Southbound migration and staging areas

Exact date of departure from the colony was unknown due to access limitations to the breeding colonies, but observations on the few intermittent visits suggested that all birds with loggers left the colony in the first week of July. The tracks showed that birds spent the immediate post-nuptial period in the North Sea region, in relative close proximity to the colony. Given the absence of any report during this period of colourringed birds from this colony in the surrounding area, despite the large number of keen birdwatchers searching for rings (DH, unpubl. data), it seems that adults and juveniles stage at sea directly after the breeding season.

At the end of July, the Arctic Terns started their migration west via the English Channel (three birds) or the Irish Sea (two birds) towards a staging area east of the Grand Banks off Newfoundland. This area in the North Atlantic is approximately 1000 km north-northwest of the Azores; here they spent 6 ± 2 days (Figure 1, Table 1).

Figure 1.

Migration routes of five Arctic Terns tracked from The Netherlands. Shown are interpolated migratory routes, staging areas during migration, and non-breeding region during the austral summer. Black lines represent southbound, and grey lines represent northbound routes. Dashed lines depict linearly interpolated latitudes during equinox periods. Density kernels represent isopleths of 0–70% of the distribution at 10% intervals within the staging areas and non-breeding region. The map is in Aitoff projection with central meridian at 40°E.

Most birds departed from this North Atlantic staging area in an easterly direction towards Portugal before bearing south. Two birds passed close to the Canary Islands, and the two others close to the Cape Verde Islands. All birds then travelled south to the African mainland, with one bird off Sierra Leone, three off Liberia, and one off Ghana. The second staging area was located in the Benguela Current (Boebel et al. 1998) off Namibian and South African coast and up to 1000 km offshore (Figure 1, Table 1). Here, most birds appeared to stage in an offshore area over a chain of seamounts called the Walvis Ridge. The terns staged here for 32 ± 16 days, from late August to late September.

All terns continued their migration towards a third staging area in subtropical waters in the Indian Ocean between 20–40°S and 65–100°E. Here, they spent 14 ± 10 days, with two terns staging near Amsterdam Island (Figure 1, Table 1). Four of the Arctic Terns then continued east to Australian waters before heading south to Wilkes Land, Antarctica. Two birds spent some time in the Great Australian Bight, one of which continued to the Tasman Sea and south of the New Zealand mainland before passing near the Auckland Islands towards the Antarctic.

After 110 ± 9 days since leaving the colony and having migrated 29,700 ± 2700 km and flown 16,100 ± 2100 km within the various staging areas (migration speed of 420 ± 24 km/day, Figure 2), the terns reached Antarctic waters between 100–170°E (median arrival date of 12 November). Here they spent the remainder of the austral summer. The maximum travel speed between staging sites on their southbound migration was 690 ± 94 km/day (Figure 2), recorded for the segment between the North Atlantic staging area and the offshore staging area off Namibia.

Antarctic non-breeding region

All five birds spent an average of 128 ± 9 days in the marginal ice zone off Wilkes Land (Figure 1, Table 1), during which they flew 23,600 ± 3160 km (daily movement of 180 ± 16 km/day, Figure 2). Although individual non-breeding ranges were very large (40–90°E, 60–100°E, 105–120°E, 25–115°E, or 120–150°E), all birds spent a large proportion of time in a more restricted region. Three birds spent most time to the east of Prydz Bay in the Amery Basin, where one of the largest glaciers flows into the sea. Another bird spent the majority of time in the Dumont D'Urville Sea off Terre Adélie. The fifth bird was mostly found near the Shackleton Ice Shelf. The tracked terns slowly moved westwards between mid November and mid March.

Northward migration and staging areas

In mid-late March, most birds left Antarctica off the coast of Dronning Maud Land (0–35°E) using an oceanic route to fly directly to the Northern Hemisphere. One bird departed directly from the Prydz Bay region and flew back to the Atlantic via the Kerguelen Islands. All returned via the North Atlantic staging area that was used during southward migration (Figure 1), but now stopped either for a shorter period (3 ± 2 days, n = 4) in mid-late April (cf. 6 ± 2 days on southward migration), or not at all (n = 1). This latter bird turned east at the latitude of the Azores and flew directly towards Europe. The return migration took only 34 ± 8 days, and covered an average distance of 19,000 ± 2600 km and 1200 ± 960 km within the North Atlantic staging area (migration speed of 610 ± 120 km/day, Figure 2). The maximum travel speed between staging sites on their northbound migration was 670 ± 280 km/day (Figure 2) recorded for the segment between the North Atlantic staging area and the colony in The Netherlands. All Arctic Terns with geolocators arrived in the colony at the end of April.

Table 1.

Timing of migration in Arctic Terns tracked from The Netherlands (n = 5), including distances travelled during different legs of migration and duration of staging in days.

Figure 2.

Migration speed ± SD (dark grey bars) during north and southbound routes (including staging time), travel speeds between staging sites ± SD (light grey bars) separated for distinctive segments of the north and southbound journeys, and average daily movement ± SD within the Antarctic non-breeding region (white bar) in km/day of Arctic Terns (n = 5) tagged in The Netherlands.

