INTRODUCTIONTop

Conflicts between cormorant species and fishery activities are a worldwide concern (Carss et al. 1997Carss D.N., Bevan R.M., Bonetti A., et al. 1997. The Diet Assessment and Food Intake Working Group. Techniques for assessing cormorant diet and food intake: towards a consensus view. Suppl. Ricerche Biol. Selvaggina 26: 197-230.). The interactions are site-specific, ranging from serious damage in breeding and wintering areas where commercial and recreational fisheries take place to unusually high or uncommon effects (Carss 1993Carss D.N. 1993. Shags Phalacrocorax aristotelis at cage fish farms in Argyll, western Scotland. Bird Study 40: 203-211., 2002Carss D.N. 2002. Reducing the conflict between Cormorants and fisheries on a pan-European scale (REDCAFE). Final Report. Natural Environmental Research Council. Centre for Ecology and Hydrology. http://www.intercafeproject.net/pdf/REDCAFEFINALREPORT.pdf, Lilliendahl and Solmundsson 2006Lilliendahl K., Solmundsson J. 2006. Feeding ecology of sympatric European shags Phalacrocorax aristotelis and great cormorant P. carbo in Iceland. Mar. Biol. 149: 979-990.). In some places on the Mediterranean coast, the European shag Phalacrocorax aristotelis spp. desmarestii (hereafter referred as the shag) and the great cormorant P. carbo spp. sinensis (hereafter referred as the cormorant) coexist during the breeding season of the former and the wintering period of the latter, i.e. they are syntopic species. One of these places is in Murcia (SE Spain; Fig. 1): Grosa Island holds a local shag breeding population of 12 to 18 pairs (Eguía-Martínez et al. 2015Eguía-Martínez S., Aguado-Giménez F., Sallent A., et al. 2015. Evolución de la población nidificante de cormorán moñudo en la Región de Murcia. Proceedings of the 5th Congreso de la Naturaleza de la Región de Murcia y II del Sureste Ibérico. Asociación de Naturalistas del Sureste. Murcia, Noviembre 2015. http://www.asociacionanse.org/download/62), and together with Redonda islet inside the nearby Mar Menor coastal lagoon, it also holds a wintering population of cormorant of about 5000 individuals (Molina 2013Molina B. 2013. El cormorán grande en España. Población reproductora e invernante 2012-2013. In: SEO/Birdlife Programas de seguimiento de avifauna, pp. 26-29. SEO/Birdlife. Madrid. http://www.seo.org/wp-content/uploads/2012/05/Seguimiento_2012_OK.pdf). During the breeding season, shag foraging areas are located near nesting colonies (Aguado-Giménez, pers. obs.), just as occurs around most breeding grounds (Wanless et al. 1991aWanless S., Harris M.P., Morris J.A. 1991a. Foraging range and feeding locations of shags Phalacrocorax aristotelis during chick rearing. Ibis 133: 30-36.). Conversely, cormorant mobility for feeding is greater during wintering, including both coastal and inland areas (Farinós and Robledano 2010Farinós P., Robledano F. 2010. Structure and distribution of the waterbird community in the Mar Menor coastal lagoon (SE Spain) and relationships with environmental gradients. Waterbirds 33: 479-493.). Although both bird species are opportunistic piscivorous predators (Carss 2002Carss D.N. 2002. Reducing the conflict between Cormorants and fisheries on a pan-European scale (REDCAFE). Final Report. Natural Environmental Research Council. Centre for Ecology and Hydrology. http://www.intercafeproject.net/pdf/REDCAFEFINALREPORT.pdf, Morat et al. 2014Morat F., Mante A., Drunat E., et al. 2014. Diet of Mediterranean European shag, Phalacrocorax aristotelis desmarestii, in a northwestern Mediterranean area: a competitor for local fisheries? Sci. Rep. Port-Cros Nat. Park 28: 113-132.), we do not expect competition between them during syntopy, in line with the findings of Lilliendahl and Solmundsson (2006)Lilliendahl K., Solmundsson J. 2006. Feeding ecology of sympatric European shags Phalacrocorax aristotelis and great cormorant P. carbo in Iceland. Mar. Biol. 149: 979-990.. Nevertheless, the large difference in their population sizes could suggest some interaction. Also, foraging of both species could increase pressure on prey populations (Lilliendahl and Solmundsson 2006Lilliendahl K., Solmundsson J. 2006. Feeding ecology of sympatric European shags Phalacrocorax aristotelis and great cormorant P. carbo in Iceland. Mar. Biol. 149: 979-990.), also interacting with the local artisanal fisheries occurring near the breeding-wintering area. Local fishermen are concerned with the increasing abundance of cormorants, though this interaction has not yet been evaluated.

