abundance, population structure and production of macro-invertebrate shredders in a mediterranean...

Estuarine, Coastal and Shelf Science 66 (2006) 437e446www.elsevier.com/locate/ecss

Abundance, population structure and production of macro-invertebrateshredders in a Mediterranean brackish lagoon, Lake Ichkeul, Tunisia

Caterina Casagranda a,b,*, Mohamed Sadok Dridi c, Charles Francois Boudouresque a

a UMR 6540 CNRS Dimar ‘‘Diversite, Evolution et Ecologie fonctionnelle marine’’, Centre d’Oceanologie de Marseille,Universite de la Mediterranee, Campus de Luminy, Case 901, 13288 Marseille Cedex 9, France

b Department of Biology, University of Freiburg, Germanyc Laboratoire d’Ecologie, Departement de Biologie, Faculte des Sciences de Tunis, Campus universitaire, 1060 Tunis, Tunisia

Received 30 March 2005; accepted 7 October 2005

Available online 9 December 2005

Abstract

Abundance, population structure and production of the macro-invertebrates belonging to the functional feeding group of the shredders werestudied in the Ichkeul wetland, northern Tunisia, from July 1993 to April 1994. Mean above-ground macrophyte biomass was at a maximum inSeptember followed by a complete breakdown of the Potamogeton pectinatus L. meadow from October onward due to high salinity following anexceptionally dry winter. Only the meadow of Ruppia cirrhosa (Petagna) Grande at Tinja remained in place. Abundance of Gammarus aequi-cauda (Martynov 1931), Idotea chelipes (Pallas 1766) and Sphaeroma hookeri Leach 1814 was significantly related to the R. cirrhosa biomass.Gammarus aequicauda presented two recruitment periods in spring and autumn, and S. hookeri a third one in winter. The population of I. che-lipes was renewed during winter by continued reproduction without any spring generation. Recruitment of all three species was not very success-ful during the study period. Life span of all three species was between 12 and 15 months. Despite their relatively low biomass and productionrate, the shredders have a key function in processing macrophyte matter to different trophic levels through fragmentation and accelerating thedecomposition of macrophyte biomass accumulated at the end of the growth season in the Ichkeul lagoon.� 2005 Elsevier Ltd. All rights reserved.

Keywords: Gammarus aequicauda; Idotea chelipes; Sphaeroma hookeri; population structure; production; Mediterranean lagoon

1. Introduction

In many brackish shallow waters on Mediterranean coasts,Potamogeton pectinatus L. and Ruppia cirrhosa (Petagna)Grande meadows form large dense stands from late spring toearly autumn. One of the most notable features of the macro-phyte beds is the high faunal biomass relative to those in ad-jacent, unvegetated habitats. Within these ecosystems, thefragmentation of the vascular plant leaves with their smallP/B ratio is a key process in the channelling of energy and

* Corresponding author. UMR 6540 CNRS Dimar ‘‘Diversite, Evolution et

Ecologie fonctionnelle marine’’, Centre d’Oceanologie de Marseille, Univer-

site de la Mediterranee, Campus de Luminy, Case 901, 13288 Marseille Cedex

9, France.

E-mail address: [email protected] (C. Casagranda).

0272-7714/$ - see front matter � 2005 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecss.2005.10.005

the cycling of nutrients through particulate detritus (Fenchel,1977). In the Ichkeul lagoon (northern Tunisia), a large pro-portion of the carbon fixed by primary production enters thedetritical pool during the autumn. These decaying leavesform dense packs on the lee side shores, often moved aroundby wave action. Three crustacean species, Gammarus aequi-cauda, Idotea chelipes and Sphaeroma hookeri, constitutethe functional feeding group of the shredders, i.e. macro-inver-tebrates whose mouthparts allow them to chew through theleaves and transform the leaf material into fine particulate or-ganic matter (FPOM) (Schwoerbel, 1993). Evidence has accu-mulated that shredders do not digest the plant matter itself, butassimilate the living components such as attached micro-organisms (Fenchel, 1977); the dead plant residue passesundigested through the intestine (Fenchel, 1970). These macro-invertebrates also weaken the structure of many more leaves

mailto:[email protected]

http://www.elsevier.com/locate/ecss

438 C. Casagranda et al. / Estuarine, Coastal and Shelf Science 66 (2006) 437e446

by shredding off layers of cells. These leaves will then bemore susceptible to fragmentation by wave action. Therefore,shredders actively contribute to macrophyte decomposition byreducing its particle size, allowing greater surface area forleaching and microbial action. Although the shredders contrib-ute little to community respiration through their own metabo-lism, their mechanical activity is of major importance as a linkbetween primary and secondary production in shallow-waterareas (Fenchel, 1970). An estimate of the annual shredder pro-duction is needed in order to obtain a quantitative measure oftheir trophic potential in the functioning of the Ichkeul ecosys-tem for supporting resident and migratory consumer popula-tions (e.g. fish, waterfowl), which utilize the macrophytebeds as feeding areas and refugia. Secondary production ofG. aequicauda was investigated in the study of Kevrekidisand Lazaridou-Dimitriadou (1988). More attention has beendevoted to Gammarus pulex (L. 1758) (Iversen and Jessen,1977; Welton, 1979; Friberg et al., 2002), Gammarus pseudo-limnaeus Bousfield 1958 (Waters and Hokenstrom, 1980;Marchant and Hynes, 1981), and Gammarus mucronatus Say1818 (LaFrance and Ruber, 1985; Fredette et al., 1990). Littleis known about the secondary production of Gammarus minusSay 1818 (Griffith et al., 1994), Gammarus locusta (L. 1758)(Costa and Costa, 1999), I. chelipes (Cloarec et al., 1983), Ido-tea baltica (Pallas 1772) (Fredette et al., 1990), and Sphaer-oma serratum (Fabricus 1787) (Makkaveeva, 1974). Noproduction study of S. hookeri is to be found in the literature.The present investigation is part of a more extensive researchprogramme on the functioning of the Ichkeul ecosystem (Tu-nisia), the overall purpose of which is to identify the ecologi-cal and physical characteristics of the ecosystem in order todraw up a predictive forecasting model with a view to devisinga conservation management programme which takes into ac-count the social and economic development of the region.The Ichkeul lagoon may be considered as a rare example ofan oligotrophic coastal lagoon in the Mediterranean basin(Tamisier and Boudouresque, 1994). What is the fate of themacrophyte biomass since a dystrophic crisis has never beenreported from the Ichkeul lagoon? The contribution of theshredders to the functioning of the ecosystem is investigated.The study describes the abundance and population dynamicsof G. aequicauda, I. chelipes and S. hookeri, and estimatestheir life span, growth and production in this temperate brack-ish lagoon which harbours a conspicuous population of winter-ing waterfowl (Tamisier et al., 1987, 2000; Tamisier andBoudouresque, 1994).

