At-sea movement and migration of the nocturnal swallow-tailed gull (Creagrus furcatus)
Dissertation submitted for the degree of Doctor of Natural Sciences
Presented by Sebastian M. Cruz
at the
Faculty of Sciences Department of Biology
Date of the oral examination: 23rd October 2013 First supervisor: Martin Wikelski
Second supervisor: Niels Rattenborg
Table of contents
1. General Introduction...3 The swallow-tailed gull (Creagrus furcatus)
Historical observations and history of the species Objectives
Additional Publications
2. At-sea behavior varies with lunar phase in nocturnal pelagic seabird, the
swallow-tailed gull………8 Introduction
Materials & Methods Results
Discussion
Figures and Tables
3. Sub-annual breeding cycles in seabirds explained by extraordinary migration strategy….………...27 Introduction
Materials & Methods Results
Discussion
Figures and Tables
!
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4. Finding!Food!at!Night:!The!Foraging!Strategies!of!a!Nocturnal!Seabird,!the!
Swallow;tailed!Gull………..34%
Introduction Materials & Methods Results Discussion Figures and Tables 5. General conclusions………63
Main Findings Limitations of the study Conservation Implications Future Directions 6. Summary / Zusammenfassung……….70
7. References………...72
8. Acknowledgements……….84
9. Author Contributions………85
10. Declaration in lieu of oath……….87
11. Appendix...………..88
1. General Introduction
Seabirds are markedly different to other avian groups in their life history characteristics, which are often referred to as extreme: they are long-lived, have deferred maturity, small clutch sizes and extended chick rearing periods (Schreiber, 2002). Historically, seabirds have been used as model organisms to address ecological questions related to the regulation of population size, foraging behavior, inter and intraspecific competition and the influence of the environment on life history traits (Piatt, 2007). This is because seabirds are relatively easy to observe, capture, mark and manipulate when they are on land to breed (Balance, 2007). These attributes have also contributed to their increased use as indicators of the condition and health of the marine environment (Burger, 2008).
In the past, research on seabirds, was restricted to the breeding colonies or observations from boats resulting in an incomplete understanding of their ecology. Seabirds are marine animals that spend most of their life over the open ocean (> 90%) covering large distances over short periods of time, making it very hard to study individual animals at-sea. This situation has changed in the past two decades and it is now increasingly easier to study seabirds at-sea, while they are foraging or migrating, thanks to the advancement of precise tracking devices and auxiliary loggers that can measure an array of environmental variables (Weimerskirch)(Wilson, 2002)(Burger, 2008). These new sources of information have provided unprecedented insights into the locomotion, physiology, foraging behavior, migration, demographics and exposure to anthropogenic threats (Burger, 2008).
Understanding the movements of seabirds at sea is highly relevant to our understanding of the ecological and evolutionary processes involved in the movement of highly mobile organisms. Furthermore, because of impacts on the marine environment from human exploitation, pollution, and climate change seabirds are currently the most threatened avian
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is critical for the development of conservation and management strategies. In addition, seabirds are increasingly being viewed as tools for oceanography and climatology capable of providing essential physical and biological information on the sea itself (Burger, 2008)
The swallow-tailed gull (Creagrus furcatus)
Swallow-tailed gulls (Creagrus furcatus) are a unique Larid species that breeds in the Galapagos Islands all year round (Harris, 1970). The main breeding population (<10000 pairs) is in the Galápagos Archipelago, occupying large and small islands alike (Harris, 1970). There is a small population (>300 individuals) on Malpelo Island of the coast of Colombia. When not breeding, it is an entirely pelagic gull, migrating eastward to the coasts of Ecuador and Peru (Harris, 1970).
Past research has revealed ecological characteristics that are unlike other gulls including obligate nocturnal pelagic foraging, no daily melatonin rhythm, aseasonal and asynchronous breeding cycles, a single egg-clutch and high adult survival rates (Harris, 1970.
Hailman, 1964; Snow & Snow, 1968; Wikelski et al., 2005). The life history traits of Swallow-tailed gulls more closely resemble those of the Procellariiformes instead of other gull species. The conservation status of Creagrus is of ‘Least Concern’ but the population trend is not known and there is scarce information on range and distribution (BirdLife , 2009). In addition, the ecological characteristics of this species make it a potentially interesting model to study tropical seabird foraging strategies and movement. I suggest that the above circumstances warranted further research with the application of technologies and techniques unavailable to previous researches.
Our research took place in the Galapagos Islands, focused primarily on the Swallow- tailed gull populations of Punta Cevallos, Española Island (1.39° S, 89.62° W) and Darwin
Bay, Genovesa Island (0.19º S, 89.57º W); smaller expeditions have taken place to the Punta Suárez, Española Island and South Plazas Island colonies.
Historical observations and history of the species
Adolph-Simon Neboux described and named Swallow-tailed gulls as Creagrus furcatus during his voyage on the French frigate La Venus, between the years 1836 and 1839.
The name means “meat hook” referring to the shape of the bill. Almost a century later the species was more thoroughly examined by Murphy (1936) who compiled information on breeding behaviour, distribution and possible nocturnal habits. Decades later Jack P. Hailman carefully observed daily cycles and confirmed that Swallow-tailed gulls forage exclusively at night (1964). Facilitated by the establishment of the Charles Darwin Research Station in 1964 several studies were conducted by researchers Barbara and David Snow, as well as Michael Harris throughout the 1960s. The Snow’s (1968) studied swallow-tailed gull behaviour and described it as “strikingly different” from other gulls. Harris (1970) produced an extensive study of the breeding ecology of the species, including estimations of adult seasonal survival, population size, phenology and chick growth rates. Due to the fact that swallow-tailed gulls have a single egg clutch despite its two brood patches, Harris conducted a brood-doubling experiment in which he concluded that swallow-tailed gulls could successfully raise two chicks without any apparent consequences to the adult or chick. Later, Agreda and Anderson (2003) found that swallow-tailed gulls were unable to successfully raise two chicks simultaneously. The last scientific study was by Wikelski et al. (2005) who carried out a comparison of plasma melatonin concentrations with a diurnal gull (Larus ridibundus). The results demonstrate that swallow-tailed gulls lack a circadian rhythm, presumably because they have to be active predominantly at night but also intermittently during the day.
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Objectives
The study of seabirds at-sea -where they spend the vast majority of their time- is essential for a comprehensive understanding of their ecology. Despite their unusual ecological characteristics, such as, obligate nocturnal pelagic foraging, a single-egg clutch, and a 9- month breeding cycle, swallow-tailed gulls are poorly studied. The following work demonstrates that important gaps of knowledge on the at-sea behavior and distribution of swallow-tailed gulls remain. The general objective of this project was to apply cutting edge tracking technology to investigate the foraging strategies, breeding distribution and migration of swallow-tailed gulls. The specific objectives where: (1) gather information and precisely describe the way a tropical obligate nocturnal pelagic seabird forages for food and to compare this foraging strategy with diurnal seabirds species; (2) gather information on the at-sea spatial distribution of several swallow-tailed gull colonies during the breeding season, explore relationships with breeding cycles, time of year and oceanographic conditions; (3) identify the main migratory pathways and non-breeding areas and investigate the migratory strategy of an non-seasonal sub-annual breeding seabird. This work will further our knowledge of swallow-tailed gull ecology and of tropical seabirds in general. Furthermore, the information provided by this study will be not only of scientific interest but also aid conservation and management strategies in the Galapagos Islands.
