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Changes in the diet composition of Pygmy Cormorant Phalacrocoraxpygmeuson Skadar lake (Southern Montenegro)

Spremembe v prehrani pritlikavega kormoranaPhalacrocorax pygmeusna Skadrskemjezeru (ju`na ^rna gora)

Andrej Vizi1 & Ondrej Vizi1

1 Natural History Museum o Montenegro, Trg Be}ir Bega Osmanagi}a 16, MN81000 Podgorica, Montenegro,email: [email protected], [email protected]

Diet changes o Pygmy Cormorant Phalacrocorax pygmeus, a piscivorous birdeeding primarily on sh up to 15 cm long, were studied on Skadar Lake. The

breeding population on the lake was estimated at over 2,000 pairs in 2005and 1,260 pairs in 2006, comprising about 58% o the regional populationo SE Europe & Turkey. The rst diet analysis, based on stomach contentso specimens hunted in the course o the breeding season, was carried outin the period 19731975 in order to identiy the infuence o the birds oncommercial shery. Further samples o regurgitated or accidentally droppedood items during the eeding o nestlings were collected and analyzed in the2006 breeding season. Results rom both periods are presented and changesin diet composition in the course o over 30 years are discussed. Between19731975 and 2006, the Pygmy Cormorants diet on Skadar Lake changeddrastically. Only one sh species, Rudd Scardinius knezevici, was ound to

be common to both study periods. Pygmy Cormorants diet in the period19731975 consisted o 11 sh species (N = 224 specimens), belonging tove amilies. The most abundant sh species were Roach Rutilus ohridanusand Albanian Roach Pachychilon pictum. Diet analysis in 2006 revealed onlysix species (N = 98 specimens) rom two amilies, and also showed that theintroduced Goldsh Carassius auratusbecame a major ood source or PygmyCormorant, constituting 84.7% o the total specimen number. Age class analysiso Goldsh items revealed that juvenile specimens (4590 mm) comprised89.0% o the total Goldsh compound. The study conrms that the PygmyCormorant is not a species-specic hunter and suggests it is not aected by thechanges in composition o sh community in the littoral zone o the lake. Fish

consumption by Pygmy Cormorants on Skadar Lake in 2006 was estimated at45 t during the most intensive oraging period (JuneAugust).

Key words:Pygmy Cormorant, Phalacrocorax pygmeus, diet, Goldsh, Carassiusauratus, Skadar Lake, MontenegroKljune besede:pritlikavi kormoran, Phalacrocorax pygmeus, Skadrsko jezero,prehrana, zlati koreselj, Carassius auratus, ^rna gora

1. Introduction

Skadar Lake, with up to 540 km2 o water surace inthe winter, is the largest lake o the Balkan Peninsula,situated between Montenegro (two thirds o the lake)and Albania (one third o the lake). The lake is a veryimportant site or the breeding, wintering and passage

o waterbirds. Up to 250,000 individuals o waterbirds

winter on the lake (Vasi} et al. 1992). Skadar Lakesupports one o the worlds largest populations oPygmy Cormorant Phalacrocorax pygmeus. Thebreeding population o this species on Skadar Lakewas estimated at over 2,000 pairs in 2005 (Savelji}2006) and 1,260 pairs in 2006 (Vizi 2009). These

Acrocephalus 31 (144): 2126, 2010doi: 10.2478/v10100-010-0003-8


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gures comprise about 58% o the regionalpopulation o SE Europe & Turkey (Delany & Scott2006).

Data on the diet o Pygmy Cormorant are rathersparse (Cramp 1998). The main diet comprises sh upto 15 cm long (del Hoyoet al.1992, Cramp 1998),besides a small contribution o amphibians and insects(Platteeuwet al. 2004). In general, cormorants arenotoriously recognized as a threat to shery. However,research showed that Pygmy Cormorant poses nothreat to commercial sh populations in Skadar Lake(Vizi 1981).

The rst sampling and analysis o the PygmyCormorants diet at Skadar Lake was perormed by O.

