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

Estuarine, Coastal and Shelf Science 66 (2006) 437e446 www.elsevier.com/locate/ecss

Abundance, population structure and production of macro-invertebrate shredders in a Mediterranean brackish lagoon, Lake Ichkeul, Tunisia Caterina Casagranda a,b,*, Mohamed Sadok Dridi c, Charles Franc¸ois Boudouresque a a

UMR 6540 CNRS Dimar ‘‘Diversite´, Evolution et Ecologie fonctionnelle marine’’, Centre d’Oce´anologie de Marseille, Universite´ de la Me´diterrane´e, Campus de Luminy, Case 901, 13288 Marseille Cedex 9, France b Department of Biology, University of Freiburg, Germany c Laboratoire d’Ecologie, De´partement 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 were studied in the Ichkeul wetland, northern Tunisia, from July 1993 to April 1994. Mean above-ground macrophyte biomass was at a maximum in September followed by a complete breakdown of the Potamogeton pectinatus L. meadow from October onward due to high salinity following an exceptionally dry winter. Only the meadow of Ruppia cirrhosa (Petagna) Grande at Tinja remained in place. Abundance of Gammarus aequicauda (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. chelipes was renewed during winter by continued reproduction without any spring generation. Recruitment of all three species was not very successful during the study period. Life span of all three species was between 12 and 15 months. Despite their relatively low biomass and production rate, the shredders have a key function in processing macrophyte matter to different trophic levels through fragmentation and accelerating the decomposition of macrophyte biomass accumulated at the end of the growth season in the Ichkeul lagoon. Ó 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 to early autumn. One of the most notable features of the macrophyte beds is the high faunal biomass relative to those in adjacent, unvegetated habitats. Within these ecosystems, the fragmentation of the vascular plant leaves with their small P/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’Oce´anologie de Marseille, Universite´ de la Me´diterrane´e, Campus de Luminy, Case 901, 13288 Marseille Cedex 9, France. E-mail address: [email protected] (C. Casagranda). 0272-7714/$ - see front matter Ó 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 proportion of the carbon fixed by primary production enters the detritical pool during the autumn. These decaying leaves form dense packs on the lee side shores, often moved around by wave action. Three crustacean species, Gammarus aequicauda, Idotea chelipes and Sphaeroma hookeri, constitute the functional feeding group of the shredders, i.e. macro-invertebrates whose mouthparts allow them to chew through the leaves and transform the leaf material into fine particulate organic matter (FPOM) (Schwoerbel, 1993). Evidence has accumulated that shredders do not digest the plant matter itself, but assimilate the living components such as attached microorganisms (Fenchel, 1977); the dead plant residue passes undigested through the intestine (Fenchel, 1970). These macroinvertebrates also weaken the structure of many more leaves

