amphipod diversity at three tunisian lagoon complexes in relation to environmental conditions

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Amphipod diversity at three Tunisianlagoon complexes in relation toenvironmental conditionsRaja Jelassia, Martin Zimmerb, Hajer Khemaissiaa, Dieter Garbe-Schönbergc & Karima Nasri-Ammara

a Unité de Bio-écologie Systématique évolutive, Faculté desSciences de Tunis, El Manar II, Tunisiab FB Organismische Biologie, AG Ökologie, Biodiversität &Evolution der Tiere, Universität Salzburg, Salzburg, Austriac Institut für Geowissenschaften, ICP-MS Labor, Universität zu Kiel,Kiel, GermanyPublished online: 08 Aug 2013.

To cite this article: Raja Jelassi, Martin Zimmer, Hajer Khemaissia, Dieter Garbe-Schönberg& Karima Nasri-Ammar (2013) Amphipod diversity at three Tunisian lagoon complexes inrelation to environmental conditions, Journal of Natural History, 47:45-46, 2849-2868, DOI:10.1080/00222933.2013.792960

To link to this article: http://dx.doi.org/10.1080/00222933.2013.792960

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Journal of Natural History, 2013Vol. 47, Nos. 45–46, 2849–2868, http://dx.doi.org/10.1080/00222933.2013.792960

Amphipod diversity at three Tunisian lagoon complexes in relation toenvironmental conditions

Raja Jelassia*, Martin Zimmerb, Hajer Khemaissiaa , Dieter Garbe-Schönbergc andKarima Nasri-Ammara

aUnité de Bio-écologie Systématique évolutive, Faculté des Sciences de Tunis, El Manar II,Tunisia; bFB Organismische Biologie, AG Ökologie, Biodiversität & Evolution der Tiere,Universität Salzburg, Salzburg, Austria; cInstitut für Geowissenschaften, ICP-MS Labor,Universität zu Kiel, Kiel, Germany

(Received 15 March 2012; accepted 2 April 2013; first published online 8 August 2013)

The amphipod communities of different wetland types belonging to three coastallagoons complexes in northern Tunisia, Ichkeul (37◦06′ to 37◦14′ N, 09◦35′ to09◦56′ E), Ghar El Melh (37◦06′ to 37◦10′ N, 10◦08′ to 10◦14′ E) and Korba (36◦34′to 36◦38′ N, 10◦52′ to 10◦54′ E), were studied with respect to species compositionand abundance and their relationship with abiotic environmental characteristics,namely air and soil temperature and humidity, soil grain size and the soil con-tent of organic matter and heavy metals. Both highest abundance and highestdiversity of amphipods were observed in the lagoon complex of Ichkeul, which ischaracterized by higher contents of organic matter but also by higher heavy metalconcentrations in the soil than the lagoon complexes of Ghar El Melh and Korba.Although amphipod abundance does not seem to linearly depend on environmentalparameters, unimodal Canonical Correspondence Analysis suggests that amphipodabundance is related to grain size of the soil, to the soil content of organic matterand to several heavy metals.

Keywords: wetland; amphipod; diversity; abundance; heavy metals

Introduction

Coastal lagoons harbour a diverse fauna, but are threatened by intense anthropogenicexploitation and pollution (Lacaze 1996). As they receive continental freshwater fromtheir catchment area, many lagoons have been subjected to severe degradation ofwater quality caused by pollution and/or eutrophication (Benrjeb and Romdhane2002). In Tunisia, semi-closed shallow lagoons are among the most sensitive areas toenvironmental stresses (Romdhane 2001; Turki and Hamza 2001).

In general, lagoon sediments are considered reservoirs of many chemicalpollutants, especially heavy metals, which represent the most prominent marinepollution agents (Phillips and Rainbow 1994) affecting local communities andhuman health (Förstner and Wittmann 1981; Boucheseiche et al. 2002). Hence,quality management of marine coastal environments becomes a priority for manycountries.

*Corresponding author. Email: [email protected]

© 2013 Taylor & Francis

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mailto:[email protected]

2850 R. Jelassi et al.

On the other hand, many environmental contaminants are essential to vari-ous organisms at low concentrations. Essential metals include iron, magnesium,manganese, cobalt, zinc, copper (Viarengo 1985), arsenic, chromium, molybdenum,nickel, selenium, tin and vanadium (Rainbow 1988). All metals are taken up byaquatic organisms from solution and from food or particles (Rainbow 1990; Rainbowand Phillips 1993), and can be accumulated in body tissues at high concentrations(Rainbow 1988) at which, whether essential or not, they may become toxic to livingorganisms (Bryan 1976; Rainbow 1985, 1993, 1995; Rainbow et al. 1990).

The littoral environment is inhabited by a large variety of arthropods, each char-acterized by particular eco-physiological requirements. Their spatial and temporaldistribution has been investigated at the population level (Colombini et al. 2005; Jelassiet al. 2012; Khemaissia et al. 2012). The sandy and rocky littoral environments areecotones in which periodic and non-periodic changes in environmental conditions arepotentially stressful, modulating many of the physiological and behavioural activitiesof organisms (Branch and Branch 1981; McLachlan and Erasmus 1983; Chelazzi andVannini 1988; Raffaelli and Hawkins 1996; Lewis et al. 2007; Pelletier et al. 2011).