Dietary studies of birds include regurgitated pellet analyses to characterize diet composition and estimate food intake through fish otolith identification (Hillersøy and Lorentsen 2012Hillersøy G., Lorentsen S.-H. 2012. Annual variation in the diet of breeding European shag (Phalacrocorax aristotelis) in central Norway. Waterbirds 35: 420-429., Morat et al. 2014Morat F., Mante A., Drunat E., et al. 2014. Diet of Mediterranean European shag, Phalacrocorax aristotelis desmarestii, in a northwestern Mediterranean area: a competitor for local fisheries? Sci. Rep. Port-Cros Nat. Park 28: 113-132.). Pellet collection is fairly easy, involving little or no disturbance to birds and analysis requires minimal laboratory facilities (Carss et al. 1997Carss D.N., Bevan R.M., Bonetti A., et al. 1997. The Diet Assessment and Food Intake Working Group. Techniques for assessing cormorant diet and food intake: towards a consensus view. Suppl. Ricerche Biol. Selvaggina 26: 197-230.). Inferring diet composition after analysing regurgitated pellets is recognized as an appropriate proxy method for studying the diet of cormorant species (Duffy and Laurenson 1983Duffy D.C., Laurenson I.J.R. 1983. Pellets of Cape Cormorants as indicators of diet. Condor 85: 305-307., Barrett et al. 1990Barrett R.T., Røv N., Loen J., et al. 1990. Diets of Shags Phalacrocorax aristotelis and Cormorants P. carbo in Norway and possible implications for gadoid stock recruitment. Mar. Ecol. Prog. Ser. 66: 205-218.). In this work, we aimed to study the diet of syntopic shags and cormorants in the vicinity of Grosa Island and the Mar Menor coastal lagoon to determine whether there is potential competition with artisanal fishery and to check for any competition for food resources between the two bird species. To this end, freshly regurgitated pellets and fish otolith identification were used to explore shag and cormorant diet qualitatively and quantitatively. However, since there are criteria for (Johansen et al. 2001Johansen R., Barrett R.T., Pedersen T. 2001. Foraging strategies of great cormorant Phalacrocorax carbo carbo wintering north of the Arctic circle. Bird Study 48: 59-67.) and against (Carss et al. 1997Carss D.N., Bevan R.M., Bonetti A., et al. 1997. The Diet Assessment and Food Intake Working Group. Techniques for assessing cormorant diet and food intake: towards a consensus view. Suppl. Ricerche Biol. Selvaggina 26: 197-230.) the utilization of pellets to infer total intake, the results obtained should be considered as a proxy.

MATERIALS AND METHODSTop

The birds

Shags and cormorants are very similar in appearance but each species has particular behavioural and morphological differentiating characteristics. From the point of view of foraging and potential competition, it is worth highlighting some of them. Both species are piscivorous but shags are almost exclusively marine birds that rarely penetrate estuaries or rivers (Harrison 2003Harrison P. 2003. Seabirds: an identification guide. Ediciones Omega. Barcelona.). On the other hand, cormorants forage in a very wide range of aquatic environments, including both salt and fresh waters (Cramp and Simmons 1977Cramp S., Simmons K.E.L. (eds). 1977. Handbook of the Birds of Europe, the Middle East and North Africa. The Birds of the Western Palearctic. Volume 1. Oxford University Press, Oxford.). Both species are colonial waterbirds, breeding and roosting in groups. However, shags forage alone or in small groups of 2-4 individuals, whereas cormorants normally hunt in flocks, harassing the fish shoals against the shore and catching them in shallow waters (Van Eerden and Voslamber 1995Van Eerden M.R., Voslamber B. 1995. Mass fishing by cormorants Phalacrocorax carbo sinensis at Lake Ijsselmeer, The Netherlands: a recent and successful adaptation to a turbid environment. Ardea 83: 199-212.). Nevertheless, cormorants also often forage alone. Cormorants are heavier (1.7 to 3.5 kg body mass) than shags (1.5 to 1.9 kg body mass) (Cramp and Simmons 1977Cramp S., Simmons K.E.L. (eds). 1977. Handbook of the Birds of Europe, the Middle East and North Africa. The Birds of the Western Palearctic. Volume 1. Oxford University Press, Oxford., Fonteneau et al. 2009Fonteneau F., Paillisson J.M., Marion L. 2009. Relationships between bird morphology and prey selection in two sympatric Great Cormorant Phalacrocorax carbo subspecies during winter. Ibis 151: 286-298., Barros et al. 2013Barros A., Álvarez D., Velando A. 2013. Cormorán moñudo – Phalacrocorax aristotelis. In: Salvador A., Morales M.B. (eds), Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid. http://www.vertebradosibericos.org). Consequently, shags have lower daily energy requirements than cormorants (Ridgway 2010Ridgway M.S. 2010. A review of estimates of daily energy expenditure and food intake in cormorants (Phalacrocorax spp.). J. Great Lakes Res. 36: 93-99.). Bill size also differs between the two species, culmen length being slightly shorter and bill depth considerably less deep in shags than in cormorants (Martínez-Abraín et al. 2006Martínez-Abraín A., Oro D., Velando A., et al. 2006. Morphometric similarities between central and peripheral populations of the European shag Phalacrocorax aristotelis. Mar. Ornithol. 34: 21-24., Fonteneau et al. 2009Fonteneau F., Paillisson J.M., Marion L. 2009. Relationships between bird morphology and prey selection in two sympatric Great Cormorant Phalacrocorax carbo subspecies during winter. Ibis 151: 286-298., Barros et al. 2013Barros A., Álvarez D., Velando A. 2013. Cormorán moñudo – Phalacrocorax aristotelis. In: Salvador A., Morales M.B. (eds), Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid. http://www.vertebradosibericos.org).

