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Arriving depleted after crossing of the Mediterranean: obligatory stopover patterns underline the importance of Mediterranean islands for migrating birds

Arriving depleted after crossing of the Mediterranean: obligatory stopover patterns underline the... Anim. Migr. 2022; 9: 14–23 Research Article Christos Barboutis*, Elisabeth Navarrete, Georgios Karris, Stavros Xirouchakis, Thord Fransson, Anastasios Bounas Arriving depleted after crossing of the Mediterranean: obligatory stopover patterns underline the importance of Mediterranean islands for migrating birds https://doi.org/10.1515/ami-2022-0117 estimates at least 180 million birds of our study species are received November 5, 2021; accepted March 29, 2022 expected to migrate through Greece, 14% of which would not be able to resume their migration without refueling. Abstract: Hundreds of millions of birds reach the Medi- The significance of small islands and coastal sites in the terranean islands or Mediterranean coast of Europe every Mediterranean as obligatory refuelling sites is discussed spring after having crossed the Sahara Desert and the and their conservation value for migratory birds is high- Mediterranean Sea. Using data from three small insular lighted under the perspective of climate change. stopover sites, we calculated body mass without fuel for 18 trans-Saharan passerine migrants. We subsequently Keywords: Stopover, Barrier crossing, Small islands, Fuel used arrival fuel loads coupled with potential flight range load, Conservation value estimates to assess the percentage of birds that are forced to perform an obligatory stopover after crossing the Med- iterranean Sea due to fuel depletion. Average arrival fuel loads were among the lowest ever recorded in the Mediter- 1 Introduction ranean region and minimum body mass values recorded for several species were lower than any other individual Every year billions of birds, of thousands of species, cover value reported. The percentage of birds that needed to enormous distances between their breeding and winter- replenish their energy stores before resuming their north- ing grounds. Those seasonal movements regularly involve ward migration journey varied from 0% to 50% depending the crossing of vast ecological barriers such as deserts, on the species and locality studied. Based on conservative mountain ranges and large water bodies. In the western Palaearctic migration system, most trans-Saharan passer- ine migrants have to cross the Sahara Desert and the Medi- terranean Sea. In the central and eastern flyway, the desert *Corresponding author: Christos Barboutis, Department of Biologi- and the sea can be considered as one ecological barrier as cal Applications and Technology, University of Ioannina, Ioannina, there are hardly any possibilities to refuel during cross- GR-45110, Greece, Email: cbarboutis@ornithologiki.gr ing [1]. Thus, prior to the barrier crossing, birds should be Christos Barboutis, Elisabeth Navarrete, Antikythira Bird Observato- ry, Hellenic Ornithological Society/BirdLife Greece, Themistokleous energetically prepared for this demanding task [2-5]. 80, Athens, GR-10681, Greece Migration is indeed the most energy-demanding task Georgios Karris, Lab of Environmental Physics, Energy and Environ- in a bird’s life cycle. When facing the Sahara Desert, a mental Biology, Department of Environment, Faculty of Environment, bird can cross it by intermittent flight, with stopovers to Ionian University, Panagoula, GR-29100, Zakynthos, Greece rest and refuel, whereas the Mediterranean Sea must be Stavros Xirouchakis, Natural History Museum of Crete, University of Crete, University Campus (Knossos), GR-71409 Heraklion, Crete, crossed in non-stop continued flight [6, 7]. Small and large Greece islands scattered in the Mediterranean Sea are often the Thord Fransson, Department of Environmental Research and Moni- first available land that migratory birds encounter after toring, Swedish Museum of Natural History, SE-104 05, Stockholm, crossing the Sea and the desert during their northward Sweden spring migration. Passerines arriving with depleted fuel Anastasios Bounas, Department of Biological Applications and Tech- reserves after crossing this large ecological barrier have nology, University of Ioannina, Ioannina, GR-45110, Greece Open Access. © 2021 Barboutis et al., published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 License. Fuel loads after crossing the Mediterranean   15 been reported in central and eastern areas of the Mediter- 2 Methods  ranean [8, 9]. A varying percentage of birds and species have enough energy reserves to resume their northward 2.1 Ethical approval migration once reaching the Thyrrenian islands in the central Mediterranean [10], whereas cases of birds with no This study was carried out in accordance with the Euro- residual fat reserves or even dying from depletion are not pean Convention for the Protection of Vertebrate Animals uncommon [11]. Arrival energy reserves and environmen- Used for Experimental and Other Scientific Purposes of tal conditions at stopover sites could lead to increased the Council of Europe (http://conventions.coe.int/Treaty/ stopover duration thus delay departure from sites [12, 13] EN/Treaties/Html/123.htm.). Ringing permits for each and could even influence the breeding phenology and location were issued annually by the Hellenic Ministry of performance of birds [14]. Nevertheless, the importance of Environment and Energy. stopover sites such as islands just after the barrier cross- ing is not only limited to refuelling purposes as birds often need to rest or sleep after endurance flights [15, 16], settle 2.2 Sampling area and data collection until more favourable meteorological conditions occurs, or even gather information and/or socially interact with Data was collected at three small Greek islands, situated conspecifics to evaluate the progress of the migration in the Libyan, the Aegean and the Ionian Sea. From south journey [17]. Therefore, stopover site availability after to north these were, Gavdos (34°50′ N, 24°5′ E) lying in the barrier crossing and habitat suitability for fuelling are of Libyan Sea, 40 km south of the island of Crete, Antikythira particular importance for a successful migration. (35° 51′ N, 23° 18′ E) between the Aegean and the Ionian According to optimal migration models [18], migrat- Sea, 40 km south of the island of Kythera and the Stro- ing birds should try to minimise either energy investment fades islands (37° 15’ N, 21° 00’ E) in the Ionian Sea, 50 or duration of migration (i.e. time-minimizing scenario). It km south of the island of Zakynthos (Fig. 1).  