Talitrid amphipods represent one of the dominant macrofaunal elements of sandybeaches (McLachlan and Jaramillo 1995), exhibiting a wide geographical distribution(Dahl 1946) according to their ecological plasticity and a dynamic equilibrium with achanging environment (Marques et al. 2003). Their ecological relevance (Mews et al.2006; Graham and Richard 2008; Prato et al. 2009) prompted worldwide studies, forinstance with respect to their behavioural strategies (Fallaci et al. 1999) and plasticity(Scapini and Fasinella 1990; Scapini et al. 1993; 1995). Other studies focused on fac-tors influencing their spatial distribution and oriented movements in sandy beaches(Scapini and Quochi 1992; Borgioli et al. 1999; Scapini et al. 1999; Pelletier et al.2011), genetic comparisons among populations (De Matthaeis et al. 1995; Bulnheimand Schwenzer 1999), bioaccumulation (Weeks 1992; Fialkowski et al. 2000), responseto heat stress (Bedulina et al. 2010), and their role in biomonitoring (Moore et al. 1991;Fialkowski et al. 2000).

In this study, we focus on environmental factors that may control the spatial distri-bution of amphipods at a regional scale in three different lagoon complexes in northernTunisia. More specifically, we test whether station characteristics (temperature andhumidity of air and soil, organic matter content, grain size distribution of soil) oranthropogenic impact (heavy metal content of the soil) affect amphipod occurrenceand abundance.

Material and methods

Study stationsIn total, 12 stations with different anthropogenic activities situated in the north ofTunisia and belonging to different types of wetlands were studied (Figure 1). Thesetypes are (i) wadi or river: a natural watercourse, usually freshwater, flowing towardsan ocean, or lake, a sea or another river; (ii) lagoon: a stretch of salt water partially orcompletely separated from the open ocean by barriers of sand or coral; (iii) sebkha: asaline flat or salt-crusted depression, commonly found in North Africa – these areas,usually temporary and rarely permanent, are surrounded by salt-tolerant vegetation;(iv) garaa or lake: a body of relatively still fresh water of considerable size, localized in a

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Journal of Natural History 2851

Mediterranean Sea

S’1 S’2S’3

S’4

S’5

B

S’’1

S’’2

S’’3

C500m

Mediterranean Sea

Mediterranean Sea

S1

S2

S3

S4

A

Bizerte lagoon

Garaet Ichkeul

0 1km

0 1km

0 10km

N

KorbaC

BizerteA

B

100 Km

Figure 1. Sampling localities in northern Tunisia. (A) lagoon complex of Ichkeul (S1: thesupralittoral zone of Bizerte lagoon, S2: Korsi, S3: Tinja; S4: supralittoral zone of garaetIchkeul); (B) lagoon complex of Ghar El Melh (S′1: site 59 km from Tunis, S′2: the supralittoralzone of the old harbour, S′3: opposite to Boughaz, S′4: the supralittoral zone of Sidi Ali Mekkilagoon, S′5: the supralittoral zone of sebkha El Ouafi); (C) lagoon complex of Korba (S′′1:estuary river-beach of korba, S′′2: Lebna river, S′′3: the supralittoral zone of Korba lagoon).

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basin that is surrounded by land. Most lakes are fed and drained by rivers and streams.Four of these stations belong to the lagoon complex of Ichkeul (37◦06′ to 37◦14′ N,09◦35′ to 09◦56′ E), which is characterized by the presence of the Tunisian Society ofmussel rearing and the Tunisian steel company “El Fouladh”: the supralittoral zoneof Bizerte lagoon (S1: 37◦13′8.0′′ N, 09◦55.0′1.0′′ E), the supralittoral zone of Korsi[S2: contact between Bizerte lagoon and Tinja river (37◦11′12.5′′ N, 009◦46′52.3′′ E)],the supralittoral zone of Tinja [S3: contact between Tinja river and garaet Ichkeul(37◦10′10.2′′ N, 009◦45′26.6′′ E)], and the supralittoral zone of garaet Ichkeul (S4:37◦0.6′37.1′′ N, 009◦41′21.8′′ E). The lengths of the supralittoral zone of these stationswere 28 m, 13 m, 14.5 m and 13 m, respectively. Five stations belong to the lagooncomplex of Ghar El Melh (37◦06′ to 37◦10′ N, 10◦08′ to 10◦14′ E): the supralittoralzone of site 59 km from Tunis (S′1: 37◦10′03.1′′ N, 010◦09′57.7′′ E), the supralittoralzone of the old harbour (S′2: 37◦10′04.7′′ N, 010◦11′40.0′′ E), the supralittoral zoneof opposite to Boughaz (S′3: 37◦10′09.4′′ N, 010◦13′12.6′′ E), the supralittoral zoneof Sidi Ali Mekki lagoon (S′4: 37◦09′50.7′′ N, 010◦14′45.1′′ E) and the supralittoralzone of sebkha El Ouafi (S′5: 37◦09′22.7′′ N, 010◦13′38.7′′ E); the lengths of thesestations were 38 m, 22 m, 8.5 m, 23.5 m and 15 m, respectively. In this lagoon com-plex, we noted the presence of new and old harbours. Three stations belong to thelagoon complex of Korba (36◦34′ to 36◦38′ N, 10◦52′ to 10◦54′ E): the supralittoralzone of the estuary river-beach of Korba (S′′1: 36◦38′58.5′′ N, 010◦54′57.4′′ E) (15 m),the supralittoral zone of Lebna river (S′′2: 36◦39′13.8′′ N, 010◦54′31.3′′ E) (20.5 m)and the supralittoral zone of Korba lagoon (S′′3: 36◦38′12′′ N, 010◦54′11′′ E) (16 m).The lagoon complexes of Ichkeul and Ghar El Melh are characterized by a halophilicvegetation of Obione portulacoides, Salicornia arabica, Suaeda maritima, Cymodoceanodosa, and some algae, whereas only Obione portulacoides (S′′3), Posidonia oceanicaand different algae (S′′1) inhabit the lagoon complex of Korba. In the lagoon com-plex of Korba, we noted the presence of preserving industries and a water purificationstation.