The longest recorded migration route

The Arctic Terns tracked in our study performed the longest avian migration recorded thus far. The total average trip length exceeded previous calculations for birds from Greenland and Iceland (Egevang et al. 2010) by almost 20,000 km. It is worth noting that both studies used similar devices and an identical approach to calculate travel distances (inclusion of distances travelled within staging areas and the non-breeding region). Migration routes and timing of migration were different between birds from Greenland and The Netherlands, as the latter made shorter, direct journeys (both in km and days) within the Atlantic Ocean (Figure 3). Also, the location of the main Antarctic nonbreeding region was strikingly different, Weddell Sea versus Indian Ocean sector of Antarctica, respectively.

A new finding is that the terns of Dutch origin used the Indian Ocean much more than the birds from Greenland, both at temperate and Antarctic latitudes. Moreover, unlike some birds from Greenland, none of the five tracked terns in this study migrated along the coasts of South America (Egevang et al. 2010). The migration routes of terns from Greenland were characterised by sinusoidal patterns (closer to the coasts of Africa and South America on southern and northern migration, respectively). Similar sinusoidal patterns are reported for other trans-equatorial migrant birds in both the Atlantic (González-Solís et al. 2007, Guilford et al. 2009, Egevang et al. 2010, Kopp et al. 2011) and the Pacific (Shaffer et al. 2006, Kopp et al. 2011). In contrast, terns from The Netherlands took rather direct routes across the Atlantic. This previously unknown migratory flyway for terns could be referred to as the North-Atlantic/Indian-Ocean flyway. Although terns from Greenland flew longer distances between the different staging sites across the Atlantic (Figure 3), total distance travelled outside the breeding season by terns from The Netherlands was much larger. Their breeding location in the Netherland and their farthest observed non-breeding location were almost exactly at opposite sides of the globe.

Well-defined staging areas during migration

Timing and migratory routes were similar in the five terns in this study. Previous studies on Arctic Terns (Egevang et al. 2010) and other long-distance transequatorial migratory seabirds from the North Atlantic (González-Solís et al. 2007, Guilford et al. 2009, Dias et al. 2012) showed larger between individual variation in north- and southward migration routes. After the breeding season all five birds from The Netherlands staged in the North Sea area, a suggested staging area for failed breeders (Camphuysen & Winter 1996). Similar to Arctic Terns from Greenland and many other migratory seabirds, the next two staging regions used on southward migration were recently identified hotspots in the North Atlantic (Egevang et al. 2010, Sittler et al. 2011, Frederiksen et al. 2012, Mosbech et al. 2012) and the Benguela Current offshore Namibia (Boebel et al. 1998, Dias et al. 2012, Stenhouse et al. 2012). Close to both regions, the junction of cold and warm water masses results in high eddy variability (Richardson et al. 2003, Egevang et al. 2010) and high primary productivity (NASA 2013). The food abundance in such areas is likely the most important factor determining the concentration of migrants (Egevang et al. 2010, Frederiksen et al. 2012), but social aspects might also drive terns to congregate (Camphuysen & Winter 1996).

In contrast to the terns from Greenland, our birds spent a shorter period in the North Atlantic staging area (∼1 week versus ∼1 month). However, our birds staged ∼1 month offshore Namibia, a region passed on migration by only four of eleven terns from Greenland. Although a few of the terns from Greenland entered the Indian Ocean (Egevang et al. 2010), they eventually returned west to join the others in the main non-breeding region in the Weddell Sea. In contrast, the Arctic Terns from The Netherlands flew directly east after rounding Southern Africa and transited towards a third staging area, formerly unknown in this species, in subtropical waters between 20–40°S and 60–100°E, north and east of Amsterdam Island. The large breeding populations of many seabirds on Amsterdam Island indicate that this is clearly a productive region, but its importance for migrant Arctic Terns was thus far unknown. There are records of Arctic Terns at temperate latitudes in the Indian Ocean, both at sea (Mörzer Bruyns & Voous, 1964), and on land (Amsterdam Island, Paulian 1953). Ring recoveries and sightings in Australian waters indicate a regular presence in this region (collated in BWPi 2006) but our study provided the first direct evidence for previous suggestions (Salomonsen 1967, Monaghan 2002) that a regular migration route through the Indian Ocean towards Australia exists. We were able to identify a relatively well-defined offshore staging area for these five individuals from two Dutch breeding colonies. These colonies are part of a declining population of Arctic Terns (DH, unpubl. data), highlighting that this tracking study provides useful knowledge for conservation, by recognizing previously unknown important areas for this specific population.

Figure 3.

Schematic comparison between the movements of Arctic Terns breeding in The Netherlands (black lines) and Greenland (white lines) during the non-breeding period, including average migration distance. Antarctic non-breeding ranges are depicted in black (terns from The Netherlands) and white (terns from Greenland) with average total movement within these areas.