Vizi in the 19731975 period, but the results were notpublished. The analysis o these data and o new datacollected during 2006 is presented here.

2. Methods

2.1. Study area

At Skadar Lake, Pygmy Cormorants breed in asingle colony, at the locality called Crni @ar (421523.18N, 191858.37E; UTM CM68) (Figure 1).

It is a mixed-species colony, which includes threebreeding species o herons and egrets Squacco HeronArdeola ralloides, Little Egret Egretta garzetta, andNight Heron Nycticorax nycticorax, as well as GlossyIbis Plegadis falcinellusand Pygmy Cormorant.

The nests are completely mixed, which meansthat there are no distinguishable zones with dierentspecies. The very densely packed colony inhabits thebushes o Grey Willow Salix cinerea, Crack WillowSalix fragilis and Monks Pepper Vitex agnus-castus,surrounded by vast elds o water lilies (Nymphaea

alba, Nuphar luteum), Water Caltrop Trapa natans,Common Club-rush Schoenoplectus lacustris andCommon Reed Phragmites australis(Vizi 1997b). Thewater in this locality is very shallow, warm and turbid,which, together with the dense vegetation, makes thecolony very hard to reach.

The colony at Crni @ar was discovered in 1977,with the Cormorant Phalacrocorax carbo as the pioneerspecies. The rst breeding o Pygmy Cormorant wasconrmed in 1991, when the colony numbered about600 nests (Vizi 1997a). However, although the location

o Pygmy Cormorants breeding site was unknownprior to 1991, they had certainly bred there wellbeore. [otiet al. (1981) claimed that, according to thespecies daily movements and distribution on SkadarLake, the colony must be located in the inaccessiblearea near the Albanian border. In 1992, Little Egret

and Squacco Heron joined the colony, which has beengrowing ever since (Vizi 1997a).

2.2. Materials and methods

The rst sampling o the Pygmy Cormorants dietin the 19731975 period included stomach contentanalysis. These data are kept in the archive o theNatural History Museum o Montenegro. A totalo 214 birds were hunted down, or obtained romhunters and shermen in that period. Bird specimenswere at that time mostly collected at the shallowlocalities o the northern swamp, which includesseveral reshwater tributaries. The birds were hunted

down on their daily roosts and eeding sites. Each birdsstomach contents were separately extracted, drained,sorted and measured on an electronic scale with 0.1g precision. The greater part o the stomach contentsconsisted o sh, with traces o herbal componentsand insects, all in dierent stages o digestion.Determination o sh remnants was accomplishedon the basis o preserved morphological characters, tothe lowest taxon possible, while other elements wereomitted rom urther analysis. For the purpose o thisresearch, we took into consideration only 64 birds,

collected rom April to August the breeding periodo the species (Vizi 1997a).The diet analysis in 2006 was based on the

collection o sh samples regurgitated or accidentallydropped during the eeding o nestlings. A total o 98specimens were collected. Sampling was perormed

A. Vizi & O. Vizi: Changes in the diet composition o Pygmy Cormorant Phalacrocorax pygmeuson Skadar lake(Southern Montenegro)

Figure 1: Position o the Pygmy Cormorant Phalacrocoraxpygmeus colony at Skadar Lake (Southern Montenegro)(Adapted rom NASA World Wind 2010)

Slika 1: Lega kolonije pritlikavega kormorana Phalacrocoraxpygmeus na Skadrskem jezeru (ju`na ^rna gora) (povzeto poNASA World Wind 2010)

Montenegro/^rna gora

Crni @ar


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Acrocephalus 31 (144): 2126, 2010

twice, on 7 Jun 2006, at the beginning o the breedingseason, and on 21 Jul 2006, at its end, in order toreduce disturbance impact. Samples were collectedmanually and xed in 4% ormaldehyde. Thestandard length measurement (SL) and taxonomicdetermination was accomplished on the basis opreserved morphological characters, according toIvanovi} (1973) and Simonovi} (2001). The GoldshCarassius auratus specimens were classied into twodierent age classes according to Mari} (1998).