Field study and laboratory analysisQuantitative samples of amphipods (n = 1207) were taken in spring (April 2010) dur-ing 10 consecutive days in the early morning hours. In the supralittoral zone of eachsite, eight quadrats of 50 × 50 cm2 were randomly placed (Figure 2). The contentof each quadrat (7-cm depth) was placed in an individual bag, and then the ani-mals were sorted by hand. Twenty minutes were devoted to each quadrat. Humidityand temperature of air and soil were measured in situ at each site. At the laboratory,amphipod specimens were preserved in 70% ethanol. Afterwards, they were identified,counted and sexed. The identification of these species was carried out under a LeicaMS 5 binocular microscope, using the key by Ruffo (1993).

Soil analysisAt each of 12 stations, three soil samples spaced at least 5 m from each other weretaken from a depth of 0 to 10 cm and subsequently homogenized to form a single com-posite sample. Grain size distribution of these composite samples was analysed usingdifferent sieves in descending order (2 mm, 630 µm, 250 µm, 160 µm, 25 µm). A sub-sample of the composite sample was brought to the ICPMS laboratory at University

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1

2

3

BarrierShoreline

Water

Roa

d

Length

4

Figure 2. Sampling method in the supralittoral zone of different stations; (1, 2, 3, 4: quadrats).

of Kiel and sieved to obtain the < 250-µm grain size fraction which was then dried andmilled (Bat and Raffaelli 1999). Heavy metals were extracted from a 250-mg sample ofpowder with 10 ml 7M nitric acid on a hot plate at 80◦C (2.5 h). The solution was madeup to 20 ml, centrifuged at 3200 g for 15 min, and the supernatant was transferredto a 20-ml sample vial. The metals vanadium (V), chromium (Cr), manganese (Mn),cobalt (Co), nickel (Ni), copper (Cu), zinc (Zn), arsenic (As), cadmium (Cd), tin (Sn),thallium (Tl), lead (Pb), and lithium (Li), rubidium (Rb) and strontium (Sr) were anal-ysed by inductively coupled plasma-mass spectrometry (ICP-MS). Average analyticalreproducibility was estimated from replicate analyses of some samples and was foundto be better than 2% RSD (1 sigma relative standard deviation) for all elements. Theaccuracy of analytical results was monitored by analysing certified reference materials(CRM): GSMS-2 (marine sediment; Chinese Academy of Geological Sciences, China)and PACS-1 (coastal sediment; NRCC Canada) as unknowns along with the samples.Results for these CRM are included in Table 1. Organic matter content was determinedby weighing before and after ashing at 450◦C for 3 h at the University of Salzburg.

Data analysisTo compare the amphipod community structure among stations, different faunisticparameters were calculated for this community using quantitative data: species rich-ness (S) expressed by the number of species at each station, relative species abundance(Ar = (ni/N)∗100) where ni is the number of individuals of each species and N is the

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Tab

le1.

Hea

vym

etal

cont

ent

(in

ppm

)of

soil

from

diff

eren

tco

llect

ion

site

sin

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hern

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isia

.

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hium

Van

adiu

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ium

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inc

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enic

Rub

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mSt

ront

ium

Cad

miu

mT

inT

halli

umL

ead

S19.

865

26.0

1726

.393

281.

748

6.05

717

.998

24.2

3410

8.24

96.

003

11.4

1943

3.49

80.

366

0.19

20.

123

58.2

49S2

0.51

40.

960

<1

17.3

76<

0.05

00.

488

<0.

28.

326

<1

0.65

588

.791

0.06

01.

019

0.02

24.

062

S36.

664

19.3

8113

.763

235.

235

5.12

112

.725

9.63

057

.766

5.13

58.

543

205.

089

0.19

80.

148

0.08

342

.668

S47.

006

13.6

7213

.325

1810

6.76

115

.984

14.2

6113

1.95

54.

211

8.18

027

0.23

20.

678

<0.

050

0.17

047

.060

S′1

5.45

523

.853

20.0

6822

9.45

54.

820

12.8

9439

.098

54.3

175.

879

8.63

030

7.06

30.

458

0.21

40.

115

34.6

42S′

21.

308

8.43

35.

958

93.1

601.

914

5.79

99.

587

26.3

574.

424

2.48

826

6.02

60.

096

0.20

30.

036

20.5

51S′

32.

016

11.1

046.

952

94.3

412.

233

5.71

410

.036

34.0

146.

933

2.77

633

5.96

90.

119

0.10

30.

057

26.7

84S′

4−0

.358

1.52

90.

902

16.4

170.

371

0.49

9<

22.

857

1.94

90.

205

132.

335

0.01

0<

0.05

00.

008

1.32

4S′

52.

131

10.4

347.

138

135.

357

3.15

06.

858

15.8

2736

.037

6.49

92.

969

531.

115

0.18

10.

121

0.05

236

.324

S′′ 1

2.86

77.

385

4.69

057

.569

1.82

63.

