Using a Three-Isotope Bayesian Mixing Model to Assess The Contribution of Refuse Dumps in The Diet...

USING A THREE-ISOTOPE BAYESIAN MIXING MODEL TO ASSESS THE CONTRIBUTION OF REFUSE DUMPS

IN THE DIET OF YELLOW-LEGGED GULL LARUS MICHAHELLIS

UTILIZACIÓN DE UN MODELO DE MEZCLA BAYESIANO CON TRESISÓTOPOS PARA EVALUAR LA CONTRIBUCIÓN DE LOS VERTEDEROS

EN LA DIETA DE LA GAVIOTA PATIAMARILLA LARUS MICHAHELLIS

Aida ABDENNADHER1, 2 *, Francisco RAMÍREZ1, 3, Mohamed Salah ROMDHANE2,Lluis JOVER4 and Carolina SANPERA1

SUMMARY.— The yellow-legged gull Larus michahellis is usually considered as an opportunisticspecies that depends on food derived from anthropogenic activity, such as garbage and fishery discards.However, although it has become a problematic species in many Mediterranean countries, there is stillno information about its status in Tunisia. The aim of this work was to assess the differential use ofmarine and terrestrial resources by the yellow-legged gulls breeding in an urban area on Chikly Island.Dietary reconstructions were performed through the analysis of regurgitates and !13C, !34S and !15N offledgling’s feathers. Contrary to most Mediterranean breeding colonies, and to our expectations, themixing model showed that yellow-legged gulls from Chikly are above all marine foragers. Whereas theLake of Tunis was the principal source of food in 2005 and 2007, chicks from 2006 were fed mainlywith prey from the Gulf of Tunis. Although the Gulf is located further from the breeding colony and hasless fishing activity than the Lake, our study demonstrated that it is used as an alternative foraginghabitat. The Bayesian mixing model approach proved to be a useful tool for evaluating temporalvariations in the feeding ecology of the colony, which is a relevant information for the management ofa wild species. This study also demonstrated the importance of isotopic variability among years forinferring diet diversity and food availability for the colony, thereby allowing demographic forecastswhen trophic resources vary in abundance or the foraging habitat is disturbed.

Key words: carbon, nitrogen, open air dump, regurgitates, seabirds, stable isotopes, sulfur, Tunisia.

Ardeola 61(2), 2014, 297-309 DOI: 10.13157/arla.61.2.2014.297

1 Dept. Biologia Animal, Facultat de Biologia, Universitat de Barcelona, Diagonal 645, 08028Barcelona, Spain.

2 Unité de Recherche (UR03AGRO) Aquatic Resources and Ecosystems Laboratory,!Institut NationalAgronomique de Tunisie, Université de Carthage, 43 Avenue Charles Nicolle, 1082 Tunis-Mahrajèn, Tunisia.

3 Estación Biológica de Doñana (EBD-CSIC), Dept. Conservation Biology, C/ Américo Vespucios/n, 41092 Sevilla, Spain.

4 Dept. Salut Pública, Facultat de Medicina, Universitat de Barcelona, Casanova 143, 08036Barcelona, Spain.

* Corresponding author: [email protected]

INTRODUCTION

Several species of Laridae have shown highpopulation growth in the Mediterranean Seaduring recent decades. This increase is mainlyexplained by (1) their trophic plasticity andability to use resources generated by humanactivity, and (2) the increasing availability ofthese anthropogenic resources over recentyears (Bosch et al., 1994; Oro et al., 1995).The yellow-legged gull Larus michahellis hasbecome regular in many coastal cities, wherethe abundance of open rubbish dumps anddiscards from the fishing activity providessignificant food sources for this species(Duhem et al., 2007; Duhem et al., 2008;Sorace and Gustin, 2009). The yellow-leggedgull population of the western Mediterraneanhas increased by 10% annually (Duhem et al.,2007; Thibault et al., 1996; Vidal et al.,1998). The Yellow-legged gull is becomingproblematic in some localities because of itsinteraction with human activities such asaviation and agriculture, as well as its role inthe transport of pathogens, and its predation