Birds were is therefore expected that birds arriving with high energy captured using 16x16mm mesh, nylon, mist nets. Mist reserves will resume their journey as soon as possible netting took place from dawn and thereafter for at least while birds with low residual energy reserves have to eight hours, except for days with adverse weather condi- restore them and remain at a stopover site. At this inter- tions. The total length of mist nets used were 150m, 90m play between migratory decisions, insular stopover sites and 60m for Antikythira, Strofades and Gavdos respec- located after ecological barriers should be extremely tively. Mist netting took place for a total of 76 days between important especially under the prospect of climate mid-April and mid-May of 2011-2013 at Gavdos, for a total change; studies employing future projections have shown of 736 days between the end of March/May of 2007-2019 that responses of European birds include poleward shifts at Antikythira and for a total of 44 days between end in their breeding and wintering distribution and such pre- of April and beginning of May in 2009 -2010, 2012 -2015 dicted changes will increase migration distances for some and 2018 at Strofades islands (Table S1). Mist nets were species rendering them susceptible to increased mortality checked for trapped birds every hour. Trapped birds in all risks [19]. sites were aged according to Svensson [20] and weighed Here, we aim to bring the significance of small islands to the nearest 0.1 g. Maximum-chord wing length [20] was in the Mediterranean into perspective and highlight their recorded to the nearest 0.5mm as a measure of body size. conservation value for migratory birds. To this aim, we use Visible subcutaneous fat was classified in 9 score ordinal empirical data coupled with avian flight models to calcu- scale (fat score) according to Kaiser [21] and bird’s pecto- late the proportion of birds from different species that ral muscle mass was visually classified in 4 score ordinal are not able to continue their migration (must perform scale (muscle score), based on its shape [22].  We consid- an obligatory stopover) at three insular stopover sites in ered data from species that are known to cross the Med- the eastern Mediterranean. Then, we use current data iterranean Sea and the Sahara Desert before arriving in on breeding population sizes and calculated the number each area in the following analyses.   of birds that migrate through the region and therefore provide a quantitative estimate of birds that could poten- tially experience future changes to their migratory jour- neys. 16   Barboutis et al. 2.3 Estimating body mass without fuel and 2.4 Estimating potential flight range arrival fuel loads Assuming that flying birds lose mass at a constant rate of We estimated body mass without fuel (m ), i.e. the body 1% per hour of flight [24, 25], potential flight ranges (Y; mass of a bird with both a fat score and a muscle score of hereafter flight range) were estimated according to the 0, according to the structural mass concept [23]. Thus, it flight range equation developed by Delingat et al. [26]:  should be noted that this is the most conservative estima- tion as it reflects a bird’s mass with neither fat nor protein Y = 100 × U × ln(1 + f ) (3) to use as fuel. We applied a regression function of the m0 (mass of all birds with both a fat score and a muscle score where U is airspeed. Regarding U, the species-specific of 0) on their respective maximum wing chord (hereafter values reported in Bruderer and Boldt [27] were used. wing length): When the species-specific value was not available the equivalent value of a closely similar species was used. m = b + b × wing length (1) Specifically for the Wood warbler (Phylloscopus sibilatrix), 0 0 1 the Collared flycatcher (Ficedula albicollis), the Sedge where b is the intercept and b a constant from the regres- warbler (Acrocephalus schoenobaenus) and the Woodchat 0 1 sion. This regression was applied separately to all species shrike (Lanius senator), we used the airspeeds measured trapped at our study sites with a sample size larger than for the Willow warbler (Phylloscopus trochilus), the Pied 10. In order to estimate the fuel load (f; bird’s body compo- flycatcher (Ficedula hypoleuca, the Reed warbler (Acro- nents which can be used as fuel), the following equation cephalus scirpaceus) and the Red-backed shrike (Lanius was used:  collurio) respectively. For two species with no availa- ble airspeeds, the Golden oriole (Oriolus oriolus) and  f = (m - m ) / m (2) the Common nightingale (Luscinia megarhynchos), the 0 0 where m, is the body mass at capture and m is the overall mean value for passerines, 10 m/s, was used [27, birds’ body mass without any fuel.  28]. Flight range was estimated under still air conditions Figure 1. Map of our study area in eastern Mediterranean. Dots and zoomed insets show our study sites (Strofades, Antikythira, Gavdos), whereas the nearest to them larger islands are also noted (Zakynthos, Kythira and Crete respectively). Fuel loads after crossing the Mediterranean   17 as wind direction is highly varying in the wider study area and the average tailwind component during the peak of the spring migration period is close to zero [29]. To esti- mate the percentage of birds that had the necessary fuel to reach the next larger island, where more refuelling oppor- tunities are expected to exist (Fig. 1), the flight range equa- tion was calculated for every individual bird trapped and we examined if they could continue their flight for 40 km in the case of birds trapped in Gavdos and in Antikythira and 50 Km in the case of birds trapped in Strofades. Due to the uneven sample size between the three study sites, the overall percentage of birds per species that could not continue their migration was estimated as the average of the estimated percentage of all sites.  2.5 Species and number of birds using the migration corridor In order to provide a quantitative estimate of the number of birds belonging to our study species that use Greek islands and coastal sites as a migration corridor during spring, we used the most recent breeding bird population estimates included in the European Red List of Birds [30], following the approach of Hahn et al. [31]. More specifi- cally, we used all ring recovery data for our study species that included birds ringed in Greece and recovered else- where during the spring migration and vice versa (data provided by the Hellenic Bird Ringing Center). Then, for each species we drew a minimum convex polygon around the recoveries and used the breeding population esti- mates for each country that was included in the polygon as an estimate of the number of birds that would migrate through Greece (Fig. S1). We did not consider non-breed- ers that could account for 15% within a population [31, 32] thus keeping our estimates rather conservative. Furthermore, we assessed the number of species of trans-Saharan migratory birds belonging to passerines and near passerines (i.e. belonging to the orders Apodi- formes, Caprimulgiformes, Cuculiformes, Coraciiformes, Piciformes, Columbiformes and Bucerotiformes) arriving to Greek islands and coastal areas