Although Common Terns breeding in Central Europe have been known to use the southeastern flyway (Cramp and Simmons 2006), we present the first detailed description of their east African migration route. Two stopover sites used during autumn migration were identified: Lower Nile and the southern part of the Red Sea, and we also confirmed a stopover in Israel during spring migration (Cramp and Simmons 2006; Kiat 2016). Terns stayed in the eastern part of the Nile Delta, around Lake Manzala, which is assigned as an Important Bird and Biodiversity Area significant for migration and wintering of waterbirds (Evans and Fishpool 2001). It is a brackish lake with more than 1000 islands, with main habitats being reed-swamps, saltmarshes and sandy areas (BirdLife 2019). Of four tracked terns, one stayed in the Lower Nile for a longer period and one seemed not to stop there at all. All four birds stopped in the southern Red Sea area, three of them for over 2 months. The southern part of the Red Sea is rich in nutrients that are brought by wind-induced horizontal advection from the Gulf of Aden during the winter monsoon season (Raitsos et al. 2015). The productivity of the southern Red Sea therefore increases at the beginning of October and stays high during winter months. However, three of four tracked terns left the area at the beginning of October, about the time when nutrients normally start to increase. We therefore presume that birds used this stopover site in order to avoid strong southwestern summer monsoons (Clemens et al. 1991) blowing in the direction opposite to their migration, and continued their movement with a tailwind of north-eastern winter monsoons. Similar to other terns with flapping flight, Common Terns are very receptive to wind speed and direction (Barrett 2016), and stopping in the southern Red Sea to wait for favourable wind conditions can minimize their travel costs during the final part of their autumn migration. Although a departure from that site coincides with the period of 3 weeks around the autumn equinox, when latitudes are difficult to determine using data from light level geolocation (Porter and Smith 2013), quick changes in longitude obvious in October indicate the start of a consecutive migration step (Additional file 2: Fig. S2). The longest stationary period during migration, as resulting from FLightR analysis, was 110 days, spent by the tern Mk006 at the southern Red Sea. However, during that period, a part of locations fell 750 km further south, near the Shebelle River in Ethiopia. Whether that latitude change, visible from Fig. 1 and Additional file 2: Fig. S2b, was erroneous or not, has to be further studied. The period spent at stopover sites was much longer in inland European Common Terns than in German North Sea populations, in which the longest stay at stopover was less than 1 month (Becker et al. 2016). Some inland North American Common Terns also have long stopovers: mean duration at stopovers was 21 and maximum 71 days (Bracey et al. 2018).
Terns tagged in Croatia wintered in the southern Mozambique Channel. That area was already identified as one of the hotspots for foraging seabirds in the tropical western Indian Ocean (Le Corre et al. 2012). Strong eddy activity typical for that area induces offshore transport of nutrient-rich coastal waters to the near-surface layer, increasing productivity (José et al. 2016). Although productivity is lower during the (northern) winter, coastal waters still have high chlorophyll concentrations (José et al. 2016), providing good feeding opportunities for wintering terns. Hungarian terns were found wintering along the coast of Kenya, close to the Tana River. Tana River delta is a Ramsar site, hosting a large number of waterbirds, including several tern species (RSIS 2019). Two main threats for foraging seabirds were identified in the Mozambique Channel and Kenyan coast: oil pollution due to maritime traffic and intensive industrial fishing (Le Corre et al. 2012). Industrial fishing is developing in the western Indian Ocean causing a threat of over-exploitation of the fish-stock, especially predatory fish such as tuna. As many other seabird species, Common Terns were shown to forage in aggregation with schools of tuna driving small fish to the surface (Goyert et al. 2014). The decline in predatory fish populations is supposed to have serious impacts on the seabirds using that foraging strategy (Feare et al. 2007).
