Sexual Differences in the Diet of Great Cormorants Phalacrocorax Carbo Sinensis Wintering in Greece
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Eur J Wildl Res (2009) 55:301–308 DOI 10.1007/s10344-008-0243-2 ORIGINAL PAPER Sexual differences in the diet of great cormorants Phalacrocorax carbo sinensis wintering in Greece Vasilios Liordos & Vassilis Goutner Received: 27 January 2008 /Revised: 30 November 2008 /Accepted: 17 December 2008 / Published online: 14 January 2009 # Springer-Verlag 2009 Abstract Sexual differences in the diet of the great cormo- tion (Orta 1992). The subspecies P. c. sinensis is found in rant, Phalacrocorax carbo sinensis, were studied in four continental Europe and Asia, and its European population, Greek wintering areas, the Amvrakikos Gulf, the Axios and although stabilising recently, has been increasing since the Evros Deltas and the Messolonghi Lagoon, through the 1970s (Debout et al. 1995; Van Eerden and Gregersen analysis of stomach contents. Great cormorants are birds 1995; Marion 2003). This increase has been attributed to sexually dimorphic in size, with males being generally larger the legal protection and increase in fish productivity due to than females. Although similar prey species were found in eutrophication of aquatic habitats (Russell et al. 1996). As a the stomachs of both sexes in all the studied areas, significant consequence, severe conflicts with angling and fisheries differences were observed with respect to the proportion of interests have been raised in many European countries species taken. Male birds ate higher proportions of large fish (Russell et al. 1996; Cowx 2003). Therefore, much research species such as grey mullets, European sea bass, Dicen- on great cormorant’s diet, energetics, impact on fish trarchus labrax, and Prussian carp, Carassius gibelio,while populations and management has been conducted, espe- female birds took higher proportions of smaller species such cially during the last 10 years (e.g. Keller 1995; Kirby et al. as big-scale sand smelt, Atherina boyeri, and black goby, 1996; Grémillet et al. 2003; Lorentsen et al. 2004; Stewart Gobius niger. As a consequence, male great cormorants were et al. 2005). found to feed on significantly larger prey than did females by The great cormorant numbers have also been increasing means of fish standard length and body mass. There was no in Greece since the 1970s. The breeding population of 550 significant difference between the sexes in the mass of food pairs counted in 1971 (Handrinos and Akriotis 1997) found in stomachs. increased to an all-time high, 5,360 pairs in 2002 (Liordos 2004). In addition, over 20,000 birds wintered in Greece in Keywords Piscivorous predator . Winter diet . recent years (V. Liordos, unpublished data). The bird’s fish- Prey selection by sex eating habits along with its population explosion also prompted an urgent need for studies on great cormorant’s diet and its impact on fish populations and fisheries in Introduction Greece. Six studies on the diet of the great cormorant have been carried out in Greece (Goutner et al. 1997; Liordos et The great cormorant, Phalacrocorax carbo, is a large-sized al. 2002; Dimitriou et al. 2003; Kazantzidis and Naziridis fish-eating waterbird with an almost cosmopolitan distribu- 2003; Liordos and Goutner 2007a, b). These studies described and compared the diet composition of the great cormorant at several Greek colonies and wintering areas, Communicated by E. Hadjisterkotis : but they did not investigate the effect of sex on the diet. V. Liordos (*) V. Goutner Great cormorants are sexually dimorphic, with males Department of Zoology, School of Biology, generally being larger and heavier than females (Cramp Aristotle University of Thessaloniki, GR-54124 Thessaloniki, Greece and Simmons 1977; Koffijberg and Van Eerden 1995; e-mail: [email protected] Liordos and Goutner 2008). The aim of this paper was 302 Eur J Wildl Res (2009) 55:301–308 therefore to examine the patterns of prey selection of the Evros Delta at the Greek–Turkish border (40°44′–40°51′ N, great cormorant in relation to sex in four major wintering 25°53′–26°8′ E) is an extensive area (190 km2) diverse in areas of Greece by analysing stomach content data from habitats. The great cormorants roosted on a poplar Populus Liordos et al. (2002) and Liordos and Goutner (2007a). sp. stand on the west bank of the river’s east branch. The Messolonghi Lagoon (37°40′–39°40′ N, 20°10′–21°30′ E) belongs to the largest Greek wetland complex and is one of Materials and methods the largest in the Mediterranean basin situated in southwest Greece, totalling 258 km2. Two winter roosts were used in The study was conducted in four major Greek wintering the area: one at Makropoula, a rocky outcrop, and another areas, the Amvrakikos Gulf, the Axios and Evros Deltas at the River Acheloos, on tamarisks Tamarix sp. and the Messolonghi Lagoon (Fig. 1), all of them Under licence by the Ministry of