in south Greece. For estimating the number of species, we used eBird’s (www. ebird.org) bar chart tool [33] to retrieve records of species at the Peloponnese, the island of Crete, South Aegean and the Ionian islands, from March to May. Additionally, the daily ornithological species list of the Antikythira Bird Observatory held since 2008 on daily bases during spring migration period was used. Only species that winter south Figure 2. Percentage of birds per species that must perform an obligatory stopover in: a) Strofades, b) Antikythira and c) Gavdos. of the desert of the Sahara and are expected to reach Orange bars depict standard error. Greece after having crossed the ecological barriers of the 18   Barboutis et al. Sahara Desert and the Mediterranean Sea were included (Lanius senator) at Gavdos (31.7± 16.4 %). Potential flight in this assessment. range estimates were calculated for 38,253 birds arriving at our three study sites. The percentage of birds that could not resume their migratory flight to the nearest more suit- able fuelling localities, varied from 50.6% in the case of 3 Results  the Collared flycatcher (Ficedula albicollis) arriving at Sto- fades islands, to 0% (all individuals could continue their Mean arrival fuel loads were estimated for 18 trans-Sa- migration) in the case of the Great reed warblers (Acro- haran migratory passerine species (Table 1; Table S2; cephalus arundinaceus) and the Woodchat shrike arriving regressions calculated for species that had more than 10 to Gavdos (Fig. 2; Table S3). Across all islands, a mean of birds with recorded wing length, body mass and fat and more than 14% of the birds belonging to our study species muscle score of 0). Fuel load of birds arriving to our study were not able to resume their migration. sites varied from 23.3% of their structural mass in the A conservative estimate of almost 184.9 million Icterine warbler (Hippolais icterina), to 8.7% in the case birds belonging to our study species migrate through of Sand martin (Riparia riparia) across the three small Greece during spring, with the Willow warbler (Phyllo- islands (Table 1). The lowest average arrival fuel load was scopus trochilus), the Barn swallow (Hirundo rustica), recorded for the Wood warbler (Phylloscopus sibilatrix) at the Common whitethroat (Sylvia communis) and the Strofades islands (2% ± 7.9 % of structural mass) and the Wood warbler being the most abundant ones, altogether largest fuel load was recorded for the Woodchat shrike accounting for almost 60% of all birds (Table S4). Of those Table 1. Arrival fuel load (% of structural mass) per species for all birds and for each study site and minimum body mass recorded per species. Antikythira Gavdos Strofades Fuel load Min body Fuel load Fuel load Fuel load Species n n n n (% ± SD) mass (% ± SD) (% ± SD) (% ± SD) Riparia riparia 8.3 ± 8.4 1592 8.1 7.5 ±8.0 1147 12.0 ± 9.4 240 8.7 ± 9.5 205 Oriolus oriolus 11.2± 10.8 1624 33.6 12.0 ± 11.0 1390 11.9 ± 11.4 87 2.8 ± 8.7 147 Delichon urbicum 11.6± 9.9 703 9.3 9.3 ± 9.9 386 17.2 ± 9.7 224 7.9 ± 10.4 93 Phylloscopus 12.3± 12.7 2768 5.5 13.2 ± 13.1 2466 15.4 ± 12.6 68 2.0 ± 7.9 234 sibilatrix Acrocephalus 14.3± 12.4 901 18.2 16.0 ± 12.9 692 19.8 ± 11.0 28 6.9 ± 10.8 181 arundinaceus Sylvia borin 14.9± 12.7 9030 9.5 17.0 ± 13.6 7116 13.1 ± 11.3 403 5.6 ± 8.8 1511 Ficedula 15.0± 12.5 3574 7.6 15.6 ± 12.8 3208 20.3 ± 10.7 80 6.4 ± 9.2 286 hypoleuca Acrocephalus 15.3± 32.5 2314 6.3 15.9 ± 35.7 2000 15.5 ± 13.6 78 10.2 ± 10.9 236 schoenobaenus Phoenicurus 15.6± 13.9 1304 9.0 16.2 ± 14.0 1131 18.0 ± 18.7 24 10.9 ± 11.8 149 phoenicurus Muscicapa striata 15.6± 12.4 3356 8.8 16.9 ± 12.6 2659 15.7 ± 12.5 230 8.2 ± 11.0 467 Hirundo rustica 16.0± 13.9 813 11.3 15.7± 13.6 598 18.0 ± 15.0 151 13.8 ± 14.3 64 Saxicola rubetra 16.5± 13.9 1379 9.5 15.9 ± 13.5 751 23.9 ± 15.6 293 11.2 ± 13.5 335 Ficedula albicollis 18.1± 13.0 1385 7.1 18.7 ± 13.1 1262 23.7 ± 12.5 41 6.7 ± 12.4 82 Phylloscopus 19.7± 17.2 1067 5.4 19.8 ± 17.1 986 21.7 ± 14.8 18 17.7± 18.6 63 trochilus Lanius senator 20.8± 11.9 1060 21.2 21.4 ± 11.8 829 31.9 ± 16.4 56 14.5 ± 11.0 175 Luscinia 21.5± 13.5 1328 11.3 21.9 ± 13.6 1261 20.3 ± 15.3 17 12.6 ± 10.7 50 megarhynchos Sylvia communis 22.5± 14.6 2515 9.3 25.1 ± 15.4 1730 24.6 ± 15.4 135 14.9 ± 12.5 650 Hippolais icterina 23.3± 14.3 1570 8.9 24.7 ± 14.8 1327 24.8 ± 14.5 67 12.3 ± 10.4 176 Fuel loads after crossing the Mediterranean   19 species the Willow warbler, Barn swallow and the Wood schoenobaenus, Muscicapa striata, Phoenicurus phoenic- warbler were also estimated to be among the species with urus, Riparia riparia, Saxicola rubetra, Sylvia borin) were the largest number of birds that need to undertake an lower than any other minimum individual value reported obligatory stopover at an island or a coastal locality when [35, 37-40]. These results complement previous reports of reaching Greece after the Mediterranean crossing (Fig. birds with depleted fuel reserves reaching insular Greece 3). Overall, an average of 30 million birds are estimated during the northward migration [9, 41, 42]. to perform an obligatory stopover. Additionally, it was The low arriving fuel loads at our study sites are prob- assessed that 48 more passerines and close to passerines ably a result of the vast length of the combined ecological (66 species in total) reach Greece every spring after cross- barrier of the Sahara Desert and Mediterranean Sea that ing the desert and the sea (Table S5).   can reach or even exceed 2800 km [29], with hardly any possibilities to refuel. Surely refueling opportunities exist in North Africa [37] and that is reflected in the high per- centage of individuals of some species that do not arrive 4 Discussion depleted (e.g Lanius senator). However, there is evidence that species adapted to mesophilic and moist habitats Birds arriving at Greek islands have either just crossed the show difficulties in successfully refuelling during migra- Sahara Desert and the Mediterranean Sea thus experience tion in dry regions [43] like those of North Africa. There- relatively low average fuel loads or stop in the islands in fore, the low arrival fuel loads we recorded in this study good condition after refueling in North Africa. Fuel loads indicate that there are probably not any widespread refu- of species caught in our study sites such as the Spotted elling possibilities close to the African coast of the Medi- Flycatcher (Muscicapa striata), the Garden Warbler (Sylvia terranean Sea before reaching the Greek islands. borin), and the Common Nightingale (Luscinia megarhy- Whether the fuel depleted birds arriving at Greek nchos) are among the lowest values reported from other islands during spring are “fall-outs”, i.e. not capable of Mediterranean sites [34-37]. Additionally, minimum body further migration [44], cannot be fully assessed based on mass values recorded for several species (Acrocephalus this study. Our data suggest that some individuals perform Figure 3. Overall percentage of birds that have to undertake a stopover in Greek islands and coastal sites and the respective cumulative estimate per species in millions of individuals. 