2. Material and methods

2.1. Study site

The study was carried out at Lake Ichkeul, an inland brack-ish lagoon of 9000 ha surrounded by 3000 ha of temporarymarshes on the northern coast of Tunisia (Fig. 1). It is linkedby a narrow channel (Tinja channel) to the lagoon of Bizertewhich in turn has an outlet to the Mediterranean Sea. The wet-land is shallow with a mean depth of 2e3 m in winter and 1 m

in summer. It is filled up with freshwater from autumn andwinter rainfall (from 7 wadis, i.e. temporary rivers) that over-flows into the lagoon of Bizerte. In summer, high evaporationlowers the water level and allows seawater to enter the lake.The salinity displays considerable seasonal changes from 3in the innermost parts in spring to over 45 at the mouth ofthe Tinja channel in autumn. Gammarus aequicauda, Idoteachelipes and Sphaeroma hookeri are the only shredder speciesthat occur in the Ichkeul lagoon.

2.2. Sampling

The lagoon was divided into four study areas on the basis ofthe macrophytal covering (Fig. 1). The western (henceforth re-ferred to as ‘Sejnene’) and the southern (Joumine) areas, sup-plied with freshwater from the wadis, are covered by extensivebeds of Potamogeton pectinatus. The eastern area (Tinja) closeto the Tinja channel and supplied with seawater is covered bya meadow of Ruppia cirrhosa. The central area of the Ichkeullagoon is completely vegetation free. Three replicate sampleswere taken monthly at a total of 21 sites (Fig. 1) from July1993 to April 1994 using a sampler which is essentially a sec-tion of a metal ventilation pipe, 30 cm in diameter, fitted witha sliding trap-net that can be closed by pulling a cable runningfrom the trap-net to the top of the sampler. It traps the full wa-ter column and 2 cm of substrate from an area of 706.86 cm�2.All samples were preserved in 75% ethanol. The three specieswere classified as juveniles (devoid of sexual characteristics),males, females and gravid females carrying eggs or embryoswhich were counted.

2.3. Sizeefrequency distribution, biomass and CHNcontent

The ash-free dry mass (AFDM) (g) was estimated as a generalpower function of total length (Lt) (mm).

Gammarusaequicauda: AFDM¼ 1.6956� 10�6Lt3.0756 (R2 ¼

99.41%, n¼ 38)Idotea chelipes: AFDM¼ 1.0407� 10�5Lt

2.1883 (R2 ¼ 99.43%,n¼ 36)Sphaeroma hookeri: AFDM ¼ 6.2140 � 10�6Lt

2.3491 (R2 ¼99.10%, n¼ 24)

The AFDM was measured as weight loss after 4 h of incin-eration at 600 �C (Bachelet, 1982) of unconserved specimensdried at 60 �C for 48 h. The average CHN content was mea-sured with a LECO 800 analyser as described by Casagrandaand Boudouresque (2002). The C- and N-content for Gamma-rus aequicauda yielded 27.8% C and 5.6% N of the AFDM,for Idotea chelipes 29.1% C and 5.8% N, and for Sphaeromahookeri 27.2% C and 5.5% N, respectively.

The total length Lt was measured from the base of theantennae to base of the telson on the extended animal. Consid-ering the curled position of Gammarus aequicauda, it is labo-rious to determine the total length. Alternatively, the cephalic

439C. Casagranda et al. / Estuarine, Coastal and Shelf Science 66 (2006) 437e446

9°39' 9°40' 9°41' 9°42' 9°43' 9°44' 9°45'

37°10'

37°12'

37°09'

37°08'

37°07'

9°38'9°37'9°36'

N

Fig. 1. The Ichkeul lagoon, with location of the sampling sites (21).

length Lc was used as there is a linear regression between Lt

and Lc which was previously determined:

Gammarus aequicauda: Lt (mm) ¼�1.80298 þ 10.6434Lc (mm) (R2 ¼ 99.84%, n¼ 25)

2.4. Production

The different age classes were regarded as separate cohorts,and production was calculated separately for each of these co-horts. The cohorts were separated according to Harding(1949), assuming that the sizeefrequency distributions of thecohorts were normally distributed. Production was estimatedby two methods using (1) the loss summation method de-scribed by Boysen-Jensen (1919) and (2) the increment sum-mation method which Masse (1968) derived from theBoysen-Jensen (1919) method.

