their final destination [4], for example. Importantly, the if some individuals had already refuelled to the north of lack of clear patterns implies that the factors that directly our study site following overwater flights. Interpretation impact migratory condition through body mass are of this result is further complicated by the fact that actual species dependent and cannot be summarized in general routes adopted by the different species that pass through relationships. This has important implications for under- the Darién have not been well documented. Nonetheless, standing which species are most vulnerable to events or among the Catharus thrushes for which geolocators have changes during migration. While we can conclude that, in described the migration routes of disparate populations general, smaller bodied species will likely be more vulner- [23, 74, 75], Veery and Swainson’s Thrush [21] showed no able to shifting wind patterns or loss of stopover habitat, clear difference in condition, despite the trans-Caribbean few other factors were as clear cut. route adopted by Veery and the trans-Gulf/Central Ameri- It was surprising to find opposite responses to predic- can route used by most Swainson’s Thrushes. tions regarding the ENSO cycle among species and while In addition to migration route, body size also had a this may in part be due to high variation between indi- significant effect on fuel load in our multi-species model. vidual strategies that could hide more general patterns, Our results showed that larger species (e.g. Veery, Gray- it suggests that the impacts of climate change [5], for cheeked Thrush, Swainson’s Thrush) arrived in better example, will not be unidirectional but instead depend on condition than smaller individuals/species (e.g. North- the location of individual species/population’s stopover ern Waterthrush, Mourning Warbler, Yellow Warbler, sites. Another important finding from this study, is that and Canada Warbler). In terms of flight efficiency, bigger increasing migration distance does not necessarily make birds have higher aspect ratios than smaller birds, which individuals more vulnerable to the rigors of migration or promote greater flight efficiency [76]. In general, smaller at least when fuel loads are considered an indicator of vul- birds have lower lift to drag ratios than larger ones, as well nerability to starvation or other lethal events. Alternative as having higher basal metabolism [76], both of which explanations for the steeper declines observed in long-dis- translate into a higher energy expenditure in order to tance migrants include a higher potential for phenologi- cover a given distance. Reduced lift [76] also means that cal mismatch at more distant points on the globe [77] or a smaller birds may be less able to counteract unfavorable lower cumulative survival probability in birds that migrate wind directions, making them more vulnerable to storms farther as they typically spend more days on migration over water and daily survival probability is generally lower during migration [10]. Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia...    37 [10] Sillett T.S., Holmes R.T., Variation in survivorship of a Acknowledgments migratory songbird throughout its annual cycle, J. Anim. Ecol., 2002, 71, 296–308 This research was funded by an operating grant to KAH [11] Calvert A.M., Walde S.J., Taylor P.D., Nonbreeding-Season Drivers of Population Dynamics in seasonal migrants : from Environment and Climate Change Canada and a Conservation parallels across taxa, Avian Conserv. Ecol., grant to NJB from the Rufford Small Grants Foundation. 2009, 4 Fieldwork and exportation of feathers was conducted [12] Bayly N.J., Gomez C., Comparison of autumn and spring under permits issued by the Autoridad Nacional de Licen- migration strategies of Neotropical migratory landbirds in cias Ambientales (ANLA) to SELVA in Colombia. We are northeast Belize, J. F. Ornithol., 2011, 82, 117–131 most grateful to F. Jimenez and M. Rubio for supporting [13] Bayly N.J., Gómez C., Hobson K.A., González A.M., Rosenberg K. V., Fall migration of the Veery (Catharus fuscescens) in this research and allowing us to work in the Tacarcuna northern Colombia: determining the importance of a stopover Nature Reserve in Sapzurro, Darién. We also thank our site, Auk, 2012, 129, 449–459 field researchers, including C. Gomez, J. Sanabria, M. [14] Bayly N.J., Gómez C., Hobson K.A., Rosenberg K. V, Rubio, V. Gomez, H. 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Journal

Animal Migrationde Gruyter

Published: Jan 1, 2021

Keywords: Bird migration; Deuterium; El Niño; fuel load; stable isotopes; vulnerability

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