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Migration patterns of the Mediterranean ShagPhalacrocorax aristotelis desmarestii (Aves:Pelecaniformes) within the northern Adriatic SeaS. Sponza a , M. Cosolo a & J. Kralj ba Department of Life Sciences, University of Trieste, Trieste, Italyb Institute of Ornithology, Zagreb, CroatiaVersion of record first published: 23 Apr 2013.

To cite this article: S. Sponza , M. Cosolo & J. Kralj (2013): Migration patterns of the Mediterranean Shag Phalacrocoraxaristotelis desmarestii (Aves: Pelecaniformes) within the northern Adriatic Sea, Italian Journal of Zoology,DOI:10.1080/11250003.2013.775365

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Italian Journal of Zoology, 2013, 1–12http://dx.doi.org/10.1080/11250003.2013.775365

Migration patterns of the Mediterranean Shag Phalacrocoraxaristotelis desmarestii (Aves: Pelecaniformes) within thenorthern Adriatic Sea

S. SPONZA1*, M. COSOLO1, & J. KRALJ2

1Department of Life Sciences, University of Trieste, Trieste, Italy and 2Institute of Ornithology, Zagreb, Croatia

(Received 21 September 2012; accepted 4 February 2013)

AbstractMovements of Mediterranean Shags (Phalacrocorax aristotelis desmarestii, Payraudeau 1826) between Croatian breedingcolonies and non-breeding areas such as the Gulf of Trieste increased consistently from the 1980s to become a migra-tory movement at the present time. In order to characterise the patterns of this migration and the behaviour of first-yearShags at their first migration, we analysed the recoveries of 812 birds that were colour-ringed at the most important Croatianbreeding colonies in the northern Adriatic. Within a period of seven years, 568 ring-readings of 234 individual Shags wereprocessed. Most sightings came from the Gulf of Trieste (43.0%) and the newly-discovered post-breeding area in VeniceLagoon (38.9%). Shags from the most distant colonies exploited mainly the Gulf of Trieste. The 48.3% of Shags sightedseveral times have been recorded in the same post-breeding area during subsequent years. This percentage increased to93.4%, if we considered just the birds observed during successive years. Variations in the timing of migration within thepost-breeding areas occurred and sustained the importance of the Slovenian coast during the return to breeding colonies.The ratio between first-year Shags and experienced Shags (immature and adults) was higher in Venice Lagoon and in gen-eral increased with the “novelty” of the site. A relevant portion of the Croatian breeding population moves to the northernAdriatic Sea after breeding. All the studied colonies concurred with this migration. We highlight a high fidelity to post-breed-ing sites, which reflects the quite sedentary “nature” of the species, and the role of first-year Shags in the discovery of newsites. We suggest that this migration is probably the later stage in a graded response to deterioration of the Shags’ feedinggrounds within the breeding area.

Keywords: Migration, Mediterranean Shag, Phalacrocorax aristotelis desmarestii, Adriatic Sea

Introduction

The European Shag (Phalacrocorax aristotelisLinnaeus, 1761) is a colonially breeding seabirdendemic to the rocky coasts of the northeast Europeand Mediterranean (Wanless & Harris 2004). In theformer area, the Atlantic subspecies Phalacrocoraxaristotelis aristotelis Linnaeus, 1761 is distributed fromIceland and northern Scandinavia to the IberianPeninsula (Nelson 2005). Iberian Shags were shownto be isolated from northern populations (Velando1997; Velando & Freire 1999). The species hasindeed always been considered as largely sedentary,although the immature may undergo post-breedingdispersive movements over short distances (DelHoyo et al. 1992). For example, extensive studies onringing and recovering have shown that no Icelandic

*Correspondence: S. Sponza, Department of Life Sciences, University of Trieste, via Giorgieri 10, 34127 Trieste, Italy. Tel: +39 040 558 8825. Fax: +39 0409828013. Email: sponza@units.it

Shags have been recovered elsewhere (Gardarsson1982; Petersen 1998), and no adults ringed inthe UK have been recovered in mainland Europe(Harris & Swann 2002). Furthermore, 95% of theShags were recorded within a radius of 8 km fromthe natal colony in eastern Britain (Aebischer 1995).