Additional Publications
During my doctoral studies I significantly contributed in the publication of two scientific articles for which I am co-author. These were published in the new peer-reviewed Movement Ecology Journal, an interdisciplinary periodical that focuses on the ecology of movement in whole organisms. The subjects of movement and seabirds, which includes foraging,
dispersals and migration, relate both publications to my thesis. My contributions in both papers satisfy the following conditions: (1) I substantially contributed to the acquisition of the data, it’s analysis and interpretation; (2) I participated in the critical revisions for intellectual content; (3) I reviewed and approved the final submitted version. Both articles are included in this thesis as supplementary material in the appendix (II, III). The titles are:
1. Safi, K., Kranstauber, B., Weinzierl, R., Griffin, L., Rees, E. C., David Cabot, Cruz, C., Proaño, C., Takekawa, Y. J., Newman, S. H., Waldenström, J., Bengtsson, D., Kays, R., Wikelski, M., Bohrer, G. Flying with the wind: scale dependency of speed and direction measurements in modelling wind support in avian flight. Movement Ecology, 1, 4 (2013).
2. Dodge, S. Bohrer, G., Weinzierl, R., Davidson, S. R., Kays, R., Douglas, D., Cruz, S., Han, J., Brandes, D., Wikelski, M. The environmental-data automated track annotation (Env-DATA) system: linking animal tracks with environmental data. Movement Ecology 1, 3 (2013).
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2. At-sea behavior varies with lunar phase in nocturnal pelagic seabird, the swallow-tailed gull
Sebastian M. Cruz, Mevin Hooten,Kathryn P. Huyvaert, Carolina B. Proaño, David J. Anderson, Vsevolod Afanasyev & Martin Wikelski
Published February 26, 2013 in PLoS ONE. doi:10.1371/journal.pone.0056889
Introduction
The lunar cycle influences the ecology, movements, and foraging behavior of many nocturnal organisms through its effect on light availability (Fingerman, 1957; Kotzerka, Garthe, & Hatch, 2010; Monaghan & Monaghan, 1996; Naylor, 2001; Tessmar-Raible, Raible, & Arboleda, 2011; R. Wilson et al., 2007). Predators such as owls, bats, and nightjars concentrate their activity within certain periods of the night and of the lunar cycle to maximize hunting success (Ballance & Ainley, 2001; Jetz, Steffen, & Linsenmair, 2003;
Weimerskirch, Le Corre, Jaquemet, & Marsac, 2005). In contrast, some nocturnally active prey animals like rats, insects, and frogs alter their activity across the lunar cycle to avoid visual predators (Daly, Behrends, Wilson, & Jacobs, 1992; Lang, Kalko, Römer, &
Bockholdt, 2006; Longhurst & Pauly, 1987; Meyer, Schwarz, & Fahr, 1999; Weimerskirch, 2007). In marine systems, the lunar phase is known to influence the diel vertical migration (DVM) of zooplankton, squid, and fish, potential prey that feed at the ocean surface at night and hide at depth from visual surface predators during the day (Ballance & Pitman, 1999;
Castro & Huber, 2009; M. Z. Gliwicz, 1986; Luecke & Wurtsbaugh, 1993). The extent of the DVM varies in concert with the degree of moonlight during the lunar cycle: the DVM is reduced on the brightest nights and is most extensive when the moon is in the new phase
(Ballance & Ainley, 2001; deBruyn & Meeuwig, 2001; Z. M. Gliwicz & Gliwicz, 1986;
Harris, 1977; Lowry, Williams, & Metti, 2007). During dark nights, surface densities of prey can be a thousand times greater than during the day; this migration is more pronounced at low than high latitudes, and in pelagic than neritic waters (Brinton, 1967).
The migration by prey in the DVM isolates them from most pelagic birds, many of which forage mostly or strictly during daylight (Ballance & Pitman, 1999). Nonetheless, some marine predators can use celestial illumination effectively to obtain prey at night, especially as the lunar phase approaches full (Fraser, 1997). Common murres, Uria aalge, dive deeper under high nocturnal illumination, matching the DVM patterns of capelin, Mallotus villosus, their main prey (Regular, Hedd, & Montevecchi, 2011). Some species of albatross show a positive correlation between nocturnal flight activity and moon phase, and nighttime activity of petrels and shearwaters matches lunar phase: they fly more and land on water more frequently during full moon conditions, suggesting that nighttime visual foraging is more effective when ambient light level is highest (Awkerman, Fukuda, Higuchi, &
Anderson, 2005; Phalan et al., 2007; Pinet, Jaeger, Cordier, Potin, & Le Corre, 2011;
Weimerskirch, Wilson, & Lys, 1997; Yamamoto, Takahashi, Yoda, & Katsumata, 2007).
These and other studies on the effects of the lunar cycle on seabird behavior involve species that are largely diurnal, but engage in some nighttime foraging activity (Awkerman et al., 2005; Ballance, 2007; Pinet et al., 2011). A concern is that marine predators that rely on optical cues to forage effectively are constrained by their visual adaptations to hunt only in a specific light range (Hall, 2007; Regular et al., 2011). The swallow-tailed gull Creagrus furcatus is an oceanic nocturnal specialist that eats squid and small fish that rise to the surface at night, capturing them by surface plunging (Ballance & Pitman, 1999; Hailman, 1964;
Harris, 1970; 1977; Schreiber, 2002; Snow & Snow, 1968) and Cruz et. al. unpublished data].
The diet of swallow-tailed gulls consists mainly of squid Sthenoteuthis oualaniensis, an
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abundant, vertically migrating species in the tropical Pacific, and also clupeid fish whose distribution varies vertically with time of day (Harris, 1970; Zuyev, Nigmatullin, Chesalin, &
Nesis, 2002). The adaptations for nocturnal foraging in swallow-tailed gulls include large eyes with a layer of tissue, the tapetum lucidum, that reflects visible light back through the retina, increasing the light available to the eye’s photoreceptors (Harris, 1977). Similar traits have evolved in a range of nocturnal predators and are thought to increase foraging efficiency (Garamszegi, Møller, & Erritzøe, 2002; Hall, 2007). Given these adaptations, the swallow- tailed gull may not be subject to the visual constraints imposed by darkness that affect many other species of seabird, such that this species presents an excellent opportunity to study the relationships between the phases of the moon and at-sea behavior in a nocturnal specialist.
In this paper we examine activity data that cover several consecutive lunar cycles to explore whether at-sea behavior varies with lunar phase in swallow-tailed gulls, complementing the extensive existing work on diurnal species (Fernandez, 2000; Phalan et al., 2007; Regular et al., 2011; Weimerskirch et al., 1997; Yamamoto et al., 2007). Recently developed global location sensors (GLS) equipped with wet/dry loggers can record bird activity over long periods of time (Croxall, 2005). Recent studies have used this technology successfully to investigate a wide range of questions regarding seabird activity at-sea (Pinet et al., 2011; Regular et al., 2011; Yamamoto et al., 2007). We deployed GLS units on a sample (n = 50) of swallow-tailed gulls, to explore their at-sea behavior in relation to lunar phase.
