Avicennia Marina Mangrove Forest

Home , Avicennia, Avicennia marina, Cerithidea decollata

MARINE ECOLOGY PROGRESS SERIES Published June 6 Mar Ecol Prog Ser

Resource competition between macrobenthic epifauna and infauna in a Kenyan Avicennia marina mangrove forest

J. Schrijvers*, H. Fermon, M. Vincx

University of Gent, Department of Morphology, Systematics and Ecology, Marine Biology Section, K.L. Ledeganckstraat 35, B-9000 Gent, Belgium

ABSTRACT: A cage exclusion experiment was used to examine the interaction between the eplbenthos (permanent and vls~tlng)and the macroinfauna of a high intertidal Kenyan Avicennia marina mangrove sediment. Densities of Ollgochaeta (families Tubificidae and Enchytraeidae), Amphipoda, Insecta larvae, Polychaeta and macro-Nematoda, and a broad range of environmental factors were followed over 5 mo of caging. A significant increase of amphipod and insect larvae densities in the cages indicated a positive exclusion effect, while no such effect was observed for oligochaetes (Tubificidae in particular), polychaetes or macronematodes. Resource competitive interactions were a plausible explanation for the status of the amphipod community. This was supported by the parallel positive exclusion effect detected for microalgal densities. It is therelore hypothesized that competition for microalgae and deposited food sources is the determining structuring force exerted by the epibenthos on the macrobenthic infauna. However, the presence of epibenthic predation cannot be excluded.

KEYWORDS: Macrobenthos . Infauna . Epibenthos - Exclusion experiment . Mangroves . Kenya

INTRODUCTION tioned that these areas are intensively used by epibenthic animals as feeding grounds, nursery areas and Exclusion experiments are a valuable tool for detect- shelters (Hutchings & Saenger 1987).In order to assess ing the influence of epibenthic animals on endobenthic the importance of the endobenthic community under communities. Most studies have been conducted in the mangrove trees as a food source, exclusion experi- temperate intertidal, soft and unvegetated areas (Reise ments were conducted in a Kenyan Avicennia marina 1977, Virnstein 1977, 1979, Hulberg & Oliver 1980, stand. Detection of epibenthic predation in such a high Federle et al. 1983, Gee et al. 1985, Marinelli & Coull intertidal zone would indicate that the mangrove forest 1987, Hall et al. 1990a), soft seagrass-covered coastal floor, and not only the creeks and flats surrounding zones (Young et al. 1976, Orth 1977, Reise 1977, 1978, it, are of importance as a feeding ground for the epi- Young & Young 1977, Vlrnsteln 1978) or salt marshes benthos. (Bell 1980, Hoffman et al. 1984). In general, predation The few exclusion studies that have been conducted was accepted as the obvious epibenthic influence on in mangroves focused mainly on the meiobenthos (Dye the macro- and meiofauna. About half of the studies & Lasiak 1986, Alongi 1989, Dittman 1993, Schrijvers which excluded large epibenthic predators mentioned et al. 1995), leaving the macrobenthos (>OSmm) as an an at least 2-fold increase in total endobenthic prey interesting endobenthic category yet to be studied. abundance (Reise 1985). When dealing with high intertidal Avicennia marina Mangrove areas are soft vegetation-covered zones sediments, it is expected that the impact of the perma- ~h:,':cteTi.~tj~ "f trcniralre--- rnactc------. !t ?c fr~ql~ont!:~met- nent ~~ihsnthnziz morp important than that nf visiting fauna. These resident organisms are mainly leaf shredders and selective or nonselective deposit feeders (crabs and gastropods). It is hypothesized that ex-