20   Barboutis et al. an obligatory stopover being unable to continue their compared to fat [46] and the low physiological stated of migration, however, other birds seem to actively decide birds arriving to our study sites, a good proportion of birds to land depending on their fuel loads and species-spe- that have been estimated to just being able to overpass cific habitat requirements [40]. Future assessment of the our study sites might not actually not make it. Our calcu- abundance of birds in the larger islands next to our study lations therefore, represent the minimum number of birds sites could shed some light on the fall-out hypothesis in whereas the true number could in fact be much higher. the eastern Mediterranean region; if lean birds are more At least 48 more species of trans-Saharan migratory pas- abundant in the “low-quality” small islands (that inher- serines and non-passerines are also migrating through ently offer fewer refuelling opportunities) it would seem Greece every spring, and probably some individuals also that birds would have no option but land at the first avail- reach the stopover sites energy depleted. Therefore, the able site after sea crossing [37]. Regarding the fate of the amount of birds that need to undertake an obligatory stop- extremely lean birds we encountered, some preliminary over at insular or coastal sites in Greece could reach up to data indicate that at least some extremely lean birds of several hundreds of millions, making these stopover sites some species could manage to recover during their stop- of outmost importance for the survival of migratory birds. over and resume their migration; having depleted a large Although replenishing of energy reserves is consid- amount of protein, mainly from the breast muscle [41] ered the main aim of stopover events, birds do not stop- and the digestive organs [45] along with the fat reserves over at insular sites in the Mediterranean only to refuel which are the main fuel [46], they are actively seeking and as shown by the large species variety of migrating birds consuming nectar [47], an energy source readily obtained recorded, of which many birds have enough fuel reserves during spring time on north Mediterranean and easy to to continue their norward journey [15]. Many birds, the assimilate after their long-distance flight [48]. Addition- numbers of which cannot yet be estimated sufficiently, ally, evidence from Mauritania indicates that individual need the stopover sites for non-fuelling purposes and birds with fuel loads much below average are capable of will continue migration the following night. After long recovering and refueling even in dire environments [39]. endurance flights over the Mediterranean Sea, birds seem On the other hand, extended incidents of birds dying from to need to recover from sleep deprivation [50-52], whereas depletion at our study sites are not unusual and have others might be forced to use stopover sites to avoid been observed during the course of this study with mor- adverse weather conditions which are not rare during tality rates being highest in Strofades islands. That could spring in the Mediterranean region [53]. Furthermore, possibly result due to Strofades geographical position local environmental conditions at stopover sites might be coupled with the general northern – northeastern spring necessary for some species to evaluate and predict condi- migration direction, so birds have to undertake a longer tion at final destinations further north [54]. barrier crossing and therefore more often reach the island The importance of Mediterranean islands is further depleted. brought into perspective if we consider the estimated The pooled data from our three study sites indicate obligatory stopover of hundreds of millions of birds under that the percentage of birds that are forced to undergo an future changes in climate. Besides, migration is an adap- obligatory stopover before leaving the islands varied from tive strategy for organisms to exploit the seasonality in 25.5% in the case of the Golden Orioles (Oriolus oriolus) resource availability. There is so far plenty of evidence down to 3.3% in the case of Woodchat Shrike. Strikingly, for the modification of migratory routes as a result of in the case of the Collared flycatcher arriving to the island climate change in several avian species, including longer of Strofades, up to half of the individuals must refuel migratory journeys [19, 55, 56]. Longer flight ranges need before resuming their migration. Based on our estima- increased energy demands which subsequently lead to tions approximately 30 million of birds belonging to the more stopovers needed and ultimately can lead to a mis- 18 study species perform an obligatory stopover at insular match between time arrival and breeding [57]. Specifically or coastal sites in Greece every spring. However, the esti- for the Western Palearctic migration system, threats are mates reported here should be treated with caution; the even more ominous; increased drought events especially fact that we used a conservative method of estimating body in areas adjacent to the Sahara Desert will effectively lead mass without fuel has subsequently led to an underesti- to the elongation of the barrier and could pose serious mation of the number of birds that perform an obligatory direct threats to migrating birds such as increased mor- stopover. Having in mind that as fat storage gets depleted, tality rates. [58]. Considering our results, showing that at the portion of protein involved in active migratory flight least 30 million of birds must perform stopover in insular increased [49], proteins produce eight time less energy or coastal sites in Greece regardless of habitat quality, Fuel loads after crossing the Mediterranean   21 even the smallest decrease of resources in these habitats References could lead to extreme consequences; phenological mis- [1] Biebach H. Strategies of trans-Saharan migrants. In: Gwinner match between migratory birds and seasonal resources E, editor. Bird migration: physiology and ecophysiology. due to climate change has already resulted in population Berlin: Springer-Verlag; 1990. p. 352–67. declines in some regions [59, 60]. However, behavioural [2] Fry CH, Ash JS, Ferguson-Lees IJ. Spring weights of some flexibility of birds and the overall adaptive potential of palaearctic migrants at lake Chad. 