on vulnerable and sensitive or protectedspecies (Finney et al., 2001). The study of thetrophic ecology of such a problematic speciesis key to understanding the demographicexpansion of its populations and to definingadequate environmental management policies(Einoder, 2009). Conventional methods fordietary reconstruction, such as analysis ofstomach contents, pellets or regurgitates,suffer from well-known limitations: notably,the time period over which dietary informationcan be inferred is short (< 1day) and dietaryestimation is biased towards bigger preythat are more resistant to digestion (Duffy andJackson, 1986; González-Solís et al., 1997;Votier et al., 2003). Nevertheless, such con-ventional tools are still necessary forobtaining data about taxonomic dietarycomposition. Analysis of regurgitates yieldsmore information than that of stomach contentsbecause regurgitated food has been morerecently consumed and is therefore less digested.

The analysis of naturally occurring stableisotopes of carbon (13C/12C, expressed as !13C),sulphur (34S/32S, expressed as !34S) and

Ardeola 61(2), 2014, 297-309

ABDENNADHER, A., RAMÍREZ, F., ROMDHANE, M. S., JOVER, L. and SANPERA, C.298

RESUMEN.—La gaviota patiamarilla Larus michahellis se considera una especie oportunista, quedepende de los recursos alimenticios generados por la actividad humana, como son la basura de losvertederos o los descartes de pesca. A pesar de que la gaviota patiamarilla se ha vuelto problemática envarios países del Mediterráneo, no existe información sobre su estado en Túnez. Este trabajo ha tenidocomo objetivo estudiar el uso diferencial de las fuentes tróficas por la población de gaviota patiamarillaque cría en Chikly, una isla sometida a gran presión urbana. Para reconstruir su dieta, se ha llevado acabo el análisis de regurgitados y de !13C, !34S y !15N en plumas de pollos. Al contrario de lo queesperábamos, teniendo como referencia lo que sucede en otras colonias del Mediterráneo, el modelo demezcla ha demostrado que la alimentación de la gaviota patiamarilla de Chikly es principalmente marina.Mientras el lago de Túnez ha sido la mayor fuente alimentaria durante 2005 y 2007, el golfo de Túnezlo fue durante 2006. Aunque el golfo está más lejos del sitio de cría y en él se dé una menor actividadpesquera, nuestro estudio ha demostrado que sigue siendo una fuente alimentaria alternativa. El modelode mezcla bayesiano ha resultado ser una herramienta con un gran potencial para evaluar los cambiosen la ecología trófica de esta colonia a lo largo de los años, un punto clave para la correcta gestión defauna salvaje. Por otro lado, cabe destacar la relevancia de la variabilidad temporal de las trazas isotópicaspara inferir la diversidad y disponibilidad de los distintos recursos para la colonia, permitiendo asíprevisiones demográficas cuando estos varían en abundancia o debido a la alteración del hábitat.

Palabras clave: aves marinas, azufre, carbono, isótopos estables, nitrógeno, regurgitados, Túnez,vertedero.

nitrogen (15N/14N, expressed as !15N) hasbecome increasingly common in the study ofthe trophic ecology of particular populations(Bearhop et al., 2004; Cherel et al., 2005;Hobson et al., 1994; Hobson and Cherel,2006) because it constitutes a relatively non-invasive way of obtaining time-integratedinformation on assimilated diets. Whereas!13C and !34S provide information on theexploited foraging habitats, such as ben-thic/pelagic or marine/continental (Dufourand Gerdeaux, 2001), !15N has been widelyused as a proxy for trophic level (Petersonand Fry, 1987). In addition, transformingisotopic information into dietary proportionsof isotopically distinct dietary sources is nowfeasible through the use of multi-sourceisotope mixing models (Moreno et al., 2010;Phillips, 2001; Phillips and Koch, 2002;Phillips et al., 2009; Ramos et al., 2009b,2011), which can provide more reliableinformation on trophic interaction.