Historical recoveries of Shags ringed at coloniesin north Europe recorded median winter movementsthat were generally less than 100 km, and winterranges of different breeding populations were rela-tively isolated (Galbraith et al. 1986). Such studyalso showed marked differences between regions inthe dispersal patterns. In addition to interpopula-tion differences, age-related, annual and longer-termvariation also occurred within populations. Somepopulations, such as the western Scottish and north

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Irish Sea birds, were comparatively consistent intheir year-to-year dispersal patterns and there wereno apparent age-related differences. Others, partic-ularly the Forth/Farnes birds, showed marked age-related and annual variation. These interpopulationand annual differences could be determined by theavailability of sheltered feeding conditions, while pos-sible causes of long-term variations might includechanging weather patterns or competition betweenage groups (Galbraith et al. 1986). Conversely,north Norwegian Shags undertook the most exten-sive movements of any of the studied populations.Dispersal distances of over 500 km suggested thatthese populations might be migratory rather thandispersive. However, preliminary results from recentinvestigations suggest that the majority of the northNorwegian Shags equipped with miniaturised dataloggers (Geolocators) wintered north of the ArcticCircle (Daunt et al. 2010).

Despite the assumption that the North Seaprovided an effective barrier to Shag movements(Galbraith et al. 1986), the most recent genetic stud-ies, even if really detecting an isolation-by-distance,have shown that microsatellite variation provided noevidence that open sea formed a complete barrier toeffective dispersal (Barlow et al. 2011). According toUK ringing recoveries, even if adult Shags do notdisperse widely from the colony in the post-breedingseason (Harris & Swann 2002; Daunt et al. 2006),2% of the juveniles have been recovered in main-land Europe (Wanless & Harris 2004). Moreover,ring recoveries have demonstrated that juvenile Shagsperform long-distance movements, on the order ofseveral hundred kilometres, from their natal colonyprior to colony recruitment (Harris & Swann 2002;Alvarez 2009).

Although the movements of the Atlantic sub-species populations are well documented, very lit-tle is known about the possible movements ofthe Mediterranean subspecies Phalacrocorax aristotelisdesmarestii Payraudeau, 1826, which is endemic tothe Mediterranean and Black Seas (Nelson 2005).This subspecies is not thought to move outside itsrecognised breeding range (Wanless & Harris 2004).Birds ringed in Corsica have been recovered in north-western Italy; 77% of the recoveries over 100 kmfrom breeding colonies were juvenile birds (Brichettiet al. 1992).

In the Adriatic Sea, Shags breed in Croatia butmany of them spend the post-breeding period inthe Gulf of Trieste (Sponza et al. 2010; Cosoloet al. 2011). This behaviour was shown to bedriven by dietary requirements (Cosolo et al. 2011).These movements within the Adriatic Sea have notalways been a habitual pattern, since they increased

consistently from the 1980s (Utmar 1999) to becomea migratory movement at the present time (Sponzaet al. 2010), in the sense of a regular back-and-forth seasonal movement of a population betweentwo areas (Berthold 2001). Moreover, Shag move-ments and distribution during the post-breedingperiod have expanded westwards over the years, actu-ally including the Venice Lagoon (Fracasso et al.2000; Bon et al. 2005; Sighele et al. 2010). At least1300–1500 pairs of the Mediterranean Shag breed inthe north and central Adriatic Sea (IOO et al. 2013).The species breeds also in the southern Adriatic;however, colonies are smaller and less numerous.Furthermore, up to 4000 individuals of all age classeswere counted on the communal roosts far fromthe colonies in the north Adriatic during late sum-mer and autumn (Škornik et al. 2011). This meansthat the post-breeding migration actually involves themajority of the population breeding in the northernAdriatic.

In this paper we characterise the patterns ofsuch migration and the behaviour of first-year birds,immature birds and adults, on the basis of seven yearsof colour-ring sightings and recoveries.

Materials and methods

Breeding colonies

The study area covered the northern Adriatic Sea,namely the Istrian coast, the Quarner archipelagoand the northern part of the Zadar archipelago.Shags were colour-ringed at the most importantCroatian breeding colonies in the northern AdriaticSea (Figure 1).

The five colonies are composed of a totalof 14 islands. Three colonies are located offthe western coast of the Istria peninsula nearVrsar (45◦09′N, 13◦35′E), Rovinj (between 45◦03′–45◦04′N and 13◦37′–13◦38′E) and on islands ofthe Brijuni archipelago (between 44◦53′–44◦56′Nand 13◦42′–13◦47′E). Of these colonies, Vrsar iscertainly the smallest and least important. Theother two colonies are located on Oruda Island(facing Lošinj Island) (44◦33′N, 14◦34′E) and onSilbanski Grebeni islands (between 44◦19′–44◦20′Nand 14◦41′–14◦43′E) (Figure 1).