794

5.39

910

.734

2.32

04.

728

146.

315

0.03

90.

174

0.03

34.

467

S′′ 2

3.92

811

.062

7.01

310

1.96

63.

443

6.30

75.

836

19.9

121.

614

5.60

624

8.96

90.

066

0.15

90.

034

4.92

5S′

′ 39.

971

23.1

5416

.012

271.

508

8.31

114

.890

11.4

7037

.963

2.47

715

.814

162.

956

0.10

50.

324

0.09

812

.896

GSM

S-2

reco

mm

ende

d51

101

5943

15.6

8381

167

357

137

7.10

073

298

0.25

02.

437

1.15

837

GSM

S-2

mea

sure

d31

.340

48.6

4320

.117

4642

.706

86.3

5417

6.07

630

4.43

211

6.36

25.

286

20.6

6025

2.71

80.

210

0.95

10.

861

35.9

65

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total number of amphipods at each station. Mean density of the amphipod communityat each station and the mean density of each species at each station were expressed asnumber of individuals per m2. Species diversity and evenness were calculated by theShannon–Weaver index (H′ = − �pi log2 pi) (Frontier 1983) (with pi = ni/N) andPielou′s evenness index (J ′ = H ′/log2 S) (Pielou 1966), respectively.

The degree of similarity between sampling stations was evaluated using similaritycluster dendrograms. For this analysis, the data matrix consisting of total abundancesof species at each site was converted into a symmetric matrix using the Bray–Curtissimilarity index. The similarity matrix was agglomerately clustered using completelinkage based on presence/absence of species. The analysis above was performed withthe PRIMER software package (Clarke and Warwick 1994). Differences in abundanceand densities among lagoons and between within-lagoon stations were tested usingKruskall–Wallis Rank tests. Correspondence analysis of amphipod distribution andsite characteristics was performed using PAST software.

Results

Heavy metalsThe lowest values of most heavy metals were found at the supralittoral zone of Korsi(Table 1) with vanadium, chromium, cobalt, copper, arsenic being equal to 0.960 ppm,< 1 ppm, < 0.050 ppm, < 0.200 ppm, < 1 ppm, respectively, and at the supralittoralzone of Sidi Ali Mekki lagoon (S′4) having manganese, nickel, zinc, cadmium, tin,thallium and lead equal to 16 ppm, 0.500 ppm, 2.900 ppm, 0.010 ppm, < 0.050 ppm,0.008 ppm and 1.300 ppm, respectively. On the other hand, the supralittoral zone ofBizerte lagoon (S1) was characterized by high concentrations of vanadium (26 ppm),chromium (26.400 ppm), nickel (18 ppm) and lead (58.200 ppm). High concentra-tions of manganese (1810 ppm), zinc (132 ppm), cadmium (0.678 ppm) and thallium(0.170 ppm) characterized Ichkeul lake (S4). The maximum concentration for cobalt(8.300 ppm) was measured at the supralittoral zone of Korba lagoon. A maximumcontent of copper (39.100 ppm) characterized the supralittoral zone of the site 59 kmfrom Tunis, the maximum contents of arsenic (6.930 ppm) and tin (1.019 ppm) werefound at the supralittoral zone of opposite to Boughaz, and at the supralittoral zoneof Korsi, respectively.

Organic matter and grain sizeThe highest percentage of organic matter was observed in the lagoon complex ofIchkeul. In this complex, organic matter varied between 0.60% in Korsi (S2) and 12.2%in the supralittoral zone of Tinja river (S3). In Ghar El Melh it ranged between 0.60%in the supralittoral zone of Sidi Ali Mekki (S′4) and 7.22% in the site 59 km from Tunis(S′1). In the lagoon complex of Korba, organic matter was 7.14% in the supralittoralzone of the estuary river-beach Korba, 4.06% in the supralittoral zone of Lebna riverand 4.02% in the supralittoral zone of Korba lagoon (Table 2). These sampling stationsdiffered in substratum composition, ranging from loamy sand (S1, S3, S4, S′1, S′2 andS′′3) to sandy loam (S2, S′3, S′5, S′′1 and S′′2) and sandy-silt-loam (S′4) (Figure 3,Table 2).

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2856 R. Jelassi et al.T

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009◦ 4

6′ 52.

3′′ ESa

ndy-

loam

0.58

29.5

27.3

6972

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◦ 10′ 1

0.2′′ N

009◦ 4

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oam

y-sa

nd12

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rE

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◦ 10′ 0

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oam

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oam

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3534

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◦ 10′ 0

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Sand

y-L

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S′′ 336

◦ 38′ 1

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sand

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6370

Not

es:S

1:th

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ofB

izer

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the

supr

alit

tora

lzon

eof

Kor

si,S

3:th

esu

pral

itto

ralz

one

ofT

inja

;S4:

the

supr

alit

tora

lzo

neof

gara

etIc

hkeu

l,S′ 1

:the

supr

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tora

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site

59km

from

Tun

is,S

′ 2:t

hesu

pral

itto

ralz

one

ofth

eol

dha

rbou

r,S′ 3

:the

supr

alit

tora

lzo

neof

oppo

site

toB

ough

az,

S′ 4:

the

supr

alit

tora

lzo

neof

Sidi

Ali

Mek

kila

goon

,S′ 5

:th

esu

pral

itto

ral

zone

ofse

bkha

El

Oua

fi,S′′ 1

:th

esu

pral

itto

ralz

one

ofes

tuar

yri

ver-

beac

hof

korb

a,S′′ 2

:the

supr

alit

tora

lzon

eof

Leb

nari

ver,

S′′ 3:t

hesu

pral

itto

ralz

one

ofK

orba

lago

on.

