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,
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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