Ringing activity

A total of 812 Shags were ringed between 2005 and2011 (seven years) (Table I). Of these, five birds wereringed at Vrsar colony (0.6%), 64 birds at Rovinjcolony (7.9%), 391 birds at Brijuni archipelago(48.2%), 120 birds at Oruda Island (14.8%) and

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Shag migration within the Adriatic Sea 3

Figure 1. Map of the study area (modified from http://it.bing.com/maps/, © Microsoft Corporation 2012). Shown on the map are: thefive breeding colonies (Vrsar, Rovinj, Brijuni archipelago, Oruda, Silbanski grebeni), the three main post-breeding areas (Gulf of Trieste,Venice Lagoon and Slovenian coast) and some locations (Pesaro, Ancona and Pelješac) which are interesting with respect to date of sighting,direction taken and distances covered.

Table I. Numbers of Mediterranean Shags ringed in the five Croatian breeding colonies between 2005 and 2011.

Colonies 2005 2006 2007 2008 2009 2010 2011

chicks adults chicks adults chicks adults chicks adults chicks adults chicks adults chicks adults

Vrsar 5Rovinj 35 2 17 10Brijuni 7 14 34 3 14 65 1 119 14 51 12 42 15Oruda 22 3 18 19 16 2 38 2Silbanski grebeni 132 10 37 1 49 3

Total 29 17 52 22 146 10 65 1 196 17 133 27 80 17

232 birds at Silbanski Grebeni islands (28.6%).701 Shags (86.3%) were ringed as chicks at the nest,while 111 (13.7%) were ringed as adults. Shags placetheir nests under dense bushes (mostly Pistacia lentis-cus Linnaeus, 1753, and Phillyrea latifolia Linnaeus,1753) close to the sea. All captures were made bywalking along the shore and quietly surrounding thebushes used for nesting. Chicks were captured gen-tly by hand on the nests, ringed and immediatelyreleased back to the nests. Adults were captured byhand on the nest or by mist-nets located near thebush entrances and released on the water near their

nests (10 m). Adults were observed to return to theirbreeding sites within 20 min.

Birds were individually marked with both metalrings and plastic colour rings, one on each tarsus.Shags were aged and handled by ringers with ring-ing permits issued by the Institute of Ornithology inZagreb (Croatia). The colour rings were large andconspicuous; the colour used was orange with a blackalphanumeric code. The code was composed of asingle letter followed by a two-digit number.

Shags typically do not breed until aged threeyears (Potts et al. 1980). Moreover, the breeding

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season in the Adriatic Sea is prolonged (from lateNovember to May). The first chick was ringed on3 February, although the majority were ringed dur-ing April (83.0%). Most of the adults were ringed inMarch (52.6%).

All sightings of colour-rings were entered into adatabase upon receipt. For each sighting, the date,the observer and the location were logged, whiledirect linear distance (km) from the colony wascalculated for each location. As Shags often movealong the coast, this value indicates the extent ofthe movement, not the length of the actual routepassed by an individual bird. Regarding the most dis-tant locations, the rough distance travelled along thecoast was calculated using the measuring distancetool of the Google Earth software to estimate thelength of the possible route passed by an individualbird.

In order to verify the effect of age in the timingof migration and direct linear distance covered, weseparately analysed the following groups: first-yearbirds at their first migration, immature birds (fromthe second to the third year of life) and adults (fromthe fourth year of life). Such distinctions were madeaccording to the date of the sighting. When compar-ing the different colonies, we excluded the colonyof Vrsar, due to the low number of Shags ringedthere.

As discussed by Camphuysen et al. (2011), colour-ringing programmes have a clear advantage giventhe multiple sightings of individual birds (withoutthe need to re-trap) over a large number of yearsand generally provide large sample sizes (number ofindividual birds monitored). On the other hand, adisadvantage of this method is caused by the fact thatthe colour-ringing data could be influenced by spatialand temporal patterns in observer efforts. We believethat the coastal and strictly marine ecology, theirgregariousness also outside the breeding period, thehabit of forming common roosts and the easy recog-nisability of Shags as well as a widespread interest forthe species and for colour-ring reading by ornitholo-gists, bird-watchers and amateurs reduced the effectof this limit. Moreover, the project over the years wasadvertised on the “CR-Birding” website, at severalornithological meetings and through the NationalRinging Scheme. Up to 29 observers contributed tothe data collection from different areas of the Adriaticcoast.