Wet measured weight o stomach is a poor sourceor quantitative ood intake estimation because dietitems are greatly damaged by digestion. This alsoapplies to regurgitated samples. Instead, we used thecalculated value o daily sh intake, based on thebirds energy requirements. For the estimation o shconsumption by Pygmy Cormorants, we used thevalue o daily sh intake o 200 g, calculated duringa similar research at the Danube delta. The equationtook into consideration the allometric relationshipbetween body mass, caloric value o sh fesh andassimilation eciency in piscivorous birds (Platteeuwet al.2004).

3. Results

3.1. Pygmy Cormorants diet in the 19731975period

A total o 11 sh species belonging to ve amilieswere ound in the Pygmy Cormorants diet, based

on samples rom the 19731975 period. The mostabundant were Roach Rutilus ohridanus, AlbanianRoach Pachychilon pictum, Freshwater BlennyBlenniusfluviatilis, and European Bitterling Rhodeus amarus,all o them exceeding 10% o the total number ospecimens in the samples (Table 1).

The mean weight o stomach contents measured inthe wet state ranged rom 28.2 to 59.4 g per monthand showed a statistically marginally signicantincrease in ood consumption (linear slope > 0; P =0.0967) rom April to August, which corresponds tothe Pygmy Cormorants breeding period (Figure 2).

3.2. Pygmy Cormorants diet in 2006

O a total o 98 sh specimens collected in 2006, 83belonged to Goldsh. This species comprised 84.7%o all prey items taken by Pygmy Cormorants. Fiveother sh species were ound in only low quantities(< 10%). The results o the taxonomic analysis o allcollected sh specimens are presented in Table 2.

Age class analysis o Goldsh shows that PygmyCormorant consumed mostly immature specimens othe class 0+ (younger than one year), and occasionally 1+(between one and two years). No older specimens wereound in the sample. Juvenile specimens belonging tothe class 0+ (4590 mm) comprised 89.0% o totalGoldsh compound.

Based on the daily sh intake o 200 g andpopulation gures or 2006, it can be estimated thatthe current Pygmy Cormorant population on Skadar

Table 1: Fish species and their abundance in Pygmy Cormorant Phalacrocorax pygmeus diet on Skadar Lake in the 19731975 period (N = 64 stomach contents)

Tabela 1: Vrste rib in njihova {tevil~nost v prehrani pritlikavega kormorana Phalacrocorax pygmeus na Skadrskem jezeru v

obdobju 19731975 (N = 64 vsebnosti `elodca)

Species / Vrsta Family / Dru`ina No. o specimens/[t. primerkov Percentage / Odstotek (%)

Rutilus ohridanus Cyprinidae 76 33.9Pachychilon pictum Cyprinidae 52 23.2Blennius fluviatilis Blenniidae 26 11.6Rhodeus amarus Cyprinidae 25 11.2Cobitis ohridana Cobitidae 20 8.9

Alburnus scoranza Cyprinidae 13 5.8Scardinius knezevici Cyprinidae 4 1.8Pomatoschistus montenegrensis Gobiidae 3 1.3Gobio scadrensis Gobiidae 2 0.9Gasterosteus gymnurus Gasterosteidae 2 0.9Squalius squalus Cyprinidae 1 0.4

Total / Skupaj 224 100.0


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Lake consumes about 500 kg o sh per day duringthe breeding season. During the most intensiveoraging period, rom the beginning o June to theend o August, sh consumption can be roughlycalculated to 45 t o sh. According to the abundanceo prey items in 2006, about 34 t were Goldshjuveniles.