(1) According to Boysen-Jensen (1919), the production DP ofa cohort can be calculated as the sum of the standing stockgain (DB) and the biomass produced but eliminated(E ) due to mortality or emigration from time t totime tþDt: DP¼DBþ E with DB¼ BtþDt� Bt andE ¼ DNw where DN¼Nt� NtþDt and w¼ 0.5(wtþwtþDt). N is the individual number and w the mean individ-ual biomass. Total cohort production is expressed as thesum of all produced biomass over all time intervals:P1 ¼

P(BtþDt� Bt) þ (Nt� NtþDt)0.5(wtþ wtþDt).

(2) According to Masse (1968), the production DP of a cohortcan be calculated as biomass gain from time t to timetþDt: DP ¼ NDw with N ¼ 0.5(NtþNtþDt) and Dw¼wtþDt� wt. The total production of the cohort is calculated

as the sum of the production increments over all timeintervals: P2 ¼

P(0.5(Ntþ NtþDt))(wtþDt� wt).

3. Results

The study period was characterized by an exceptionally drywinter, only negligible rainfall was registered and the waterlevel remained low. Inflow of seawater into the lagoon contin-ued from summer to winter and was reversed only in Februaryand March due to some precipitation during January and Feb-ruary (2 months instead of 8 in average years). At the end ofspring 1994, unusually high average salinity of 28 instead of10e12 in average years (BCEOM (Bureau Central d’Etudespour les Equipements d’Outre-Mer), unpublished data) wereobserved. The meadows of Potamogeton pectinatus had preco-ciously disappeared from October onward and thick layers ofdead vegetation piled up in particular along the southernshores which constitutes an unusual event. Gammarus aequi-cauda, Idotea chelipes and Sphaeroma hookeri had disap-peared from these areas as a consequence of the P.pectinatus decline from October onward precluding any popu-lation analysis. The three shredder species were never found inthe vegetation free centre of the lagoon. Only the meadow ofRuppia cirrhosa at Tinja remained in place allowing popula-tion analysis during the study period.

3.1. Abundance and population composition

The shredders Gammarus aequicauda, Idotea chelipes andSphaeroma hookeri occurred at annual mean abundance of578 � 231, 487 � 192 and 760 � 234 individuals m�2, respec-tively at Tinja. Idotea chelipes never formed a dense


population. The abundance of the three species increased syn-chronously in October followed by a sharp decrease inNovember (Fig. 2) following the macrophyte decrease in bio-mass (BCEOM, unpublished data) until the end of the studyperiod. Regression coefficients of linear regressions of specificabundance vs. macrophyte biomass were all significant and anANCOVA did not reveal significant differences ( p> 0.05).

Gammarus aequicauda e Juveniles had an abundance peakin October and an abundance increase in April (Fig. 3). Maleswere dominant in autumn and winter suggesting a higher mor-tality of females during summer. Gravid females were morenumerous in summer and spring, all indicating a bivoltinelife cycle.

Idotea chelipes e Males were always dominant especiallyduring summer and spring with a sex ratio between 2 and 8,suggesting a longer life span for males than for females. Fe-males, especially gravid females, were more numerous fromOctober to February (sex ratio < 2). Juveniles were continu-ously present with peaks in October, December and Februaryrenewing the population during winter. The period of sexualrest is assumed to be in summer and spring.

Sphaeroma hookeri e Juveniles always occurred during thestudy period but were particularly abundant in October andFebruary/March. Males were dominant in July, October/No-vember and March, gravid females had three peaks in October,December/January and April which suggests a third recruit-ment period in May/June.

3.2. Population structure and growth

Gammarus aequicauda e Sizeefrequency distribution con-firmed the bivoltine life cycle with 2 cohorts (Fig. 4) in

autumn (0e1) and spring (0e2). Life span was found to be15 months, the maximum of 18 months was recorded in theI-1 cohort. Fastest growth (Fig. 5) took place during Octo-bereDecember with a maximum recorded length of 13.3 mm.

Idotea chelipes e Three cohorts were found in October (0e1), December (0e2) and February (0e3) (Fig. 4) although notvery successful. Cohort abundance steadily decreased duringthe study period. Juvenile decrease in November was partlydue to fast growth from October to December. Life spanwas between 12 and 15 months with a maximum length of17.5 mm in males of the I-1 cohort.

Sphaeroma hookeri e Three recruitments were found inJuly (0e1), October (0e2) and February (0e3). The recruit-ment of the 0e1 cohort probably took place at the end ofspring. Fastest growth was recorded in autumn. Life spanwas estimated to be 12e15 months, greatest size recordedwas 11.3 mm.

3.3. Production

The Gammarus aequicauda production at Tinja achievedby loss summation was 0.81 g AFDM m�2, the productionof Idotea chelipes and Sphaeroma hookeri amountedto 1.19 g AFDM m�2 and 0.38 g AFDM m�2, respectively(Table 1). Major production took place during autumn whengrowth and recruitment were at their maximum for the studyperiod. The total shredder production (biomass) from Julyto April achieved by loss summation amounted to2.37 g AFDM m�2 (1.14 g AFDM m�2). The total C- andN-production from July to April yielded 0.64 g C m�2 and0.12 g N m�2 at Tinja. The resulting turnover (P/B ratio)

0

200

400

600

800

1000

1200

1400

1600

1800

2000

Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr

Abu

ndan

ce [

ind.

m-2

]

0

50

100

150

200

250R

uppi

a ci

rrho

sa [

g D

M m

-2]

Ruppia cirrhosa

Idotea chelipes (R²=49.95; p=0.049)

Gammarus aequicauda (R²=59.87; p=0.024)

Sphaeroma hookeri (R²=56.26; p=0.032)

Fig. 2. Over time changes in abundance (individuals m�2) of Gammarus aequicauda, Idotea chelipes and Sphaeroma hookeri in relation to the macrophyte biomass

(g DM m�2) at Tinja. Macrophyte biomasses according to BCEOM (unpublished data). DM ¼ dry mass. R2 ¼ coefficients of determination of linear regressions of

specific abundances vs. macrophyte biomass. All regression coefficients were significant ( p< 0.05; F0.05(1), 1, n�2). Bars ¼ standard error.