Contingency tables tested by the chi-square test(χ2) were used to compare the numerical frequen-cies. Other statistical differences were assessed withthe Kruskal-Wallis test. The significance thresholdwas set at P < 0.05 and the analysis was performedusing SPSS 13.0 and STATISTICA 7.1 software.

Results

Until the end of 2011, 234 Shags (28.8%) hadbeen re-sighted on at least one occasion. The major-ity (212 birds, 90.6%) were ringed as chicks, while22 birds (9.4%) as adults. Generally, 150 birds werereported at least once during their first year, whichled to 216 sightings.

Moreover, 214 Shags (91.4%) were reported alive,17 individuals (7.3%) were recovered dead, whilethree birds (1.3%) were observed first alive and sub-sequently found dead. Eight out of the 20 recoveries(40.0%) belonged to birds drowned in fishing nets orfish traps.

A total of 568 ring-readings from 45 locations werereceived and processed (Table II). All sightings camefrom coastal areas.

Origin of the north Adriatic population in thepost-breeding period

Most sightings (81.9%) came from the Gulf ofTrieste (43.0%) and from Venice Lagoon (38.9%).These localities indicate that Shags could regularlytravel up to 300 km along the coast. The Sloveniancoast follows with 13.9% of sightings. All other loca-tions amounted to 4.2%. Of these, the three sightingsfrom Pesaro (central Italy, cardinal direction: W–SW; 43◦55′N, 12◦54′E, coastal distance ca. 540 km)and Ancona (central Italy, SW; 43◦31′N, 13◦37′E,ca. 580 km), together with the sighting at Pelješac(Croatia, SE; 42◦58′N, 17◦07′E, ca. 370 km) showedatypical long-distance movements, i.e. direct lineardistance >100 km (Figure 1).

The number of Shags sighted, split by thecolony of origin, did not vary significantly betweenthe post-breeding areas (χ2 = 14.62; df = 9;P > 0.10; Figure 2). At Venice Lagoon, we recordeda higher percentage of Shags from Rovinj andBrijuni colonies, while Shags from Silbanski Grebenicolonies showed a slight preference towards the Gulfof Trieste (Figure 2).

In this respect, when we compared the num-ber of sightings from the main post-breeding areas,partitioned by the colony of origin, the prefer-ence of Shags from Silbanski Grebeni towards theGulf of Trieste contributed significantly to thedifference (χ2 = 35.62; df = 6; P < 0.0001;Silbanski Grebeni contribution/total chi-square con-tribution = 22.08/35.62).

Links between the post-breeding areas

The same colour-ringed birds were never observedin both Venice Lagoon and in the Gulf of Trieste,

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Shag migration within the Adriatic Sea 5

Table II. Numbers of sightings and number of Shags sighted for each colony. Data have been categorised according to both (A) the year ofringing and (B) the year of sighting.

Year ofringing

Brijuni Oruda Silbanski grebeni Rovinj Vrsar

n.sightings

n. Shagssighted

n.sightings

n. Shagssighted

n.sightings

n. Shagssighted

n.sightings

n. Shagssighted

n.sightings

n. Shagssighted

(A)2005 28 7 30 72006 36 8 12 72007 17 2 110 422008 55 222009 125 50 9 6 39 14 2 22010 27 18 15 7 14 8 9 72011 25 17 15 10

Total 313 124 72 31 133 56 48 21 2 2

(B)2005 5 4 7 52006 15 7 14 92007 8 6 5 3 30 262008 32 15 4 3 21 142009 80 47 5 2 20 13 19 12 2 22010 82 48 12 8 35 21 25 132011 91 49 25 13 27 14 4 3

60

50

40

30

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10

70

0Gulf of Trieste Slovenia Venice Others

Brijuni Oruda Rovinj Silbanski grebeni

% o

f Sh

ags

sigh

ted

Figure 2. Percentage of the number of Shags sighted in the post-breeding areas per colony.

neither in the same nor in different years. Irrespectiveof the routes taken by individual Shags, on the basisof sightings and recoveries processed, currently thereare no links between the two most important post-breeding areas in the north Adriatic Sea.