4. Discussion

Pygmy Cormorants diet on Skadar Lake has changeddrastically over the last 30 years. Only one shspecies, Rudd Scardinius knezevici, was ound as

the diet component in both periods o our study. Anumber o species that used to be common in PygmyCormorants diet during 19731975 were missingin 2006, e.g. Bleak Alburnus scoranza, EuropeanBitterling, Freshwater Blenny and especially twomost numerous species, Roach Rutilus ohridanusand Albanian Roach. On the other hand, our newprey items were ound in 2006 sampling, including

the most abundant Goldsh, as well as two otherintroduced species, European Perch Perca fluviatilisand Topmouth Gudgeon Pseudorasbora parva. Thending o recently introduced sh species in the dietconrms that Pygmy Cormorant is not a species-specic hunter. Similar diet research in the Danubedelta (Platteeuwet al.2004) ound it to orage on 15sh species, including European Perch, Carp Cyprinuscarpio, Common Rudd Scardinius erythrophthalmus,Goldsh and Roach Rutilus ohridanus, together withten other species not present in Skadar Lake.

Despite the relatively small sample size, it can beconcluded that Goldsh became the major prey itemo Pygmy Cormorant. Goldsh is believed to havebeen introduced intentionally to Skadar Lake in the1970s, since the rst catch occurred in 1973 (Mari}1995). Similarly, European Perch and TopmouthGudgeon appeared in Skadar Lake in the late 1970s(Mari} & Krivokapi} 1997), and have adaptedsuccessully ever since. In the light o the much morevaried diet in 19731975, this act suggests thatPygmy Cormorant is not aected by the changes incomposition o the sh community. Being a non-specic sh eater, Pygmy Cormorant diet refects thecomposition o sh populations in the lakes littoralzone. The prevalence o Goldsh based on samples rom2006 can be interpreted in terms o its ecological traits.Most sh species start their reproduction in spring,

Table 2: Fish species and their abundance in Pygmy Cormorant Phalacrocorax pygmeus diet on Skadar Lake during the2006 breeding season (N = 98 fsh samples collected in the colony)

Tabela 2: Vrste rib in njihova {tevil~nost v prehrani pritlikavega kormorana Phalacrocorax pygmeus na Skadrskem jezeru v

gnezditvenem obdobju 2006 (N = 98 ribjih primerkov, zbranih v koloniji)

Species / Vrsta Family / Dru`ina No. o specimens/[t. primerkov Percentage / Odstotek (%)

Carassius auratus Cyprinidae 83 84.7Pseudorasbora parva Cyprinidae 6 6.1Cyprinus carpio Cyprinidae 5 5.1Perca fluviatilis Percidae 2 2.0Barbus rebeli Cyprinidae 1 1.0Scardinius knezevici Cyprinidae 1 1.0

Total / Skupaj 98 100.0

Figure 2: Mean weight o the wet stomach contentso Pygmy Cormorant Phalacrocorax pygmeus (N = 64)collected on Skadar Lake rom April to August in the 19731975 period (linear slope > 0, P = 0.0967)

Slika 2: Povpre~na mokra masa vsebnosti v `elodcih

pritlikavega kormorana Phalacrocorax pygmeus (N = 64),zbranih na Skadrskem jezeru med aprilom in avgustom vobdobju 19731975 (linearni naklon > 0, P = 0,0967)


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Acrocephalus 31 (144): 2126, 2010

rom March to June, depending on water temperature(Jankovi} 1971, Ivanovi} 1973 & Kneèvi} 1984). TheGoldsh reproductive period spans the warm part o

the year because its reproductive cycle can be triggeredby seven other species o cyprinid sh (Mari} 1998).This means that Goldsh is the most abundant in theshallow littoral zone where spawning takes place, andthereore heavily exploited by Pygmy Cormorants,which are known to hunt in shallow waters (Cramp1998, own data). The presence o species like FreshwaterBlenny and European Bitterling in the 1970s researchconrms the Pygmy Cormorant to be a littoral hunter,since these sh species inhabit small reshwaterstreams in the shallow northern part o the lake. The

most abundant sh in Skadar Lake at the time, BleakAlburnus scoranza, did not equally eature in the dietowing to its dispersion in the pelagial zone o the lakeduring the birds breeding season (Ivanovi} 1968, thisstudy). Adult Pygmy Cormorants are observed huntingall over the littoral zone o Skadar Lake during thebreeding season (Vizi & Dubak 2008), which conrmsnot only that regurgitated samples do not necessarilyorigin rom the colony or adjacent localities, but alsothat changes in the composition o sh communityoccurred throughout the littoral zone.