Gammarus aequicauda

0%

20%

40%

60%

80%

100%

0%

20%

40%

60%

80%

100%

0%

20%

40%

60%

80%

100%Idotea chelipes

Sphaeroma hookeri

Jul Aug Sep Oct Nov Dec Jan F eb Mar Apr

Juveniles Malesnon-gravid Femalesgravid Females

Fig. 3. Over time changes in population composition of Gammarus aequicauda, Idotea chelipes and Sphaeroma hookeri at Tinja.

was about 2. The estimate according to Masse’s (1968) method(2.34 g AFDM m�2) was insignificantly lower (Table 1).According to Dauvin and Joncourt (1989), the calorific valueis 21.10 kJ g AFDM�1 rendering the shredder production as50 kJ m�2. The shredder consumption of macrophytes calcu-lated from published data on consumption rates of G. aequi-cauda, I. chelipes and S. hookeri feeding on green anddecomposing Ruppia cirrhosa (Verhoeven, 1980; Menendezand Comın, 1990) was 8818 kJ m�2. Using the detritus pro-duction rates of G. aequicauda and S. hookeri according toMenendez and Comın (1990) and of I. chelipes accordingto Verhoeven (1980) feeding on green and decomposing R.cirrhosa, the detritus production of the shredders amountsto 8583 kJ m�2. Therefore, the total shredder ‘‘net’’ con-sumption (C ) i.e. the actually consumed matter at Tinjawas estimated at 235 kJ m�2. The organic income from themacrophyte meadows at Tinja was calculated to be9923 kJ m�2 (BCEOM, unpublished data; Defosse and Poy-denot, unpublished data). On the basis of this value, theshredders would have reduced 86% of the energy incomefrom the lagoon macrophytes to detritus.

4. Discussion

4.1. Abundance and population composition

Gammarus aequicauda and Idotea chelipes were often foundsympatrically in relatively deep stations with living vegetationand hard substrate (sand, gravel). According to Robertson andMann (1980), I. chelipes spends most of its active time shred-ding and browsing green, living leaves whereas G. aequicaudaprefers shredding intact dead leaves recently released fromplants and filtering. Daytime observation revealed that amongthe three species only I. chelipes was swimming actively. Juve-niles were mainly found in the shallow areas. Gravid or emptyfemales were rarely found in shallow stations. According toKouwenberg and Pinkster (1984) it seems that juveniles are re-leased in the deeper areas and swim actively to shallower areasto complete their first life stages. Sphaeroma hookeri mainlyoccurred at relatively shallow stations with plenty of detritusand silty substrate. The functional relationship between shred-ders and macrophytes may be nutritional. The meadow alsoprovides the shredders with nursery and some refuge from


Fre

quen

cy [

%]

Gammarus aequicauda

I-1

I-2

0

5

10

15

20

25

0-1

I-2

I-1

0

5

10

15

20

25

I-1

0-1

I-2

0

5

10

15

20

25

I-1

I-2

0-1

0

5

10

15

20

25

I-1

I-2

0-1

0

5

10

15

20

25

0-1

I-2

I-10

5

10

15

20

25

I-2

0-1

0

5

10

15

20

25

0-1

0-2

0

5

10

15

20

25

0-1

2-3

4-5

6-7

8-9

10-

11

12-

13

Julyn=223

Novembern=934

Decembern=1047

Januaryn=750

Februaryn=297

Marchn=85

Apriln=198

Octobern=1500

Length classes [mm]

Idotea chelipes

I-3

I-2

I-1

0

5

10

15

20

25 Julyn=137

I-1

I-2

I-3

0-1

0

5

10

15

20

25

I-1

I-2I-30-1

0

5

10

15

20

25 Novembern=453

I-1

I-2

I-30-10-2

0

5

10

15

20

25 Decembern=1231

I-1

0-2

0-1

I-3 I-2

0

5

10

15

20

25 Januaryn=210

I-2I-30-1

0-2

0-3

0

5

10

15

20

25 Februaryn=674

I-2I-3

0-1

0-2

0-3

0

5

10

15

20

25 Marchn=298

0-2

0-10-3

0-2

0

5

10

15

20

25

0-1

2-3

4-5

6-7

8-9

10-

11

12-

13

14-1

5

16-1

7

Apriln=68

Sphaeroma hookeri

I-1

I-2

I-3

0

5

10

15

20

25 Julyn=713

I-1I-2

I-3

0-1

0

5

10

15

20

25Octobern=1019

Octobern=1783

I-1

I-2

I-3

0-1

0

5

10

15

20

25 Novembern=963

I-1I-2

I-3

0-1

0

5

10

15

20

25 Decembern=934

I-1I-2

I-3

0-1

0

5

10

15

20

25 Januaryn=523

I-2I-3

0-1

0-2

0

5

10

15

20

25 Februaryn=849

I-2

I-3

0-1

0-2

0

5

10

15

20

25 Marchn=198

I-2I-3

0-1

0-2

0

5

10

15

20

25

0-1

2-3

4-5

6-7

8-9

10-

11

Apriln=103

Fig. 4. Over time changes in sizeefrequency distribution of Gammarus aequicauda, Idotea chelipes and Sphaeroma hookeri at Tinja.


wave action, predation, salinity and temperature variations.According to Kouwenberg and Pinkster (1984), sexual activ-ity is not regulated by temperature but salinity and daylength; it is high at low salinities. Temperature is consideredas a modifying factor resulting in faster egg development andgrowth in summer but smaller average size. In winter, howev-er, low temperatures result in higher mean numbers of eggsand larger animals. In the Ichkeul lagoon the macrophytefall, in particular in the Sejnene and Joumine area wherethe Potamogeton pectinatus meadow has completely disap-peared, had a negative effect on the shredder abundance be-cause of increased water turbulence, predation and reducedfood availability.