Just five Shags were recorded at different areaswithin the same year: four birds were observedinitially in the Gulf of Trieste (location: Isonzoriver mouth; 45◦49′N, 13◦31′E) and then alongthe Slovenian coast (location: Secovlje Salina;45◦28′N, 13◦35′E) and one bird was recorded ini-tially in Venice Lagoon (location: Chioggia; 45◦12′N,

12◦15′E) and then in Slovenia (location: SecovljeSalina; 45◦29′N, 13◦35′E).

Fidelity to post-breeding areas

As regards the Shags sighted several times (118 outof 234 birds), 48.3% were recorded in the samepost-breeding area during subsequent years. If weconsider just the birds observed during successiveyears (excluding those birds observed several timesin the same year), the percentage increased to 93.4%.The comparison of the number of birds sighted in the

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same area during successive years, split by the colonyof origin, with the total number of Shags sightedfor each colony showed that all the colonies con-curred equally in fidelity to the post-breeding areas(χ2 = 1.71; df = 3; P > 0.60).

Timing of migration

The timing of migration was similar among thedifferent colonies (number of Shags sighted permonth, period May–December: χ2 = 16.43; df = 21;P > 0.70), while the seasonal use of the mainpost-breeding areas differed considerably (numberof Shags sighted per month in different post-breeding areas, period May–December: χ2 = 93.93,df = 14, P < 0.0001; Figure 3). The main con-tributions to the difference were: the high num-ber of Shags sighted during September along theSlovenian coast (September contribution/total con-tribution = 29.93/93.93) and during October inVenice Lagoon (October contribution/total contri-bution = 20.48/93.93), and the low number of Shagssighted in Slovenia during July (July contribution/

total contribution = 11.15/93.93) and duringAugust in Venice Lagoon (August contribution/totalcontribution = 16.19/93.93) (Figure 3).

Age-related movements

When we compared Shags from different colonies,both immature birds and adults showed a simi-lar timing of migration (number of Shags sighted,period May–December: immature birds, χ2 = 24.01,df = 21, P > 0.25; adults, χ2 = 12.93, df = 21,P > 0.90). First-year birds behaved similarly, with

an exception in June when we found a higher rate ofjuveniles from Silbanski Grebeni leaving the colony(number of Shags sighted: χ2 = 32.95, df = 18,P < 0.05; Silbanski Grebeni: June contribution/totalcontribution = 15.21/32.95).

A significant difference was recorded by comparingthe three age-groups, i.e. first-year birds, imma-ture birds and adults (number of Shags sighted:χ2 = 27.38, df = 14, P < 0.05). In fact, bothimmature birds and adults begin to leave thecolonies during May or even earlier, whereas first-year Shags depart in June (May contribution/totalcontribution = 19.14/27.38; Figure 4). The contri-bution of immature birds was particularly high inMay (May contribution of immature/total contribu-tion = 11.64/27.38).

We found no differences in the direct lin-ear distances covered by first-year Shags, imma-ture birds and adults (considering only indepen-dent data: Kruskal-Wallis test: H2,175 = 5.05,P > 0.05) while the seasonal use of the threemost important post-breeding areas by first-yearShags, immature birds and adults differed signif-icantly (number of Shags sighted: first-year birds,period June–December, χ2 = 52.52; df = 12;P < 0.0001; immature birds, period May–December,χ2 = 38.52, df = 14, P < 0.001; adults, periodMay–December, χ2 = 28.62, df = 14, P < 0.05;Figure 4). These differences were particularly evidentfor first-year birds during September (Septembercontribution/total contribution = 22.96/52.52), dueto the increased presence along the Sloveniancoast (Figure 4A). As regards immature birds(Figure 4B), the main contribution to the totalchi-square was recorded during October (October

60

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40

30

20

10

70

0Jan Feb Mar

Gulf of Trieste Slovenia Venice Lagoon

N. S

hags

sig

hted

Apr May Jun Jul Ago Sep Oct Nov Dec

Figure 3. The proportion of all Shags colour-ringed in Croatia seen each month in the main post-breeding areas. Lines drawn in order tovisualize trends only.

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Shag migration within the Adriatic Sea 7

A) First-year Shags

B) Immature

C) Adults

30

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N. S

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hags

sig

hted

Jul Ago Sep Oct Nov Dec

Jan Feb Mar Apr May Jun Jul Ago Sep Oct Nov Dec

Jan Feb Mar Apr May Jun Jul Ago Sep Oct Nov Dec

Gulf of Trieste Slovenia Venice Lagoon

Figure 4. Seasonal use of the main post-breeding areas (Gulf of Trieste, Venice Lagoon, Slovenian coast) by (A) first-year, (B) immatureand (C) adult birds expressed as numbers of individuals sighted. Lines drawn in order to visualize trends only.