Agricultural Develop- designated as wetlands of international importance under ment and Food, 22 birds were collected in collaboration the Ramsar Convention. The Amvrakikos Gulf (38°59′–39° with hunters at the Amvrakikos Gulf (February 2002), 13 in 11′ N, 20°44′–21°07′ E) covers a total of 405 km2, 220 of the Axios Delta (October 2001), 28 in the Evros Delta which belong to a variety of wetland habitats (e.g. open and (December 1999) and 16 at the Messolonghi Lagoon closed lagoons, salt marshes, salt flats, reed swamps) and (February 2002). Spatial variation in diet has previously the rest to open water. The great cormorants roost mainly been found to be significant (Liordos and Goutner 2007a), on the Gaidaros islet, a rocky outcrop of about 1 ha in size and data therefore could not be pooled together. located close to the gulf’s mouth (Aktion Strait). The Axios Marquiss and Carss (1997) analysed stomach contents Delta (40°27′–40°38′ N, 22°33′–22°52′ E) belongs to a by recording only intact items and by also including items large wetland complex covering a total of 68.7 km2 situated identified by key bones and found that large fish were near the city of Thessaloniki. The great cormorants roosted recorded with similar frequency by both methods, but at sea over water on mussel aquaculture infrastructure. The smaller fish were more likely to be recorded from key Fig. 1 The study areas in Greece BULGARIA Evros Delta F.Y.R.O.M. Axios Delta ALBANIA TURKEY Aegean Sea Amvrakikos Gulf Messolonghi Lagoon 0 30 km Eur J Wildl Res (2009) 55:301–308 303 bones than intact. Therefore, in order to derive as much Table 1 Common and scientific names of the fish species found in information as possible from the samples, whole fish were the diet of male and female great cormorants wintering in Greece during 1999–2002 first identified and measured, and then hard key bones, mainly otoliths and chewing pads, were extracted and Common names Scientific names appropriately identified and measured according to Carss et Atherinidae al. (1997). Fish length and body mass were subsequently Big-scale sand smelt Atherina boyeri calculated using regression equations found in literature or Blenniidae constructed by the authors (see Liordos and Goutner 2007a Peacock blenny Salaria pavo and references therein). For a more detailed description of Carangidae the methods of bird collection, storage, dissection and prey Horse mackerel Trachurus spp. identification and measurement, please refer to Liordos et Clupeidae al. (2002) and Liordos and Goutner (2007a). The sex of Twaite shad Alosa fallax European pilchard Sardina pilchardus each bird was identified by gonadal inspection. Round sardinella Sardinella aurita Prey types found in the stomachs of male and female Cyprinidae great cormorants were quantified by (1) relative abundance Bleak Alburnus alburnus by numbers (N%), as the percentage of each prey type out Prussian carp Carassius gibelio of all prey types found in the sample, (2) relative abundance Common carp Cyprinus carpio carpio by biomass (B%), as the percentage of the biomass of each Roach Rutilus rutilus prey type out of the estimated total biomass of the sample Engraulidae and (3) frequency of occurrence (F%), which is the European anchovy Engraulis encrasicolus Gobiids Gobiidae percentage of samples that contained each prey type (Duffy Black goby Gobius niger and Jackson 1986). The above parameters were used to Moronidae provide an index of relative importance (IRI) and IRI% for European sea bass Dicentrarchus labrax each prey type (i; Pinkas et al. 1971; Sanger 1987; Martin Grey mullets Mugilidae et al. 1996; Mariano-Jelicich et al. 2007) as: Thicklip grey mullet Chelon labrosus Golden grey mullet Liza aurata IRIi ¼ Fi% Â ðÞNi% þ Bi% ; and Thinlip mullet Liza ramado Leaping grey mullet Liza saliens ¼ ðÞÂ = : IRIi% IRIi 100 IRItotal Flathead mullet Mugil cephalus Mullidae Variation in diet composition between the sexes was Red mullet Mullus barbatus barbatus assessed by comparing numbers (N) of fish prey taken by Sparidae each sex with G tests (Zar 1999). IRI% was then used to Gilthead sea bream Sparus aurata identify the most important prey (Hart et al. 2002). Number Syngnathidae of fish per stomach, total estimated fish biomass per Pipefish Syngnathus spp. stomach and fish standard length (SL) and body mass Zeidae (BM) for each sex class were estimated and compared by John dory Zeus faber sex using Mann–Whitney (M–W) U tests (Zar 1999). Common and scientific names are taken from FishBase online (www. Median and range are presented for each variable. fishbase.org) Results most important prey for females, accounting for the 52.7% of the diet, followed by gobiids (18.1%). The median The common and scientific names of the fish taxa found in number of fish found in the stomachs did not vary the stomachs of male and female great cormorants from all significantly between the sexes (males: median 3 fish, the areas studied are given in Table 1.