Both birds tracked during prenuptial migration shortly stopped in Israel in early April, a stopover that was not used by either of the tracked birds during post-breeding migration. This data is in accordance with earlier findings indicating Israel as an important stopover site for Central European Common Tern populations during spring migration, but rendering its importance lower in autumn (Cramp and Simmons 2006; Kiat 2016). As a result of long stopovers, post-breeding migration lasted more than four times longer than prenuptial migration. Similar results were found for inland Common Terns in North America (Bracey et al. 2018). Faster spring migration is a general pattern among birds (Nilsson et al. 2013), however in case of Common Terns the opposite was found for several individuals of a German North Sea population wintering along the West African coast (Becker et al. 2016). The northward movement of both Croatian birds in late February could be described either as winter movement or the start of the prenuptial migration; late February is a period of departure from wintering grounds for terns breeding in Germany and wintering along east African coasts (Becker et al. 2016). On the other hand, substantial movements during winter were reported for other Common Tern populations (Neves et al. 2015; Bracey et al. 2018). The area where Croatian birds spent late February and early March lays further south than the wintering area of two Hungarian terns revealed by this study. This suggests that Central European terns utilize a large span of the Kenyan and Mozambique coasts as wintering grounds. Further studies are therefore needed to elucidate winter movements of Common Terns.
Although using the same east African flyway, there were some differences between Hungarian and Croatian terns’ migration pattern. The two birds from Croatia had a very similar migration pattern, and were probably migrating in the same flock. Similarly, two colour-ringed birds from the same colony were observed together during dispersion or autumn migration on several occasions (Additional file 3: Table S1). The departure of Hungarian terns in 2014 was almost a month later than the departure of Croatian terns in 2016. This difference is more likely to be related to individual variations within the same colony or interannual changes than to the breeding site. For example, changes of water level affect the start of the breeding season while clutch failure and renesting affect its termination, both capable of causing the difference in departure date. Individual and annual differences in the timing of departure were recorded by several studies of Common and Arctic Tern Sterna paradisaea migration (Becker et al. 2016; Bracey et al. 2018; Redfern and Bevan 2019).
There are several possible explanations for the differences in wintering areas between Hungarian and Croatian birds. As one Hungarian logger stopped in early November, it is possible that this bird did not reach its final wintering area during that time. Furthermore, interannual changes in the primary productivity in the Western Indian Ocean affect phytoplankton-feeding fishes (Monticelli et al. 2007) and could cause differences in the abundance of tern prey, which might affect their choice of wintering area. Although many seabirds have high wintering site fidelity, it is known that some birds showed flexibility in wintering site, stopover behaviour and migratory schedule (Dias et al. 2011). Recoveries of a Hungarian-ringed bird in Mozambique and Kwazulu-Natal province of the Republic of South Africa indicate that at least some birds in some years reach the Mozambique Channel. However, we cannot exclude the possibility of some level of migratory connectivity (i.e. segregation of wintering areas of birds from different colonies), as recorded for the Artic Tern (Sterna paradisaea) (Fijn et al. 2013). Further studies of several Central European populations are needed to get a better understanding of temporal and spatial differences in migration of Central European Common Terns.
Studies based on ring recoveries or resightings are affected by bias caused by spatial and temporal heterogeneity in ring re-encounter probability (Korner-Nievergelt et al. 2012). Therefore, they reflect both bird distribution and the number and activity of potential observers. In spite of the considerable number of terns ringed in Hungary and Croatia, recovery data are limited. Observations from Italy, Spain, Tunisia and Senegal indicate the use of the southwestern route, while recoveries in Serbia, Romania, Ukraine, Jordan and Israel confirmed the movement of terns towards the eastern Mediterranean. However, a great part of recoveries belong to immature birds, whose movements prior to returning to breeding grounds are insufficiently known. Therefore, they might represent either a migration route or wandering of immature birds. The number of long-distance recoveries from other Central European countries is also small but indicates migration routes used. Common Terns breeding in Czechia migrate mostly in a southwestern direction to the western Mediterranean and further along the western coast of Africa, with recoveries in Liberia and DR Congo. However, an autumn recovery in Hungary of a Common Tern from southern Moravia, together with a spring recovery of a bird ringed in Slovakia and found on the Evros delta in Greece, suggests the use of the south-eastern migration route (Krestova 2008). The only recovery of a bird hatched in the Adriatic population in Croatia was from a subadult (3rd year) bird found in September 2000 in Huelva, Spain (Kralj 2013), confirming east–west migration through the Mediterranean Sea. Numerous recoveries of Common Terns breeding on the other side of the Adriatic Sea, in northern Italy, showed the use of the western route, with recoveries from Spain to Gabon (Spina and Volponi 2008).