East Antarctic non-breeding range

Arctic Terns from The Netherlands spent the austral summer in the marginal ice-zone along the coast of the Antarctic continent between 35–100°E (Enderby Land and Wilkes Land). This region supports high concentrations of (breeding) seabirds (Montague 1988, Woehler & Croxall 1997, Woehler et al. 2003), and Arctic Terns are one of the most abundant bird species present here during the austral summer (e.g. van Oordt & Kruijt 1954, Veit & Hunt Jr. 1991). Egevang et al. (2010), the U.S. Fish & Wildlife Service (2013) and the High Arctic Institute (2013) showed that Arctic Terns from colonies in East and West Greenland as well as Maine (USA), spent the austral summer solely in the Weddell Sea region. Egevang et al. (2010) even suggested that this is the main non-breeding area for all North Atlantic Arctic Terns. However, none of the birds from The Netherlands staged in or near the Weddell Sea region. Given that many seabirds show high fidelity to non-breeding ranges (e.g. Phillips et al. 2005, Magnusdottir et al. 2012), this absence in the Weddell Sea region suggests that the typical Antarctic non-breeding range of the terns from the North Sea breeding range lies much further east. Also a recovery of a ringed individual from Denmark supports our findings that terns from breeding colonies in the North Sea region occur in Antarctica between 35–100°E (Bønløkke et al. 2006). An East Antarctic non-breeding area might seem less suitable for terns because primary production is relatively low compared to the Weddell Sea (Arrigo et al. 2007). However, this area might have beneficial habitat quality, weather, food availability, or reduced inter- and intra-specific competition. Comparative studies in both East- and West Antarctica are needed to shed light on the mechanisms behind this apparent contradiction.

Differences in north and southbound migration

Timing and duration of the return migration were similar between Arctic Terns from Greenland (40 days, range: 36–46) and The Netherlands (34 days, range: 25–45), although the routes differed markedly (Figure 3). Northward migration was much faster than southbound (34 (range: 25–45) versus 110 (range: 100–125) days). Rapid northward migration towards the colony and a slower southward migration have been found in many bird species (Tøttrup et al. 2012, Vardanis et al. 2011). The more coastal route during southward migration and the pelagic route during northward migration are congruent with the relatively small number of ring recoveries on the African coasts at different times of the year (Monaghan 2002, Lyngs 2003, Bønløkke et al. 2006). Also, in this study, the terns did not take the route along the coasts of South America, which has been recorded for birds from Greenland (Egevang et al. 2010). Neither was evidence found for the theory of Gudmundsson et al. (1992), who suggested a possible clockwise circumpolar movement of some Arctic Terns in order to reduce the overall travel distance.

Timing and duration of the southward migration was quite different: the Arctic Terns from The Netherlands took longer (110 days, range: 100–125) to arrive in the Antarctic non-breeding region than those from Greenland (93 days, range: 69–103). In addition, terns in this study arrived three to four weeks earlier in the staging areas in the Atlantic (in line with the earlier ending of the breeding season), but did not arrive earlier in their non-breeding region in the Antarctic (mid November).

The clear spatial segregation in wintering areas of Arctic Terns from the east and west Atlantic is congruent with previous studies of migration patterns in seabirds of a variety of taxonomic groups (e.g. Phillips et al. 2007, Grémillet et al. 2000, Rayner et al. 2011, Shaffer et al. 2006, Magnusdottir et al. 2012). Birds can breed in separate areas and spend the non-breeding season in the same region (e.g. Black-legged Kittiwakes, Frederiksen et al. 2012). They can also breed in the same areas but segregate in the non-breeding area (e.g. Sooty Shearwater, Shaffer et al. 2006). Or they can be segregated in both breeding and non-breeding areas (e.g. Great Skua, Magnusdottir et al. 2012). The first system, i.e. mixing in the non-breeding grounds, was assumed for Arctic Terns by Egevang et al. (2010) and Monaghan (2002). A high degree of population mixing in the staging areas and non-breeding range was suggested, based on the lack of evidence for distinct races of Arctic Terns (Monaghan 2002). However, our data do not support their statements. Although sample sizes and study durations in both tracking studies were relatively small, our data clearly indicate a segregation in Antarctic non-breeding ranges used by Arctic Terns from Greenland and from The Netherlands. This would imply that Arctic Terns show a stronger migratory connectivity (cf. Webster et al. 2002) than assumed previously, which has considerable implications for their ecology, evolution, and conservation.

Prospects

This study showed that tracked terns from The Netherlands use a different Antarctic region than the tracked terns from Greenland, Iceland and Maine, and that they travel the largest distances outside the breeding season. Do Arctic Terns from The Netherlands indeed make the longest migratory avian flights? Hypothetically, Arctic Terns from colonies on the coasts of Norway, Svalbard and Arctic Russia could make even longer migrations when they use East Antarctic nonbreeding ranges. Tracking of these birds will be one of the future challenges if we are to understand the potential scale and extent of the longest avian migrations. The other key question that remains is why Arctic Terns from The Netherlands spend the non-breeding season in the Antarctic Indian Ocean when suitable habitat is present much closer in the Weddell Sea.