We tested the hypothesis that swallow-tailed gulls maximize their foraging activity when prey is most available. Accordingly, we predicted that foraging activity, measured as the proportion of nighttime spent on water, is higher during darker periods of the lunar cycle, coinciding with the strongest DVM and highest prey density. We included sea surface
temperature (SST) as a factor in our analysis because a mild El Niño Southern Oscillation (ENSO) event occurred during the study period, which increased the variability of SST (Climate Prediction Center, National Centers for Environmental Prediction NOAA/National Weather Service). Large fluctuations in the amplitude of SST during ENSO events influence seabird reproduction, probably mediated by temperature-related changes in the abundance of marine prey (Ballance, Pitman, & Fiedler, 2006; Cubaynes, Doherty, Schreiber, & Gimenez, 2011).
Materials and Methods
Study Site and Sensor Deployment and Recovery
Archival global location sensors (GLS) with a wet/dry sensor (MK14, mass 1.5g; size 20 x 9 x 5.5mm; British Antarctic Survey) were deployed on 50 adult swallow-tailed gulls between 18-21 October, 2009 at Punta Cevallos, Española Island, Galápagos, Ecuador (1° 23' S, 89 °37' W). Swallow-tailed gulls breed asynchronously; this study included adults at the egg laying (n = 33), incubating (n = 9), chick rearing (n = 1), and fledgling (n = 7) stages.
Birds were captured by hand at their nest or while resting on rocks and then held by one member of a two-person team. Each bird was fitted on its left leg with a plastic band (Pro- Touch Engraving, Canada) to which the GLS had been attached earlier with epoxy resin and cable ties (mass of logger, band, epoxy and cable tie: 2 g, ~ 0.3% of adult body mass). Bird capture and handling times were ~5 min during logger deployment and recovery. We did not detect any adverse effects from handling or tag attachment on reproduction as none of the tagged breeding birds abandoned their nests or other parental care in the days following tag deployment. Recaptures occurred at different times during 2010 and 2011 due to the asynchronous breeding schedules of swallow-tailed gulls, such that the deployment period for each bird was between six and sixteen months. Each logger was equipped with a wet/dry sensor that detects immersion in seawater. Wet or dry status was recorded every 3 s as a 1 or
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0; these data were summed over 10 min intervals by the loggers, providing a value from 0 to 200 that represents the proportion of time an individual spent in the water during each 10 min period. The Galápagos National Park Service approved of and granted the research permits for this work.
Post-deployment Data Processing and Analysis
Immersion data, our indicator of foraging activity, were uploaded and decompressed with BAStrak software version 8 (British Antarctic Survey, March 2010). The raw data from the unit were values from 0 to 200, indicating the number of 3 s periods during 10 min blocks that the sensor on the unit was wet. We were interested in the proportion of time that breeding individuals spent in the water at night. To calculate this, the values from all 10 min blocks (blocks per night = 72) were summed for each night, providing an aggregated count of 3 s sub-periods in which a bird was on the water. These were transformed to the total proportion of time a bird was in the water by finding the quotient of the aggregate count and 14,400, the maximum count possible (72 * 200= 14,400). Nighttime was defined as the 12- hour period between 18:00 and 6:00 local Galápagos time, appropriate for this equatorial location.
To examine activity patterns in further detail we calculated the number of “wet bouts”
per night during the breeding season. Wet bouts were not used in our model they are only presented graphically in our results. A wet bout was defined as a continuous sequence of 10 min blocks during each of which the bird spent at least 3 s on the water. Alternatively, during a “flying bout” every 10 min block was completely dry. Nighttime wet bouts were estimated using our immersion data following Phalan et al. (2007).
An ENSO episode was underway in 2010 during a portion of our study period (Climate Prediction Center, National Centers for Environmental Prediction NOAA/National
Weather Service). Because ENSO conditions are known to affect seabirds (Cubaynes et al., 2011) we included this as a temporal covariate in our analysis of swallow-tailed gull at-sea behavior.
Data for SST were obtained from the Charles Darwin Foundation Climate Database (http://www.darwinfoundation.org/datazone/climate/select-eng). The fraction of the moon illuminated each night was obtained using calendars from the U.S Naval Observatory and Astronomical Applications Department
(http://aa.usno.navy.mil/data/docs/MoonFraction.php).
We used R 2.13.1 (The R Foundation for Statistical Computing, Vienna, Austria) for data management and statistical analyses and the R package ggplot2 (H. Wickham, New York, 2009) for graphics.
Model Specification
We monitored m total birds over a sequence of T total nightly periods. For these observations, we recorded a discrete response variable for each gull, because we were interested primarily in the effect of the lunar phase on at-sea activity, and the sensor was able to detect wet versus dry as a binary response, such that the variable we actually modeled is a count, !!,!, that is less than or equal to 14,400 (the maximum number of wet 3 second sub- periods in 12 hours). In order to model these counts such that we could quantify the probability of wet versus dry on each 12-hour nightly period, we assumed a binomial model for the !!,! with:
!!,! ∼!Binom(14400, !!,!),!for ! =1,…!,! and!!=1,…!,!T!.!
To complete the model specification so that we could make inference on a set of
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potentially influential covariates, the wet probabilities, !!,!! were linked formally to the environmental conditions. The traditional way to accomplish this is to express the logit link function of the !!,!!!as a linear combination of the effects. That is, consider the generalized linear mixed model (GLMM) specification:
logit(!!,!)=!!,!+!!,!SST!,!!+!!,!!PHASE!,!!,
=x!,!! !!!!, (1) where the !! coefficients correspond to the potential effects specific to bird !, and x!,!!are the covariates relative to bird ! on nightly period !. In this case, the covariates were the sea surface temperature and moon phase (ranging from zero for new to one for full).
In this model, each bird can have its own reaction to the environment (including moon phase), in terms of their behavior at-sea, but we were ultimately interested in the population- level response to moon phase. The model in (1) uses the nightly 12-hour period as the sample unit, yet we wanted to draw inferences about the effects of the covariates using individual birds as the sample units to allow population-level inference. We assumed that each coefficient vector !! came from a population-level distribution (as a random effect). We desired inference on the mean of this distribution !!!where:
!!!~!N !!,!! . (2)
The latent process model presented in (2) implies a hierarchical specification for the GLMM and we had two components that needed prior distributions. In completing the model specification, let !!~N !,!!∙!I !and !!!~!Wish S! !!,! ,!where the prior for the inverse covariance matrix !!!!is a Wishart distribution, a proper probability distribution for precision matrices. This model allows the !!!coefficient vectors to be correlated.
We used a Markov Chain Monte Carlo (MCMC) algorithm to sample from the posterior distribution of the unknown parameters given the data. In this case, the posterior distribution can be written as proportional to the likelihood multiplied by the process model and prior as follows:
!! ,!!,!! !!,! ∝ !!!! !!!! !!,! !!,! !! !! !!,!! !! !! , (3)
where the square bracket notation [·|·] corresponds to a probability density function.
By sampling from each of the full-conditional distributions sequentially, one can implement an MCMC and obtain samples from the joint posterior distribution of interest (Gelman, Carlin, Stern, & Rubin, 2003). In this model, we used hyper parameters (!=!,
!!=1000, S=0.01·I, and !=4) and ran the MCMC algorithm for 10,000 iterations,
discarding the first 1,000 iterations as a burn-in period (i.e., the period before the Markov
chains have converged).