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by shredding off layers of cells. These leaves will then be more susceptible to fragmentation by wave action. Therefore, shredders actively contribute to macrophyte decomposition by reducing its particle size, allowing greater surface area for leaching and microbial action. Although the shredders contribute little to community respiration through their own metabolism, their mechanical activity is of major importance as a link between primary and secondary production in shallow-water areas (Fenchel, 1970). An estimate of the annual shredder production is needed in order to obtain a quantitative measure of their trophic potential in the functioning of the Ichkeul ecosystem for supporting resident and migratory consumer populations (e.g. fish, waterfowl), which utilize the macrophyte beds as feeding areas and refugia. Secondary production of G. aequicauda was investigated in the study of Kevrekidis and Lazaridou-Dimitriadou (1988). More attention has been devoted to Gammarus pulex (L. 1758) (Iversen and Jessen, 1977; Welton, 1979; Friberg et al., 2002), Gammarus pseudolimnaeus Bousfield 1958 (Waters and Hokenstrom, 1980; Marchant and Hynes, 1981), and Gammarus mucronatus Say 1818 (LaFrance and Ruber, 1985; Fredette et al., 1990). Little is known about the secondary production of Gammarus minus Say 1818 (Griffith et al., 1994), Gammarus locusta (L. 1758) (Costa and Costa, 1999), I. chelipes (Cloarec et al., 1983), Idotea baltica (Pallas 1772) (Fredette et al., 1990), and Sphaeroma serratum (Fabricus 1787) (Makkaveeva, 1974). No production study of S. hookeri is to be found in the literature. The present investigation is part of a more extensive research programme on the functioning of the Ichkeul ecosystem (Tunisia), the overall purpose of which is to identify the ecological and physical characteristics of the ecosystem in order to draw up a predictive forecasting model with a view to devising a conservation management programme which takes into account the social and economic development of the region. The Ichkeul lagoon may be considered as a rare example of an oligotrophic coastal lagoon in the Mediterranean basin (Tamisier and Boudouresque, 1994). What is the fate of the macrophyte biomass since a dystrophic crisis has never been reported from the Ichkeul lagoon? The contribution of the shredders to the functioning of the ecosystem is investigated. The study describes the abundance and population dynamics of G. aequicauda, I. chelipes and S. hookeri, and estimates their life span, growth and production in this temperate brackish lagoon which harbours a conspicuous population of wintering waterfowl (Tamisier et al., 1987, 2000; Tamisier and Boudouresque, 1994). 2. Material and methods 2.1. Study site The study was carried out at Lake Ichkeul, an inland brackish lagoon of 9000 ha surrounded by 3000 ha of temporary marshes on the northern coast of Tunisia (Fig. 1). It is linked by a narrow channel (Tinja channel) to the lagoon of Bizerte which in turn has an outlet to the Mediterranean Sea. The wetland is shallow with a mean depth of 2e3 m in winter and 1 m

in summer. It is filled up with freshwater from autumn and winter rainfall (from 7 wadis, i.e. temporary rivers) that overflows into the lagoon of Bizerte. In summer, high evaporation lowers the water level and allows seawater to enter the lake. The salinity displays considerable seasonal changes from 3 in the innermost parts in spring to over 45 at the mouth of the Tinja channel in autumn. Gammarus aequicauda, Idotea chelipes and Sphaeroma hookeri are the only shredder species that occur in the Ichkeul lagoon. 2.2. Sampling The lagoon was divided into four study areas on the basis of the macrophytal covering (Fig. 1). The western (henceforth referred to as ‘Sejnene’) and the southern (Joumine) areas, supplied with freshwater from the wadis, are covered by extensive beds of Potamogeton pectinatus. The eastern area (Tinja) close to the Tinja channel and supplied with seawater is covered by a meadow of Ruppia cirrhosa. The central area of the Ichkeul lagoon is completely vegetation free. Three replicate samples were taken monthly at a total of 21 sites (Fig. 1) from July 1993 to April 1994 using a sampler which is essentially a section of a metal ventilation pipe, 30 cm in diameter, fitted with a sliding trap-net that can be closed by pulling a cable running from the trap-net to the top of the sampler. It traps the full water column and 2 cm of substrate from an area of 706.86 cm
2. All samples were preserved in 75% ethanol. The three species were classified as juveniles (devoid of sexual characteristics), males, females and gravid females carrying eggs or embryos which were counted. 2.3. Sizeefrequency distribution, biomass and CHN content The ash-free dry mass (AFDM) (g) was estimated as a general power function of total length (Lt) (mm). Gammarus aequicauda: AFDM ¼ 1.6956  10
6L3.0756 (R2 ¼ t 99.41%, n ¼ 38) Idotea chelipes: AFDM ¼ 1.0407  10
5L2.1883 (R2 ¼ 99.43%, t n ¼ 36) Sphaeroma hookeri: AFDM ¼ 6.2140  10
6L2.3491 (R2 ¼ t 99.10%, n ¼ 24) The AFDM was measured as weight loss after 4 h of incineration at 600  C (Bachelet, 1982) of unconserved specimens dried at 60  C for 48 h. The average CHN content was measured with a LECO 800 analyser as described by Casagranda and Boudouresque (2002). The C- and N-content for Gammarus aequicauda yielded 27.8% C and 5.6% N of the AFDM, for Idotea chelipes 29.1% C and 5.8% N, and for Sphaeroma hookeri 27.2% C and 5.5% N, respectively. The total length Lt was measured from the base of the antennae to base of the telson on the extended animal. Considering the curled position of Gammarus aequicauda, it is laborious to determine the total length. Alternatively, the cephalic