Study area

The shag breeding colony is located on Grosa Island, and the cormorant roosting places on both Grosa Island and Redonda Islet (Murcia, SE Spain; Fig. 1; 37°46'00"N, 0°50'00"W). Grosa Island and Redonda Islet are about 7.5 km apart. Also, there are two clearly differentiated roosting places at Grosa Island, one of them used by wintering cormorants and the other by post-breeding shags. Grosa Island is surrounded by one of the most extensive Posidonia oceanica meadows of the Mediterranean (Ruiz et al. 2015Ruiz J.M., Guillén E., Ramos Segura A., et al. 2015. Atlas de las praderas marinas de España. IEO/IEL/UICN, Murcia-Alicante-Málaga, 681 pp.), interspersed with sandy patches and rocky reefs, and wide shallow sandy bottoms (MAPAMA 2017MAPAMA. 2017. Ministerio de Agricultura y Pesca, Alimentación y Medio Ambiente. Ecocartografía de Murcia. Comunidades marinas. http://www.mapama.gob.es/es/costas/temas/proteccion-costa/ecocartografias/ecocartografia-murcia.aspx). As mentioned above, during the breeding season shags spend most of the time foraging next to the colony. Silty-sandy bottoms with low-density Cymodocea nodosa seagrasses dominate the nearshore seabed of the Mar Menor. At depths greater than –3 m, the sea floor becomes muddy and covered by a dense Caulerpa prolifera and C. nodosa mixed meadow (MAPAMA 2017MAPAMA. 2017. Ministerio de Agricultura y Pesca, Alimentación y Medio Ambiente. Ecocartografía de Murcia. Comunidades marinas. http://www.mapama.gob.es/es/costas/temas/proteccion-costa/ecocartografias/ecocartografia-murcia.aspx). Cormorants often hunt in the shallowest zones of the Mar Menor, and their foraging area overlaps with the main fishing grounds in the Mar Menor.

Pellet sampling

In Grosa Island, shag pellets were collected early in the morning from nest platforms during the 2016 breeding season, in mid-February. To minimize disturbance to shags, pellets were collected during a single event coinciding with the chick-ringing campaign. During 2016 wintering, also in mid-February, cormorant pellets were taken from the roosting areas on Grosa Island and Redonda Islet at noon, when there were almost no cormorants in the area. For both bird species only fresh pellets were collected. Cormorants move between Grosa Island and Redonda Islet to roost on them indistinctly (Eguía-Martínez et al. 2015Eguía-Martínez S., Aguado-Giménez F., Sallent A., et al. 2015. Evolución de la población nidificante de cormorán moñudo en la Región de Murcia. Proceedings of the 5th Congreso de la Naturaleza de la Región de Murcia y II del Sureste Ibérico. Asociación de Naturalistas del Sureste. Murcia, Noviembre 2015. http://www.asociacionanse.org/download/62), so both roosting places can be considered as a single functional unit, and data from pellets obtained on the two islands were therefore considered as replicates. Each pellet was sealed individually in plastic bags, labelled and stored frozen (–20°C) until processing.

Diet analysis

Pellets were processed according to Privileggi (2003)Privileggi N. 2003. Great Cormorants Phalacrocorax carbo sinensis wintering in Friuli Venezia Giulia, Northern Adriatic: specific and quantitative diet composition. Vogelwelt 124: 237-243.. Otoliths were extracted and identified up to the lowest possible taxonomic level, comparing them with images from the atlas compiled by Tuset et al. (2008)Tuset V.M., Lombarte A. Assis C.A. 2008. Otolith atlas for the western Mediterranean, north and central eastern Atlantic. Sci. Mar. 72S1: 7-198. and the manual by Artzi et al. (2009)Artzi Y., Gisis G., Goldstein H. 2009. Manual for freshwater fish-otoliths-Israel. Israel Natural and Parks Authority, 21 pp. http://www.nature-conservation.org.il/BuildaGate5/portals/conserve/imagesP/sub72/725026172.pdf for marine and freshwater species, respectively. From each pellet, right and left otoliths of each fish species were separated and the most numerous side was used to resolve the number of individuals from each species in the pellet. Fish species composition and total abundance were recorded for each pellet. Otolith length (OL) was also measured to the nearest 0.01 mm under a dissecting microscope. Fish species length (FL) was estimated using the OL-FL equations from Giménez et al. (2016)Giménez J., Manjabacas A., Tuset V.M., et al. 2016. Relationship between otolith and fish size from Mediterranean and north-eastern Atlantic species to be used in predator-prey studies. J. Fish Biol. 89: 2195-2202. and Amouei et al. (2013)Amouei F., Valinassab T., Haitov A. 2013. Age determination and morphological study using otoliths in Cyprinus carpio Linnaeus, 1758 in the southern Caspian Sea Iranian. J. Fish. Sci. 12: 759-769. for marine and freshwater fish species, respectively. Fish weight (FW) was estimated using the FL-FW equations obtained from Froese and Pauly (2007)Froese R., Pauly D. 2007. FishBase. World Wide Web electronic publication. http://www.fishbase.org. Strongly eroded otoliths were recorded as unidentified species. For total abundance analysis, only half the eroded otoliths were arbitrarily considered. For total biomass analysis, we assigned the average weight of all the identified species to unidentified otoliths to estimate total biomass per pellet. Considering that daily pellet production of shags (and probably cormorants) is variable through seasons (Russell et al. 1995Russell A.F., Wanless S., Harris M.P. 1995. Factors affecting the production of pellets by Shag Phalacrocorax aristotelis. Seabird 17: 44-49.), the daily biomass intake by shags and cormorants was estimated as a range from the average biomass estimated for each pellet, considering that both bird species may regurgitate one or two pellets per day (Johnstone et al. 1990Johnstone I.G., Harris M.P., Wanless S., et al. 1990. The usefulness of pellets for assessing the diet of adult shags Phalacrocorax aristotelis. Bird Study 37: 5-11.).