Gammarus aequicauda

0-1

I-2

I-1

0

2

4

6

8

10

12

14

Idotea chelipes

0-30-20-1

I-3

I-2

I-1

0

2

4

6

8

10

12

14

16

18

Mea

n si

ze [

mm

]

0-20-1

I-3

I-2

I-1

0

2

4

6

8

10

12

Jul Sep Nov Jan Mar

Sphaeroma hookeri

Fig. 5. Growth of age classes of Gammarus aequicauda, Idotea chelipes and

Sphaeroma hookeri at Tinja. Bars ¼ standard error.

4.2. Production

As pointed out by Siegismund (1982), the method de-scribed by Masse (1968) underestimates the production of a co-hort during a period of recruitment in which the density isincreasing. The Siegismund (1982) modification probably stillunderestimates production as it neglects the production of in-dividuals recruited during the period of increasing density andeliminated before observation at the end of the period. Forthese reasons and also because of the migration phenomenonwithin the system the production estimates by the loss summa-tion method (Boysen-Jensen, 1919) were favoured here. Al-though determined for only 10 months, this probablyapproximates the total annual production since the highly ad-verse environmental conditions from October onward did notimprove but worsened. The hydrological situation deviatedstrongly from the normal situation described above. Salinitycontinued to increase reaching 43.2 � 0.5 in June (BCEOM,unpublished data). In the Sejnene and the Joumine area, thePotamogeton pectinatus meadow did not regrow in spring.The estimate of annual Gammarus aequicauda production of0.8 g AFDM m�2 is within the range obtained for Gammaruslocusta (1.8 g AFDM m�2 yr�1) by Costa and Costa (1999)in the Sado estuary. Makkaveeva (1974) found 846 g DMm�2 yr�1 produced by Sphaeroma serratum in the BlackSea, a surprisingly high value. Since the available productiondata are obtained by widely varying methods of biomass deter-mination, it is difficult to compare the published productionvalues. However, the turnover rate (P/B) of 3.8 for G. aequi-cauda, 1.6 for Idotea chelipes and 2.3 for Sphaeroma hookerifall within the ranges of collected published data (Table 2).LaFrance and Ruber (1985) who divided their sizeefrequencydistribution into 5 cohorts and considered Gammarus mucro-natus as multivoltine found exceptionally high P/B valuesfor G. mucronatus in salt marsh pools. If the species is consid-ered as univoltine with prolonged reproduction, the adjusted P/B (6.5) falls within the range (2e6) of published data. Accord-ing to Waters (1977) in his review of secondary productionand to Dridi (unpublished data), I. chelipes is univoltine withprolonged reproduction renewing the population at Ichkeulduring winter. The bivoltine life cycle of G. aequicauda con-firms the findings of Dridi (unpublished data) at Ichkeul whodescribed a spring generation of fast growth which was deci-mated during summer and a more successful autumn genera-tion. The continuous presence of S. hookeri juvenilesindicates continued reproduction throughout the study period.On the other hand the constant presence of empty or not incondition females disproves the hypothesis of continuous re-production. In the sizeefrequency distributions 2 cohortsborn during the study period could be distinguished. The I-3cohort of small individuals in July and the increase of gravidfemales in April indicate a third reproduction period. In hisstudy on the reproductive cycle of different Sphaeroma speciesin Tunisia, Rezig (1979) found for S. hookeri three relativelyshort reproduction periods but there were not the same femalesincubating a brood in each period. Older females which havealready finished an annual cycle would be able to rapidly


Table 1

Mean biomass (g AFDM m�2), production during the study period (g AFDM m�2) and P/B ratio of Gammarus aequicauda, Idotea chelipes and Sphaeroma hookeri

at Tinja. P1 ¼ production as loss summation (Boysen-Jensen, 1919), P2 ¼ production as increment summation (Masse, 1968)