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Clay

80 60 40 20100

Clay

Silty Clay

Silty Clay Loam

Silt LoamSandy Silt Loam

Clay Loam

Sandy Loam

Sandy Clay Loam

Sandy Clay

S2, S‘3, S‘5, S“1, S‘‘2 S‘4

Figure 3. Granulometry of different sampling sites. S1: the supralittoral zone of Bizerte lagoon,S2: Korsi, S3: Tinja; S4: supralittoral zone of garaet Ichkeul, S′1: site 59 km from Tunis, S′2: thesupralittoral zone of the old harbour, S′3: opposite to Boughaz, S′4: the supralittoral zone ofSidi Ali Mekki lagoon, S′5: the supralittoral zone of sebkha El Ouafi, S′′1: estuary river-beachof korba, S′′2: Lebna river, S′′3: the supralittoral zone of Korba lagoon.

Species richness, diversity and similarityA total of eight species of talitrid amphipods were collected, namely Orchestia mon-tagui Audouin, 1826, Orchestia mediterranea Costa, 1853, Orchestia gammarellus(Pallas, 1766), Orchestia stephenseni Cecchini, 1928, Orchestia cavimana Heller,1865, Platorchestia platensis (Kroyer, 1845), Deshayesorchestia deshayesii (Audouin,1826) and Talitrus saltator (Montagu, 1808). All of these eight species were collectedat the lagoon complex of Ichkeul, four of them were caught at the lagoon complex ofGhar El Melh, and only one species, T. saltator, was collected at the lagoon complexof Korba (Table 3).

The highest diversity of amphipods was observed at the Ichkeul lagoon complex,especially at the supralittoral zone of Bizerte lagoon (S1) (H′ = 2.779; J′ = 0.926)(Table 3). In contrast, the lowest diversity was observed in the supralittoral zone ofSidi Ali Mekki (H′ = 1.287; J′ = 0.811) (Table 3). According to the Bray–Curtis index,stations were clustered with respect to the distribution and the presence/absence ofdifferent species. Two clusters were distinguished that were represented by stationsbelonging to Northern Tunisia (lagoon complexes of Ichkeul and Ghar El Melh) versus

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Tab

le3.

Som

eec

olog

ical

para

met

ers:

spec

ies

rich

ness

(S),

Cou

nt(N

),re

lati

veab

unda

nce

(%)

dive

rsit

yin

dice

s(H

′ :Sh

anno

n–W

iene

rin

dex;

J′ :ev

enne

ssin

dex)

ofam

phip

odco

mm

unit

ies

atdi

ffer

ent

sam

plin

gsi

tes.

Typ

eof

lago

ons

Site

sS

Orc

hest

iam

onta

gui

Orc

hest

iam

edit

erra

nea

Orc

hest

iaG

amm

arel

lus

Orc

hest

iast

ephe

nsen

iO

rche

stia

cavi

man

aP

lato

rche

stia

plat

ensi

sD

esha

yeso

rche

stia

desh

ayes

iiT

alit

rus

salt

ator

N/si

tes

J′H

′

Ichk

eul

S18

17.2

%25

.7%

18.8

%13

.3%

7.0%

7.9%

6.2%

3.9%

483

0.92

72.

779

S26

−19

.6%

13.5

%12

.3%

−21

.6%

16.6

%16

.0%

162

0.99

22.

564

S35

−22

.4%

19.4

%−

−37

.3%

3.0%

17.9

%67

0.92

62.

151

S45

−26

.5%

17.1

%19

.4%

−19

.4%

17.6

%−

170

0.99

22.

302

Gha

rE

lM

elh

S′1

1−

−10

0.0%

−−

−0

−1

−−

S′2

4−

39.1

%41

.3%

10.9

%−

8.7%

0−

920.

885

1.71

1S′

34

−22

.0%

24.4

%29

.3%

−24

.4%

0−

820.

993

1.98

8S′

41

−−

100.

0%−

−−

0−

10.

811

1.28

7S′

53

−46

.7%

46.7

%−

−−

6.7%

−15

−−

Kor

baS′

′ 11

−−

−−

−−

−10

0.0%

134

−−

S′′ 2

0−

−−

−−

−−

−−

−−

S′′ 3

0−

−−

−−

−−

−−

−−

N/sp

ecie

s83

278

222

152

3415

790

191

1207

Not

es:S

1:th

esu

pral

itto

ralz

one

ofB

izer

tela

goon

,S2:

the

supr

alit

tora

lzon

eof

Kor

si,S

3:th

esu

pral

itto

ralz

one

ofT

inja

;S4:

the

supr

alit

tora

lzon

eof

gara

etIc

hkeu

l,S′

1:th

esu

pral

itto

ralz

one

ofsi

te59

kmfr

omT

unis

,S′ 2

:the

supr

alit

tora

lzon

eof

the

old

harb

our,

S′3:

the

supr

alit

tora

lzon

eof

oppo

site

toB

ough

az,S

′ 4:t

hesu

pral

itto

ralz

one

ofSi

diA

liM

ekki

lago

on,S

′ 5:t

hesu

pral

itto

ralz

one

ofse

bkha

ElO

uafi,

S′′ 1

:the

supr

alit

tora

lzon

eof

estu

ary

rive

r-be

ach

ofko

rba,

S′′ 2

:the

supr

alit

tora

lzon

eof

Leb

nari

ver,

S′′ 3

:the

supr

alit

tora

lzon

eof

Kor

bala

goon

.