Statistical analyses

Differences between shag and cormorant diet were assessed using univariate and multivariate variables. Univariate analyses were performed for species richness (number of species), total abundance (number of individuals) and total biomass per sample. Furthermore, fish species were assigned to one of the following functional groups: small pelagic, demersal, benthic and freshwater. Then, multivariate analyses were performed for functional groups in terms of both abundance and biomass. Unidentified species were not included in any multivariate analysis. One-way non-parametric permutational univariate analysis of variance (PERM-ANOVA) or multivariate analysis of variance (PERM-ANOVA) (Anderson et al. 2008Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth.) were used to test the above hypothesis. PERM-
ANOVA was based on Euclidean distances of normalized species richness, total abundance and total biomass data, and PERM-ANOVA on the Bray-Curtis dissimilarities (Clarke and Warwick 1994Clarke K.R., Warwick R.M. 1994. Change in marine communities: an approach to statistical analysis and interpretation. PRIMER-E, Plymouth.) of square-root transformed functional group data (Clarke 1993Clarke K.R. 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18: 117-143.) in terms of abundance and biomass. Both univariate and multivariate analyses were tested under unrestricted 4999 permutations of raw data (Anderson 2001aAnderson M.J. 2001a. A new method for non-parametric multivariate analysis of variance. Aust. Ecol. 26: 32-46.). The Monte Carlo P-value (P(MC)) was also calculated and considered preferentially (Anderson 2001bAnderson M.J. 2001b. Permutation tests for univariate or multivariate analysis of variance and regression. Can. J. Fish. Aquatic Sci. 58: 626-639., 2005Anderson M.J. 2005. PERMANOVA. Permutational Multivariate Analysis of Variance. A Computer Program. Department of Statistics, University of Auckland, NZ, p. 24.). A SIMPER test was run to establish the contribution of the functional groups and fish species, in terms of both abundance and biomass, with respect to the differences between the diet of shags and cormorants during syntopy. All analyses were carried out using PRIMER-E v. 7.0.10 and PERMANOVA +1 (PRIMER-E 2015PRIMER-E. 2015. PRIMER 7 version 7.0.10. PRIMER-E, Plymouth, UK.).

Shag and great cormorant abundance

Monthly abundance of shags from November 2015 to March 2016 was estimated by counting the shags in the roosting and nesting places early in the morning fortnightly, and then averaging. Monthly abundance of cormorants in the study area was assigned from abundance data derived from the 2013 winter census (Molina 2013Molina B. 2013. El cormorán grande en España. Población reproductora e invernante 2012-2013. In: SEO/Birdlife Programas de seguimiento de avifauna, pp. 26-29. SEO/Birdlife. Madrid. http://www.seo.org/wp-content/uploads/2012/05/Seguimiento_2012_OK.pdf), after considering that abundance increases progressively from the beginning of the season, reaching a maximum at the time of counting (mid-January), and then decreasing to the end of the season (as shown below).

Competition with local artisanal fisheries inside Mar Menor coastal lagoon

Fish species identified from otoliths in shag and cormorant pellets were classified into three categories depending on their local economic importance: high, medium and low. Potential consumption of these fish species by shags and cormorants throughout the season was estimated monthly from bird abundance and average biomass intake data, according to the overall contribution of fish to the diet of shags and cormorants over the season. Artisanal fishing in the Grosa Island and Mar Menor area is carried out by the Fishermen´s Association of San Pedro del Pinatar (hereafter FASP). Monthly fishing effort was estimated as a percentage in line with the range of gear allowed and deployed, as provided by the FASP. Also, the FASP provided us with monthly total catch (TC) data for the fish species of high local commercial interest which were found in the diet of shags and cormorants during syntopy, from November 2015 to March 2016.

Maximum potential catches (MPC, calculated as if the fishing effort was always 100%) were calculated monthly and for the whole season. The TC/MPC ratio was defined as a measure of similarity between how much was captured for the fishing effort applied (TC) and how much could have been captured if the fishing effort had been the maximum every month (MPC). TC/MPC was calculated for the whole season. This ratio goes from 0 to 1, so the less close to 1, the higher the possibility of competition.

RESULTSTop

A total of 18 shag pellets were collected at nests on Grosa Island, and 78 cormorant pellets were removed from their roosting places on Grosa Island and Redonda Islet. Altogether, a total of 2130 otoliths were obtained, of which 10.4% were too eroded and were recorded as unidentified. A total of 1065 fish were identified, belonging to 14 families and 23 species. Mugilidae were identified only up to family level. Table 1 shows the species composition of shag and cormorant diet in terms of abundance and biomass, as well as the assignation of fish species to functional groups and categories of economic importance.

Comparing the diet of shags and cormorants

Species richness and total abundance in the diet (Table 2) were higher (PERM-ANOVA, Pseudo-F_{2, 62}=9.11 and 9.24, respectively; P<0.01 and P<0.001, respectively) for shag than for cormorant. However, no differences were detected for total biomass between the two species (PERM-ANOVA, Pseudo-F_{2, 62}=0.53; P>0.05). Despite this, estimated daily biomass intake was slightly higher for cormorant than for shag (Table 2). In terms of both abundance and biomass, shags preyed mostly on small pelagic fish and cormorants on demersal fish (PERM-ANOVA, Pseudo-F_{2, 62}=8.76 and 20.04, respectively; P<0.001 for both) (Table 3). Benthic fish was the functional group least predated on by both bird species. Freshwater fish were present only in cormorant diet.