The aim of this work was to evaluate thedifferential use of two marine habitats andlandfill by a colony of YLGs breeding onChikly Island: the Lake of Tunis, the Gulf ofTunis and landfill sites. Defining theimportance of each habitat being exploited bya population is fundamental for wildlifemanagement and conservation, sinceaccessibility to trophic resources and their useplays a key role in survival and reproductivesuccess. We therefore reconstructed the dietof the yellow-legged gull colony over threeyears by combining two complementarytechniques: the analysis of regurgitates offledglings and stable isotope analysis of theirgrowing mantle feathers. To determine thecontribution of each of the three foraginghabitats to the diet of the colony and theirvariation over time, we applied a mixingmodel for each monitored year.

Although similar studies have beencarried out on this species in the westernMediterranean (Moreno et al., 2010), this isthe first study on the North African coast.

MATERIAL AND METHODS

Study area

A study of the yellow-legged gull po-pulation breeding on Chikly Island was carriedout over three years (2005, 2006 and 2007).The island is in the northern part of the Lake ofTunis (36° 49’ N, 10° 13’ E), a brackish urbanlagoon surrounded by the capital city (fig. 1).The lake is divided into a northern and asouthern part by a navigation channel. TheLake of Tunis has a well-known history ofsevere eutrophication with resulting anoxia andmassive fish death, especially before therestoration work that was carried out in themid-1980s (Harbridge et al., 1976; Mastouriand Brahim, 1996). The northern part, whichcovers an area of 2,480 ha, continues to sufferintense human pressure, as it is the subject of agrowing urban development project. It alsoreceives water inputs from several rainfall-collecting channels, as well as from theadjacent Gulf of Tunis. The Gulf of Tunis ispart of the Mediterranean Sea, and extends overnearly 150 km between Cape Sidi Ali El Mekkiand the northeastern tip of the Cap Bonpeninsula (37° 0’ N, 10° 30’ E). The Tunisianlegislation on benthic fishing activities in theGulf of Tunis is very strict as this arearepresents a nursery for several fish species. Itis opened for only a few months per yeardepending on a decision taken yearly followingstudies of the status of fish stocks.

Sample collection

During the breeding periods of 2005, 2006and 2007, we collected growing mantlefeathers of 21, 40 and 25 fledglings, res-pectively. Spontaneous fledgling regurgitates(N = 16, 44 and 11, in 2005, 2006 and 2007,respectively) were also collected, individuallyplaced in sealed plastic bags and stored at"20ºC until laboratory analysis. Only one

Ardeola 61(2), 2014, 297-309

299TROPHIC ECOLOGY OF LARUS MICHAHELLIS

fledgling was sampled from each brood, toavoid pseudo-replication arising from parentsfeeding the same prey to all their offsprings.

Analysis of regurgitates

Regurgitate prey items were individuallyidentified to taxonomic order level and weighed(wet weight). With the aim of estimating the

contribution of the different foraging habitats tothe chick’s diet, food items were also classifiedaccording to their ecological categories: marineprey (including all fish and cuttlefish),landfill (including all kinds of domestic food),freshwater invertebrates, and terrestrial inver-tebrates. For each year and, in order to estimatethe relative importance of each category, bothprey biomass percentage (% B) and numericpercentage (% N) were estimated.

Ardeola 61(2), 2014, 297-309


FIG. 1.—Study area showing the breeding colony of yellow-legged gulls on Chikly island and bothmarine foraging habitats: the Lake and Gulf of Tunis.[Área del estudio en la que se muestra la colonia de cría de gaviota patiamarilla en la isla de Chikly,así como las áreas marinas de forrajeo: el lago y el golfo de Túnez.]