In earlier studies, the use of light-level geolocators attached to the tarsus of Common Terns showed no negative effect on the behaviour and fitness of tagged birds (Kürten et al. 2019). In our study, we found no weight loss or visible injuries on tagged birds. The low ratio of retrieved geolocators (22%) is a result of the relative instability of studied colonies compared with coastal ones (Becker et al. 2016). Riverine breeding sites are often less stable than coastal ones because of interannual water level changes and predation (Scharf 1981; Bogliani et al. 1982). In Croatia, recoveries of adult birds showed frequent changes of breeding colonies between years, and in 2018 even within the breeding season (Martinović et al. 2019). Between 2016 and 2018 Common Terns bred on seven different islands in the study area: two sites were occupied in 2016, three sites in 2017 when low water level created additional islands and four in 2018 when water level was exceptionally high and the main island at Rakitje gravel pit was submerged and was unsuitable for breeding until mid-June. Furthermore, in the middle of the breeding season of 2016, all nests were destroyed on all platforms at the Hungarian colony, presumably by an Otter (Lutra lutra). This prevented us from deploying all available loggers, and from retrieving further loggers deployed in 2014. This predation event might also have been the reason for a remarkably low breeding pair density in 2017.
In many studies, geolocator data yielded supplementary information about non-breeding distribution and timing of migration already known from recoveries of ringed birds, but in some cases, different migration patterns were revealed (Korner-Nievergelt et al. 2012). During this study, geolocators revealed the use of east African route for Croatian birds, a fact that had not been obvious from recoveries of ringed birds processed before 2010 (Kralj 2013). Retrieved data of four birds enabled us to outline the migration strategy of Central European inland breeding Common Terns using the east African route for the first time. Stopover areas at Lower Nile and the southern Red Sea were identified, as well as wintering sites along the Kenyan coast and in the southern Mozambique Channel.
Identified stopover and wintering sites face multiple threats either currently or potentially: Lake Manzala in the Nile delta is threatened by pollution from waste-waters, increasing salinity, land reclamation and illegal killing of birds (Evans and Fishpool 2001). The southern Red Sea is generally in a healthy state and lengthy stopovers confirm that the area is favourable for foraging Common Terns. However, due to its semi-enclosed nature and the petroleum-industry of economies in the region, it faces high risk of oil pollution (Gladstone et al. 1999). The Mozambique Channel and Kenyan coast are also threatened by oil pollution and overfishing (Le Corre et al. 2012). Climate change, identified as one of the greatest threats to Common Terns worldwide (Palestis 2014; Bracey et al. 2018), might also have serious impacts on wintering areas in the Indian Ocean. The relatively cool and productive western Indian Ocean is reported to be undergoing a long-term warming trend, with anticipated effects on monsoon circulation and marine food webs (Roxy et al. 2014). Surprisingly, warming of the Indian Ocean is shown to increase productivity of the Red Sea due to stronger winds amplifying the northward advection of nutrient-rich waters from the Gulf of Aden (Raitsos et al. 2015). It is possible that the southern Red Sea will thus become an even more important feeding area for European Common Terns.
Differences in migration between Hungarian and Croatian breeders point to the importance of further studying the migration of Central European populations of the Common Tern. This, along with exploring their exposure to environmental factors and threats along the migration route, might help stakeholders in designing and implementing conservation measures for the protection of long-distance migratory seabirds along their migration routes.