An advantage of this hierarchical model specification was that we could account directly for the uncertainty present in the original data while allowing rigorous inference to be made on the population-level effects (!!).
Results
Forty-six of 50 devices (92%) were recovered, and data were successfully uploaded from 45 (98%). Thirty-seven of the 45 (82%) loggers recorded at least one breeding attempt per individual, which average 120 days (Harris, 1970). Breeding attempts were considered to occur between migration events; apparent breeding periods before the first migration and after the last migration were not included. We analyzed movement data derived from the GLS loggers to determine migration periods, with migration defined as a period of 3 moths or more when birds are away from the Galapagos Islands. Swallow-tailed gulls breed
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asynchronously, and the breeding periods of different birds overlapped to varying degrees.
Therefore, the total period studied (249 days) is longer than the average breeding period. We collected a total of 4,518 bird-days of continuous wet/dry data during the breeding period.
We did not monitor the tagged birds during the periods of deployment and so we have no information on their breeding status except at the time of deployment.
The activity patterns of three birds across their breeding attempts are shown in Figure 1.
Throughout the breeding season, daytime values of percentage of time spent on water remained very low and near zero, with the exception of eleven occasions; we deduce that birds did not return to their nests on these occasions, staying on the sea surface to rest throughout the daylight hours. The proportion of time spent on water at night varied with lunar phase for these birds as well; most noticeably, the proportion was close to zero during full moons and increased up to 49% during new moon periods.
The proportion of time at night that breeding birds spent on the water (at-sea activity) followed a rhythmic pattern that coincided with the lunar cycle (Fig. 2). Likewise, the number of nocturnal wet bouts varied with lunar phase, peaking during new moons and falling during full moons (Fig. 3). The proportion of time spent on water, our response variable, was strongly correlated with the number of wet bouts (R2 = 0.70, P < 0.0001, slope
= 97.5). The wet activity was clearly reduced during the brightest period of the cycle, the full moon, as shown by the clear, almost horizontal bands in Figure 4. Bands of wet activity (dark) and dry periods (clear) are not perfectly horizontal, related to the daily shift of the time of moonrise and moonset that occurs during the lunar cycle.
Model Results
All population-level coefficients were significant (no credible intervals overlapped
zero; Fig. 5, Table 1). The results of our modeling efforts indicate a positive relationship between sea surface temperature and the probability of birds being wet in the population as a whole, and a negative relationship between the probability of a bird being wet and increased illumination related to the moon phase.
The posterior predictive distribution for the probability of wet (i.e.,!!!) was obtained by sampling the full-conditional distribution of !!within the MCMC algorithm for each day on which data were collected. Figure 6 shows a periodic effect of moon phase on the wet probability, reaching its maximum during full moons, coupled with a much larger scale periodicity, appearing as a downward trend linked to decreasing sea surface temperatures over the period of the study.
Discussion
Our data show a clear negative association between the at-sea behavior of breeding swallow-tailed gulls and the lunar cycle. The number of wet bouts increased during new moon periods and the percentage of time on water was highest during the darkest periods of each month. Consequently, our results support the hypothesis that swallow-tailed gulls increase their foraging activity when prey is most available; that is, the gull’s presence on the water coincides with the availability of prey following the DVM cycle (M. Z. Gliwicz, 1986).
Other variables, such as the forager’s breeding stage (which we were not able to include in our model), may also explain some variation in foraging behavior, but the strong signal that we have detected from lunar cycle indicates its predominance.
Tropical waters, in general, have different food web structures, are less productive, less structured, and less predictable than are waters of temperate and polar regions (Longhurst
& Pauly, 1987). It has been proposed that selection has favored different foraging strategies
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in seabirds from temperate or polar compared to tropical waters (Weimerskirch, 2007). For example, Ballance et al. (Ballance & Pitman, 1999) suggested that a good strategy for locating prey, for pelagic birds in the tropics, would be simply to look for them at night due to increased prey availability at the sea surface. Swallow-tailed gulls appear to do just that, and have adaptive characteristics such as large, night-adapted eyes and no discernible melatonin rhythm, to exploit nocturnal conditions at-sea (Wikelski, Tarlow, Eising, Groothuis, & Gwinner, 2006). Therefore, it is not surprising that they have become attuned to the fluctuation in prey availability due to moonlight changes throughout the lunar cycle, consistent with other studies showing that birds adjust their daily patterns of foraging behavior to match activity patterns of their prey (Irons, 1998; Regular et al., 2011; Van Gils
& Piersma, 1999).
Swallow-tailed gulls, like other seabirds, match their nocturnal activity patterns to the lunar cycle. Swallow-tailed gulls have specialized to forage during nighttime, and they become more active during the darker periods of the month, with peak activity during the new moon. In this respect, they resemble the nocturnal Galápagos fur seal, rather than other seabirds. Changes in the foraging patterns of fur seals over the lunar cycle correlate with the suppression of the vertical migration of prey by lunar light, and consequently, the fur seal’s feeding efficiency might be much higher on dark nights (Horning & Trillmich, 1999;
Trillmich & Mohren, 1981). Likewise, the activity patterns of Lophostoma silvicolum bats decreases significantly during the brightest nights of the month, and the reduction in activity is strongly correlated with the behavior of prey in connection with the lunar cycle (Lang et al., 2006). Frigatebirds (Fregata spp.) pursue and kleptoparasitze swallow-tailed gulls during daylight hours (Snow & Snow, 1968), but not at night, at least in the vicinity of the breeding colony (pers. obs.). Kleptoparasitism by frigatebirds could have contributed to the evolution of nocturnality [25], although this remains to be thoroughly tested, but probably not to the
pattern revealed by this study.
Swallow-tailed gulls capture their prey by surface plunging, and have access only to the upper 1m of the water column (S. Cruz, unpublished data). Therefore, changes in the depth of their prey are especially significant because vertically migrating fish or squid are out of reach to gulls when at depths greater than 1m (Harris, 1977). During well-lit nights, such as full moon periods, it is possible that the foraging efficiency of gulls is compromised. This notion seems to be supported by our data: the proportion of time spent in water at night of individual birds during full moon is very low (~ zero). We suggest that birds either stay on land attending their nest or chick or encounter less prey at sea during well-lit nights, which results in fewer attempts to capture them and therefore less time in the water overall. This pattern is evident both at the individual and population levels.
The SST around the Galápagos Islands had a discernible positive relationship with at- sea behavior of swallow-tailed gulls. Overall, foraging activity decreased with lower SST.
We suggest two possible hypotheses that could explain this observation: (1) increased productivity due to colder waters around the Galápagos means that prey are more available when the water is colder, swallow-tailed gulls capture more prey per landing, and we observed this as birds spending less time on water; (2) colder SST may have reduced the availability of swallow-tailed gull prey, due to their temperature preferences, resulting in poorer foraging conditions, fewer prey captures and, therefore, less time spent on the water.
We are unable to test these hypotheses at present because data on prey availability do not exist.
