population
Adam M. Fudickar and Jesko Partecke
In Review
Abstract
Partial migration occurs when a breeding population consists of seasonal migrants and year round residents. Although it is common among birds, the basis of individual movement decisions within partially migratory populations is still unresolved.
Due to the existence of both migratory and sedentary strategies within partially migratory populations, partial migration is considered an intermediate stage between fixed migratory and sedentary life histories at the population and species level.
Over four years we used state of the art tracking techniques, a combination of
geolocators and radio transmitters, to follow individual European blackbirds, Turdus merula, year round from a partially migratory population to determine individual strategies and departure and arrival dates. The individual-based tracking combined with measures of energetic and hormonal (corticosterone) state enabled us to test several classical hypotheses of partial migration: the ‘Arrival time’-, ‘Dominance’- and ‘Thermal Tolerance’-hypotheses. Two distinct migratory periods were observed during the study; one in early autumn, and another during the midst of winter. While blackbirds that migrated in autumn were never observed overwintering within 300 km of the study site, four individuals that departed in the winter were observed within 40 km. Females were significantly more likely to migrate in autumn than males but there was no difference in the age or body size of migrants and non-migrants in autumn.
Just prior to autumn migration, migrants had higher fat scores than non-migrants and tended to have higher levels of baseline corticosterone. Unlike autumn migrants, we found no difference between the tendency for males and females to migrate in winter, nor did we find any difference in body size or age of winter migrants. Autumn
migration was sex biased and resembled obligate migration. Our results provide strong support for The Arrival Time hypothesis for partial migration in the autumn.
By tracking individuals year round, we were able to identify a second period of departures. Overall, these results suggest the co-occurrence of obligate autumn migrants, facultative winter migrants and sedentary individuals within a single population.
Introduction
Seasonal migration is a common trait in a diverse range of taxa that facilitates the exploitation of temporally pulsing resources in geographically distant habitats. Seasonal migration optimizes reproductive fitness during the critical phase of offspring rearing while increasing survival the remainder of the year. Even in the tropics, where seasonal environmental variability is less extreme compared to temperate latitudes, many species migrate annually (Greenberg 1980; Joseph 1997; Jahn et al. 2006). Migrations are often anticipatory: animals start migrating at times when environmental conditions are still benign where they are, escaping before conditions deteriorate. Despite the predictive nature of migration, many migratory species are flexible in their migratory behaviour, allowing for adjustments to unpredictable environmental conditions during migration (Jenni and Schaub 2003; Schmaljohann et al. 2009; Schmaljohann and Naef-Daenzer 2011).
Ongoing changes in habitat phenology and broad scale changes in weather patterns have resulted in variable responses by migratory populations. Some migratory populations have adapted to these changes and flourished while others are apparently limited in their ability to respond (Wilcove 2008). For migratory birds at north temperate latitudes, some populations have advanced the timing of their spring arrival in response to changing spring phenologies and in some cases the frequency, distances and even
directions of migrations are changing (Hüppop and Hü ppop 2003; Bearhop et al. 2005;
Pulido and Berthold 2010). Given the rate at which the earth’s biosphere is changing, it is clear that individual flexibility and population variability are critical for the survival of migratory populations globally.
Migratory patterns within populations can be variable. One exceptional case of variable migration strategies within a population is partial migration. Partially migratory populations consist of both seasonal migrants and year round residents. Therefore, partial migration is thought of as an intermediate stage between fixed migratory and fixed sedentary life histories (Berthold 2001). Increased knowledge on the interaction of migrants with the environment and the selective pressures that shape migratory life histories is important for our basic understanding of the evolution of migration but also for informing policy decisions directed at preserving migratory populations.
The mechanisms responsible for individual strategies within partially migratory bird populations are still mostly unresolved. Although the mechanisms most likely vary between species and populations, two general hypotheses have been advanced:
genetically controlled and condition dependent partial migration. Genetic determination of migratory behaviour within partially migratory bird populations was proposed almost as early as the phenomenon was identified in the literature (Thomson 1921; Nice 1933;
Lack 1944). Controlled lab studies over the past four decades have provided estimates for the heritability of nocturnal locomotor activity “Zugunruhe” which coincides with the timing of autumn and spring migration for free-living counterparts. Heritability estimates for onset, termination and intensity of Zugunruhe for partially migratory populations range from 0.16 to 0.67 (Newton 2008). Although these results are intriguing, it is difficult to interpret what Zugunruhe corresponds to in wild populations. Helm and Gwinner (2006) found that resident African stonechats, Saxicola torquata, express seasonal Zugunruhe in captivity. The author’s interpretation of their findings was that
Zugunruhe could be a regular feature of the endogenous program of birds that might act to facilitate periodic movements in non migrants.