C. Casagranda et al. / Estuarine, Coastal and Shelf Science 66 (2006) 437e446 9°36'

9°37'

9°38'

9°39'

9°40'

9°41'

9°42'

9°43'

9°44'

439 9°45'

37°12'

N

37°10'

37°09'

37°08'

37°07'

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 10.6434 Lc (mm) (R2 ¼ 99.84%, n ¼ 25)

2.4. Production The different age classes were regarded as separate cohorts, and production was calculated separately for each of these cohorts. The cohorts were separated according to Harding (1949), assuming that the sizeefrequency distributions of the cohorts were normally distributed. Production was estimated by two methods using (1) the loss summation method described by Boysen-Jensen (1919) and (2) the increment summation method which Masse´ (1968) derived from the Boysen-Jensen (1919) method. (1) According to Boysen-Jensen (1919), the production DP of a cohort can be calculated as the sum of the standing stock gain (DB) and the biomass produced but eliminated (E ) due to mortality or emigration from time t to time t þ Dt: DP ¼ DB þ E with DB ¼ BtþDt
Bt and E ¼ DNw where DN ¼ Nt
NtþDt and w ¼ 0.5(wt þ wtþDt). N is the individual number and w the mean individual biomass. Total cohort production is expressed as the sum P of all produced biomass over all time intervals: P1 ¼ (BtþDt
Bt) þ (Nt
NtþDt)0.5(wt þ wtþDt). (2) According to Masse´ (1968), the production DP of a cohort can be calculated as biomass gain from time t to time t þ Dt: DP ¼ NDw with N ¼ 0.5(Nt þ NtþDt) and Dw ¼ wtþDt
wt. The total production of the cohort is calculated

as the sum of P the production increments over all time intervals: P2 ¼ (0.5(Nt þ NtþDt))(wtþDt
wt).

3. Results The study period was characterized by an exceptionally dry winter, only negligible rainfall was registered and the water level remained low. Inflow of seawater into the lagoon continued from summer to winter and was reversed only in February and March due to some precipitation during January and February (2 months instead of 8 in average years). At the end of spring 1994, unusually high average salinity of 28 instead of 10e12 in average years (BCEOM (Bureau Central d’Etudes pour les Equipements d’Outre-Mer), unpublished data) were observed. The meadows of Potamogeton pectinatus had precociously disappeared from October onward and thick layers of dead vegetation piled up in particular along the southern shores which constitutes an unusual event. Gammarus aequicauda, Idotea chelipes and Sphaeroma hookeri had disappeared from these areas as a consequence of the P. pectinatus decline from October onward precluding any population analysis. The three shredder species were never found in the vegetation free centre of the lagoon. Only the meadow of Ruppia cirrhosa at Tinja remained in place allowing population analysis during the study period. 3.1. Abundance and population composition The shredders Gammarus aequicauda, Idotea chelipes and Sphaeroma hookeri occurred at annual mean abundance of 578  231, 487  192 and 760  234 individuals m
2, respectively at Tinja. Idotea chelipes never formed a dense

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440

population. The abundance of the three species increased synchronously in October followed by a sharp decrease in November (Fig. 2) following the macrophyte decrease in biomass (BCEOM, unpublished data) until the end of the study period. Regression coefficients of linear regressions of specific abundance vs. macrophyte biomass were all significant and an ANCOVA did not reveal significant differences ( p > 0.05). Gammarus aequicauda e Juveniles had an abundance peak in October and an abundance increase in April (Fig. 3). Males were dominant in autumn and winter suggesting a higher mortality of females during summer. Gravid females were more numerous in summer and spring, all indicating a bivoltine life cycle. Idotea chelipes e Males were always dominant especially during summer and spring with a sex ratio between 2 and 8, suggesting a longer life span for males than for females. Females, especially gravid females, were more numerous from October to February (sex ratio < 2). Juveniles were continuously present with peaks in October, December and February renewing the population during winter. The period of sexual rest is assumed to be in summer and spring. Sphaeroma hookeri e Juveniles always occurred during the study period but were particularly abundant in October and February/March. Males were dominant in July, October/November and March, gravid females had three peaks in October, December/January and April which suggests a third recruitment period in May/June. 3.2. Population structure and growth Gammarus aequicauda e Sizeefrequency distribution confirmed the bivoltine life cycle with 2 cohorts (Fig. 4) in