Species Age class Biomass P1 P2 P1/B P2/B

G. aequicauda I-1 0.08 0.24 0.24 2.89 2.89

I-2 0.10 0.32 0.32 3.10 3.10

0e1 0.07 0.25 0.24 3.67 3.65

0e2 <0.01 <0.01 <0.01 1.00 0.50

Total AFDM 0.25 0.81 0.81 3.18 3.17

Total C 0.07 0.22 0.22 3.18 3.17

Total N 0.01 0.05 0.05 3.18 3.17

I. chelipes I-1 0.22 0.22 0.22 0.99 0.99

I-2 0.28 0.38 0.38 1.39 1.39

I-3 0.10 0.34 0.35 3.27 3.36

0e1 0.05 0.17 0.16 3.18 2.97

0e2 0.02 0.06 0.05 2.89 2.45

0e3 <0.01 0.01 0.01 3.63 2.82

Total AFDM 0.68 1.19 1.17 1.74 1.72

Total C 0.20 0.35 0.34 1.74 1.72

Total N 0.04 0.07 0.07 1.74 1.72

S. hookeri I-1 0.08 0.08 0.08 0.91 0.91

I-2 0.05 0.09 0.09 1.73 1.73

I-3 0.04 0.13 0.12 3.24 3.11

0e1 0.02 0.07 0.07 3.19 2.99

0e2 <0.01 0.01 0.01 2.91 2.28

Total AFDM 0.20 0.38 0.36 1.86 1.80

Total C 0.04 0.07 0.07 1.86 1.80

Total N <0.01 0.01 0.01 1.86 1.80

Total Tinja (3 km2) AFDM 1.14 2.37 2.34 2.08 2.06

C 0.31 0.64 0.63 2.08 2.06

N 0.06 0.12 0.12 2.08 2.06

incubate another 2 broods one after the other which givesa winter generation in addition to the two main reproductionperiods in spring and autumn. On this basis, S. hookeri canbe considered as multivoltine at Ichkeul but with not very suc-cessful recruitment during the study period.

4.3. Consumption

In the Ichkeul lagoon, no major macrophyte grazing bymacro-invertebrates and fish species was observed (Hollis,1986; BCEOM, unpublished data). As during the study periodthe macrophyte production was not consumed by waterfowl,the decay and decomposition were quantitatively the principalprocesses. Shredders appear to be more generalists in theirfeeding habits than expected, using and even preferring other‘‘atypical’’ food resources such as green algae to their naturalfood resource of tougher texture in laboratory experiments(Friberg and Jacobsen, 1999). However, under natural condi-tions, the shredder abundance, biomass and production aremuch higher in waters dominated by the least preferred foodresources than in waters dominated by the most preferredfood resources (Friberg et al., 2002). In the study by Fribergand Jacobsen (1999), growth was less closely related to foodquality than was consumption, partly because the study spe-cies compensated by eating more food of low nutritional

value. According to Swiss and Johnson (1976) there is a criticallevel of assimilation which must be maintained to achieve anadequate energy storage efficiency. Food species producingslowly decaying litter such as macrophytes might partly ex-plain the large shredder populations despite the poorer nutri-tional value. Laboratory experiments (Robertson and Mann,1980) showed that isopods or amphipods seem to prefer leavesthat had aged for more than 5 weeks to leaves just releasedfrom plants. Macrophytes contain secondary substances whichinhibit grazing by invertebrates (e.g. phenolic-acids in Zosteramarina, Harrison, 1982) which may have leached from theleaves during senescence. A significant proportion (10e25%) of the plant material leaches out of plants as dissolvedorganic matter during the first few weeks after death (Fenchel,1977). The senescent plant parts are rapidly colonized by mi-croscopial algae, aquatic microbes and microfauna (Fenchel,1977). Twenty four genera of mainly saprophytic fungi werefound on Ruppia maritima in the Chesapeake Bay, USA(Motta, 1978). Gammarus aequicauda, Idotea chelipes andSphaeroma hookeri remove the surface fouling by scrapingand shredding from intact leaves but do not digest the plantmatter itself (Fenchel, 1970). Scraping and shredding increasethe macrophyte decomposition by reducing its particle size, al-lowing greater surface area for leaching and microbial action.Verhoeven (1980) found that half of the plant material had


Table 2

Comparison of published data on mean biomass (B in g AFDM m�2), annual production (P in g AFDM m�2) and P/B ratios. AFDM ¼ ash-free dry mass,

DM ¼ dry mass

Study area B P P/B Authors

Gammarus pseudolimnaeus

Valley creek (MN, USA) DM 2.7 16.3 6.0 Waters and Hokenstrom (1980)c

Credit river (Ontario, Canada) DM 0.6 2.9 4.7 Marchant and Hynes (1981)b

G. pulex

Rold Kilde springbrook (Denmark) DM 1.9 3.8 2.0 Iversen and Jessen (1977)b

Tadnoll Brook (UK) DM 4.6 12.9 2.8 Welton (1979)a

Tadnoll Brook (UK) DM 4.6 12.8 2.8 Welton (1979)c

Jutland Beech forest (Denmark) AFDM 1.2 2.5 2.1 Friberg et al. (2002)c

Jutland mixed forest (Denmark) AFDM 1.2 2.6 2.2 Friberg et al. (2002)c

G. minus

Allegheny plateau (VA, USA) DM 0.4 2.4 5.5 Griffith et al. (1994)c

G. aequicaudaEvros delta (Greece) DM 4.2 22.4 5.3 Kevrekidis and Lazaridou-Dimitriadou (1988)c

Ichkeul lagoon (Tunisia) AFDM 0.3 0.8 3.8 This studya

G. mucronatusSalt marsh pools (MA, USA) DM 1.0 14.8 14.8 LaFrance and Ruber (1985)c

Salt marsh pools (MA, USA) DM 1.0 15.8 15.8 LaFrance and Ruber (1985)d

Salt marsh pools (MA, USA) DM 1.0 12.5 12.4 LaFrance and Ruber (1985)d

Chesapeake Bay (VA, USA) DM 0.3 7.7 23.6 Fredette et al. (1990)c

Idotea chelipes

Arcachon basin (France) DM 0.5e 2.4e 5.3 Cloarec et al. (1983)b


I. baltica

Chesapeake Bay (VA, USA) DM 0.1 1.1 9.5 Fredette et al. (1990)c

Sphaeroma hookeri


a Loss summation.b Increment summation.c Sizeefrequency method.d Instantaneous growth.e Per 100 g DM Ruppia cirrhosa.