If migratory behaviour is a genetic dimorphism, then in order for both migratory and sedentary morphs to be maintained within a population, differences in survival and reproduction should vary across years. If one strategy were to maintain a fitness
advantage, it could become fixed within the population relatively fast (Pulido and Berthold 2010). Further, if genetic determination of migratory strategy is a true dimorphism in a population, then there should be equal age and sex ratios of migrants unless the trait is either 1) a sexual dimorphism or 2) an ontogenetic trait that changes throughout an individual’s lifetime.
The ‘Arrival Time’ hypothesis of partial migration posits that if the reproductive fitness of one sex is partly influenced by the acquisition of a territory in early spring, and quality territories are limited, then it is to the advantage of individuals of that sex to be at the breeding grounds as early as possible (Ketterson and Nolan 1976). If lifetime fitness is on average increased by remaining at breeding grounds year round, then selection could lead to residency among the sex that establishes a territory. Conversely, if over-winter survival of the sex which chooses a mate based on territory quality is increased by leaving the breeding grounds during the non breeding season and no net fitness advantage results from residency, then selection could promote migratory behaviour in that sex.
Conditional differences that result in differences in overwintering strategies within a population could occur if breeding habitat is only sufficient enough to support a fraction of the population through the non breeding season. In this case, partial migration results from individual asymmetries where migration is a conditional strategy and
migrants are making the “best of a bad job” (Lundberg 1987; Lundberg 1988). The
‘Dominance’ hypothesis of partial migration, also referred to as The ‘Competitive Release’ hypothesis, proposes that competition for limited food requires subordinate individuals to leave the breeding grounds during the non breeding season. Field based studies on temperate breeding birds have provided support for The ‘Dominance’
hypothesis (Schwabl 1983; Lundberg 1985; Smith and Nilsson 1987; Nilsson et al.
2008). Individual asymmetries that might lead to variation in migratory strategy are not limited to competitive ability; the ‘Thermal Tolerance’ hypothesis of partial migration, also referred to as The ‘Body Size’ hypothesis, predicts that individual differences in thermal efficiency result in differences in migratory tendency (Able and Belthoff 1998).
Previous studies at north temperate latitudes have found correlations between body size and migratory tendency, with smaller individuals most likely to migrate (Chapman et al.
2011). The interpretation of these results has been that larger individuals are more capable of surviving extreme temperatures and limited food during the winter due to greater metabolic efficiency and are therefore less likely to migrate than smaller individuals.
In the current study, we tested predictions of The ‘Arrival Time’, ‘Thermal Tolerance’ and ‘Dominance’ hypotheses of partial migration by tracking European blackbirds from a partially migratory population in southern Germany year-round using automated radio telemetry and light-level loggers (geolocators) (Table 1). Male
blackbirds compete for quality territories during the early spring (Lundberg 1985).
Therefore, our prediction for The ‘Arrival Time’ hypothesis was that female blackbirds would migrate more frequently than males (Table 1). During the non-breeding season a
Table 1. Hypotheses and predictions of partial migration.
Hypothesis Description Prediction
Arrival time
(Ketterson and Nolan 1976) Intrasexual competition for breeding territory promotes residency among the territorial sex.
male blackbirds should migrate less frequently than females
Thermal tolerance
(Ketterson and Nolan 1976) Individual differences in thermal efficiency leads to migration among the least efficient.
the tendency to migrate among blackbirds should increase with decreasing body size
Dominance
(Gauthreaux 1982) Competition for limited food
leads to migration among subordinates.
resident --- migrant adult ♂ > adult ♀ > 1st year ♂ > 1st year ♀
clear dominance hierarchy exists in European blackbird foraging flocks. Adults are dominant over juveniles and males are dominant over females during aggressive
encounters over food (Lundberg and Schwabl 1983; Lundberg 1985). Our prediction for The ‘Dominance’ hypothesis was that first year birds would migrate more frequently than adults and females would migrate more frequently than males (Table 1). For The
‘Thermal Tolerance’ hypothesis we predicted that smaller individuals would migrate more frequently than larger individuals (Table 1). Age and sex related differences in local movements during the non-breeding season could bias migration estimates towards juveniles and non-territorial individuals. Using a combination of year-round radio
telemetry and geolocators we were able to distinguish between true migration events and local dispersal. We also compared physiological correlates of energetic state of autumn migrants and non-migrants in the weeks preceding autumn departures from the breeding grounds. By comparing the energetic state of migratory and sedentary individuals in the weeks prior to autumn migration, we aimed to test whether individual condition, as measured by energetic state, is an indicator of the decision to migrate. Further, by
comparing age, sex, body size and energetic state of migrants and non-migrants our aim was to identify if migratory behaviour is a fixed or condition dependent strategy.