Mixing model

With the aim of estimating the relativeimportance of the different foraging habitatsfor gulls from the studied colony, we used athree-isotope approach (!13C, !34S and !15N),defining three endpoints: the Lake of Tunis,Gulf of Tunis and a terrestrial ecosystem. Thelast category was a source of mainly landfillitems and terrestrial invertebrates. We did notconsider freshwater invertebrates since theyconstituted a very small proportion in termsof both numeric and biomass percentage inthe diet of the colony (< 0.01%).

The stable isotope signatures of the threeforaging habitats (Gulf, Lake and terrestrialecosystem) were estimated using the stableisotope signatures of all prey found inregurgitates collected in the three years ofmonitoring. As marine prey found in fledglingregurgitates could have come from either theLake of Tunis or the Gulf of Tunis, we used ourresults from a previous study that allowed us toassign each prey item to its source based on its!34S (Abdennadher et al., 2011).

In order to ascertain the relative con-tribution of the different types of prey to theendpoint signature, we weighted prey isotopesignatures and elemental concentrations byprey fresh biomass.

We used a Bayesian stable-isotopemixing model (SIAR), which allowed theinclusion of the isotopic signatures of theconsumers, potential dietary resources, ele-mental concentrations and diet-tissue isotopicdiscrimination factors, along with the un-certainty of these values. We used means andstandard deviations for all diet-tissue isotopicdiscrimination factors except for S. S is lesscommonly used than C and N, and thus theliterature did not provide an SD, so we tookSD = 0 for the sulphur discrimination factor.The isotopic discrimination factors (mean ±SD) used in the model were obtained from theliterature: "13C = 1.15 ± 0.18 (Caut et al.,2009), "34S=1.3 (Ramos et al., 2009b;Peterson et al., 1987) and "15N = 2.91 ± 0.16(Caut et al., 2009). Estimations were obtainedusing the SIAR package (Parnell et al., 2008)for R (http://r-project.org).

Ardeola 61(2), 2014, 297-309


TABLE 1

Taxonomic analysis of regurgitated prey and their numeric (%N) and biomass percentage (%B) in thediet of yellow-legged gulls from Chikly colony.[Análisis taxonómico de las presas encontradas en los regurgitados, y sus importancias numéricas (%N)y de biomasa (%B) en la dieta de las gaviotas patiamarillas en la colonia Chikly.]

Year Index Marine prey Landfill Freshwater Terrestrialinvertebrate invertebrate

2005 %N 63.2% 26.3% 5.3% 5.3%%B 73.9% 22.8% < 0.01% 3.3%

2006 %N 75.9% 18.5% 5.6%%B 68.0% 25.1% 7.0%

2007 %N 83.3% 16.7%%B 78.4% 21.6%

Stable isotope analysis

Measurements of !13C, !34S and !15N offledgling feathers were carried out during thethree years. Feathers were initially washed in a0.25M sodium hydroxide solution and rinsedthoroughly in distilled water to remove anysurface contamination. Both feathers and preywere oven-dried at 60°C to constant weight andground to a fine and homogeneous powderusing an impactor mill (Freezer/mill6750 –Spex Certiprep) that operates at liquid nitrogentemperature. In order to reduce variability dueto differences in lipid content, individualisedprey from regurgitates were treated wholly andsubjected to lipid extraction by successiverinsing in a chloroform and methanol solution(2:1) (Folch et al., 1957; Logan et al., 2008).Sub-samples of the powdered feathers (0.36 mgfor !15N and !13C; 3.6 mg for !34S analyses)and prey (0.5 mg for !15N and !13C; 8 mg for!34S analyses) were packed in Sn capsules andcombusted for isotopic determination by EA-IRMS (Elemental Analysis-Isotope Ratio MassSpectrometry) using a ThermoFinnigan Flash1112 (for N and C)/1108 (for S) elementalanalyser coupled to a Delta isotope ratio massspectrometer via CONFLOIII interface (ServeiCientifico-Tècnics of the University ofBarcelona). Stable isotope ratios were expre-ssed in parts per thousand according to theconventional equation: !X (‰) = [(RSample /RStandard) - 1] * 1000, where !X (‰) is !13C,!15N or !34S, Rsample is the corresponding ratioof 13C/12C, 15N/14N or 34S/32S in the analysedtissue, and RStandard is the corresponding ratio of13C/12C, 15N/14N or 34S/32S related to the standardvalues. RStandard values for !13C, !15N and !34Swere those of Pee Dee Belemnite (PDB),atmospheric nitrogen (AIR) and CanyonDiablo Troilite (CDT), respectively. We usedinternational standards (IAEA) in each batch of12 samples to calibrate the system. Replicateassays of standard materials indicated standarddeviations of ± 0.1‰, ± 0.2‰ and ± 0.2‰, forcarbon, sulphur and nitrogen, respectively.