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S3

S2

S1

S’3

S’2

S4

S’ 4

S’5

S’1

S’’1

100806040200Similarity (%)

Figure 4. Cluster analysis of the spatial distribution of Talitridae in different sites (Bray–Curtisindex, presence/absence, complete linkage). S1: the supralittoral zone of Bizerte lagoon, S2:Korsi, S3: Tinja; S4: supralittoral zone of garaet Ichkeul, S′1: site 59 km from Tunis, S′2: thesupralittoral zone of the old harbour, S′3: opposite to Boughaz, S′4: the supralittoral zone ofSidi Ali Mekki lagoon, S′5: the supralittoral zone of sebkha El Ouafi, S′′1: estuary river-beachof korba, S′′2: Lebna river, S′′3: the supralittoral zone of Korba lagoon.

stations belonging to Cap Bon (lagoon complex of Korba at the northeastern shore ofTunisia). The first cluster could be divided into three sub-clusters. Hence, stations thatbelong to the same lagoon complex were more similar, with a similarity close to 77%for Ichkeul (Figure 4).

Count, relative abundance and occurrence frequencyConsidering the three lagoon complexes with a total of 1207 amphipod specimens,Ichkeul revealed the highest amphipod abundance (n = 882). Here, Bizerte lagoonharboured the highest number of individuals (n = 483). At the lagoon complex of GharEl Melh, the highest number of animals was found in the old harbour (n = 92) andBoughaz (n = 82). The total number of animals in this complex was 191 individuals,but it was significantly lower (n = 134) in the lagoon complex of Korba (χ2 = 587.33;df = 2; p = 0) (Table 3).

Orchestia mediterranea and P. platensis were the most abundant species in thelagoon complex of Ichkeul especially in S1 (25.7 %) and S4 (26.5 %) for the first speciesand in S2 (21.6%) and S3 (37.3%) for the second species, whereas in the lagoon com-plex of Ghar El Melh, O. gammarellus (100% in S′1 and S′5) and O. stephenseni (29.3%in S′3) were the most abundant species. Talitrus saltator is the only species that wascollected at the lagoon complex of Korba (Table 3).

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Overall, O. mediterranea, O. gammarellus and P. platensis were found at more thansix stations and were qualified as constant species. Orchestia stephenseni, T. saltatorand D. deshayesii were qualified as accessory species, while O. cavimana and O. mon-tagui were collected only at the supralittoral zone of Bizerte lagoon and were qualifiedas accidental species (c.f. Table 3).

Density of amphipod communitiesThe mean density of amphipod communities at different study stations was calcu-lated. On a smaller spatial scale, highest mean densities were found at the supralittoralzone of Bizerte lagoon (S1, lagoon complex of Ichkeul) with 242 ± 235 ind. m−2.For the other stations, mean densities reached 81 ± 62.8 ind. m−2 at Korsi (S2),34 ± 32.7 ind. m−2 at Tinja (S3) and 85 ± 93.3 ind. m−2 at Garaet Ichkeul (S4)(Figure 4A). Within the lagoon complex of Ghar El Melh, mean densities were higherat the old harbour (S′2) (46 ± 68.1 ind. m−2) and Boughaz (S′3) (41 ± 40.9 ind. m−2)than at the sampling stations of Sidi Ali Mekki (S′4), Km59 (S′1) and sebkha ElOuafi (S′5) with mean densities of 7.5 ± 14.3 ind. m−2, 0.5 ± 1.4 ind. m−2 and0.5 ± 1.4 ind. m−2 respectively (χ2 = 18.497; df = 4, p = 0.001) (Figure 5A).Stations within the lagoon complex of Korba differed from each other with respectto mean density (χ2 = 8.586; df = 2, p = 0.01), with the estuary river beach of Korba(S′′1) harbouring most amphipods (67 ind. m−2) (Figure 5A).

Orchestia gammarellus reached the highest density in the supralittoral zone of thestation 59 km from Tunis (S′1) (0.5 ind. m−2), of old harbour (S′2) (19 ind. m−2), ofSidi Ali Mekki (S′4) (3.5 ind. m−2) and sebkha El Ouafi (S′5) (0.5 ind. m−2). In thesupralittoral zone of Bizerte lagoon and of Ichkeul Lake, it was rather O. mediterraneathat had the highest densities of 62 ind. m−2 and 22.5 ind. m−2, respectively. Moreover,the highest densities were observed for P. platensis in Korsi (S2) (17.5 ind. m−2) andTinja (S3) (12.5 ind. m−2), for O. stephenseni in opposite to Boughaz (S′3) (12 ind. m−2)and for T. saltator in the estuary river beach of Korba (S′′1) (67 ind. m−2) (Figure 5B).

Detrended and canonical correspondence analysisUnconstrained ordination of species through detrended correspondence analysis withenvironmental parameters subsequently projected to the ordination diagram (Figure 6)revealed Eigenvalues of 0.275 and 0.088 for axes 1 and 2, respectively. Based on this, wecalculated a direct constrained ordination (constrained correspondence analysis) tak-ing into account the variation in species composition that is explained by the measuredenvironmental parameters (Figure 7). Axis 1 (λ = 0.689) most strongly correlated withthe soil contents of thallium, cadmium, zinc and coarse sand, and explained 71% ofspecies abundance at different sites. Axis 2 (λ = 0.161), most strongly correlated withair humidity and the soil contents of lithium, rubidium and tin, and added another17% of explanation. Stepwise reducing the number of potentially redundant, i.e. cor-related, environmental parameters through backward selection to reduce arching ofthe second axis, owing to the quadratic dependence of the second axis on the first one(Lepš and Šmilauer 2003), did not increase the explanatory value of the constrainedcorrespondence analysis above 88% (not shown).