autumn (0e1) and spring (0e2). Life span was found to be 15 months, the maximum of 18 months was recorded in the I-1 cohort. Fastest growth (Fig. 5) took place during OctobereDecember with a maximum recorded length of 13.3 mm. Idotea chelipes e Three cohorts were found in October (0e 1), December (0e2) and February (0e3) (Fig. 4) although not very successful. Cohort abundance steadily decreased during the study period. Juvenile decrease in November was partly due to fast growth from October to December. Life span was between 12 and 15 months with a maximum length of 17.5 mm in males of the I-1 cohort. Sphaeroma hookeri e Three recruitments were found in July (0e1), October (0e2) and February (0e3). The recruitment of the 0e1 cohort probably took place at the end of spring. Fastest growth was recorded in autumn. Life span was estimated to be 12e15 months, greatest size recorded was 11.3 mm. 3.3. Production The Gammarus aequicauda production at Tinja achieved by loss summation was 0.81 g AFDM m
2, the production of Idotea chelipes and Sphaeroma hookeri amounted to 1.19 g AFDM m
2 and 0.38 g AFDM m
2, respectively (Table 1). Major production took place during autumn when growth and recruitment were at their maximum for the study period. The total shredder production (biomass) from July to April achieved by loss summation amounted to 2.37 g AFDM m
2 (1.14 g AFDM m
2). The total C- and N-production from July to April yielded 0.64 g C m
2 and 0.12 g N m
2 at Tinja. The resulting turnover (P/B ratio) 250

2000 1800

Abundance [ind. m-2]

1400 150

1200 1000

100

800 600

Ruppia cirrhosa [g DM m-2]

200

1600

50

400 200

0

0 Jul

Aug

Sep

Oct

Ruppia cirrhosa Idotea chelipes (R²=49.95; p=0.049)

Nov

Dec Jan Feb Mar Apr 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.

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441

Gammarus aequicauda 100% 80% 60% 40% 20% 0%

Idotea chelipes 100% 80% 60% 40% 20% 0%

Sphaeroma hookeri 100% 80% 60% 40% 20% 0% Jul

Aug Juveniles

Sep

Oct

Nov

gravid Females

Dec

Jan

F eb

non-gravid Females

Mar

Apr Males

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 value is 21.10 kJ g AFDM
1 rendering the shredder production as 50 kJ m
2. The shredder consumption of macrophytes calculated from published data on consumption rates of G. aequicauda, I. chelipes and S. hookeri feeding on green and decomposing Ruppia cirrhosa (Verhoeven, 1980; Mene´ndez and Comı´n, 1990) was 8818 kJ m
2. Using the detritus production rates of G. aequicauda and S. hookeri according to Mene´ndez and Comı´n (1990) and of I. chelipes according to Verhoeven (1980) feeding on green and decomposing R. cirrhosa, the detritus production of the shredders amounts to 8583 kJ m
2. Therefore, the total shredder ‘‘net’’ consumption (C ) i.e. the actually consumed matter at Tinja was estimated at 235 kJ m
2. The organic income from the macrophyte meadows at Tinja was calculated to be 9923 kJ m
2 (BCEOM, unpublished data; Defosse and Poydenot, unpublished data). On the basis of this value, the shredders would have reduced 86% of the energy income from the lagoon macrophytes to detritus.

4. Discussion 4.1. Abundance and population composition Gammarus aequicauda and Idotea chelipes were often found sympatrically in relatively deep stations with living vegetation and hard substrate (sand, gravel). According to Robertson and Mann (1980), I. chelipes spends most of its active time shredding and browsing green, living leaves whereas G. aequicauda prefers shredding intact dead leaves recently released from plants and filtering. Daytime observation revealed that among the three species only I. chelipes was swimming actively. Juveniles were mainly found in the shallow areas. Gravid or empty females were rarely found in shallow stations. According to Kouwenberg and Pinkster (1984) it seems that juveniles are released in the deeper areas and swim actively to shallower areas to complete their first life stages. Sphaeroma hookeri mainly occurred at relatively shallow stations with plenty of detritus and silty substrate. The functional relationship between shredders and macrophytes may be nutritional. The meadow also provides the shredders with nursery and some refuge from