The Bayesian hierarchical model used in this study allowed us to establish the link between lunar cycles and at-sea activity patterns of swallow-tailed gulls and provided intuitive and meaningful inference. Furthermore, a large sample size both in number of
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individuals and days recorded provided a robust dataset from which we derived our conclusions. Moreover, our approach offers an alternative method for modeling information from activity loggers and environmental data, which could be useful for the increasing number of tracking studies of seabirds around the world. We provide a specific example of how animals can adjust behaviorally to environmental changes. Our study demonstrates how animals can use strong and predictable environmental cues, such as the lunar cycle, to inform behavioral decisions (Dall, 2005; Fernández-Duque, la Iglesia, & Erkert, 2010). Finally, we recommend that efforts be increased to study tropical species that show contrasting ecological traits from those in temperate regions, so that management and conservation strategies in the tropics are informed by the best available and relevant data rather than less applicable temperate zone information.
Figures
Figure 1. Percentage of time spent on water of three swallow-tailed gulls (Creagrus furcatus) during the breeding season. Black circles represent nighttime values and grey circles daytime values; solid black line represents the lunar cycle.
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Figure 2. Percentage of time spent on the water by day (grey) and night (black) for 37 swallow-tailed gulls (Creagrus furcatus) during the breeding period on Española Island.
Upper filled and unfilled circles represent new and full moons, respectively.
Figure 3. Number of landings on the surface of the water at night for 37 swallow-tailed gulls (Creagrus furcatus) during the breeding period on Española Island. Filled and unfilled symbols at top represent new and full moons, respectively.
Figure 4. The nighttime activity patterns of 37 swallow-tailed gulls (Creagrus furcatus) during the breeding period from Española Island, during the study period extending from March to September 2010. Each small square represents the mean proportion of time the sensors were wet during 10-minute blocks throughout each night of the study. Darker blocks indicate higher proportions of time wet and lighter blocks indicate small proportions of time wet. Curved line and circles represent the lunar cycle from full (black line, open circles) to new moon (yellow line, filled circles).
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Figure 5. Histograms of MCMC samples depicting the marginal posterior distributions for each of the population-level coefficients.
Figure 6. Posterior predictive distribution for p (probability of wet) for each of the nights of data collection. The grey area represents the posterior predictive 95% credible interval for this quantity while the solid line represents the posterior predictive mean. Bottom two panels represent moon phase and SST, respectively. Numbers above represent the month of the year, vertical grey lines separate each month accordingly.
26 Tables
Table 1. Population level posterior means, standard deviations, and 95% credible intervals from a fit of the hierarchical model. That is, these results pertain to the estimation of population coefficients μβ, rather than the individual coefficients βi.
Parameter Posterior Mean Posterior SD Posterior 95% CI Intercept -5.82 0.283 (-5.83, -4.71)
SST 0.04 0.012 (0.02, 0.07)
Phase -0.74 0.083 (-0.90, -0.57)
3. Sub-annual breeding cycles in seabirds explained by extraordinary migration strategy
Sebastian M Cruz, Carolina Proaño, David J. Anderson & Martin Wikelski
Submitted to Science Brevia (note format of manuscript) Introduction
The majority of vertebrates, particularly birds, breed on an annual cycle. However, some tropical birds pose a long-standing enigma in ecology by breeding on a shorter (~9 month) cycle (Gwinner, 2003), apparently escaping some common constraint and reaping the fitness benefit of a short reproductive cycle. It has been suggested that tropical seabirds can stop reproductive activities at any time of year, moving into non-breeding feather molt and other somatic recovery, because equatorial waters provide food year-round (Harris, 1970). We disprove this idea for Galápagos swallow-tailed gulls: unlike many migratory birds, which move toward the tropics between breeding bouts, these tropical seabirds make an extraordinary non-seasonal post-breeding migration to higher latitude, targeting a specific temperate region, the NW-Chilean upwelling area of the Humboldt current. This area offers an unusual combination of aseasonal food supply and moderate temperature, and we identify four such temperate marine regions around the planet that might facilitate sub-annual breeding cycles (Fig. 1a). We suggest that many young seabirds whose locations are unknown as pre-breeders also occupy these areas during their early ontogeny.
At the population level, swallow-tailed gulls are known to breed asynchronously in Galápagos at any time of year in 9-10 month cycles (Harris, 1970). We used light-based geolocators with wet/dry activity loggers to record the migration and activity patterns at the
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individual level of a seabird with a sub-annual breeding cycle for the first time. We tracked 45 birds, of which 37 recorded two consecutive migrations and one complete breeding period (Figs. 1a, 1b). Swallow-tailed gulls migrated to the west coast of Chile, a 3,000 km trip, regardless of date, and did so consistently every seven months (n = 39, mean = 217.6 days, SD = 29.5), after breeding bouts of four months (n = 39, mean = 119.2 days, SD = 28.6) on Española Island. Birds move east toward the coast of South America and then fly south to waters west of Chile (Fig. 1d), remaining 5-100 km offshore for 3.3 months (n = 74, mean = 100 days, SD = 12). After molting they return directly to Galápagos (Harris, 1970), during non-breeding they spent, on average, 17.8 hours/day on the water (n = 7094 bird-days, SD = 3.6), but only 1.9 hours (n = 3296 bird-days, SD = 0.11) while in Galápagos. Flight constraints during molt may explain their extended residence on the water when not breeding.
A key choice for tropical seabirds is that of staying in generally low productivity tropical waters year-round or migrating to higher productivity at higher latitude (Pinet, 2011).
Migration to the temperate Humboldt upwelling at any time of year moves Galápagos swallow-tailed gulls (and many high latitude seabirds) to one of the most productive coastal upwelling systems in the world, but may also challenge an equatorial bird thermally.
However, this area is heavily influenced by a subtropical anticyclone, the semi-permanent South Pacific High Pressure Area, maintaining an atypically mild climate (Schwedtfeger, 1976) for this latitude with coastal temperatures ranging from 10 to 17oC (NOAA data from Movebank.org).
We propose that sub-annual breeding cycles can be maintained in equatorial seabirds by migration to higher latitude when the following conditions are met (1) their food resource between breeding bouts is aseasonal, reliable, and sufficient to cover the costs of molt and recovery, and (2) climatic conditions in their non-breeding range are mild enough that tropical species can cope in thermoregulation.
Furthermore, the return dates of swallow-tailed gulls to the colony did not coincide with the lunar cycle, even for known breeding pairs. This has been the suggested mechanism for synchronization of the Sooty (Sterna fuscata) population breeding on Ascension Island and appears to be the case for annual breeding Barau’s petrel (Pterodroma baraui) (Pinet, 2011, Chapin, 1959). Swallow-tailed gulls returned to Española Island regardless of lunar phase and season.
Methods
We fitted archival light loggers (MK14, mass 1.4 g; British Antartic Survey), attached to plastic leg bands (mass of logger, ring, tape and cable tie: 2 g, ~ 0.3% of adult body mass), to 50 adult birds between the 18th and 21st of October 2009 at Española Island (1° 23' S, 89
°37' W), Galapagos Archipelago. There are approximately 200-300 pairs breeding at any moment in the colony at different stages of reproduction, ranging from recently arrived unemployed birds to pairs with juveniles. In total 33 unemployed, 9 eggs and 8 chicks were equipped with light loggers. Twelve of the equipped birds were members of the pair.
Forty-six of the fifty loggers were recovered subsequently at the colony. Because swallow-tailed gulls are aseasonal asynchronous breeders, recoveries took place at separate times between 2010 and 2011.