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contribution/total contribution = 14.28/38.52), dueto the higher number of Shags in Venice Lagoon withrespect to the Gulf of Trieste. As regards the adults(Figure 4C), the main contribution to the total chi-square was recorded during September (Septembercontribution/total contribution = 9.52/28.62), dueto the increased presence along the Sloveniancoast.

Age and migration patterns

Given the lack of differences in the use of the post-breeding areas between immature birds and adults(number of Shags sighted: χ2 = 0.77, df = 3,P > 0.85), we created the category “experiencedShags”, which included all sightings after the firstcalendar year. In order to highlight the behaviourof juvenile Shags at their first migration, we anal-ysed just the first sighting of each bird to verifywhether the destinations and the behaviour of first-year birds differed from those of experienced Shags.The abundance of first-year and experienced Shagsdiffered significantly between the three main post-breeding areas (χ2 = 9.43; df = 2; P < 0.01). Themain contribution to the total chi-square was dueto the low presence of experienced Shags in VeniceLagoon, compared to the Gulf of Trieste and theSlovenian coast (Venice Lagoon: experienced Shagscontribution/total contribution = 3.63/9.43).

Accordingly, we display in Figure 5 the ratiobetween first-year birds and experienced Shagsrecorded at the Croatian breeding area, at each of thepost-breeding areas (Slovenian coast, Gulf of Trieste,Venice Lagoon) and at the “new sites”. This lattercategory takes into account new locations that are

interesting if we consider the date, the direction andthe distances covered (Figure 1 and Table III).

Discussion

There are different methodological approaches tostudy bird migration. Each method has advantages aswell as disadvantages and the results are complemen-tary rather than standalone descriptions of migratorypathways and dispersal patterns (Camphuysen et al.2011). We recognise the possible limits of the colour-rings method (Galbraith et al. 1986; Camphuysenet al. 2011), particularly for possible bias result-ing from ring-reading efforts, but we feel confidentof the description of the patterns of this migra-tion, given the perspective used and the ecology andbehaviour of the Mediterranean Shag (see Materialsand methods).

The effective conservation of seabird populationsneeds the ability to detect adverse changes as quicklyas possible to assess their significance and to deter-mine the possible causes (Croxall & Rothery 1991).Shag habitual movements between the Croatianbreeding colonies and the Gulf of Trieste tookplace just during the 1980s (Utmar 1999; Sponzaet al. 2010) and were driven by dietary requirements(Cosolo et al. 2011). Johansen (1975) identifiedchanges in food distribution as one of the maindrives of long-term variations in the dispersal pat-terns of European Shags. The other causes werechanging weather patterns or competition betweenage groups (Galbraith et al. 1986). According toJohansen (1975) and Galbraith et al. (1986), webelieve that this migration is probably the later

100%

80%

60%

40%

20%

0%Croatia Slovenia Gulf of Trieste

Breeding areas Post-breeding areas

First-year Shags Experienced Shags

Venice New sites

Figure 5. Age structure of Shags (first-year and experienced Shags) recorded in different areas of the northern Adriatic Sea. The “Newsites” category takes into account the locations which are interesting with respect to date of sighting, direction taken and distances covered.

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Shag migration within the Adriatic Sea 9

Table III. Sightings of particular interest, given the novelty of the location and the direction anddistance covered by birds. ∗It was considered 2007 only, as the first-year with sightings of colour-rings. ∗∗All individuals were immature.

New Site Year First-yearShags

ExperiencedShags

Colony of origin

Ancona 2011 1 − OrudaPesaro 2007–2008 2 − Silbanski grebeniVenice∗ 2007 12 5 4 Brijuni, 3 Oruda,

10 Silbanski grebeniPelješac 2011 1 − Brijuni

Total – 16 5∗∗ −

stage in a graded response to deteriorating envi-ronmental conditions. In this regard, Sponza et al.(2010) highlighted that the maximum amount offish landed in the Adriatic Sea (about 220,000 tons)was recorded in 1981, which was followed by amarked decline (Mannini et al. 2005). In particu-lar, demersal fisheries decreased by 67% along theeastern Adriatic Sea coastline (Slovenia, Croatia,Bosnia–Herzegovina, Montenegro and Albania), asa consequence of overfishing. We suggest that theGulf of Trieste was a profitable area to buffer suchalterations.