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442

Gammarus aequicauda July n=223

25 20 15

Sphaeroma hookeri July n=137

I-3

20 15

I-1

10

Idotea chelipes 25

5

5

0

0

25

October n=1500

0-1 20

I-3

20 15

10

I-2

July n=713

25

I-2

I-2

10 I-1

5

I-1

0

25

October n=1019

20

25 20

October n=1783

0-1

I-3 15

15 I-2

10

15

0-1

10

5

I-2

5

I-1

I-3

10

I-2 I-1

5 I-1

0

0

November n=934

25 0-1

20

November n=453

25 20 15

15

I-2

December n=1047

0-1 20 15

25

December n=1231

20

December n=934

0-1

20

I-3

10

0-2

0-1

5

0

I-1

I-3

January n=750

0-1

20

25

I-2

January n=210

0-1

20 15

15

I-1

February n=297

25

I-3

5

I-2

0-1

I-1

15 10

I-2

February n=674

20

10

0-3

I-3

I-2

5

I-1

February n=849

25 20

0-2 0-1

15 0-2

10 0-1

5

5

January n=523

0-1 20

0

25

15

25

10

0

0

I-1

15

0-2

10

5

I-2

5 0

0

20

25

15

10 I-1

10

I-1

I-2

5

25

I-2

0

15 I-2

10

I-3

5

0

25

0-1

I-1

I-1

0

20

10

5

5

November n=963

25

15

I-3

0-1

10

I-2

10

Frequency [%]

0

I-3

I-2

I-3

I-2

5

I-1 0 25

10

10

5

5

0

0

25

April n=198

0-2

20

0-2

15

0-3 0-1 I-3

25

5

April n=68

0-2

25 0-1

10

0-1

16-17

14-15

12-13

8-9

10-11

6-7

I-3

5

0-2 4-5

April n=103

0-2

20 15

0-3

0-1

12-13

8-9

10-11

6-7

0

4-5

0

2-3

5 0-1

5

I-2

I-2

20 10

0-1

I-3

0

2-3

10

0-1

10

15

15

March n=198

0-2

20

0

I-2 10-11

15

25

8-9

15 I-2

March n=298

20

6-7

March n=85

0-1

4-5

20

2-3

25

0

0-1

0

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

C. Casagranda et al. / Estuarine, Coastal and Shelf Science 66 (2006) 437e446 14

4.2. Production

Gammarus aequicauda

12 10 8 I-1 6 4 I-2 2 0-1 0 18

Idotea chelipes

16

Mean size [mm]

14 I-1

12 10

I-2

8 6

I-3

4 2

0-2

0-1

0-3

0 12

Sphaeroma hookeri

10 I-1

8 6

I-2 4 I-3

2

0-1

0-2

0 Jul

Sep

443

Nov

Jan

Mar

Fig. 5. Growth of age classes of Gammarus aequicauda, Idotea chelipes and Sphaeroma hookeri at Tinja. Bars ¼ standard error.

wave action, predation, salinity and temperature variations. According to Kouwenberg and Pinkster (1984), sexual activity is not regulated by temperature but salinity and day length; it is high at low salinities. Temperature is considered as a modifying factor resulting in faster egg development and growth in summer but smaller average size. In winter, however, low temperatures result in higher mean numbers of eggs and larger animals. In the Ichkeul lagoon the macrophyte fall, in particular in the Sejnene and Joumine area where the Potamogeton pectinatus meadow has completely disappeared, had a negative effect on the shredder abundance because of increased water turbulence, predation and reduced food availability.