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0

125

250

S1 S2 S3 S4 S'1 S'2 S'3 S'4 S'5 S"1 S"2 S"3

Mea

n de

nsity

(in

d. m

–2)

Sites

Figure 5. Mean densities of amphipod community (A) and mean density of each species (B)at each site.(S1: the supralittoral zone of Bizerte lagoon, S2: Korsi, S3: Tinja; S4: supralit-toral zone of garaet Ichkeul, S′1: site 59 km from Tunis, S′2: the supralittoral zone of the oldharbour of Ghar El Melh, S′3: opposite to Boughaz, S′4: the supralittoral zone of Sidi AliMekki lagoon, S′5: the supralittoral zone of sebkha El Ouafi, S′′1: estuary river-beach of korba,S′′2: Lebna river, S′′3: the supralittoral zone of Korba lagoon, O. mon: Orchestia montagui,O. med: Orchestia mediterranea, O. g: Orchestia gammarellus, O. s: Orchestia stephenseni, O. c:Orchestia cavimana, P. p: Platorchestia platensis, D. d: Deshayesorchestia deshayesii, T. s: Talitrussaltator).

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400

200

–200

100 200 300

P.p

T.s

O.mon

O.med

O.gO.s

D.d

O.c

fine sand

coarse sand

silt & clay

Hsoil

Hair

Tair

Tsoil

Axis 1

Axis

2

Figure 6. Species ordination through Detrended Correspondence Analysis. Dots depict species;arrows assign environmental factors, subsequently projected to the ordination diagram. Arrowswithout label represent heavy metals. Eigenvalues: λ (axis 1) = 0.275; λ (axis 2) = 0.088. O. mon:Orchestia montagui, O. med: Orchestia mediterranea, O. g: Orchestia gammarellus, O. s: Orchestiastephenseni, O. c: Orchestia cavimana, P. p: Platorchestia platensis, D. d: Deshayesorchestiadeshayesii, T. s: Talitrus saltator.

From linear correlations of amphipod abundances and station characteristics,we obtained slightly different explanations of amphipod distribution at our sam-pling stations. The abundance of several amphipod species significantly (p < 0.05:O. mediterranea, O. gammarellus, O. stephenseni, P. platensis, D. deshayesii) ormarginally (p < 0.1: O. montagui, O. cavimana) correlated with the soil content ofzinc. Further, the abundances of O. mediterranea, O. gammarellus and O. stephensenisignificantly (p < 0.05) correlated with the soil lead content, and O. montagui, O. cav-imana and those of P. platensis did so marginally (p <0.1). The latter (O. montaguiand O. cavimana) significantly (p < 0.05) correlated with the soil chromium content.Talitrus saltator did not exhibit any significant correlation with any of the tested sitecharacteristics.

Discussion

According to the constrained correspondence analysis, the abundance of differ-ent amphipod species at the three lagoon complexes in northern Tunisia could bebest explained by the soil contents of several heavy metals, namely zinc, thalliumand cadmium and the proportion of the coarse sand fraction (O. mediterranea,O. gammarellus). Talitrus saltator abundance, by contrast, negatively corresponded tothese stations characteristics. Air and soil temperature were the best predictors for

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O.mon

O.c

O.med

O.gT.s

D.d

P.p

O.s

–1 1 2

2

1

–1Axis 1

Axis

2

OM

silt & clay

fine sand

coarse sand

Sn

Rb

Hair

Hsoil

Cr

V

CuSr

Li

As

Pb

Ni

Co

ZnTl

Cd

Tair Tsoil

Mn

Figure 7. Ordination of species and environmental factors through Canonical CorrespondenceAnalysis. Dots depict species, arrows assign environmental factors. Eigenvalues: λ (axis1) = 0.689; λ (axis 2) = 0.161.,(O. mon: Orchestia montagui, O. med: Orchestia mediterranea, O.g: Orchestia gammarellus, O. s: Orchestia stephenseni, O. c: Orchestia cavimana, P. p: Platorchestiaplatensis, D. d: Deshayesorchestia deshayesii, T. s: Talitrus saltator.

O. stephenseni abundance that negatively corresponded with the proportion of thefine sand fraction and the organic matter content of the soil. Orchestia montagui andO. cavimana abundances corresponded positively with air humidity and the soil lithiumand rubidium contents but negatively with the soil tin content and the proportion ofthe silt and clay fraction. D. deshayesii and P. platensis did not exhibit any clear corre-spondence with station characteristics. Overall, we observed little accordance betweenlinear correlation and unimodal correspondence, suggesting that the dependence ofamphipods on environmental parameters is not linear.