Statistical analysis

Normality of the stable isotope signatureswas visually checked using quantile plots.Comparison among years was done by meansof one-way analysis of variance (ANOVA),with Welch correction when appropriate toaccount for variance heterogeneity. Post-hocpairwise comparisons were performed byTukey’s or Tamhane’s procedure, dependingon whether or not the variances werehomogeneous. Statistical analysis was carriedout using SPSS 15.0.

RESULTS

Analysis of regurgitates

Identification of prey found in regurgitatesshowed that terrestrial invertebrates were onlypresent in 2005. Freshwater invertebrates madea minor contribution to the colony diet,especially during 2005, when their percentageof the biomass was very low (%B < 0.01%).

Marine prey and landfill categories werethe most recurrent and important in terms ofboth numeric and biomass indices (table 1).According to these indices, marine prey wasthe most important resource during the threeyears of the study.

Mixing model

Stable isotopes of prey, pooled together tocalculate endpoint means, are presented in table2. In order to disentangle the contribution of thetwo marine habitats together with the terrestrialecosystem to the diet of the colony, we applieda three-isotope Bayesian Mixing Model. Themixing model showed, in accordance with theanalysis of regurgitates, that regardless of theyear considered, use of the terrestrial ecosystemwas minor. The diet of the studied colonyconsisted mainly of marine prey from both theLake of Tunis and the Gulf. In 2005, Gulf use

Ardeola 61(2), 2014, 297-309


Ardeola 61(2), 2014, 297-309


TABL

E2

Identi

ficati

on, s

table

isotop

e sign

atures

(!13

C, !34

S, !15

N) an

d con

centr

ation

s (ca

rbon %

, nitr

ogen

%, s

ulphu

r %) o

f prey

foun

d in r

egurg

itates

ofye

llow-

legge

d gull

and p

ooled

toge

ther t

o calc

ulate

endp

oint m

eans

for e

ach f

oragin

g hab

itat u

sed by

yello

w-leg

ged g

ulls f

rom th

e Chik

ly Isl

and

colon

y. En

dpoin

t mea

ns ar

e esti

mated

by w

eighti

ng th

e fres

h weig

ht of

each

prey

.[Id

entif

icació

n, sig

natur

as is

otópic

as (#

13C,

#34S,

#15N)

y co

ncen

tracio

nes (

carb

ono %

, nitr

ógen

o %, a

zufre

%) d

e las

pres

as en

contr

adas

en lo

sreg

urgit

ados

y ag

rupa

das p

ara c

alcula

r la m

edia

para

cada

fuen

te ali

menta

ria us

ada p

or la

gavio

ta pa

tiama

rilla

de la

colon

ia de

la is

la de

Chik

y.La

s med

ias de

las f

uente

s alim

entar

ias se

estim

aron

pond

eran

do la

firma

isotó

pica d

e cad

a pres

a por

su pe

so fr

esco

.]

GULF

! 13C

‰! 15

N ‰

! 34S ‰

Carb

on %

Nitro

gen %

Sulph

ur %

Orde

rSp

ecies

Nme

ansd

mean

sdme

ansd

mean

sdme

ansd

mean

sd

Clup

eiform

eSa

rdina

sp.