0 Inter-Research 1996 Resale of full art~clenot permitted 124 Mar Ecol Prog Ser 136: 123-135, 1996

1 ] baregrounds

Rhizophoramucronala dominated mainland,terrestrialvegetation

A~icenniarnarifia,tall trees

1water Fig. 1. Map of the western creek of Gazi Bay with indication of vegetation types and location of the Avicennla marinastation (arrow) clusion of the epibenthos would therefore result in: sometimes remained in puddles durlng low tide. The (1) leaf accumulation, favouring infaunal leaf shred- permanent epibenthic community mainly consisted of ders; (2) accumulation of detritus, bacteria, protozoans gastropods (Terebralia palustris and Cerithidea decol- and microalgae, favouring infaunal deposit feeders. lata) and crabs (Sesarma meinerti and Metopograpsus thukuhar). Experimental design. All epibenthic and hyperben- MATERIAL AND METHODS thic animals (h.ereafter called 'epibenth.osl) (>2 mm) were excluded from cages and the influence on the Study area. The study site was a non-exploited Avi- macrobenthic infaunal structure was followed through cennia marina mangrove vegetation zone bordering time. Experimental design sensu Hurlbert (19841, cage the westbank of the western creek of Gazi Bay, about construction and execution procedures were identical 50 km south of Mombasa. Kenya (Fig. 1). This zone to those used by Schrijvers et al. (1995). Besides the full was situated >3 m above mean low water spring level cages (C) (an enclosed 1 X l m sediment surface), 2 and was thus only inundated during the high water of control treatments were chosen: tr.ue blanks (B) and a spring tide. It represented a typical high intertidal partial cages (P) (an enclosed 1 X 1 m sediment surface mangrove forest habitat, covering a total area of with 1 open side). B controlled natural temporal varia- >0.5 km2 The zone was visited by several epibenthic tion, while P corrected for poss~bleprocedural impacts. animals (authors' pers. obs.), e.g. gobiid fish which Each treatment was employed in 3 units. Schrijvers et al.: Resource competition in a mangrove forest 125

Six series of samples were taken over time: terize the granulometry of the sediment. This analysis - Period 1 before caging (6 August 1992); was done both before and after combustion at 600°C. - Period 2: after 22 d of caging (28 August 1992); Before analysis, the > 1 mm fraction was mechanically - Period 3: after 50 d of caging (25 September 1992); separated by sieves. It consisted mainly of root mater- - Period 4: after 85 d of caging (30 October 1992); ial. An important granulometric characteristic was the - Period 5: after 112 d of caging (26 November 1992), median of the sediment. This is a measure for the gen- - Period 6: after 139 d of caging (23 December 1992). eral grain-size tendency of the sediment and corre- Core holes were immediately filled with silicon plugs sponds to the 50% line of the cumulative distribution or sediment bags to avoid effects on the surrounding curve (Holme & McIntyre 1984). The lower this sediment that was to be sampled later in the experi- median, the siltier the sediment (negatively correlated ment (Marinelli & Coull 1987). with the 'X,of mud). Environmental factors. One 6 cm diameter core The upper layers of a 1 cm diameter core (0 to 2 cm sample was taken in each unit per period to a depth of and 2 to 4 cm) were used to estimate the percentage of >l0 cm. The bottom water in the sample holes was organic carbon with a Carlo Erba NA 1500 series 2 C- analyzed for bulk values of pH, salinity and dissolved analyser These layers were also analyzed for chloro- oxygen (DO2)with a combined pH bottom electrode, a phyll a and fucoxanthin pigment concentrations (using refractometer, and a Clark type 737 electrode respec- a Gilson HPLC-chain according to a slightly modified tively. Other measurements were performed on the method of Mantoura & Llewellyn 1983). Chlorophyll a upper slice and the rest fraction of the core (0 to 2 cm could be correlated with the general concentration of and 2 cm to rest). Temperature and redox potential microalgae in the sediment (Gerold & Hughes 1994a). were measured using a bar thermometer sensitive to Fucoxanthin pigments pointed to diatoms in particular O.Ol°C and a combined redox electrode respectively. (D. Van Gansbeke pers. comm.). The percentage of particulate organic matter (POM) Biotic factors. Endobenthic samples were obtained and some granulometric variables were determined. by taking 1 handcore (12.5 cm diameter) (Fig. 2) per After drying at 100°C, the POM was quantified via the unit (with 3 replicate units per treatment). The long loss in weight following combustion at 600°C for 4 h. A handle permitted sampling of the cage and partial CoulterRLS Particle Size Analyser was used to charac- cage treatments without disturbing the surrounding