In shag diet, the most abundant fish species in increasing order were Boops boops (40.9%), Trisopterus sp. (14.3%) and Coris julis (10.3%), and the greatest biomass was obtained from B. boops (46.1%), C. julis (12.8%) and Diplodus annularis (7.9%). In cormorant diet, the most abundant preys in increasing order were Sparus aurata (35.3%), Atherina boyeri (12.6%), Cyprinus carpio (12.2%) and Dicentrarchus labrax (10.1%), and the greatest biomass was obtained from S. aurata (43.8%), D. labrax (17.1%), C. carpio (9.9%) and Mugilidae (9.1%) (Table 1). The SIMPER test revealed that the fish species which most contributed to differences between shag and cormorant diet with regard to abundance were B. boops and Trisopterus sp. with a greater abundance in shag diet, and S. aurata and A. boyeri with a greater abundance in cormorant diet. As for biomass, differences between shag and cormorant were supported by the higher biomass in shag diet of B. boops and, to a lesser extent, C. julis (absent in the cormorant diet), and also to higher biomass in cormorant diet of S. aurata (absent in the shag diet) and D. labrax. Average size of cormorant prey was considerably greater (14.40 cm) than that of shags (9.70 cm), particularly in the case of D. labrax. Exceptionally, cormorant preyed on very large fish, such as a Mugilidae specimen of almost 51 cm (Table 4). For shag and cormorant, modal prey size (8.74 and 6.51 cm, respectively) was lower than mean size (Table 4).

Shag and cormorant abundance

Monthly abundance of shag showed no large variations, ranging from 23 to 43 individuals throughout the season around Grosa Island (Table 5). For cormorant, we assigned an increasing abundance from the beginning to the middle of the season, from which it descended to the end of the season, based on a maximum abundance of ca. 5000 specimens in the middle of the season at Grosa Island and Redonda Islet jointly, in agreement with Molina (2013)Molina B. 2013. El cormorán grande en España. Población reproductora e invernante 2012-2013. In: SEO/Birdlife Programas de seguimiento de avifauna, pp. 26-29. SEO/Birdlife. Madrid. http://www.seo.org/wp-content/uploads/2012/05/Seguimiento_2012_OK.pdf, as shown in Table 5.

Fishing catch of species of high commercial value and consumption by shags and cormorants

The fish species of high commercial interest (Table 1) captured by FASP fishermen which were also found in shag and/or cormorant diet were S. aurata, D. labrax, A. boyeri, Mugilidae and D. annularis. For these species, Table 5 shows monthly fishing effort, TC data, fishing MPC and the overall TC/MPC ratio. Fishing effort was the maximum possible during November 2015, dropping progressively in winter and increasing in early spring. Conversely, fishing effort on A. boyeri was low at the beginning of the season, increasing gradually up to its maximum in early spring. For the study period, the increasing order of catch by species corresponds to the species listed above. S. aurata was captured profusely, and seasonal TC data constituted an absolute historical record (FASP, pers. comm.). S. aurata and D. labrax TC decreased as the season progressed, unlike A. boyeri, Mugilidae and D. annularis TC, which were irregular throughout the season. TC/MPC values for the whole season reveal that catches of S. aurata (0.87) and D. annularis (0.82), and to a lesser extent A. boyeri (0.75), were close to the maximum possible for FASP over the study period, but D. labrax (0.52) and Mugilidae (0.47) could have been more abundant, so competition for the two latter species was alike. It is noteworthy that catches of D. annularis by cormorants could be higher than the expected MPC.

Monthly consumption of fish species of high commercial value by shags and cormorants is shown in Table 5. Shag biomass intake was derived mainly from fish species of medium commercial value (47.9 %), while the diet of cormorant was composed largely of species of high commercial value (79.0 %) (Table 6). Biomass intake by shags throughout the season was very low for all five fish species. Only D. annularis intake exceeded 100 kg for the whole season. For no fish species did the biomass consumed by shags exceed the fishing MPC. Cormorants consumed a considerable biomass of the five species, particularly S. aurata, D. labrax and Mugilidae. Biomass intake of D. labrax, Mugilidae and D. annularis by cormorants exceeded the fishery MPC.

DISCUSSIONTop

Shag diet was mainly based on small pelagic fish species, but demersal fish are also an important resource. The shag diet is more varied and focused on smaller prey than the cormorant diet during syntopy in the study area, but the size range of cormorant preys is larger. Cormorants fed mainly on demersal fish, so there is no sign of competition with shags throughout their syntopic period. Likewise, there is no suspicion of competition between shags and local fishermen. However, cormorants may compete with local fishermen for D. labrax, Mugilidae and, to a lesser extent, for D. annularis.