5-17

.70.2

11.0

0.617

.80.3

41.2

2.513

.40.6

1.00.1

Unide

ntifie

d clup

eiform

e1

-13.7

10.8

17.4

28.2

6.90.6

Perci

forme

Diplo

dus a

nnula

ris2

-14.7

0.215

.60.5

18.4

0.435

.90.3

11.9

0.51.0

0.1Li

thogh

nathu

s mor

myru

s1

-13.4

13.5

16.3

34.3

11.3

1.1Tr

achu

russ

p.2

-18.5

0.310

.50.7

17.6

0.640

.70.3

13.1

0.41.1

0.0Un

identi

fied c

arang

idae

2-17

.00.1

12.2

0.017

.10.1

41.1

2.314

.00.4

1.80.8

Sepii

daSe

piasp

.4

-15.7

2.312

.11.4

17.6

1.037

.21.7

12.3

0.72.3

0.3En

dpoin

t valu

e-16

.41.9

12.0

1.717

.60.7

38.4

3.912

.51.7

1.40.6

LAKE

! 13C

‰! 15

N ‰

! 34S ‰

Carb

on %

Nitro

gen %

Sulph

ur %

Orde

rSp

ecies

Nme

ansd

mean

sdme

ansd

mean

sdme

ansd

mean

sd

Angu

illifor

mes

Angu

illa an

guilla

2-14

.31.0

13.8

0.212

.31.1

34.1

5.210

.62.5

0.40.6

Athe

rinifo

rmes

Athe

rinas

p.1

-20.7

13.6

7.831

.510

.10.0

Clup

eiform

esUn

identi

fied c

lupeif

orme

7-18

.11.2

14.2

2.611

.73.1

37.4

7.410

.92.2

0.70.5

Mug

iliform

esLiz

a aur

ata1

-19.7

13.6

12.5

43.2

13.7

0.0Li

za ra

mada

2-19

.10.6

11.8

2.811

.52.7

32.0

0.89.8

0.90.0

0.0M

ugils

p.1

-14.1

8.313

.742

.114

.11.1

Unide

ntifie

d mug

ilidae

12-18

.33.7

13.1

1.68.6

2.741

.44.4

13.2

1.50.5

0.6

Ardeola 61(2), 2014, 297-309


LAKE

! 13C

‰! 15

N ‰

! 34S ‰

Carb

on %

Nitro

gen %

Sulph

ur %

Orde

rSp

ecies

Nme

ansd

mean

sdme

ansd

mean

sdme

ansd

mean

sd

Perci

forme

Blen

nius p

avo

2-12

.10.6

14.0

1.613

.40.2

35.4

9.711

.13.4

0.00.0

Gobiu

s nige

r2

-14.7

0.813

.10.2

7.43.2

39.5

2.512

.70.7

1.40.2

Dice

ntrarc

hus l

abra

x1

-17.4

20.0

5.637

.512

.4Mu

lluss

p.1

-16.3

13.0

10.5

37.2

11.5

1.1Sc

ombe

r sco

mbru

s1

-18.9

10.4

13.7

Boop

s boo

ps1

-18.8

7.714

.038

.510

.30.8

Diplo

dus v

ulgar

is1

-16.4

15.0

14.4

41.0

13.4

0.9Lit

hogh

nathu

s morm

yrus

2-15

.63.7

12.0

2.414

.02.1

27.4

9.08.1

4.06.6

8.4Sc

orpaen

iform

eUn

identi

fied t

riglid

ae1

-16.3

11.2

14.9

24.2

7.70.0

Sepii

daSe

piasp.