Forty-five of the forty-six loggers were downloaded successfully. Light data were processed following the instructions suggested in the BAS Geolocator manual version 8.
Times of sunrise and sunset were calculated from light records and converted to location estimates using TransEdit and BirdTracker (BAS) using thresholds of 10, an angle of elevation of −3.5°, and applying the compensation for movement. The mean error of locations determined by geolocation is 186 km (Harris, 1969). Locations 15 days prior and after Equinox were eliminated from the dataset due to the inherent problems of estimating
30
latitude when day length is essentially equal everywhere. Latitudes were unavailable during the breeding season because of the close proximity to the equator, where day length is essentially the same throughout the year. After eliminating periods with light level interference and periods around equinoxes the filtered datasets contained between 94 and 377 days of locations (mean = 252.08 days, SD = 76.41, n = 45). In total the dataset contains 2,314 bird-days of data.
32 Figures
Figure 1a. Breeding, non-breeding and migration periods of 37 adult Swallow-tailed gulls.
Figure 1b. Migration of 45 Swallow-tailed Gulls breeding in the Galápagos Islands towards the west coast of Chile. The tracking period was divided in trimesters to show more clearly migrations occurring regardless of season.
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Figure 1c. Four ocean regions with high productivity and the anticyclones that influence them (based on Longhurst 1981).
4. Finding Food at Night: The Foraging Strategies of a Nocturnal Seabird, the Swallow-tailed Gull
Sebastian M. Cruz1, 3†, Carolina Proaño1, 3, David J. Anderson3, Martin Wikelski1, 3
1Max Planck Institute for Ornithology, Am Obstberg 1, 78315 Radolfzell, Germany
2 Wake Forest University, Department of Biology, Winston-Salem, NC 27109, USA
3 Konstanz University, 78457 Konstanz, Germany
†E-mail: cruz.seb@gmail.com
Introduction
Seabirds are top marine predators that optimize their foraging by overlapping in space and time with their prey (Benoit-Bird et al., 2013; MacArthur & Pianka, 1966). For this reason, the foraging behavior of seabirds largely depends on the distribution, predictability and motility of the animals they feed on (Tremblay, Bertrand, & Henry, 2009). The foraging strategies of seabirds are often extreme due to the inherent complexities of finding food at sea, such as, locating prey that are underwater whilst travelling over-water; or nesting on land when food may be hundreds or even thousands of kilometers from the breeding site (Benoit- Bird et al., 2013; Weimerskirch, 1998; Weimerskirch et al., 2005). The life history traits of pelagic seabirds reflect and help overcome the difficulties of foraging at-sea, particularly during reproduction. Compared to other birds, seabirds are more likely to delay maturation, have slow reproductive rates, be colonial and live longer (Ashmole, 1965; Irons, 1998). In addition to these adaptations, seabirds also exhibit a wide range of behaviors that enable them to exploit marine resources (Block et al., 2011; Schreiber, 2002).
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Gathering information on the foraging behavior of seabirds is essential for an understanding of both their ecological roles and the constraints acting upon them in marine ecosystems (Benoit-Bird et al., 2013; Kotzerka et al., 2010; MacArthur & Pianka, 1966;
Monaghan & Monaghan, 1996; R. Wilson et al., 2007). Nonetheless, the foraging ecology of seabirds is not completely understood, more so in the tropics where they have historically been understudied (Ballance & Ainley, 2001; Tremblay et al., 2009; Weimerskirch et al., 2005). In general, tropical waters are less productive, have a more patchy distribution of resources and a different food web structure than temperate or polar regions (Benoit-Bird et al., 2013; Longhurst & Pauly, 1987; Weimerskirch, 1998; 2007; Weimerskirch et al., 2005).
The foraging strategies of tropical seabirds reflect these differences in oceanographic conditions. For example, most tropical seabirds range widely and forage in multi-species flocks that follow sub-surface predators such as tuna and dolphins that bring prey up to the sea surface (Ashmole, 1965; Ballance & Pitman, 1999; Irons, 1998). Other foraging strategies include solitary feeding scavenging and nocturnal feeding (Ballance & Ainley, 2001; Block et al., 2011; Harris, 1977; Schreiber, 2002).
The ecology, strategies and behaviors regarding nocturnal foraging in tropical seabirds remain understudied (Ballance & Pitman, 1999). This lack of knowledge may be related to the fact that most seabirds are visual hunters whose foraging activity occurs predominantly during daylight hours (Ballance, 2007). Light availability is an important factor influencing foraging behavior such that many seabirds tend not to forage when efficiency is compromised by low light levels (Jetz et al., 2003). During daytime the sun is out and the sky is bright, whereas nighttime is characterized by much reduced light levels or the lack of light. The peculiarities of being night-active include: (1) prey items are harder to spot in dim light; (2) lower air temperatures, (3) increased humidity; and (4) decreased air currents (Martin, 1990). It is expected that nighttime at-sea conditions affect the foraging
behavior of seabirds. For example, it is known that several species of albatross fly during the day over wide areas in search of food, but the same birds change to a sit and wait foraging strategy during the night. If nazca boobies (Sula granti) spend a night at sea, 99% of the time they are resting on the water surface (Zavalaga, 2012). Nonetheless, some seabird species are active at night possibly to take advantage of the increased prey availability, or to avoid competition with other seabirds, avoid diurnal predators, or to take advantage of prey aggregations attracted by artificial lighting (Cruz et al., 2013; Hailman, 1964a; Harris, 1970;
Santos, Lourenço, Miranda, Granadeiro, & Palmeirim, 2008; Zavalaga, Dell'Omo, Becciu, &
Yoda, 2011). Three general behavioral or ecological trends have been linked to nocturnal foraging in seabirds: first, nocturnal feeders tend to be pelagic; second, nocturnality appears to be more prevalent in tropical and southern hemisphere species than cool-water northern species; lastly, nocturnal foraging is often associated with a diet composed of squid caught in the open ocean (Brooke & Prince, 1990).