Composition of shag diet has been studied at different places and seasons in the Atlantic and the Mediterranean, mainly from otoliths in regurgitated pellets (Velando and Freire 1999Velando A., Freire J. 1999. Intercolony and seasonal differences in the breeding diet of European shags on the Galician coast (NW Spain). Mar. Ecol. Prog. Ser. 188: 225-236., Al-Ismail et al. 2013Al-Ismail S., McMinn M., Tuset V.M., et al. 2013. Summer diet of European shags Phalacocorax aristotelis desmarestii in southern Mallorca. Seabird 26: 8-23., Morat et al. 2014Morat F., Mante A., Drunat E., et al. 2014. Diet of Mediterranean European shag, Phalacrocorax aristotelis desmarestii, in a northwestern Mediterranean area: a competitor for local fisheries? Sci. Rep. Port-Cros Nat. Park 28: 113-132.), but also by assessing stomach content (Lilliendahl and Solmundsson 2006Lilliendahl K., Solmundsson J. 2006. Feeding ecology of sympatric European shags Phalacrocorax aristotelis and great cormorant P. carbo in Iceland. Mar. Biol. 149: 979-990.), or using combined methods (Harris and Wanless 1993Harris M.P., Wanless S. 1993. The diet of shag Phalacrocorax aristotelis during the chick-rearing period assessed by three methods. Bird Study 40: 135-139.). These studies agree on the variety in shag diet, revealing geographical differences in diet composition and biomass intake, and variations over time related to the life-cycle phase and resource availability. The diet of the Atlantic shag subspecies (P. a. aristotelis) is mainly composed of sand-eels (Ammodytes spp.), and some authors have therefore suggested some degree of specialization (Harris and Wanless 1993Harris M.P., Wanless S. 1993. The diet of shag Phalacrocorax aristotelis during the chick-rearing period assessed by three methods. Bird Study 40: 135-139., Velando and Freire 1999Velando A., Freire J. 1999. Intercolony and seasonal differences in the breeding diet of European shags on the Galician coast (NW Spain). Mar. Ecol. Prog. Ser. 188: 225-236.). Shag diet composition depends on habitat diversity in the foraging area, which will largely determine prey diversity and availability. Local environmental conditions strongly affect fish recruitment, which also influences species composition and abundance (Myers 1997Myers R.A. 1997. Recruitment variation in fish populations assessed using meta-analysis. In: Chambers R.C., Trippel E.A. (eds). Early life history and recruitment in fish populations. Fish and Fisheries Series 21. Pp. 451-467. Chapman and Hall, London (UK).). Availability of local resources at a given time seems to be the main driver of diet composition for shags (Carss 1993Carss D.N. 1993. Shags Phalacrocorax aristotelis at cage fish farms in Argyll, western Scotland. Bird Study 40: 203-211., Lilliendahl and Solmundsson 2006Lilliendahl K., Solmundsson J. 2006. Feeding ecology of sympatric European shags Phalacrocorax aristotelis and great cormorant P. carbo in Iceland. Mar. Biol. 149: 979-990.). In our case, prey availability was unknown, so we hypothesize that for the studied season shag must feed on the most abundant species. Therefore, they could be considered as truly adaptable opportunists. Not surprisingly, some authors suggest the possibility of studying local resource availability based on the diet composition of this bird (Barrett et al. 1990Barrett R.T., Røv N., Loen J., et al. 1990. Diets of Shags Phalacrocorax aristotelis and Cormorants P. carbo in Norway and possible implications for gadoid stock recruitment. Mar. Ecol. Prog. Ser. 66: 205-218., Barrett 1991Barrett R.T. 1991. Shags (Phalacrocorax aristotelis L.) as potential samplers of juvenile saithe (Pollachius virens (L.)) stocks in northern Norway. Sarsia 76: 153-156.). Some studies suggest that Atlantic shag is a predominantly benthic feeder (Wanless et al. 1998Wanless S., Grémillet D., Harris M.P. 1998. Foraging activity and performance of Shag Phalacrocorax aristotelis in relation to environmental characteristics. J. Avian Biol. 29: 49-54, Watanaki et al. 2008Watanaki Y., Daunt F., Takahashi A., et al. 2008. Microhabitat use and prey capture of a bottom-feeding top predator, the European Shag, shown by camera loggers. Mar. Ecol. Prog. Ser. 356: 283-293.). Our results revealed that in the study area shags fed predominantly on small-size pelagic fish (B. boops, Trisopterus sp.), though demersal resources (C. julis, D. annularis) were also important in their diet. These results agree with those of Al-Ismail et al. (2013)Al-Ismail S., McMinn M., Tuset V.M., et al. 2013. Summer diet of European shags Phalacocorax aristotelis desmarestii in southern Mallorca. Seabird 26: 8-23. studying shag diet in Mallorca (Balearic Islands) regardless of differences in the submerged habitat. In our study, the shag foraging area includes a vast Posidonia oceanica meadow, wide shallow sandy bottoms and, to a lesser extent, rocky reefs (MAPAMA 2017MAPAMA. 2017. Ministerio de Agricultura y Pesca, Alimentación y Medio Ambiente. Ecocartografía de Murcia. Comunidades marinas. http://www.mapama.gob.es/es/costas/temas/proteccion-costa/ecocartografias/ecocartografia-murcia.aspx). Most fish species identified here are totally or partially linked to the meadow, even small pelagic species (Cetinić et al. 2011Cetinić P., Škeljo F., Ferri J. 2011. Discards of the commercial boat seine fisheries on Posidonia oceanica beds in the eastern Adriatic. Sci. Mar. 75: 289-300.). Small-size B. boops, Trisopterus sp. and Spicara smaris form large shoals at different depths in the water column over the meadow canopy, where they find food and some shelter from predators. Therefore, these species may behave as purely pelagic but also as demersal (epibenthic) occasionally, and then shags may capture them both in the water column and near the bottom. Assignation of fish to a particular functional group is somewhat controversial, increasing discrepancies with regard to considering shags pelagic, demersal or benthic feeders. Nevertheless, most authors agree on the importance of the seabed in provisioning this bird, and also its foraging flexibility (Wanless et al. 1991bWanless S., Burger A.E., Harris M.P. 1991b. Diving depths of shags Phalacrocorax aristotelis breeding on Isle of May. Ibis 133: 37-42., Grémillet et al. 1998Grémillet D., Argentin G., Schulte B. et al. 1998. Flexible foraging techniques in breeding Cormorants Phalacrocorax carbo and Shags Phalacrocorax aristotelis: benthic or pelagic feeding? Ibis 140: 113-119., Cosolo et al. 2011Cosolo M., Privileggi N., Cimador B., et al. 2011. Dietary changes of Mediterranean shags Phalacrocorax aristotelis desmarestii between the breeding and post-breeding seasons in the upper Adriatic Sea. Bird Study 58: 461-472.).