The Pygmy Cormorants breeding periodcorresponds to the spawning period o Skadar Lakeshes. They start building nests there in April andto lay eggs in June (Vizi 1997a). The incubationperiod is 2730 days (Cramp 1998), which suggeststhat the period o intensive eeding o the nestlingsbegins in July and lasts till the end o August (Vizi1997a). In 2006, most o the samples were collectedduring the rst visit on 7 Jun. The second visit, on21 Jul, yielded only ew samples, suggesting thatPygmy Cormorant had already passed the peak o the

breeding season. However, a number o nests at thecolony still contained young nestlings and un-hatchedeggs. In general, this is consistent with the increase inthe stomach contents mean weight in the latter parto the breeding season.

The annual catch o Goldsh is roughly estimatedat over 200 t (Mari} 1995), based on the obsoletecommercial catch statistics. Pygmy Cormorantsconsumption o this sh during the breeding season,calculated rom its energy requirements, amountsto 38 t. Another act that excludes the suggestion

o competition with shermen on Skadar Lake isthat Pygmy Cormorant orages mostly on immaturespecimens, which are not being caught by shing gearas being undersized and inaccessible swamp dwellers.The research proves that Pygmy Cormorant apparentlyhunts the most abundant species in the littoral zone

o the lake, which is generally benecial or the lakeecosystem. Due to the act that, as a piscivorous bird,it occupies a high trophic level in the ood chain, its

diet changes indicate deep and comprehensive changesin the ecosystem o Skadar Lake, which need to beinvestigated separately.

5. Povzetek

Avtorja ~lanka sta na Skadrskem jezeru preu~evalaspremembe v prehrani pritlikavega kormoranaPhalacrocorax pygmeus, ribojede vrste, ki izbirapredvsem med ribami, dolgimi do 15 cm. Ob jezerugnezde~a kolonija je bila leta 2005 ocenjena na ve~

kot 2.000 parov, leta 2006 pa na 1.260 parov, kar jepomenilo 58% regionalne populacije te vrste v JVEvropi in Tur~iji. Prva analiza prehrane, temelje~ana vsebnostih v èlodcih pritlikavih kormoranov,ulovljenih v gnezditveni sezoni, je bila opravljena vobdobju 19731975, in sicer kot poskus, da se ugotovivpliv teh ptic na lokalno ribi{tvo. V gnezditveni sezoni2006 so bili zbrani in analizirani vzorci plena, izbljuvaniali po nesre~i spu{~eni med hranjenjem mladi~ev vgnezdih. ^lanek predstavlja rezultate, dobljene za obeobdobji, in razpravlja o spremembah v sestavi prehrane

v zadnjih tridesetih letih. Najpomembnej{a ugotovitevje, da se je med obdobjem 19731975 in letom 2006prehrana pritlikavega kormorana na Skadrskem jezerudrasti~no spremenila. Le ena ribja vrsta, rde~eperkisorodnaScardinius knezevici, je bila v prehrani najdenav obeh preu~evanih obdobjih. Prehrana pritlikavegakormorana v obdobju 19731975 je obsegala 11ribjih vrst (N = 224 primerkov), pripadajo~ih petimdruìnam. Naj{tevil~nej{i med njimi sta bili Rutilusohridanusin Pachychilon pictum. Analiza prehrane leta2006 pa je razkrila, da vsebuje samo {est ribjih vrst (N =

98 primerkov) iz dveh druìn in da je v jezeru naseljenizlati koreselj Carassius auratuspostal glavni vir hranepritlikavega kormorana, saj je sestavljal kar 84,7% vsehprimerkov. Analiza starostnega razreda zlatega koresljaje pokazala, da mladi primerki (4590 mm) sestavljajo89,0% skupne koli~ine te ribje vrste. [tudija je hkratipotrdila, da pritlikavi kormoran ni vrstno speci~enplenilec in da ga niso prizadele spremembe v sestavi ribjezdru`be v obre`nem pasu jezera. Avtorja ocenjujeta, daso leta 2006, v obdobju najbolj intenzivnega hranjenja(junijavgust), pritlikavi kormorani v Skadrskem jezeru

pojedli 45 t rib.