To our knowledge, this is the first Shag pop-ulation in which it is possible to ascribe specificchanges in dispersal patterns to alterations in foodaccessibility and availability. Both juvenile and adultShags from the northern Adriatic undertake longer-distance movements than other studied populations,with the exception of the northern Norwegian birds(Galbraith et al. 1986).

On the other hand, this is an interesting case inwhich changes in post-breeding dispersal patternsled to a migratory movement within a period of30 years (Sponza et al. 2010). If a species is migra-tory, a higher-than-expected proportion of birdsshould move beyond the closer-distance zones, giv-ing a step-shaped distribution when recoveries areplotted against distance (Coulson 1961; Coulson &Brazendale 1968; Galbraith et al. 1986). Accordingto this approach, the analysis of the post-breedingmovements of Adriatic Shags, since a rapid shift indistances over 60 km for Brijuni colony and over160 km for Oruda and Silbanski Grebeni coloniesis recorded, shows that Adriatic Shags are migratoryrather than dispersive (Figure 6).

Actually, Shag movements and distribution duringthe post-breeding period have expanded westwardover the years, now including not only the Gulf ofTrieste but also the Venice Lagoon (Fracasso et al.2000). In fact, from 2003–2004 the species was reg-ularly observed in the Venice Lagoon throughout thesummer season (Bon et al. 2005). Large groups have

been reported since 2006 and the first colour-ringwas read on 2 July 2007 (Bon et al. 2007, 2009;Sighele et al. 2009, 2010). Recently, in the lagoonof Venice, about 300 individuals have been counted(Sighele et al. 2010). Moreover, numbers are fur-ther increasing in the Gulf of Trieste, where about3000 individuals were counted during the last sum-mer seasons. Given the high sensitivity of Shags tohuman disturbance during breeding (Guyot 1993),neither the Gulf of Trieste nor the Venice Lagoonoffers suitable, low disturbance places for nesting,which are largely present instead on Croatian islets.

All the studied colonies concurred with this migra-tion, regardless of the distance between the colonyand the post-breeding areas. Moreover, individualsfrom different colonies were observed at each of themain post-breeding areas (Gulf of Trieste, VeniceLagoon, Slovenian coast). It is interesting to highlighthow Shags from the most distant colony (SilbanskiGrebeni) exploit mostly the Gulf of Trieste, whichwas historically the first post-breeding area (Sponzaet al. 2010). In contrast, the nearest colonies (Brijuniarchipelago and Rovinj colony) are more linked withthe Venice Lagoon, a newly discovered area (Fracassoet al. 2000; Bon et al. 2005; Sighele et al. 2010).Given the high fidelity to the post-breeding areas,we assume that this migration originated in the mostdistant colonies and subsequently it has spread like awave, involving the northern colonies. These coloniesare indeed localised on the coastal route that con-nects the central Adriatic colonies to the Gulf ofTrieste.

The European Shag shows high breedingphilopatry, with about 99.0% of adults breed-ing at the same colony across years (Potts 1969;Aebischer 1995; Velando & Freire 2002). We havefew useful sightings to highlight a possible fidelityto the Adriatic breeding sites by the Mediterraneansubspecies, while the fidelity to post-breeding areasis quite evident. For example, the Shag “E39” fromSilbanski Grebeni has been recorded 17 times inthe Gulf of Trieste during four successive years;

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Brijuni archipelago

2.200

2.100

2.000

1.900

2.300

1.800

2.100

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1.800

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1.6000 20 40 60 80

Direct linear distance (km)

100 120 140 160 180 200

Oruda and Silbanski greberi colonies

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Figure 6. Post-breeding seasonal movements through succeeding distance zones, at intervals of 20 km. All age classes were combined.We analysed just the sightings towards the Gulf of Trieste. On this strictly coastal “route” Shags can stop at any place. However, at thepresent time we do not know if Shags follow the coast or cross the sea to go to Venice. We also split the analysis for Brijuni archipelago (nsightings = 163) and for Oruda and Silbanski grebeni colonies (n sightings = 146) to reduce the problem of the distance between colonies.The line represents the distribution expected if a purely dispersive movement was taking place.

all sightings originated from the same location(Miramare Castle, 45◦42′N, 13◦43′E). The lack ofringed birds sighted both in the Gulf of Trieste andin Venice Lagoon is another element in favour ofhigh fidelity to the post-breeding areas.