Our study reveals that shags prey preferably on small pelagic fish and cormorants on demersal fish. Similar results were obtained by Lillendahl and Solmundsson (2006)Lilliendahl K., Solmundsson J. 2006. Feeding ecology of sympatric European shags Phalacrocorax aristotelis and great cormorant P. carbo in Iceland. Mar. Biol. 149: 979-990. in Iceland. Conversely, shag diet was more diverse than cormorant diet during their period of syntopy around Grosa Island than in Iceland. However, both species show a noteworthy dietary variability at different spatial and temporal scales. We estimated that shag daily biomass intake was slightly less (but the difference was not statistically significant) than that of cormorant, in agreement with the results of Grémillet et al. (1996Grémillet D., Wanless S., Harris M.P., et al. 1996. Determining food intake by great cormorants and European shags with electronic balances. J. Field Ornithol. 67: 637-648., 1998)Grémillet D., Argentin G., Schulte B. et al. 1998. Flexible foraging techniques in breeding Cormorants Phalacrocorax carbo and Shags Phalacrocorax aristotelis: benthic or pelagic feeding? Ibis 140: 113-119.. However, shag mean prey size was smaller than that of cormorant, so shags had to compensate for the small size of preys caught by intensifying catch effort and number of prey per feeding event to obtain a comparable biomass. Barrett et al. (1990)Barrett R.T., Røv N., Loen J., et al. 1990. Diets of Shags Phalacrocorax aristotelis and Cormorants P. carbo in Norway and possible implications for gadoid stock recruitment. Mar. Ecol. Prog. Ser. 66: 205-218. and Lillendahl and Solmundsson (2006)Lilliendahl K., Solmundsson J. 2006. Feeding ecology of sympatric European shags Phalacrocorax aristotelis and great cormorant P. carbo in Iceland. Mar. Biol. 149: 979-990. also found that cormorant preys tend to be larger than those of shag. Consistently, cormorants from our study area needed less than half the prey numbers of shags to achieve their daily intake, due to the ability of cormorant to hunt larger fish. Differences in mean prey size between shag and cormorant could be related to differences in bill size. Though mean prey size of cormorant is larger than that of shag, the former also hunted small prey frequently, mainly A. boyeri. This meant that their prey modal size was even smaller than that of shags. However, the contribution of those small fish to the diet of cormorant was very low in terms of biomass intake.

The differences in diet composition between shag and cormorant during syntopy were notable, and the species most represented in their diets also differed. Therefore, it seems that trophic competition, as we expected, did not occur between these two coexisting bird species around Grosa Island. Lillendahl and Solmundsson (2006)Lilliendahl K., Solmundsson J. 2006. Feeding ecology of sympatric European shags Phalacrocorax aristotelis and great cormorant P. carbo in Iceland. Mar. Biol. 149: 979-990. also noticed segregation in diets of Icelandic shags and cormorants in syntopy. A partial spatial segregation in our study area between the two coexisting birds with regard to their preferred fishing zones must also explain the lack of competition. While the shag is a strictly marine bird, cormorants forage both in the open sea and inside the coastal lagoon, and even in fresh water irrigation ponds and reservoirs on the mainland tens of kilometres inland (Farinós and Robledano 2010Farinós P., Robledano F. 2010. Structure and distribution of the waterbird community in the Mar Menor coastal lagoon (SE Spain) and relationships with environmental gradients. Waterbirds 33: 479-493.), where they prey on C. carpio. This freshwater fish represented a considerable fraction in their diet (about 10% in biomass). In Spain, C. carpio is considered an exotic invasive species included in eradication programmes (BOE 2013BOE. 2013. Real Decreto 630/2013, de 2 de Agosto, por el que se regula el Catálogo español de especies exóticas invasoras. Boletín Oficial del Estado 185: 56764-56786. http://www.boe.es/boe/dias/2013/08/03/pdfs/BOE-A-2013-8565.pdf), so its consumption by cormorants can be considered an ecosystem service (Constanza et al. 1997Constanza R., d’Arge R., de Groot R., et al. 1997. The value of the world’s ecosystem and natural capital. Nature 387: 253-260.). This pattern agrees with Mizutani et al. (1990)Mizutani H., Fukuda M., Kabaya Y., et al. 1990. Carbon isotope ratio reveals feeding behaviour of cormorants. The Auk 107: 400-403., who observed that large groups of great cormorants (>2000 individuals) tend to segregate spatially to forage over an environmental gradient, in our case alternating between marine waters, the coastal lagoon and inland freshwater bodies. Conversely, shags rarely enter the coastal lagoon and never forage in inland ponds, but forage in the open sea most of the time.