Several species of squid, fish and zooplankton remain at depth during the day and surface at night in what is known as diel vertical migration (DVM), a well-studied phenomenon in marine ecosystems (Lampert, 1989; Loose, 1994). The DVM of prey is principally an avoidance strategy from visual predators that rely on environmental light to locate and capture their prey (M. Z. Gliwicz, 1986). For this reason, nighttime sea surface densities of prey can be up to 1000 times greater than during the day (Brinton, 1967). This vertical migration is more significant at low rather than at high latitudes, and in oceanic rather than neritic waters (Ashmole, 1971) and, because of this, nocturnal foraging has been hypothesized to represent a suitable strategy for locating prey, particularly for pelagic birds in the tropics (Ballance & Pitman, 1999). However, finding food at night in the open ocean appears not to be a prevalent strategy among seabirds. A detailed literature review found that obligate nocturnality, whereby seabirds forage exclusively at night, is uncommon (12.5% of
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species). In addition, 42% of species for which data are available, are active at night to varying extents (Table 1). The majority of seabirds appear to be entirely diurnal foragers (46%). Finding food during the nighttime at-sea is a rare foraging strategy among seabirds, presumably because it requires a suite of physiological, morphological and behavioral adaptations to compensate for the constraints imposed by the lack of ambient light. To effectively locate and capture prey in low light conditions requires adaptations such as large sensitive eyes. Nonetheless, visual adaptations for foraging at one light level generally
compromise efficiency at another (Fraser, 1997). In the case of visual predators this is particularly important because diurnal species tend to have adaptations for spatial and temporal sharpness and color sensitivity, whereas nocturnal species compromise on these aspects to increase light sensitivity at night (Fraser, 1997). Taken together, these constraints generate a situation that limits an organism to being either nocturnal or diurnal. Therefore, we
expect strictly nocturnal seabirds to be uniquely adapted for nighttime conditions, very much like owls, renowned earthbound nocturnal predators. Swallow-tailed gulls (Creagrus furcatus) present an extreme example of visual evolution in seabirds, and they are one of the
few seabird species in the tropics that feeds entirely at night (Ballance & Pitman, 1999;
Hailman, 1964b; 1964a; Harris, 1970). Studies have found behavioral, morphological, and physiological traits in swallow-tailed gulls suited to feeding at night to a degree that appears to essentially restrict them to nocturnal foraging. Swallow-tailed gulls leave their colonies at dusk and return before dawn; they remain at their nests or in the vicinity during the day
(Harris, 1970). They have very large eyes relative to their body size, when compared with the eyes of other gulls (Hailman, 1964a). The eyes of Swallow-tailed gulls include a layer of tissue, the tapetum lucidum, which reflects visible light back through the retina, increasing the light available to the eye’s photoreceptors. They lack a daily melatonin rhythm, possibly facilitating activity and alertness when foraging at night (Wikelski et al., 2006). Nighttime
at-sea activity of breeding swallow-tailed gulls varies with lunar phase; they avoid activity during well-lit nights and activity is highest during the darkest nights around new moons
(Cruz et al., 2013).
Research on the movement of seabirds at-sea has seen a huge increase thanks to the
development and miniaturization of tracking technologies (Weimerskirch, Pinaud, Pawlowski, & Bost, 2007). High-resolution tracks can, for example, reveal the area covered, distance travelled and small scale adjustments seabirds make while foraging, providing information about the locomotion, foraging behavior, distribution, migration and exposure to threats (Burger & Shaffer, 2008; Pinaud & Weimerskirch, 2007)
As part of extensive studies on the swallow-tailed gull, we documented foraging behaviors during reproduction to better understand sources of variability in the gulls’ trips to foraging areas related to their nocturnal habits, breeding status, location and oceanographic
conditions. We tested the hypothesis that swallow-tailed gulls are constrained to nocturnal activity by nocturnal specialization; we predicted no diurnal foraging activity during reproduction. To this end, we used miniature GPS data logger to gather high-resolution tracks of the foraging trips of this species in order to: first, define the spatial scale and time periods over which breeding swallow-tailed gulls travel to feed; second, describe the foraging characteristics of swallow-tailed gulls; and third, examine foraging differences between separate colonies. To achieve these aims, we tracked birds over a period of two years on three separate islands and from four different colonies. We also examine the relevance of the Galapagos Marine Reserve (GMR) protected zone, the largest marine reserve in a developing
country and the second largest reserve in the world, to the foraging of swallow-tailed gulls during breeding (Anderson et al., 2003). In this paper we provide the first foraging movements and activities patterns at sea of an exclusively nocturnal seabird. Subsequently we examined the possible causes and consequences of nocturnal foraging.
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Materials and Methods
Study Site
We studied swallow-tailed gulls during nesting on islands located in the north, center and south of the Galapagos archipelago. The sites were: (1) Punta Cevallos [Lat -1.393228°, Lon
-89.618577°] and Punta Suarez [Lat -1.371901°, Lon -89.744395°] colonies situated on the southern-most island of Española near the end of the Galapagos platform; (2) South Plazas [Lat -0.582610°, Lon -90.166321°] situated the central area of the Galapagos archipelago; (3) and Genovesa [Lat 0.322939°, -89.954530°] in the north of the archipelago and removed of the Galapagos platform. Approximately 2000 pairs of swallow-tailed gulls breed on the rocky
cliffs and shores of Española Island; and 1000 pairs breed on the rocky cliffs, shores, and beaches of Genovesa island. Swallow-tailed gulls are a-seasonal and asynchronous breeders (Harris, 1970). Nests with eggs, chicks and juveniles can be found year-round in the colonies.
During the course of our study, we worked with birds in all stages of reproduction, incubating, brooding, rearing and fledging. Our sample included birds that had recently arrived to the colony and were searching for mates; we call these birds ‘unemployed’.
Data Logging
Our main study sites were in areas that had sub-colonies with accessible nests, i.e. birds were on shore under or near rocks or directly on sand, away from rocky cliffs. Prior to capturing the birds in the colony was surveyed and any active nest was marked with flagging tape and its contents were recorded. Upon capture (see below), swallow-tailed gulls were fitted with GPS /acceleration loggers (22 g; L 60 x W 22 x H 15 mm) manufactured by e-obs GmbH©
Digital Telemetry (Munich, Germany). Tracking devices were deployed on birds at Española during August 2008 (2-11), November-December 2008 (29-11), April 2009 (14-18), October
2009 (18-21), March 2010 (12-24), and on Genovesa during March 2009 (8-16) and November 2009 (13-24). Loggers were programmed to record GPS fixes every 5 minutes.
Each bird was tracked continuously for a maximum of 48 hours, unless the device fell off during the deployment period. The E-obs GPS loggers we used transmit data via radio signal to a handheld base station that can be outfitted with a high-gain directional antenna. The net download speed of the UHF radio link is about 1 MByte per min. The GPS/ACC loggers were programmed to contact the base station with a frequency of 20 seconds. Thus it was possible to retrieve both GPS data without recapturing birds.
Birds were hand caught at the nest and loggers were attached to feathers in the middle of the back with TESA® tape. Before deployment, each bird was weighed to the nearest 5 g using a spring balance, and wing-cord was measured to the nearest centimeter. Additionally, chicks were captured and weighed to the nearest 5 g using a spring balance. Upon recapture and removal of the device, adult birds were weighed again. Handling time was approximately 10 minutes for deployment and 5 minutes for logger removal. The mass of the logger was between 3 and 4% of average bodyweight (645.3±57.5 g).
Data Processing
GPS data provide the location of birds at-sea but do not indicate if an animal is foraging.
Therefore we used flight speed and direction, from GPS-based instantaneous speed and direction, as an indicator of foraging activity (Hyrenbach, 2003; Safi et al., 2013;
Weimerskirch et al., 2005). We used flight speed as an indicator of foraging activity, when flight speed where less than 2.8 m/s between at least 3 successive locations. Foraging activity, measured based on flight speed, generally took place within the most distant section of the trip.
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GPS points were plotted using Google Earth for quick visualization and R was used (packages Maptools, Raster and sp) for further analysis and creation of maps. These software packages allowed the determination of active flights to foraging locations. For the analysis of utilization distributions we used the R package Move for the analysis of animal tacking data stored in Movebank.org (Kranstauber, Kays, LaPoint, Wikelski, & Safi, 2012). The following indexes were calculated per foraging trip: trip length, maximum distance, trip duration, heading and number of dives per trip.