As pointed out by Siegismund (1982), the method described by Masse´ (1968) underestimates the production of a cohort during a period of recruitment in which the density is increasing. The Siegismund (1982) modification probably still underestimates production as it neglects the production of individuals recruited during the period of increasing density and eliminated before observation at the end of the period. For these reasons and also because of the migration phenomenon within the system the production estimates by the loss summation method (Boysen-Jensen, 1919) were favoured here. Although determined for only 10 months, this probably approximates the total annual production since the highly adverse environmental conditions from October onward did not improve but worsened. The hydrological situation deviated strongly from the normal situation described above. Salinity continued to increase reaching 43.2  0.5 in June (BCEOM, unpublished data). In the Sejnene and the Joumine area, the Potamogeton pectinatus meadow did not regrow in spring. The estimate of annual Gammarus aequicauda production of 0.8 g AFDM m
2 is within the range obtained for Gammarus locusta (1.8 g AFDM m
2 yr
1) by Costa and Costa (1999) in the Sado estuary. Makkaveeva (1974) found 846 g DM m
2 yr
1 produced by Sphaeroma serratum in the Black Sea, a surprisingly high value. Since the available production data are obtained by widely varying methods of biomass determination, it is difficult to compare the published production values. However, the turnover rate (P/B) of 3.8 for G. aequicauda, 1.6 for Idotea chelipes and 2.3 for Sphaeroma hookeri fall within the ranges of collected published data (Table 2). LaFrance and Ruber (1985) who divided their sizeefrequency distribution into 5 cohorts and considered Gammarus mucronatus as multivoltine found exceptionally high P/B values for G. mucronatus in salt marsh pools. If the species is considered as univoltine with prolonged reproduction, the adjusted P/ B (6.5) falls within the range (2e6) of published data. According to Waters (1977) in his review of secondary production and to Dridi (unpublished data), I. chelipes is univoltine with prolonged reproduction renewing the population at Ichkeul during winter. The bivoltine life cycle of G. aequicauda confirms the findings of Dridi (unpublished data) at Ichkeul who described a spring generation of fast growth which was decimated during summer and a more successful autumn generation. The continuous presence of S. hookeri juveniles indicates continued reproduction throughout the study period. On the other hand the constant presence of empty or not in condition females disproves the hypothesis of continuous reproduction. In the sizeefrequency distributions 2 cohorts born during the study period could be distinguished. The I-3 cohort of small individuals in July and the increase of gravid females in April indicate a third reproduction period. In his study on the reproductive cycle of different Sphaeroma species in Tunisia, Rezig (1979) found for S. hookeri three relatively short reproduction periods but there were not the same females incubating a brood in each period. Older females which have already finished an annual cycle would be able to rapidly

444

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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 I-2 0e1 0e2

0.08 0.10 0.07 <0.01

0.24 0.32 0.25 <0.01

0.24 0.32 0.24 <0.01

2.89 3.10 3.67 1.00

2.89 3.10 3.65 0.50

0.25 0.07 0.01

0.81 0.22 0.05

0.81 0.22 0.05

3.18 3.18 3.18

3.17 3.17 3.17

0.22 0.28 0.10 0.05 0.02 <0.01

0.22 0.38 0.34 0.17 0.06 0.01

0.22 0.38 0.35 0.16 0.05 0.01

0.99 1.39 3.27 3.18 2.89 3.63

0.99 1.39 3.36 2.97 2.45 2.82

0.68 0.20 0.04

1.19 0.35 0.07

1.17 0.34 0.07

1.74 1.74 1.74

1.72 1.72 1.72

I-1 I-2 I-3 0e1 0e2

0.08 0.05 0.04 0.02 <0.01

0.08 0.09 0.13 0.07 0.01

0.08 0.09 0.12 0.07 0.01

0.91 1.73 3.24 3.19 2.91

0.91 1.73 3.11 2.99 2.28

Total AFDM Total C Total N

0.20 0.04 <0.01

0.38 0.07 0.01

0.36 0.07 0.01

1.86 1.86 1.86

1.80 1.80 1.80

1.14 0.31 0.06

2.37 0.64 0.12

2.34 0.63 0.12

2.08 2.08 2.08

2.06 2.06 2.06

Total AFDM Total C Total N I. chelipes

I-1 I-2 I-3 0e1 0e2 0e3 Total AFDM Total C Total N

S. hookeri

Total Tinja (3 km2)