Considering the low shag population density, their low predation on FASP target species and the facts that most fishing effort is focused inside the lagoon where shags rarely forage, there is virtually no interaction between shag and fishermen in the study area. Morat et al. (2014)Morat F., Mante A., Drunat E., et al. 2014. Diet of Mediterranean European shag, Phalacrocorax aristotelis desmarestii, in a northwestern Mediterranean area: a competitor for local fisheries? Sci. Rep. Port-Cros Nat. Park 28: 113-132. did not observe major competition between shags and fisheries on the French Mediterranean coast either. However, in other places where shag population density is higher, they might affect commercially important fish stocks (Barrett et al. 1990Barrett R.T., Røv N., Loen J., et al. 1990. Diets of Shags Phalacrocorax aristotelis and Cormorants P. carbo in Norway and possible implications for gadoid stock recruitment. Mar. Ecol. Prog. Ser. 66: 205-218., Lillendahl and Solmundsson 2006Lilliendahl K., Solmundsson J. 2006. Feeding ecology of sympatric European shags Phalacrocorax aristotelis and great cormorant P. carbo in Iceland. Mar. Biol. 149: 979-990.). Unlike shag, cormorants enter and leave the Mar Menor frequently, investing considerable fishing effort inside the lagoon during autumn and winter months. Taking into account the FASP fishing effort for those months and the estimated cormorant biomass intake, our results reveal that cormorants may compete for some commercially targeted fish such as D. labrax, and Mugilidae species and, to a lesser extent, for D. annularis. The magnitude of this interaction might change depending on fish availability, fishing effort and variations in cormorant population density. However, such a high consumption of S. aurata by cormorants does not automatically mean there is competition over fish resources, in accordance with Östman et al. (2013)Östman Ö., Boström M.K., Bergström U., et al. 2013. Estimating competition between wildlife and humans: a case of cormorants and coastal fisheries in the Baltic Sea. PLoS ONE 8: e83763., especially if we consider that FASP beat the previous catch record for this species in the Mar Menor during the studied season (FASP, pers. comm). Regarding D. annularis, it seems that cormorants are more efficient than the recruitment to the fishing gear. A side-effect of the intense interaction between cormorants and fisheries is the high mortality of cormorants (about 10% of the wintering population in 2014), most of them young and sub-adult specimens trapped in fishing nets deployed in the Mar Menor (Zamora 2015Zamora D. 2015. III Censo de Aves Orilladas del Mar Menor 2013-2014. Asociación de Naturalistas del Sureste. Murcia, Spain. 56 pp. http://www.asociacionanse.org/medio-millar-de-aves-muertas-en-artes-de-pesca-en-el-mar-menor/20141130).

Geographical and temporal variability in diet composition of shags and cormorants may cause varied intensities of competition with fisheries (Östman et al. 2013Östman Ö., Boström M.K., Bergström U., et al. 2013. Estimating competition between wildlife and humans: a case of cormorants and coastal fisheries in the Baltic Sea. PLoS ONE 8: e83763.), from minimal (Liordos and Goutner 2007Liordos V., Goutner V. 2007. Diet of the great cormorant (Phalacrocorax carbo L. 1758) at two Greek colonies. J. Biol. Res. 7: 51-57.) to strong competition (Steffens 2011Steffens W. 2011. Great cormorant Phalacrocorax carbo is threatening fish populations and sustainable fishing in Europe. Am. Fish. Soc. Symp. Ser. 75: 1-12.). Measures to prevent economic impact on fisheries caused by cormorants are mostly focused on the control of nesting at breeding grounds through egg-oiling or nest destruction, and of population density at nesting and wintering places through harassment or culling. However, the effectiveness of all these measures is in question (Carss 2002Carss D.N. 2002. Reducing the conflict between Cormorants and fisheries on a pan-European scale (REDCAFE). Final Report. Natural Environmental Research Council. Centre for Ecology and Hydrology. http://www.intercafeproject.net/pdf/REDCAFEFINALREPORT.pdf, Taylor and Dorr 2003Taylor J.D., Dorr B.S. 2003. Double-crested cormorant impacts to commercial and natural resources. In: Fagerstone K.A., Witmer G.W. (eds) Proceedings of the 10th Wildlife Damage Management Conference, pp: 43-51.). At Grosa Island and in the Mar Menor area, no management actions are implemented to deal with this interaction. To the complaints of fishermen regarding cormorant catches, we must add those of conservationist organizations about the high fishing effort and accidental bird by-catches which include not only cormorant but also ducks, gulls and grebes (Zamora 2015Zamora D. 2015. III Censo de Aves Orilladas del Mar Menor 2013-2014. Asociación de Naturalistas del Sureste. Murcia, Spain. 56 pp. http://www.asociacionanse.org/medio-millar-de-aves-muertas-en-artes-de-pesca-en-el-mar-menor/20141130). Therefore, it seems obvious that the sustainability of natural resources will not have to focus only on controlling cormorant wintering population, but also on preventing fishing side-effects and managing fishing effort of both fishermen and cormorants.

ACKNOWLEDGEMENTSTop

The authors thank Beatriz López Pastor, Francisco García Castellanos, Ángel Sallent, Gonzalo G. Barberá, Pedro García and Mario León for their help in collecting pellets at nest and roost sites, and the Office of Socio-Economic Impact of the Environment (Department of Agriculture, Water and Environment of Murcia, Spain) for facilitating access to shag and cormorant breeding and roosting places. The authors are very grateful to the two reviewers for comments and suggestions that improved the final version of the manuscript. This research was funded by the Autonomous Government of Murcia, Spain (Department of Agriculture, Water and Environment) (Regional Programme co-funded by FEDER, project grant number RM-POI-07-043).

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