Materials and methods
European blackbirds, Turdus merula, were captured over four years (2009 – 2012) in a mixed coniferous/deciduous forest in southern Germany (N 47° 47’, E 9° 2’). Birds were initially captured in spring and summer using mist nets. 5-12 mist nets (12 m wide x 3 m tall) were opened between civil twilight and 12:00, when weather permitted. Nets were placed on the edge of breeding habitat next to known foraging areas. Nets were checked every 30 min. Age and sex of individuals was determined based on plumage differences (Svensson 1992). Prior to first pre-basic molt, the sex of hatch-year blackbirds cannot be determined based on plumage differences. 50 μl of blood was collected from hatch-year birds from the brachial vein by venipuncture for molecular sex determination. Tarsus length has been shown to be a reliable measure of body size in blackbirds as in many other species (Alatalo and Lundberg 1986; Richner 1989, Merilä 1997). We used tarsus length as a measure of structural body size and it was measured to the nearest 0.5 mm using dial calipers to compare the body size of migrants to non migrants.
Mk 10S and Mk 12S geolocators (≤ 1.2 g; British Antarctic Survey, Cambridge, UK) connected to radio transmitters (≤ 2.6 g; Sparrow Systems, Fisher, IL, USA) with heat shrink tubing (≤ 0.4 g), were attached to birds via leg-loop harnesses. A range of harness sizes were built from 1 mm elastic beading cord to fit the naturally occurring body sizes of blackbirds in the population (Naef-Daenzer 2007). Each backpack weighed
< 5% of the mass of the individual that it was deployed on. Once a harness was fitted to a
bird, it was inspected for appropriateness of fit. All birds were observed for as long as possible after release and throughout deployment to ensure normal behaviour. All transmitters and geolocators were manufactured to last at least one year. Beginning each March, birds tagged the previous year were recaptured for backpack removal and
deployment of a new backpack consisting of a new transmitter and geolocator. In 2010 and 2011, newly captured birds were also tagged with backpacks.
To identify presence of individuals at the breeding site and departure dates, all birds were tracked using radio telemetry whenever present at the study site. In the first year, all birds were located twice per week from the date of capture until 1 December 2009. Beginning 1 December, birds were tracked once per week by ground until recapture the following spring. In the second and third years, birds were tracked twice per week by ground after capture until recapture the next spring except from 20
December – 10 January when birds were monitored from automated receivers
exclusively. Ground tracking was done using the combination of either a handheld three element Yagi antenna (AF Antronics, Inc., Urbana, IL, USA) and AR 8200 MKIII handheld receiver (AOR U.S.A., Inc., Torrance, CA, USA) or a handheld H antenna (Andreas Wagener Telemetry Systems, Köln, DE) and a Yaesu VR 500 handheld receiver (Vertex Standard USA, Cypress, CA, USA). If an individual could not be located by ground tracking, aerial searches encompassing a 20 km radius (minimum) of the study site were performed using a Cessna airplane equipped with two H-antennas, one per wing, and two Biotrack receivers, one per antenna (Lotek, Newmarket, ON, Can).
Individuals were classified as migrants after at least two searches from the air without a signal.
Three to five stationary automated receivers (Sparrow Systems, Fisher, IL, USA) were present at the study site throughout the study to monitor the presence of individuals, and departure and arrival dates (Kays et al. 2011; Mitchell et al. 2012). Each automated receiver searched for 16 frequencies every 60 seconds. Automated receivers were connected to H antennas (ATS, Isanti, MN, USA), mounted 3 – 6 m high. Not all birds were captured within range of an automated receiver; therefore, manual tracking was the only means for monitoring their presence. After a departure was identified, extensive ground and air tracking was done to confirm absences. After recapture, geolocators were used to confirm departure and arrival dates (see Fudickar et al. 2012 for detail of methods for geolocator analysis).
In each year we observed a bimodal distribution in post breeding departures from our study site (one in early autumn and one in winter). We performed a k-means cluster analysis with an a priori criterion of two clusters to classify migrants into one of the two categories (“autumn” or “winter”). We justified separating migrants into two periods given that the periods were bimodal with autumn departures occurring immediately after post-breeding molt and before the onset of winter conditions while winter departures occurred in the midst of winter during periods of extreme minimum temperatures.
To compare the energetic state of migrants and non-migrants just prior to autumn departure, we recaptured tagged individuals (14 migrants and 22 non migrants) between 20 September and 20 October in 2010 and 2011 (referred to as the “pre-migratory period”). The same catching procedure was used during the pre-migratory period as in spring and summer however, only 1 – 6 mist nets were opened. Based on 2009 departure dates, this period was chosen because it provided the best opportunity to capture migrants
just prior to departure. To ensure that all individuals were in a similar resorptive state, only individuals captured between civil twilight and 09:30 were used for comparison.
Migratory birds undergo a suite of endogenously controlled physiological changes prior to migration to prepare for the energetically taxing behaviour of migration.