decomposed within two months and that after a year practicallyno plant material was left. In less than 4 days, the mechan-ical activity of amphipods may increase the detritical O2

uptake by 110% of their own metabolic rate (Fenchel,1970). The fecal pellets of the shredders still contain muchplant material and are in turn colonized by a layer of microbesand are food for suspension feeders (e.g. Cerastoderma glau-cum (Poiret), Mercieriella enigmatica Fauvel, Conopeum seur-ati (Canu)), or browsers (Hydrobia ventrosa (Montagu),Haminea navicula (Da Costa)) and deposit-feeders (Scrobicu-laria plana (Da Costa), Abra tenuis (Montagu), Corophiumvolutator Pallas, Cyathura carinata (Krøyer)). Using themean annual assimilation efficiency (A/C ) of G. aequicaudaand S. hookeri according to Menendez and Comın (1990)and of I. chelipes according to Verhoeven (1980) feeding ongreen and decomposing Ruppia cirrhosa, the total shredder as-similation at Tinja during the study period amounts to152 kJ m�2 yielding a net growth efficiency (P/A) of 33%. Acritical assimilation level must be maintained to achievehigh energy storage efficiency (Swiss and Johnson, 1976).The P/A value calculated from the published feeding rates isprobably an overestimation because it includes immaturesgrowing at a faster rate than they would maintain later. But

even this inflated value could be low enough to retard develop-ment to a point that it no longer coincides with appropriate en-vironmental conditions with a subsequent decline of theseorganisms in the benthic community. Low growth efficiency,of course, means a smaller proportion of energy flow availablefor the next trophic level. The elimination (E ) calculated bythe Boysen-Jensen (1919) method amounts to 52 kJ m�2, ren-dering the ecological efficiency (E/C ) of the shredders as 22%available to the next trophic level such as outswimming mi-grant fish (eels, mullets) during winter. The shredders, charac-terized by high P/B ratios and high importance for predation,do not play an important role in the direct consumption ofmacrophyte biomass but in processing organic matter to differ-ent trophic levels through macrophyte fragmentation. In theIchkeul lagoon, the role of the shredders as a link between pri-mary producers and predators and detritus feeders was propor-tionally enhanced during the study period due to the thicklayers of dead Potamogeton pectinatus matter which was notappreciated by the wintering waterfowl. The vascular plant tis-sue poor in essential nutrients and slowly degradable is neces-sary for the survival of heterotrophic organisms. The time lagin the utilization of the slowly degradable detritical materialassures a constant energy source for heterotrophic organisms


throughout the year, in contrast to photosynthesis which is sea-sonal in temperate climates.

Acknowledgements

This study was carried out as part of the international pro-gramme ‘‘Etude pour la sauvegarde du Parc National de l’Ich-keul’’ financed by the Kreditanstalt fur Wiederaufbau (KfW)under the aegis of the Tunisian authorities, in particular theAgence Nationale pour la Protection de l’Environnement.Thanks are due to the team from the Groupement d’InteretScientifique (GIS) Posidonie for field assistance and to col-leagues at UMR 6540 CNRS Dimar (Diversite, Evolution etEcologie fonctionnelle marine) for advice and work facilities.The present research was supported by a Ph. D. grant from theLandesgraduiertenforderungsgesetzes (LGFG) Germany. Thestudy would not have been possible without the support ofProf. Jurgen Schwoerbel, mentor and friend. Finally, the au-thors are grateful to Michael Paul for improving the Englishtext and to two anonymous referees for very valuablecomments.

References

Bachelet, G., 1982. Quelques problemes lies a l’estimation de la production

secondaire. Cas des bivalves Macoma balthica et Scrobicularia plana.

Oceanologica Acta 5, 421e431.

Boysen-Jensen, P., 1919. Valuation of the Limjord: 1. Studies on the fish food

in the Limfjord, 1909e1917, its quantity, variation and annual production.

Report of the Danish Biological Station 26, 5e44.

Casagranda, C., Boudouresque, C.F., 2002. A sieving method for rapid deter-

mination of sizeefrequency distribution of small gastropods. Example of

the mud snail Hydrobia ventrosa (Gastropoda: Prosobranchia). Hydrobio-

logia 485, 143e152.

Cloarec, M., Labourg, P.J., Lasserre, G., 1983. Cycle, croissance et production

d’un isopode Idothea chelipes (PALLAS) d’une lagune amenagee du bas-

sin d’Arcachon. Cahiers de Biologie Marine 24, 21e33.

Costa, F.O., Costa, M.H., 1999. Life history of the amphipod Gammarus

locusta in the Sado estuary (Portugal). Acta Oecologica 20, 305e314.

Dauvin, J.-C., Joncourt, M., 1989. Energy values of marine benthic inverte-

brates from the western English channel. Journal of the Marine Biological

Association of the UK 69, 589e595.

Fenchel, T., 1970. Studies on the decomposition of organic detritus derived

from the turtle grass Thalassia testudinum. Limnology and Oceanography

15, 14e20.

Fenchel, T., 1977. Aspects of the decomposition of seagrasses. In:

McRoy, C.P., Helfferich, C. (Eds.), Seagrass Ecosystems, a Scientific Per-

spective. Dekker publ., New York, NY, USA, pp. 123e146.

Fredette, T.J., Diaz, R.J., Monterans, I., Orth, R.J., 1990. Secondary production

within a seagrass bed (Zostera marina and Ruppia maritima) in lower

Chesapeake Bay. Estuaries 13, 431e440.

Friberg, N., Jacobsen, D., 1999. Variation in growth of the detritivore-shredder

Sericostoma personatum (Trichoptera). Freshwater Biology 42, 625e635.

Friberg, N., Larsen, A.D., Rodkjaer, A., Thomsen, A.G., 2002. Shredder guilds

in three Danish forest streams contrasting in forest type. Archiv fur Hydro-

biologie 153, 197e215.