13-12

.51.7

12.9

1.613

.62.6

37.1

10.4

11.6

4.02.0

1.0En

dpoin

t valu

e-16

.03.4

13.1

2.211

.53.3

37.4

7.611

.62.8

1.21.9

TERR

ESTR

IAL

! 13C

‰! 15

N ‰

! 34S ‰

Carb

on %

Nitro

gen %

Sulph

ur %

Orde

rSp

ecies

Nme

ansd

mean

sdme

ansd

mean

sdme

ansd

mean

sd

Dipte

raUn

identi

fied s

yrphid

ae4

-18.5

5.05.5

2.32.5

7.925

.16.3

5.42.8

0.90.4

Refus

eFo

od ty

peBr

ead

1-18

.83.5

6.340

.611

.81.0

Chee

se4

-17.5

4.55.5

1.27.5

5.036

.414

.09.9

5.11.0

0.3Do

mesti

cated

fowl

12-17

.62.8

6.11.3

6.33.0

37.0

5.89.8

2.71.0

0.4Un

defin

ed re

mains

1-13

.45.0

8.017

.02.4

0.6Pla

nt2

-24.7

0.95.5

0.07.0

1.439

.07.1

6.86.7

3.03.9

Endp

oint v

alue

-18.1

3.75.8

1.36.7

3,136

.28.6

9.33.8

1.11.2

TABL

E2

(cont.

)

was at its minimum, and use of the terrestrialresource peaked, in comparison with 2006 and2007. The contribution of the terrestrialresource varied between 29.5% (in 2006) and49.3% (in 2005). In 2006, the most exploitedfeeding habitat was the Lake of Tunis and theless used was the Gulf. The Lake of Tuniswas the most important foraging habitat usedby the yellow-legged gull colony during thethree years of the study. The contributions ofthe various sources and their 95% credibilityintervals are shown in figure 2.

Stable isotope analysis of fledgling feathers

The isotopic composition of fledglingfeathers showed a normal distribution in eachof the three years of the study. !15N showedno significant difference among years (!15N:F2!83 = 3.24, P = 0.72). On the contrary, !13Cand !34S showed a slight increase between2005 and 2006 (!13C: F2,!83 = 5.4, P = 0.006;!34S! : F2,! 81 = 4.5, P = 0.014), whereashomogeneous mean values were found in the2006 and 2007 breeding seasons (fig. 3).

Ardeola 61(2), 2014, 297-309


FIG. 2.—Contributions of the different foraging habitats to yellow-legged gull diet provided by theBayesian mixing model with 95%, 75% and 50% credibility intervals.[Diagrama de cajas generado por el SIAR revelando las contribuciones (%) de las diferentes fuentesde alimentación en la dieta de la gaviota patiamarilla proporcionadas por el modelo de mezclabayesiano, con intervalos de credibilidad al 95%, 75% y 50%.]

FIG. 3.—Isotopic signatures of fledgling feathers (!13C, !34S, !15N) from the colony of yellow-leggedgulls breeding on Chikly in 2005, 2006 and 2007.[Signaturas isotópicas (medias y desviaciones estándares, con intervalos de confianza al 95%) de lasplumas de pollos (#13C, #34S, #15N) de la colonia de cría de gaviota patiamarilla en Chikly durante2005, 2006 y 2007.]

DISCUSSION

During the three years of the study,fledgling feathers showed a slight butsignificant increase in isotopic signatures ofcarbon and sulphur between 2005 and 2006,pointing to an increased consumption ofmarine resources (!34S) and a greater use ofbenthic resources (!13C) in 2006 (Newsomeet al., 2007). This change from one year toanother could be explained by a change inprey availability, probably related to fisheryactivity. The yellow-legged gull is wellknown for its opportunistic behaviour andability to adapt its diet to the most readilyavailable resource (Duhem et al., 2007;González-Solís et al., 1997; Moulai, 2008;Oro et al., 1995). Even if yellow-legged gullsused the available resources differentlyduring the three years of monitoring, novariation was detected in !15N.