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Body fat influences departure from stopover sites in migratory birds: evidence Acknowledgements: We thank the numerous volunteers from whole-island telemetry. Biol Lett. 2010;6(4):478–81. of Antikythera Bird Observatory for their assistance. Field [13] Smith AD, Mcwilliams SR. What to do when stopping over: work at all sites were carried out with the relevant permits behavioral decisions of migrating songbird during stopover are dictated by initial change in their body condition and form the Hellenic Ministry of Environment and Energy. mediated by key environmental conditions. Behav Ecol. We thank the local authorities, the Management Agency 2014;25(6):1423–35. of the National Marine Park of Zakynthos, the National [14] Finch T, Pearce-Higgins JW, Leech DI, Evans KL. Carry-over Coastguard Authorities, and the Metropolis of Zakynthos effects from passage regions are more important than for facilitating the fieldwork in Strofades and issuing rel- breeding climate in determining the breeding phenology and performance of three avian migrants of conservation concern. evant permits. Rings were supplied free of charge by the Biodivers Conserv. 2014;23(10):2427–44. Hellenic Bird Ringing Centre. This work is part of ROUTES [15] Ferretti A, Maggini I, Fusani L. How to recover after sea research project, supported by the Hellenic Foundation crossing: the importance of small islands for passerines for Research and Innovation (H.F.R.I.) under the “2nd during spring migration. Ethol Ecol Evol. 2021;33(3):307–20. Call for H.F.R.I. Research Projects to support Post-Doc- [16] Maggini I, Trez M, Cardinale M, Fusani L. Stopover toral Researchers” (Project Number: 805). 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Lett. 2020;4(1):4–18. of climate change are most severe for long-distance migrants in seasonal habitats. Proc Royal Soc B. 2010;277(1685):1259–66. Supplemental material: The online version od this article: (DOI: 10.1515/ami-2022-0117) offers supplementary material. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Animal Migration de Gruyter

Arriving depleted after crossing of the Mediterranean: obligatory stopover patterns underline the importance of Mediterranean islands for migrating birds

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Abstract

Anim. Migr. 2022; 9: 14–23 Research Article Christos Barboutis*, Elisabeth Navarrete, Georgios Karris, Stavros Xirouchakis, Thord Fransson, Anastasios Bounas Arriving depleted after crossing of the Mediterranean: obligatory stopover patterns underline the importance of Mediterranean islands for migrating birds https://doi.org/10.1515/ami-2022-0117 estimates at least 180 million birds of our study species are received November 5, 2021; accepted March 29, 2022 expected to migrate through Greece, 14% of which would not be able to resume their migration without refueling. Abstract: Hundreds of millions of birds reach the Medi- The significance of small islands and coastal sites in the terranean islands or Mediterranean coast of Europe every Mediterranean as obligatory refuelling sites is discussed spring after having crossed the Sahara Desert and the and their conservation value for migratory birds is high- Mediterranean Sea. Using data from three small insular lighted under the perspective of climate change. stopover sites, we calculated body mass without fuel for 18 trans-Saharan passerine migrants. We subsequently Keywords: Stopover, Barrier crossing, Small islands, Fuel used arrival fuel loads coupled with potential flight range load, Conservation value estimates to assess the percentage of birds that are forced to perform an obligatory stopover after crossing the Med- iterranean Sea due to fuel depletion. Average arrival fuel loads were among the lowest ever recorded in the Mediter- 1 Introduction ranean region and minimum body mass values recorded for several species were lower than any other individual Every year billions of birds, of thousands of species, cover value reported. The percentage of birds that needed to enormous distances between their breeding and winter- replenish their energy stores before resuming their north- ing grounds. Those seasonal movements regularly involve ward migration journey varied from 0% to 50% depending the crossing of vast ecological barriers such as deserts, on the species and locality studied. Based on conservative mountain ranges and large water bodies. In the western Palaearctic migration system, most trans-Saharan passer- ine migrants have to cross the Sahara Desert and the Medi- terranean Sea. In the central and eastern flyway, the desert *Corresponding author: Christos Barboutis, Department of Biologi- and the sea can be considered as one ecological barrier as cal Applications and Technology, University of Ioannina, Ioannina, there are hardly any possibilities to refuel during cross- GR-45110, Greece, Email: cbarboutis@ornithologiki.gr ing [1]. Thus, prior to the barrier crossing, birds should be Christos Barboutis, Elisabeth Navarrete, Antikythira Bird Observato- ry, Hellenic Ornithological Society/BirdLife Greece, Themistokleous energetically prepared for this demanding task [2-5]. 80, Athens, GR-10681, Greece Migration is indeed the most energy-demanding task Georgios Karris, Lab of Environmental Physics, Energy and Environ- in a bird’s life cycle. When facing the Sahara Desert, a mental Biology, Department of Environment, Faculty of Environment, bird can cross it by intermittent flight, with stopovers to Ionian University, Panagoula, GR-29100, Zakynthos, Greece rest and refuel, whereas the Mediterranean Sea must be Stavros Xirouchakis, Natural History Museum of Crete, University of Crete, University Campus (Knossos), GR-71409 Heraklion, Crete, crossed in non-stop continued flight [6, 7]. Small and large Greece islands scattered in the Mediterranean Sea are often the Thord Fransson, Department of Environmental Research and Moni- first available land that migratory birds encounter after toring, Swedish Museum of Natural History, SE-104 05, Stockholm, crossing the Sea and the desert during their northward Sweden spring migration. Passerines arriving with depleted fuel Anastasios Bounas, Department of Biological Applications and Tech- reserves after crossing this large ecological barrier have nology, University of Ioannina, Ioannina, GR-45110, Greece Open Access. © 2021 Barboutis et al., published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 License. Fuel loads after crossing the Mediterranean   15 been reported in central and eastern areas of the Mediter- 2 Methods  ranean [8, 9]. A varying percentage of birds and species have enough energy reserves to resume their northward 2.1 Ethical approval migration once reaching the Thyrrenian islands in the central Mediterranean [10], whereas cases of birds with no This study was carried out in accordance with the Euro- residual fat reserves or even dying from depletion are not pean Convention for the Protection of Vertebrate Animals uncommon [11]. Arrival energy reserves and environmen- Used for Experimental and Other Scientific Purposes of tal conditions at stopover sites could lead to increased the Council of Europe (http://conventions.coe.int/Treaty/ stopover duration thus delay departure from sites [12, 13] EN/Treaties/Html/123.htm.). Ringing