Endogenously controlled fat accumulation, prior to migration, provides migrants with the fuel reserves required for their journey (Berthold 1996). All tagged individuals recaptured during the “pre-migratory period” received a subcutanteous furculum fat score based on a scale of 0 – 5 (Helms and Drury 1960). To rule out the potential for observer differences in fat scores, all scores were assigned by AMF.
Immediately after capture, during the pre-migratory period, we collected 400 – 500 μl of blood from recaptured individuals from the brachial vein by venipuncture. All samples used for analysis were collected ≤ 180 seconds. Blood samples were
immediately stored on ice and transported to Vogelwarte Radolfzell for plasma extraction within 3 hours of collection. Plasma samples were stored at -70°C until they were
assayed. To assess the physiological state of migrants and non-migrants, we compared plasma levels of triglycerides and baseline corticosterone of migrants and non migrants during the “pre-migratory period” (20 September – 20 October).
Plasma levels of triglycerides (TRIG) have been used in avian studies to asses the physiological state and condition of free living individuals. Circulating plasma TRIG levels have been shown to increase during feeding and decrease during fasting (Jenni-Eiermann and Jenni 1998). Plasma TRIG levels were determined using a standard spectrophotometric assay (see Masello and Quillfeldt 2004). We added 6 μl of undiluted plasma to 600 μl Triglycerides reagent (n° 981786, Thermo Fisher Scientific) (warmed to
37°C). Standard curves were calculated for each run using the combination of 6 μl of sCal (n° 981831, Thermo Fisher Scientific) and 600 μl Triglycerides reagent. Plasma samples and standards were incubated for 5 minutes at 37°C after addition to the Triglycerides reagent. Absorptions were then measured at 540 nm wavelength. All samples were run on the same day but not in the same run. New standard curves were calculated for each run.
Glucocorticosteroid corticosterone (CORT) is produced in the adrenal cortex of birds and acts to increase carbohydrate metabolism and mediate the effects of stressful stimuli (Nelson 2005). Circulating levels of CORT have also been shown to be elevated in migrating birds (Piersma et al. 2000; Holberton et al. 2008). Migration is an
energetically demanding activity and CORT acts to mobilize energy reserves. We compared baseline CORT (≤ 180 seconds) of autumn migrants with residents during the pre-migratory period. Following methods in Ouyang et al. (2011), CORT concentrations were determined from 7 μl plasma samples after a diethyl-ether extraction using an enzyme immunoassay kit (Cat. No. 900-097, Enzo Life Sciences). The intra-plate coefficient of variation of two replicate standards was 8.3%.
For comparisons of migrants and non-migrants we performed tests comparing 1) autumn migrants with those who stayed behind through the autumn migration period and 2) winter migrants with those who stayed through the winter. To determine if different ages and sexes were more or less migratory as predicted by The ‘Arrival Time’ and The
‘Dominance’ Hypotheses we ran separate Fisher’s exact tests for autumn and winter periods. Separate multinomial logistic regressions were run to explore the correlates of migrating in either autumn or winter as a function of year, age, sex, tarsus and the
interactions between sex and tarsus and age and year using stepwise backward elimination. To explore differences in physiological measures of energetic state of autumn migrants and non-migrants we ran one multivariate general linear model with migratory strategy (yes/no) as a fixed factor and baseline CORT (log transformed), fat (log transformed) and TRIG (log transformed) as dependent variables. A priori, we excluded CORT and TRIG outliers from statistical analyses. All statistical analyses were performed in SPSS 15.0.
Results
Out of 153 blackbirds monitored, 68 (44.4%) were classified as migrants. 15 birds which were included as non-migrants in the autumn died between December and February and are therefore (conservatively) not included in the comparison of winter migrants and sedentary birds. The cluster analysis assigned 19 individuals to the winter migration group (mean: 30 December, range: 30 November – 7 February) and 47 to the autumn migration group (mean: 15 October, range: 19 September – 9 November) (Fig. 1).
Throughout the study, autumn migrants were never observed by aerial radio tracking less than 300 km from the study site after the date of departure and before arrival date. The results of aerial tracking of autumn migrants were confirmed by all geolocators that were recaptured. Unlike autumn migrants, four winter migrants were located by airplane tracking (range: 6 – 38 km from the study site). Four winter migrants, which were not located after departure, were recaptured the following spring. Geolocator estimates
Throughout the study, autumn migrants were never observed by aerial radio tracking less than 300 km from the study site after the date of departure and before arrival date. The results of aerial tracking of autumn migrants were confirmed by all geolocators that were recaptured. Unlike autumn migrants, four winter migrants were located by airplane tracking (range: 6 – 38 km from the study site). Four winter migrants, which were not located after departure, were recaptured the following spring. Geolocator estimates