The analysis of prey from regurgitatesshowed that marine prey consumed by the gullsfrom the studied colony could have come fromthe Gulf or the Lake of Tunis. In addition, theanalysis of regurgitates showed that these twofood sources were used fairly constantly overthe three years, whereas terrestrial andfreshwater invertebrates were accessoryresources, consumed only occasionally. Theimportance of this prey appeared when lookingat numeric (%N) or biomass percentages (%B)of invertebrates: whereas %B indicated a smallcontribution of invertebrates to the colony diet,the %N was higher.

Knowing the isotopic signatures asso-ciated with the main foraging habitats usedby this generalist consumer, a three-isotopeBayesian mixing model allowed us toascertain the quantitative importance of thedifferent food sources available to the colony(Caut et al., 2009; Ramos et al., 2009b). Inagreement with the conventional approach(analysis of regurgitates), the isotopicanalysis suggested that marine prey was the

most important food resource of the colony.The mixing model also allowed us to knowthat marine prey consumed by the colonyduring the monitoring period came mostlyfrom the nearest aquatic habitat, the Lake ofTunis. Despite the availability of several openair dumps, yellow-legged gulls from theChikly colony seem to be mainly marineforagers, in contrast with other studies(Arizaga et al., 2013; Bosch et al., 1994;Moreno et al., 2010). In other Mediterraneanareas chicks are described as extremelydependent on open-air rubbish dumps(Duhem et al., 2007, 2008; Ramos et al.,2009a). The dietary contribution of marineprey (Lake and Gulf together) was majorthroughout the three years of the study, whilethe contribution of food of terrestrial originwas far less.

Combining conventional methods withstable isotope analysis provided an integratedview of the diet of the studied colony. Whileisotopic signatures yield data aboutassimilated food, analysis of regurgitates onlygives information about ingested food. Inaddition, stable isotope analysis providedinformation about the foraging habitatexploited which, when integrated into amixing model, allowed us to define theimportance of each of the available foodsources. Mixing models are widely used toprovide quantitative indices of food sourcecontributions to a diet (Moreno et al., 2010;Phillips and Koch, 2002). They require priorconventional diet analysis for a moreinformed selection of data for input into themixing model. As the colony has two marineforaging habitats available, the isotopicdiscrimination between prey from the Lake orthe Gulf (Abdennadher et al., 2011) was veryhelpful in estimating the importance of eachone, which would have been impossiblebased on taxonomic data alone. Thesimultaneous use of three isotopes in aBayesian SIAR mixing model showed a high

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discriminatory power for the study of ageneralist forager like the yellow-legged gull.Another study has compared results from aBayesian mixing model and an isosourcemixing model and has shown that the formeris more appropriate for the study of ageneralist diet (Moreno et al., 2010). Froma conservation perspective, knowing themain food source of the colony is essentialfor decision-making and environmentalmanagement. An isotopic approach hasproven to be a useful tool for evaluatingtemporal variation in the feeding ecology ofpopulations, and may become extremelyuseful for the management and conservationof wild species.

In summary, the analysis of regurgitateswas the most effective for taxonomicidentification but did not yield informationabout which foraging habitat was moreexploited. In contrast, the isotopic approachenabled us to identify changes in thecolony’s use of feeding resources over time.The mixing model showed that the Lake ofTunis was the most important source ofmarine prey for the studied colony, whosetrophic ecology could therefore benegatively affected by any environmentaldisturbance of this habitat. The coupling ofthe two techniques has resulted in a valuablecontribution to understanding the trophicecology of the yellow-legged gull. The dataobtained may be useful in preven-ting anyhuman disturbance or modification of thefeeding habitats exploited by the colony,particularly since its breeding area onChikly Island is submitted to such intenseanthropogenic pressure.

ACKNOWLEDGEMENTS.—This paper was sup-ported by a MAEC-AECI grant to Aida Abden-nadher. Funds were provided by AECI-PCISpanish–Tunisian projects A/2907/05 andA/6165/06 and project CGL 254 2008-05448-C02-01 (MICIN, Spain).

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Received: 26 December 2013Accepted: 9 August 2014

Editor: Rodrigo Vásquez

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