permits for each and could even influence the breeding phenology and location were issued annually by the Hellenic Ministry of performance of birds [14]. Nevertheless, the importance of Environment and Energy. stopover sites such as islands just after the barrier cross- ing is not only limited to refuelling purposes as birds often need to rest or sleep after endurance flights [15, 16], settle 2.2 Sampling area and data collection until more favourable meteorological conditions occurs, or even gather information and/or socially interact with Data was collected at three small Greek islands, situated conspecifics to evaluate the progress of the migration in the Libyan, the Aegean and the Ionian Sea. From south journey [17]. Therefore, stopover site availability after to north these were, Gavdos (34°50′ N, 24°5′ E) lying in the barrier crossing and habitat suitability for fuelling are of Libyan Sea, 40 km south of the island of Crete, Antikythira particular importance for a successful migration. (35° 51′ N, 23° 18′ E) between the Aegean and the Ionian According to optimal migration models [18], migrat- Sea, 40 km south of the island of Kythera and the Stro- ing birds should try to minimise either energy investment fades islands (37° 15’ N, 21° 00’ E) in the Ionian Sea, 50 or duration of migration (i.e. time-minimizing scenario). It km south of the island of Zakynthos (Fig. 1).  Birds were is therefore expected that birds arriving with high energy captured using 16x16mm mesh, nylon, mist nets. Mist reserves will resume their journey as soon as possible netting took place from dawn and thereafter for at least while birds with low residual energy reserves have to eight hours, except for days with adverse weather condi- restore them and remain at a stopover site. At this inter- tions. The total length of mist nets used were 150m, 90m play between migratory decisions, insular stopover sites and 60m for Antikythira, Strofades and Gavdos respec- located after ecological barriers should be extremely tively. Mist netting took place for a total of 76 days between important especially under the prospect of climate mid-April and mid-May of 2011-2013 at Gavdos, for a total change; studies employing future projections have shown of 736 days between the end of March/May of 2007-2019 that responses of European birds include poleward shifts at Antikythira and for a total of 44 days between end in their breeding and wintering distribution and such pre- of April and beginning of May in 2009 -2010, 2012 -2015 dicted changes will increase migration distances for some and 2018 at Strofades islands (Table S1). Mist nets were species rendering them susceptible to increased mortality checked for trapped birds every hour. Trapped birds in all risks [19]. sites were aged according to Svensson [20] and weighed Here, we aim to bring the significance of small islands to the nearest 0.1 g. Maximum-chord wing length [20] was in the Mediterranean into perspective and highlight their recorded to the nearest 0.5mm as a measure of body size. conservation value for migratory birds. To this aim, we use Visible subcutaneous fat was classified in 9 score ordinal empirical data coupled with avian flight models to calcu- scale (fat score) according to Kaiser [21] and bird’s pecto- late the proportion of birds from different species that ral muscle mass was visually classified in 4 score ordinal are not able to continue their migration (must perform scale (muscle score), based on its shape [22].  We consid- an obligatory stopover) at three insular stopover sites in ered data from species that are known to cross the Med- the eastern Mediterranean. Then, we use current data iterranean Sea and the Sahara Desert before arriving in on breeding population sizes and calculated the number each area in the following analyses.   of birds that migrate through the region and therefore provide a quantitative estimate of birds that could poten- tially experience future changes to their migratory jour- neys. 16   Barboutis et al. 2.3 Estimating body mass without fuel and 2.4 Estimating potential flight range arrival fuel loads Assuming that flying birds lose mass at a constant rate of We estimated body mass without fuel (m ), i.e. the body 1% per hour of flight [24, 25], potential flight ranges (Y; mass of a bird with both a fat score and a muscle score of hereafter flight range) were estimated according to the 0, according to the structural mass concept [23]. Thus, it flight range equation developed by Delingat et al. [26]:  should be noted that this is the most conservative estima- tion as it reflects a bird’s mass with neither fat nor protein Y = 100 × U × ln(1 + f ) (3) to use as fuel. We applied a regression function of the m0 (mass of all birds with both a fat score and a muscle score where U is airspeed. Regarding U, the species-specific of 0) on their respective maximum wing chord (hereafter values reported in Bruderer and Boldt [27] were used. wing length): When the species-specific value was not available the equivalent value of a closely similar species was used. m = b + b × wing length (1) Specifically for the Wood warbler (Phylloscopus sibilatrix), 0 0 1 the Collared flycatcher (Ficedula albicollis), the Sedge where b is the intercept and b a constant from the regres- warbler (Acrocephalus schoenobaenus) and the Woodchat 0 1 sion. This regression was applied separately to all species shrike (Lanius senator), we used the airspeeds measured trapped at our study sites with a sample size larger than for the Willow warbler (Phylloscopus trochilus), the Pied 10. In order to estimate the fuel load (f; bird’s body compo- flycatcher (Ficedula hypoleuca, the Reed warbler (Acro- nents which can be used as fuel), the following equation cephalus scirpaceus) and the Red-backed shrike (Lanius was used:  collurio) respectively. For two species with no availa- ble airspeeds, the Golden oriole (Oriolus oriolus) and  f = (m - m ) / m (2) the Common nightingale (Luscinia megarhynchos), the 0 0 where m, is the body mass at capture and m is the overall mean value for passerines, 10 m/s, was used [27, birds’ body mass without any fuel.  28]. Flight range was estimated under still air conditions Figure 1. Map of our study area in eastern Mediterranean. Dots and zoomed insets show our study sites (Strofades, Antikythira, Gavdos), whereas the nearest to them larger islands are also noted (Zakynthos, Kythira and Crete respectively). Fuel loads after crossing the Mediterranean   17 as wind direction is highly varying in the wider study area and the average tailwind component during the peak of the spring migration period is close to zero [29]. To esti- mate the percentage of birds that had the necessary fuel to reach the next larger island, where more refuelling oppor- tunities are expected to exist (Fig. 1), the flight range equa- tion was calculated for every individual bird trapped and we examined if they could continue their flight for 40 km in the case of birds trapped in Gavdos and in Antikythira and 50 Km in the case of birds trapped in Strofades. Due to the uneven sample size between the three study sites, the overall percentage of birds per species that could not continue their migration was estimated as the average of the estimated percentage of all sites.  