We believe that the high breeding philopatry (Potts1969; Aebischer 1995; Velando & Freire 2002), thelow occurrence of long-distance or cross-sea move-ments (Barlow et al. 2011) and, actually, a highfidelity to post-breeding sites, reflect the quite seden-tary “nature” of this species and, as a consequence,the role of changes in the environmental conditionsas presumably decisive elements in these distribu-tional variations.

While there were no Shags observed both in theGulf of Trieste and Venice Lagoon, four birds wererecorded both in the Gulf of Trieste and along theSlovenian coast, and one bird both in the Venice

Lagoon and along the Slovenian coast. In all cases,Shags were flying to Slovenia. According to the tim-ing of migration, these observations highlight therole of Slovenia, especially during the return to thebreeding colonies. The most important element incomparing the three main post-breeding areas is thelargest number of first-year Shags in Venice Lagoon.Moreover, the ratio between first-year birds andexperienced Shags increased with the “novelty” ofthe site (Figure 5). This highlights the role of youngShags in the discovery of new sites. Such a rolecould be attributed to “boom and bust” popula-tion dynamics, with periodic population crashes fol-lowed by rapid population growth (Aebischer 1986;Harris & Wanless 1996; Frederiksen et al. 2008).Following crashes, juvenile Shags have been shown tomove about 38% further than during non-crash years(Potts 1969). More likely, this behaviour could be

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Shag migration within the Adriatic Sea 11

identified as an “exploratory migration” (sensu Baker1978) or “intermittent migration” (sensu Berthold2001). According to the exploration model of migra-tory movements, young birds alternate migration inthe standard direction for the population with move-ments towards unusual directions. Suitable habitatslocated during this process can be used by birds infuture years. This behaviour may help to identifynovel feeding areas. Is this the case for the VeniceLagoon? Surely, this could explain why Shags arenow restricted in the North Adriatic Sea. From thispoint of view, the “discovery” of the Gulf of Triestewas sustained by a profitable change in the diet(Cosolo et al. 2011).

Conservation perspectives

Twenty colour-ringed Shags (8.6%) were recovereddead. Forty percent of these recoveries belonged tobirds drowned in fishing nets or fish traps. Otherauthors reported high values of mortality caused byfishing gear, possibly affecting the survival rate ofbirds (Velando & Freire 2002). These data are par-ticularly important, given that the MediterraneanShag is listed in Annex I of the Birds Directive2009/147/CE and is the focus of an Action Plan(Aguilar & Fernandez 2002).

According to Velando and Freire (2002), an effec-tive conservation of the Adriatic population shouldpass through: (1) the protection of the breedingsites as well as the feeding and roosting areas, and(2) the regulation of demersal fisheries in the feedingareas. Moreover, to better understand the mech-anisms underlying this migration we highlight theimportance to (1) characterise the feeding areas, inparticular the benthic community, and (2) accuratelyidentify the migration routes by the application ofminiaturised data loggers.

Acknowledgements

We thank all ringers who took part in Shag ringinggenerally and in particular T. Blažev, B. Cimador, B.Ende, D. Gatolin, M. Malatestinic, K. Mandic, K.Mikulic, A. Radalj. Moreover, we thank P. Utmar,C. Trani, F. Roppa, N. Ventolini, M. Tofful, R.Kriscjak and M. Kuljeric for help in the field. At VeliLošinj (Croatia) we thank the Blue World staff, inparticular N. Rako and P. Makelworth. At Brijuniarchipelago (Croatia), we thank the local author-ity of the Brijuni National Park. We are thankfulto numerous observers who submitted their valu-able observations, in particular M. Basso, B. Bašic,R. Benassi, I. Brajnik, S. Candotto, H. Cižmek, D.Degrassi, R. Fae, I. Jambrošic, S. Jovic, P. Kanuch,

A. Katalinic, K. Kravos, G. Lui, I. Maiorano, M.Mercker, A. Peruško, P. Ronconi, S. Rudolf, L.Sattin, S. Sava, I. Škornik, P. Spadoni, E. Stival,P. Ugo, P. Utmar, G. Vicario, A. Walderstein andE. Zanolini. We are grateful to A. Talamelli and N.Baccetti at the Institute for Environmental Protectionand Research (ISPRA), who coordinated the col-lection of colour-ring recoveries for Italy. We finallythank E.A. Ferrero and the two anonymous refereesfor valuable criticism.

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