AFDM C N

incubate another 2 broods one after the other which gives a winter generation in addition to the two main reproduction periods in spring and autumn. On this basis, S. hookeri can be considered as multivoltine at Ichkeul but with not very successful recruitment during the study period. 4.3. Consumption In the Ichkeul lagoon, no major macrophyte grazing by macro-invertebrates and fish species was observed (Hollis, 1986; BCEOM, unpublished data). As during the study period the macrophyte production was not consumed by waterfowl, the decay and decomposition were quantitatively the principal processes. Shredders appear to be more generalists in their feeding habits than expected, using and even preferring other ‘‘atypical’’ food resources such as green algae to their natural food resource of tougher texture in laboratory experiments (Friberg and Jacobsen, 1999). However, under natural conditions, the shredder abundance, biomass and production are much higher in waters dominated by the least preferred food resources than in waters dominated by the most preferred food resources (Friberg et al., 2002). In the study by Friberg and Jacobsen (1999), growth was less closely related to food quality than was consumption, partly because the study species compensated by eating more food of low nutritional

value. According to Swiss and Johnson (1976) there is a critical level of assimilation which must be maintained to achieve an adequate energy storage efficiency. Food species producing slowly decaying litter such as macrophytes might partly explain the large shredder populations despite the poorer nutritional value. Laboratory experiments (Robertson and Mann, 1980) showed that isopods or amphipods seem to prefer leaves that had aged for more than 5 weeks to leaves just released from plants. Macrophytes contain secondary substances which inhibit grazing by invertebrates (e.g. phenolic-acids in Zostera marina, Harrison, 1982) which may have leached from the leaves during senescence. A significant proportion (10e 25%) of the plant material leaches out of plants as dissolved organic matter during the first few weeks after death (Fenchel, 1977). The senescent plant parts are rapidly colonized by microscopial algae, aquatic microbes and microfauna (Fenchel, 1977). Twenty four genera of mainly saprophytic fungi were found on Ruppia maritima in the Chesapeake Bay, USA (Motta, 1978). Gammarus aequicauda, Idotea chelipes and Sphaeroma hookeri remove the surface fouling by scraping and shredding from intact leaves but do not digest the plant matter itself (Fenchel, 1970). Scraping and shredding increase the macrophyte decomposition by reducing its particle size, allowing greater surface area for leaching and microbial action. Verhoeven (1980) found that half of the plant material had

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

445

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

Gammarus pseudolimnaeus Valley creek (MN, USA) Credit river (Ontario, Canada)

DM DM

2.7 0.6

16.3 2.9

6.0 4.7

Waters and Hokenstrom (1980)c Marchant and Hynes (1981)b

G. pulex Rold Kilde springbrook (Denmark) Tadnoll Brook (UK) Tadnoll Brook (UK) Jutland Beech forest (Denmark) Jutland mixed forest (Denmark)

DM DM DM AFDM AFDM

1.9 4.6 4.6 1.2 1.2

3.8 12.9 12.8 2.5 2.6

2.0 2.8 2.8 2.1 2.2

Iversen and Jessen (1977)b Welton (1979)a Welton (1979)c Friberg et al. (2002)c Friberg et al. (2002)c

G. minus Allegheny plateau (VA, USA)

DM

0.4

2.4

5.5

Griffith et al. (1994)c

G. aequicauda Evros delta (Greece) Ichkeul lagoon (Tunisia)

DM AFDM

4.2 0.3

22.4 0.8

5.3 3.8

Kevrekidis and Lazaridou-Dimitriadou (1988)c This studya

G. mucronatus Salt marsh pools (MA, USA) Salt marsh pools (MA, USA) Salt marsh pools (MA, USA) Chesapeake Bay (VA, USA)

DM DM DM DM

1.0 1.0 1.0 0.3

14.8 15.8 12.5 7.7

14.8 15.8 12.4 23.6

Idotea chelipes Arcachon basin (France) Ichkeul lagoon (Tunisia)

DM AFDM

0.5e 0.7

2.4e 1.1

5.3 1.6

Cloarec et al. (1983)b This studya

I. baltica Chesapeake Bay (VA, USA)

DM

0.1

1.1

9.5

Fredette et al. (1990)c

Sphaeroma hookeri Ichkeul lagoon (Tunisia)

AFDM

0.2

0.5

2.3

This studya

a b c d e

P

P/B

Authors

LaFrance and Ruber (1985)c LaFrance and Ruber (1985)d LaFrance and Ruber (1985)d Fredette et al. (1990)c