2.5 Species and number of birds using the migration corridor In order to provide a quantitative estimate of the number of birds belonging to our study species that use Greek islands and coastal sites as a migration corridor during spring, we used the most recent breeding bird population estimates included in the European Red List of Birds [30], following the approach of Hahn et al. [31]. More specifi- cally, we used all ring recovery data for our study species that included birds ringed in Greece and recovered else- where during the spring migration and vice versa (data provided by the Hellenic Bird Ringing Center). Then, for each species we drew a minimum convex polygon around the recoveries and used the breeding population esti- mates for each country that was included in the polygon as an estimate of the number of birds that would migrate through Greece (Fig. S1). We did not consider non-breed- ers that could account for 15% within a population [31, 32] thus keeping our estimates rather conservative. Furthermore, we assessed the number of species of trans-Saharan migratory birds belonging to passerines and near passerines (i.e. belonging to the orders Apodi- formes, Caprimulgiformes, Cuculiformes, Coraciiformes, Piciformes, Columbiformes and Bucerotiformes) arriving to Greek islands and coastal areas in south Greece. For estimating the number of species, we used eBird’s (www. ebird.org) bar chart tool [33] to retrieve records of species at the Peloponnese, the island of Crete, South Aegean and the Ionian islands, from March to May. Additionally, the daily ornithological species list of the Antikythira Bird Observatory held since 2008 on daily bases during spring migration period was used. Only species that winter south Figure 2. Percentage of birds per species that must perform an obligatory stopover in: a) Strofades, b) Antikythira and c) Gavdos. of the desert of the Sahara and are expected to reach Orange bars depict standard error. Greece after having crossed the ecological barriers of the 18   Barboutis et al. Sahara Desert and the Mediterranean Sea were included (Lanius senator) at Gavdos (31.7± 16.4 %). Potential flight in this assessment. range estimates were calculated for 38,253 birds arriving at our three study sites. The percentage of birds that could not resume their migratory flight to the nearest more suit- able fuelling localities, varied from 50.6% in the case of 3 Results  the Collared flycatcher (Ficedula albicollis) arriving at Sto- fades islands, to 0% (all individuals could continue their Mean arrival fuel loads were estimated for 18 trans-Sa- migration) in the case of the Great reed warblers (Acro- haran migratory passerine species (Table 1; Table S2; cephalus arundinaceus) and the Woodchat shrike arriving regressions calculated for species that had more than 10 to Gavdos (Fig. 2; Table S3). Across all islands, a mean of birds with recorded wing length, body mass and fat and more than 14% of the birds belonging to our study species muscle score of 0). Fuel load of birds arriving to our study were not able to resume their migration. sites varied from 23.3% of their structural mass in the A conservative estimate of almost 184.9 million Icterine warbler (Hippolais icterina), to 8.7% in the case birds belonging to our study species migrate through of Sand martin (Riparia riparia) across the three small Greece during spring, with the Willow warbler (Phyllo- islands (Table 1). The lowest average arrival fuel load was scopus trochilus), the Barn swallow (Hirundo rustica), recorded for the Wood warbler (Phylloscopus sibilatrix) at the Common whitethroat (Sylvia communis) and the Strofades islands (2% ± 7.9 % of structural mass) and the Wood warbler being the most abundant ones, altogether largest fuel load was recorded for the Woodchat shrike accounting for almost 60% of all birds (Table S4). Of those Table 1. Arrival fuel load (% of structural mass) per species for all birds and for each study site and minimum body mass recorded per species. Antikythira Gavdos Strofades Fuel load Min body Fuel load Fuel load Fuel load Species n n n n (% ± SD) mass (% ± SD) (% ± SD) (% ± SD) Riparia riparia 8.3 ± 8.4 1592 8.1 7.5 ±8.0 1147 12.0 ± 9.4 240 8.7 ± 9.5 205 Oriolus oriolus 11.2± 10.8 1624 33.6 12.0 ± 11.0 1390 11.9 ± 11.4 87 2.8 ± 8.7 147 Delichon urbicum 11.6± 9.9 703 9.3 9.3 ± 9.9 386 17.2 ± 9.7 224 7.9 ± 10.4 93 Phylloscopus 12.3± 12.7 2768 5.5 13.2 ± 13.1 2466 15.4 ± 12.6 68 2.0 ± 7.9 234 sibilatrix Acrocephalus 14.3± 12.4 901 18.2 16.0 ± 12.9 692 19.8 ± 11.0 28 6.9 ± 10.8 181 arundinaceus Sylvia borin 14.9± 12.7 9030 9.5 17.0 ± 13.6 7116 13.1 ± 11.3 403 5.6 ± 8.8 1511 Ficedula 15.0± 12.5 3574 7.6 15.6 ± 12.8 3208 20.3 ± 10.7 80 6.4 ± 9.2 286 hypoleuca Acrocephalus 15.3± 32.5 2314 6.3 15.9 ± 35.7 2000 15.5 ± 13.6 78 10.2 ± 10.9 236 schoenobaenus Phoenicurus 15.6± 13.9 1304 9.0 16.2 ± 14.0 1131 18.0 ± 18.7 24 10.9 ± 11.8 149 phoenicurus Muscicapa striata 15.6± 12.4 3356 8.8 16.9 ± 12.6 2659 15.7 ± 12.5 230 8.2 ± 11.0 467 Hirundo rustica 16.0± 13.9 813 11.3 15.7± 13.6 598 18.0 ± 15.0 151 13.8 ± 14.3 64 Saxicola rubetra 16.5± 13.9 1379 9.5 15.9 ± 13.5 751 23.9 ± 15.6 293 11.2 ± 13.5 335 Ficedula albicollis 18.1± 13.0 1385 7.1 18.7 ± 13.1 1262 23.7 ± 12.5 41 6.7 ± 12.4 82 Phylloscopus 19.7± 17.2 1067 5.4 19.8 ± 17.1 986 21.7 ± 14.8 18 17.7± 18.6 63 trochilus Lanius senator 20.8± 11.9 1060 21.2 21.4 ± 11.8 829 31.9 ± 16.4 56 14.5 ± 11.0 175 Luscinia 21.5± 13.5 1328 11.3 21.9 ± 13.6 1261 20.3 ± 15.3 17 12.6 ± 10.7 50 megarhynchos Sylvia communis 22.5± 14.6 2515 9.3 25.1 ± 15.4 1730 24.6 ± 15.4 135 14.9 ± 12.5 650 Hippolais icterina 23.3± 14.3 1570 8.9 24.7 ± 14.8 1327 24.8 ± 14.5 67 12.3 ± 10.4 176 Fuel loads after crossing the Mediterranean   19 species the Willow warbler, Barn swallow and the Wood schoenobaenus, Muscicapa striata, Phoenicurus phoenic- warbler were also estimated to be among the species with urus, Riparia riparia, Saxicola rubetra, Sylvia borin) were the largest number of birds that need to undertake an lower than any other minimum individual value reported obligatory stopover at an island or a coastal locality when [35, 37-40]. These results complement previous reports of reaching Greece after the Mediterranean crossing (Fig. birds with depleted fuel reserves reaching insular Greece 3). Overall, an average of 30 million birds are estimated during the northward migration [9, 41, 42]. to perform an obligatory stopover. Additionally, it was The low arriving fuel loads at our study sites are prob- assessed that 48 more passerines and close to passerines ably a result of the vast length of the combined ecological (66 species in total) reach Greece every spring after cross- barrier of the Sahara Desert and Mediterranean Sea that ing the desert and the sea (Table S5).   