Griffith, M.B., Perry, S.A., Perry, W.B., 1994. Secondary production of macro-

invertebrate shredders in headwater streams with different baseflow alka-

linity. Journal of the North American Benthological Society 13, 345e356.

Harding, J.P., 1949. The use of probability paper for the graphical analysis of

polymodal frequency distributions. Journal of the Marine Biological Asso-

ciation of the UK 28, 141e153.

Harrison, P.G., 1982. Control of microbial growth and of amphipod grazing by

water-soluble compounds from leaves of Zostera marina. Marine Biology

67, 225e230.

Hollis, G.E. (Ed.), 1986. Modelling and Management of the Internationally

Important Wetland at Garaet El Ichkeul, Tunisia. IWRB (International

Waterfowl Research Bureau) Publ., Slimbridge, UK, 121 pp.

Iversen, T.M., Jessen, J., 1977. Life-cycle, drift and production of Gammarus

pulex L. (Amphipoda) in a Danish spring. Freshwater Biology 7, 287e296.

Kevrekidis, T., Lazaridou-Dimitriadou, M., 1988. Relative growth and second-

ary production of the amphipod Gammarus aequicauda (Martynov, 1931)

in the Evros Delta (N. Aegean Sea). Cahiers de Biologie Marine 29,

483e495.

Kouwenberg, J., Pinkster, S., 1984. Population dynamics of three brackish

water isopods species (Crustacea) in the lagoon system of BageseSigean

(France). II. Life cycles, sexual activity and fecundity. Vie et Milieu 35,

79e92.

LaFrance, K., Ruber, E., 1985. The life cycle and productivity of the amphipod

Gammarus mucronatus on a northern Massachusetts salt marsh. Limnology

and Oceanography 30, 1067e1077.

Makkaveeva, E.B., 1974. Rost i produktsiya Sphaeroma serratum (FABR.) v

Chernom more. Biologiya Morya 32, 43e52.

Marchant, R., Hynes, H.B.N., 1981. The distribution and production of Gam-

marus pseudolimnaeus (Crustacea: Amphipoda) along a reach of the Credit

River, Ontario. Freshwater Biology 11, 169e182.

Masse, H., 1968. Sur la productivite des peuplements marins benthiques. Cah-

iers de Biologie Marine 9, 363e372.

Menendez, M., Comın, F.A., 1990. Consumption of macrophytes by inverte-

brates in Tancada lagoon (NE Spain). Scientia Marina 54, 139e144.

Motta, J.J., 1978. The occurrence of fungi on some rooted aquatics from the

Chesapeake Bay. Estuaries 1, 101e105.

Rezig, M., 1979. Etude comparee du cycle biologique de quelques especes du

genre Sphaeroma (Isopodes flabelliferes) en Tunisie. Bulletin de l’Institut

National Scientifique et Technique d’Oceanographie et de Peche Salambo

6, 93e121.

Robertson, A.I., Mann, K.H., 1980. The role of isopods and amphipods in the

initial fragmentation of eelgrass detritus in Nova Scotia, Canada. Marine

Biology 59, 63e69.

Schwoerbel, J. (Ed.), 1993. Einfuhrung in die Limnologie, 7 Aufl. Gustav

Fischer Verlag, Stuttgart/Jena/New York, 387 pp.

Siegismund, H.R., 1982. Life cycle and production of Hydrobia ventrosa and

H. neglecta (Mollusca: Prosobranchia). Marine Ecology Progress Series 7,

75e82.

Swiss, J.J., Johnson, M.G., 1976. Energy dynamics of two benthic crustaceans

in relation to diet. Journal of the Fisheries Research Board of Canada 33,

2544e2550.

Tamisier, A., Bonnet, P., Bredin, D., Dervieux, A., Rehfish, M., Rocamora, G.,

Skinner, J., 1987. L’Ichkeul (Tunisie), quartier d’hiver exceptionnel d’Ana-

tides et de foulques. Importance, fonctionnement et originalite. L’Oiseau et

RFO (Revue Francaise d’Ornithologie) 57, 296e306.

Tamisier, A., Boudouresque, C.F., 1994. Aquatic bird populations as possible

indicators of seasonal nutrient flow at Ichkeul lake, Tunisia. Hydrobiologia

279/280, 149e156.

Tamisier, A., Dehorter, O., Defosse, A., Poydenot, F., Gravez, V.,

Boudouresque, C.F., 2000. Modelling aquatic ecosystems: benefits, costs

and risks for a field biologist. Ichkeul lake, Tunisia, a case study. In:

Comin, F.A., Herrera, J.A., Ramırez, J. (Eds.), Limnology and Aquatic

Birds. Monitoring, Modelling and Management. Universidad Autonoma

de Yucatan publ., Merida, Mexico, pp. 185e203.

Verhoeven, J.T.A., 1980. The ecology of Ruppia-dominated communities in

western Europe. III. Aspects of production, consumption and decomposi-

tion. Aquatic Botany 8, 209e253.

Waters, T.F., 1977. Secondary production in inland waters. Advances in Ecol-

ogy Research 10, 91e164.

Waters, T.F., Hokenstrom, J.C., 1980. Annual production and drift of the

stream amphipod Gammarus pseudolimnaeus in Valley Creek, Minnesota.

Limnology and Oceanography 25, 700e710.

Welton, J.S., 1979. Life-history and production of the amphipod Gammaruspulex in a Dorset chalk stream. Freshwater Biology 9, 263e275.

abundance, population structure and production of macro-invertebrate shredders in a mediterranean...

Documents