Loss summation. Increment summation. Sizeefrequency method. Instantaneous growth. Per 100 g DM Ruppia cirrhosa.

decomposed within two months and that after a year practically no plant material was left. In less than 4 days, the mechanical 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 much plant material and are in turn colonized by a layer of microbes and are food for suspension feeders (e.g. Cerastoderma glaucum (Poiret), Mercieriella enigmatica Fauvel, Conopeum seurati (Canu)), or browsers (Hydrobia ventrosa (Montagu), Haminea navicula (Da Costa)) and deposit-feeders (Scrobicularia plana (Da Costa), Abra tenuis (Montagu), Corophium volutator Pallas, Cyathura carinata (Krøyer)). Using the mean annual assimilation efficiency (A/C ) of G. aequicauda and S. hookeri according to Mene´ndez and Comı´n (1990) and of I. chelipes according to Verhoeven (1980) feeding on green and decomposing Ruppia cirrhosa, the total shredder assimilation at Tinja during the study period amounts to 152 kJ m
2 yielding a net growth efficiency (P/A) of 33%. A critical assimilation level must be maintained to achieve high energy storage efficiency (Swiss and Johnson, 1976). The P/A value calculated from the published feeding rates is probably an overestimation because it includes immatures growing at a faster rate than they would maintain later. But

even this inflated value could be low enough to retard development to a point that it no longer coincides with appropriate environmental conditions with a subsequent decline of these organisms in the benthic community. Low growth efficiency, of course, means a smaller proportion of energy flow available for the next trophic level. The elimination (E ) calculated by the Boysen-Jensen (1919) method amounts to 52 kJ m
2, rendering the ecological efficiency (E/C ) of the shredders as 22% available to the next trophic level such as outswimming migrant fish (eels, mullets) during winter. The shredders, characterized by high P/B ratios and high importance for predation, do not play an important role in the direct consumption of macrophyte biomass but in processing organic matter to different trophic levels through macrophyte fragmentation. In the Ichkeul lagoon, the role of the shredders as a link between primary producers and predators and detritus feeders was proportionally enhanced during the study period due to the thick layers of dead Potamogeton pectinatus matter which was not appreciated by the wintering waterfowl. The vascular plant tissue poor in essential nutrients and slowly degradable is necessary for the survival of heterotrophic organisms. The time lag in the utilization of the slowly degradable detritical material assures a constant energy source for heterotrophic organisms

446

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throughout the year, in contrast to photosynthesis which is seasonal in temperate climates. Acknowledgements This study was carried out as part of the international programme ‘‘Etude pour la sauvegarde du Parc National de l’Ichkeul’’ financed by the Kreditanstalt fu¨r Wiederaufbau (KfW) under the aegis of the Tunisian authorities, in particular the Agence Nationale pour la Protection de l’Environnement. Thanks are due to the team from the Groupement d’Inte´reˆt Scientifique (GIS) Posidonie for field assistance and to colleagues at UMR 6540 CNRS Dimar (Diversite´, Evolution et Ecologie fonctionnelle marine) for advice and work facilities. The present research was supported by a Ph. D. grant from the Landesgraduiertenfo¨rderungsgesetzes (LGFG) Germany. The study would not have been possible without the support of Prof. Ju¨rgen Schwoerbel, mentor and friend. Finally, the authors are grateful to Michael Paul for improving the English text and to two anonymous referees for very valuable comments. References Bachelet, G., 1982. Quelques proble`mes lie´s 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 determination of sizeefrequency distribution of small gastropods. Example of the mud snail Hydrobia ventrosa (Gastropoda: Prosobranchia). Hydrobiologia 485, 143e152. Cloarec, M., Labourg, P.J., Lasserre, G., 1983. Cycle, croissance et production d’un isopode Idothea chelipes (PALLAS) d’une lagune ame´nage´e du bassin 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 invertebrates 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 Perspective. 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 fu¨r Hydrobiologie 153, 197e215. Griffith, M.B., Perry, S.A., Perry, W.B., 1994. Secondary production of macroinvertebrate shredders in headwater streams with different baseflow alkalinity. 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 Association of the UK 28, 141e153.

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