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Montenegro, Biological station, Titograd.Jankovi}, D. (1971): Razmnoàvanje {arana (Cyprinuscarpio L.) iz Skadarskog jezera. Arhiv biolo{kih nauka /

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Mari}, D. (1995): Rasprostranjenje i brojnostintrodukovanog srebrnog kara{a (Carassius gibelio, Bloch1782) u Skadarskom jezeru u periodu 1972/92. GlasnikRepubli~kog zavoda za za{titu prirode u Podgorici 27/28:113127.

Mari}, D. (1998): Adaptacija introdukovanog srebrnogkara{a (Carassius auratus gibelio, Bloch 1782) naSkadarskom jezeru. Doktorska disertacija, Univerzitetu Kragujevcu, Prirodno-matemati~ki akultet, Instututza biologiju.

Mari}, D. & Krivokapi}, M. (1997): Stanje aune riba uslivu Skadarskog jezera. pp. 215223 In: Miju{kovi},M. (ed.): Prirodne vrijednosti i za{tita Skadarskog jezera:radovi sa nau~nog skupa, knjiga 44. Crnogorskaakademija nauka i umjetnosti, Podgorica.

Platteeuw, M., Kiss, J.B., Zhmud M.Y. & Sadoull, N.(2004): Colonial Waterbirds and Their Habitat Use inthe Danube Delta, as an example o a large-scale naturalwetland. RIZA Report 2004. Institute or Inland

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[oti, J., Vizi, O. & Krsmanovi}, L. (1981): Teìna i mere

malog kormorana, Phalacrocorax pygmaeus(Pallas), 1773sa Skadarskog jezera (Jugoslavija). Glasnik Republi~kogzavoda za za{titu prirode i Prirodnja~kog Muzeja Titograd14: 5362.

Vasi}, V., Puzovi}, S. & Vizi, O. (1992): Capacities O LakeSkadar in Relation to European Regional Populations O

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Vizi, A. (2009): Uticaj ptica iz reda Pelecaniormes tokomperioda gnije|enja na aunu riba Skadarskog jezera. Magistarski rad, Prirodno-matemati~ki akultet,Univerzitet Crne Gore, Podgorica.

Vizi, O. (1981): Some aspects o relationships between thesh populations and populations o swamp birds at LakeSkadar. pp. 414419 In: Karaman, G.S. & Beeton,

A.M. (eds.): The Biota and Limnology o Lake Skadar. Institution o medical and biological research inMontenegro, Biological station, Titograd.

Vizi, O. (1997a): Crni àr nova kolonija mo~varnih pticana Skadarskom jezeru. pp. 309320 In: Miju{kovi}, M.

(ed.): Prirodne vrijednosti i za{tita Skadarskog jezera:radovi sa nau~nog skupa, knjiga 44. Crnogorskaakademija nauka i umjetnosti, Podgorica.

Vizi, O. (1997b): Neki eekti eutrozacije Skadarskogjezera na primjeru makrotske vegetacije. pp. 299308In: Miju{kovi}, M. (ed.): Prirodne vrijednosti i za{titaSkadarskog jezera: radovi sa nau~nog skupa, knjiga 44. Crnogorska akademija nauka i umjetnosti, Podgorica.

Vizi, O. & Dubak, N. (2008) Izvje{taj o rezultatimamonitoringa vodenih ptica gnjezdarica u NP Skadarsko

jezero u 2008. godini. JP za Nacionalne parkove CrneGore, Podgorica.

Arrived / Prispelo: 6.3.2008Accepted / Sprejeto: 15.10.2010


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