In this study, heavy metal content in soils varied both between and within lagooncomplexes. Relatively high concentrations at the lagoon complex of Ichkeul may relateto a number of possible sources: the Tunisian Society of mussel rearing, the Tunisiansteel company “El Fouladh”, the military arsenal, the Menzel Bourguiba waste dis-posal (Ben Garali et al. 2009) or the high load of sewage at this complex. Whencompared with data from Henin (1983), lead concentrations of the different stationsstudied here are lower than the maximum tolerance value of 100–150 ppm as definedby Henin (1983). The high concentrations of lead observed in the supralittoral zonesof Tinja (42.7 ppm Pb) and Bizerte lagoon (58.2 ppm Pb) may be a result of the sewagedischarge (Nassali et al. 2000, 2002). At these two stations, we also observed the highestconcentration of nickel (16.0 and 18.0 ppm Ni, respectively). However, these concen-trations are lower than the maximum value (50 ppm Ni) tolerated for soil by Henin(1983). The high metal concentrations at these stations correlate with high organicmatter of 12.2% and 9.5%, respectively, which may act as a natural enrichment agent

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for heavy metals. Consequently, elevated metal concentrations in organic rich soilsdo not necessarily imply elevated input of metals from anthropogenic sources (c.f.,Figures 5 and 6). In comparison with data for cadmium and lead reported in otherstudies on different North African lakes, the lagoon complex of Ichkeul exhibits highmetal levels, higher than Ghar El Melh lagoon (present study) and Egyptian lakes(Saad et al 1985). However, these levels were much lower than those found in LagosLake in Nigeria (Okoye et al. 1991). The highest copper concentration measured at thesampling station 59 km from Tunis (39.1 ppm Cu) could be due to copper-rich dis-cards or to atmospheric, agricultural and urban origins. The studied soils do not havean abnormal concentration of copper and we do not consider these soils contaminatedby this element. The maximum tolerable value of copper was estimated at 100 ppm(Henin 1983). In the lagoon complex of Korba, the different heavy metal levels mea-sured are lower than in the other lagoon complexes of Ichkeul and Ghar El Melh.Possible anthropogenic sources for these metals may be related to discharges fromlocal preserving industries and to the fact that Korba lagoon receives water dischargesfrom the station of water purification (STEP) of Korba town (ANPE 2008).

Our study showed that these amphipods tolerate moderate concentrations of heavymetals, the highest being those in the Ichkeul lagoon complex. At the same time,amphipod diversity was highest at the lagoon complex of Ichkeul and was lower inGhar El Melh and Korba. Given their potential toxic effects on various organisms(Mitchelmore et al. 2007; Sabdono 2009) it seems counterintuitive that amphipodabundance at the studied lagoon complexes corresponded positively with heavy metalconcentration in the soil. Besides being toxic at high concentrations, heavy metals areessential to most organisms at low concentrations (Matini et al. 2011). Compared withseverely contaminated coastal regions worldwide, for example the west coast of India(Zodape et al. 2011) and Nemunas River in Lithuania (Kruopiene 2007), the soil heavymetal contents presented herein are modest.

It is possible that the amounts of bioavailable metal ions are within the rangeof increasing value to amphipods with increasing metal concentration. In fact,organic matter increases the adsorption of metals in soil by the formation of stableclay/organic matter/metal complexes (Barbier 1999). Accordingly, the lagoon com-plex of Ichkeul and Ghar El Melh, which is characterized by high organic mattercontents of the soil, is host to the most species-rich amphipod fauna, despite therelatively high concentrations of heavy metals in the soil. We conclude that semi-terrestrial amphipods in coastal areas are only slightly affected by (moderate) heavymetal contamination of the soil.

Results show that two-thirds of amphipods were collected in the lagoon com-plex of Ichkeul; this complex was more diverse with eight species present. This resultcan be explained by the connection of oued Tinja to Bizerte lagoon and Ichkeullake. Moreover, this difference among stations was attributed to physicochemicalparameters. At the Zouaraa beach (northern coast of Tunisia), only two sympatricspecies, T. saltator and Talorchestia brito, were found (Charfi-Cheikhrouha et al.2000). In Bizerte beach three species of Talitridae were recorded, namely: T. saltator,D. deshayesii and O. gammarellus (Ayari and Nasri-Ammar 2011).

Whatever the study site, the highest diversity, abundance and density were observedin the lagoon complex of Ichkeul especially in the supralittoral zone of Bizerte lagoonwith 242 ind. m−2. In the Zouaraa beach, Charfi-Cheikhrouha et al. (2000) showedthat the total density of T. saltator and Talorchestia brito was 860 ind. m−2. At Ouderef,

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Gabès and Zarrat beaches (Gulf of Gabès, Tunisia), the amphipod T. saltator was themost abundant species, present in the three beaches studied, with the highest densitiesin Ouderef beach (Pérez-Domingo et al. 2008). Orchestia montagui and Talorchestiadeshayesii, in the Bay of Bou Ismail reached more than 45.000 ind. m−2 (Louis 1980)and O. mediterranea in the estuary of Bou Regreg attained 7000 ind. m−2 (El Kaïmet al. 1985). On the Isle of Man, densities of Talitrus saltator were estimated at80–400 ind. m−2 (Williams 1995). Marsden (1991) and Cardoso and Veloso (1996)showed that fluctuations in population density were frequent in talitrids and indicatedperiods of intense reproduction. They observed, in fact, similar patterns of variationfor Talorchestia quoyana and Pseudorchestoidea brasiliensis, respectively, with highestdensities in summer and late winter.

Acknowledgements

The study was supported by the Research Unit of Bio-ecology and Evolutionary Systematics(UR11ES11), Faculty of Science of Tunis, University of Tunis El Manar.

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amphipod diversity at three tunisian lagoon complexes in relation to environmental conditions

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