can reach or even exceed 2800 km [29], with hardly any possibilities to refuel. Surely refueling opportunities exist in North Africa [37] and that is reflected in the high per- centage of individuals of some species that do not arrive 4 Discussion depleted (e.g Lanius senator). However, there is evidence that species adapted to mesophilic and moist habitats Birds arriving at Greek islands have either just crossed the show difficulties in successfully refuelling during migra- Sahara Desert and the Mediterranean Sea thus experience tion in dry regions [43] like those of North Africa. There- relatively low average fuel loads or stop in the islands in fore, the low arrival fuel loads we recorded in this study good condition after refueling in North Africa. Fuel loads indicate that there are probably not any widespread refu- of species caught in our study sites such as the Spotted elling possibilities close to the African coast of the Medi- Flycatcher (Muscicapa striata), the Garden Warbler (Sylvia terranean Sea before reaching the Greek islands. borin), and the Common Nightingale (Luscinia megarhy- Whether the fuel depleted birds arriving at Greek nchos) are among the lowest values reported from other islands during spring are “fall-outs”, i.e. not capable of Mediterranean sites [34-37]. Additionally, minimum body further migration [44], cannot be fully assessed based on mass values recorded for several species (Acrocephalus this study. Our data suggest that some individuals perform Figure 3. Overall percentage of birds that have to undertake a stopover in Greek islands and coastal sites and the respective cumulative estimate per species in millions of individuals. 20   Barboutis et al. an obligatory stopover being unable to continue their compared to fat [46] and the low physiological stated of migration, however, other birds seem to actively decide birds arriving to our study sites, a good proportion of birds to land depending on their fuel loads and species-spe- that have been estimated to just being able to overpass cific habitat requirements [40]. Future assessment of the our study sites might not actually not make it. Our calcu- abundance of birds in the larger islands next to our study lations therefore, represent the minimum number of birds sites could shed some light on the fall-out hypothesis in whereas the true number could in fact be much higher. the eastern Mediterranean region; if lean birds are more At least 48 more species of trans-Saharan migratory pas- abundant in the “low-quality” small islands (that inher- serines and non-passerines are also migrating through ently offer fewer refuelling opportunities) it would seem Greece every spring, and probably some individuals also that birds would have no option but land at the first avail- reach the stopover sites energy depleted. Therefore, the able site after sea crossing [37]. Regarding the fate of the amount of birds that need to undertake an obligatory stop- extremely lean birds we encountered, some preliminary over at insular or coastal sites in Greece could reach up to data indicate that at least some extremely lean birds of several hundreds of millions, making these stopover sites some species could manage to recover during their stop- of outmost importance for the survival of migratory birds. over and resume their migration; having depleted a large Although replenishing of energy reserves is consid- amount of protein, mainly from the breast muscle [41] ered the main aim of stopover events, birds do not stop- and the digestive organs [45] along with the fat reserves over at insular sites in the Mediterranean only to refuel which are the main fuel [46], they are actively seeking and as shown by the large species variety of migrating birds consuming nectar [47], an energy source readily obtained recorded, of which many birds have enough fuel reserves during spring time on north Mediterranean and easy to to continue their norward journey [15]. Many birds, the assimilate after their long-distance flight [48]. Addition- numbers of which cannot yet be estimated sufficiently, ally, evidence from Mauritania indicates that individual need the stopover sites for non-fuelling purposes and birds with fuel loads much below average are capable of will continue migration the following night. After long recovering and refueling even in dire environments [39]. endurance flights over the Mediterranean Sea, birds seem On the other hand, extended incidents of birds dying from to need to recover from sleep deprivation [50-52], whereas depletion at our study sites are not unusual and have others might be forced to use stopover sites to avoid been observed during the course of this study with mor- adverse weather conditions which are not rare during tality rates being highest in Strofades islands. That could spring in the Mediterranean region [53]. Furthermore, possibly result due to Strofades geographical position local environmental conditions at stopover sites might be coupled with the general northern – northeastern spring necessary for some species to evaluate and predict condi- migration direction, so birds have to undertake a longer tion at final destinations further north [54]. barrier crossing and therefore more often reach the island The importance of Mediterranean islands is further depleted. brought into perspective if we consider the estimated The pooled data from our three study sites indicate obligatory stopover of hundreds of millions of birds under that the percentage of birds that are forced to undergo an future changes in climate. Besides, migration is an adap- obligatory stopover before leaving the islands varied from tive strategy for organisms to exploit the seasonality in 25.5% in the case of the Golden Orioles (Oriolus oriolus) resource availability. There is so far plenty of evidence down to 3.3% in the case of Woodchat Shrike. Strikingly, for the modification of migratory routes as a result of in the case of the Collared flycatcher arriving to the island climate change in several avian species, including longer of Strofades, up to half of the individuals must refuel migratory journeys [19, 55, 56]. Longer flight ranges need before resuming their migration. Based on our estima- increased energy demands which subsequently lead to tions approximately 30 million of birds belonging to the more stopovers needed and ultimately can lead to a mis- 18 study species perform an obligatory stopover at insular match between time arrival and breeding [57]. Specifically or coastal sites in Greece every spring. 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Journal

Animal Migration – de Gruyter

Published: Jan 1, 2022

Keywords: Stopover; Barrier crossing; Small islands; Fuel load; Conservation value

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