Bathymetric data for the Galapagos Islands were compiled by Bill Chadwick, Oregon State University (http://www.pmel.noaa.gov/vents/staff/chadwick/galapagos.html). Using the Env-DATA tool available at www.Movebank.org, swallow-tailed gull tracks were annotated with Ocean Net Primary Production (NPP) data from the Ocean productivity datasets (http://www.science.oregonstate.edu/ocean.productivity/). For the annotation 6-hour, 2.5°
NCEP Reanalysis 2, and 8-day, 2160x4320 ocean NPP datasets are used.
Results
We captured and fitted 182 birds with GPS loggers for 1-2 days. Twelve birds lost the logger;
the feathers to which the device had been attached had clearly been pulled off. Twenty loggers failed to record data because of battery malfunction and/or software malfunctions.
Ten loggers did not record complete tracks due to battery malfunction. Three birds did not leave their nests for the duration of the logger deployment. We used the data from the remaining 137 successful deployments for the analysis of foraging patterns of swallow-tailed gulls. In total we obtained 182 complete foraging tracks, 115 from birds from Española and 67 from birds from Genovesa. Table 2 shows the breeding stages of the birds that were successfully tracked on both islands; the majority of birds were rearing a chick.
Diel Patterns of Foraging
All 201 foraging trips of breeding swallow-tailed gulls occurred solely during nighttime (Fig.
1). Departures occurred predominantly at dusk (~18:00) and continued until midnight with few exceptions (Fig. 2). Likewise, arrivals occurred mostly before or during dawn and to a lesser extent throughout the night (Fig. 2). No foraging trips were recorded during daytime, the period between 6:00 and 18:00 for this location. The majority of foraging trips (99.5%, n=201) were on a nightly basis, birds being away from the nest a maximum of 11h and 40min. Only in one instance did a bird spend more than 12 h away from the colony. This individual flew 100 km from the nest heading Southwest (Fig. 3). The bird stopped flying the following day between 06:30 am and 17:30 pm, and returned to the nest at 18:15 pm (Fig. 3).
During daylight hours, this bird spent 96.7% of the time floating on the surface of the sea, interspersed with 3 short flights (total duration = 25 min). The movement of the bird during this floating period was unidirectional (303° Northeast) at an average speed of 2.7 km/h; this coincides with the predominant currents for this part of the Galapagos Islands (Sweet et al., 2007). This bird was rearing a fledgling at the nest.
Foraging Zones
The main foraging areas for swallow-tailed gulls breeding on Punta Cevallos were east (47.2%, n = 115) and southeast (34.3%, =115), and to a lesser extent birds flew north-east (10.2%, n = 115) and north (7.4%, n = 115)(Fig. 4a). Birds stayed mostly over bathypelagic waters < 2000 m deep (92.2%, n=115). The majority of birds flew over waters on the Galapagos platform (68.7%, n=115) and platform slope (23.48%, n =115). On a few occasions, birds flew over abyssopelagic waters > 3000 m deep, beyond the Galapagos platform south of Española. The majority of foraging trips from Punta Cevallos took place within the protected waters of the GMR (88.5%, n=115). On a meso-scale (Weimerskirch,
44
2007) foraging zones for birds from Punta Cevallos appear to be relatively stable over time, birds go east of Española regardless of season or year (Fig. 5, 6). Swallow-tailed gulls from Punta Suarez on the western coast of Española flew northwest (Fig. 4d). The foraging trips (n=5) of birds in this location were over the Galapagos platform, waters < 500 m deep, and within the GMR. The main foraging zones for birds nesting on Genovesa were south (35.3%, n = 67) and southeast (17.7%, n = 67); to a lower extent birds travelled northeast (7.4%, n = 67) and west (7.4%, n = 67)(Fig 4b). Birds generally foraged over mesopelagic waters (500- 1000m deep), except one bird that headed north over waters 2000 m deep. All the foraging trips in this study from birds breeding on Genovesa were within the GMR limits. Birds tracked on the central islet of Plazas Sur headed northeast (33.3%, n=15), north (26.7%, n=15), southeast (20%, n=15), east (13.3%, n=15) and south (6.7%, n=15)(Fig. 4c). For Plazas Sur birds, water depths in the area of the foraging trips did not exceed 500 m in depth and all trips were inside the GMR. At-sea utilization distributions of swallow-tailed gull foraging activity place the 50-90% density contour east of Española, in contrast to birds from Genovesa where the 50-90% density contours are south of the island (Fig 6a and 6b).
Foraging Movements
After leaving the nest swallow-tailed gulls headed directly for foraging areas. The overall majority of birds (75.2%, n=182) commuted, that is, trips were directional return journeys with parallel and close outward return paths (Weimerskirch, 2007). The remaining trips (24.8%) were loop shaped, birds did not return to the colony from the same direction from which they left. The mean flight speed recorded by GPS was 25.7 km/h, with a maximum speed of 89.6 km/h (Fig. 7). Foraging trips typically started with rapid movements away from the colony with a near constant speed and linear heading; then direction and speed became more variable, presumably due to foraging. Foraging patches generally coincided with the
maximum trip distance achieved by a bird. Return flights to the nest were near constant and straight, small bouts of floating on the sea surface occurred near the island. Differences in the duration, distance and number of trips per night were found between the colonies of Punta Cevallos and Genovesa. In general, the foraging trips of birds nesting on Punta Cevallos were 40% longer, in distance and duration than the trips of birds nesting on Genovesa. The foraging trip duration of birds breeding on Punta Cevallos varied from 1.4 to 31.6 h (mean 6.9 h, SD 4.1h) and total distance travelled varied from 16.8 to 254.2 km (mean 105.3 km, SD 48.7 km). Trip duration of birds nesting on Genovesa varied from 1 to 8.2 h (mean 3.04 h, SD 2.2 h) and total distance travelled varied from 15.8 to 95.1 km (mean 41.7 km, SD 24.4 km). The differences between these sites were significant in both duration (Mann-Whitney, U
= 863.0, p < 0.0001) and distance travelled (Welch’s t-test, t = 8.339, p < 0.0001)(Fig.8).
Furthermore, the majority of birds nesting on Punta Suarez took mostly one trip per night (93.9%, n = 115). In contrast, birds from Genovesa frequently undertook two trips per night (26.8%, n=67). Sample size of Punta Suarez and Plazas Sur were not sufficient to extract meaningful comparisons. Trip duration on Punta Suarez varied from 2.53 to 5.36 h (mean 3.5 h, SD 1.3 h), total distance travelled varied from 53.9 to 97.7 km (mean 68.8 km, SD 19.7 km). Likewise the trip duration of birds on nesting on Plazas Sur varied from 1.15 to 8.9 h (mean 3.8 h, SD 2.6 h), total distance travelled varied from 23.3 to 142.4 (mean 67.8 km, SD 48.8 km). None of the birds tracked for at least 2 successive trips returned to the same area to forage.
During incubation, birds from Genovesa foraged at an average distance of 16.89 km (SD 9.1, max = 40.4 km, min = 6.5, n=11) from the colony. During chick-rearing, the range decreased to 14.98 km (SD 8.6, max = 34.1 km, min = 3.6, n=41) (non-parametric ANOVA KruskalWallis = 6.8, p = 0.0334). When a bird attended a fledgling the foraging range increased to 22.5 km (SD 8.6, max = 41.3 km, min = 12.5, n=10). The distance travelled was