Fig. 2. Corer for macrofauna samples. COlmponents (a) separated and [b) attached Mar Ecol Prog Ser 136: 123-135, 1996

sediment. The core was taken to a depth of 20 cm and drilus sp.) and Enchytraeidae (mainly Marionina divided into 2 parts consisting of the top 2 cm and the sp.) (C. Erseus pers comm.); rest. Before sieving, both parts were preserved in a - Insect larvae: families Dolichopodidae and Limoni- cold 8% neutralized formalin solution. Extraction of idae (B. Goddeeris pers. comm.); macrofauna from the sediment was achieved by siev- - Amphipoda: family Grandidierellidae (Grandidier- ing with mesh sizes of 0.5, 1 and 2 mm. All the taxa ella sp.) (S. De Grave pers. comm.); (Oligochaeta, Amphipoda, Polychaeta, Insecta larvae, - Polychaeta: families Nereidae (Namalycastis sp.) Nematoda, Gastropoda and Cnidaria) were counted. and Opheliidae (Armandia sp.) (Day 1967); Several trials revealed that less than 10 % of the macro- - Nematoda: family Oncholaimidae (mainly Oncho- fauna occurred deeper than 2 cm. This led us to con- lairnus sp.) (Platt & Warwick 1988); centrate only on the upper layer. Densities are ex- - Gastropoda: not identified; pressed as numbers of individuals per 1 m2. - Cnidaria, not identified. The oligochaetes of 2 replicates of Periods 1, 2 and 5 While comparisons between temperate and tropical and all the insect larvae were identified to family and regions usually reveal a higher benthic diversity in the the amphipods, polychaetes and nematodes to genus latter, the number of taxa in this mangrove study was level. low. This probably reflects the high intertidal position Amphipod length (from peduncle to telson) was of the sampling site, which resulted in extreme anaer- measured with a drawing mirror under a stereoscopic obic conditions with abrupt changes in salinity, tem- microscope. The average individual arnphipod length perature, redox and DO2 (Tietjer, & Alongi 1990). per sample was calculated in order to test for adult Fig. 3 shows the relative abundance (average of all invasion or reproduction in the cages. blank units over all periods) of the macrobenthic taxa. Statistical analysis. An analysis of variance It is clear that the oligochaetes (78% tubificids and (ANOVA) was used to test for significant differences of 22% enchytraeids) made up the largest part of the macrofauna densities in different treatments (B, P and C) and periods (1 to 6) for the top 2 cm of the sediment. A 3 X 6 between-groups factorial design (f)was used, considering treatments and periods as independent groups. The total variance of all groups was used as error variance in the analysis. Moreover, a 3 (between groups) X 6 (within subjects) mixed design (m) was constructed, with treatments as groups and periods as subjects repeated over time. In this case, error variance was limited to the within-period variances. Detailed comparison between groups was made by contrast analysis. Exclusion effects (E)were defined as significant differences (p < 0.05) between cage and blank- partial cage, while procedural effects (Pr) yielded significant differences (p < 0.05) between cage-partial cage and blank. The density data were root-root transformed, and the % values of environmental factors were transformed angularly to meet the ANOVA assumptions (normality, homogeneity of variances, and non-correlation between means and variances). In those cases where these assumptions were not met, the non-parametnc Kruskal-Wallis and Median tests were applied (e.g. for oligochaete family densities using only 2 replicates).

RESULTS

Endobenthic composition Fig. 3. Relative abundance (%) of the major macrobenthir: The endobenthos was composed of the following taxa: infaunal taxa and oligocbaete farnllies (average of blank sites - Oligochaeta: families Tubificidae (mainly Ainu- over all periods) Schrilvers et a1 . Resource competition in a mangrove forest 127

macrobenthic infauna (94 %). Within a Chlorophyll a concentrat~on(ngig DM) the remaining 6%, the amphipod 8000, 1 genus Grand~d~erella(56 %) domi- - nated it was followed by the poly- 70001 blank chaete genus Nsmalycast~s (21 X), 6000 / partial cage gastropods (10.7 %), maci-obenthlc nematodes (?X), lnsect larvae (5%) 5000 and cnidailans (0 3 %) The polychaete 4000 genus Armandia was found only in the sediment of one single cage unit In 3000, ;,X I \ Period 5 . . ,-- \

Experimental results I

Environmental factors 0 2 2 50 85 112 139 Exclusion effect.A highly significant number of days after caglng exclusion effect after 50 and 85 d of caging was demonstrated for the con- b Medlan before cornbustlon (!m) centration of chlorophyll a Chloro- 400 phyll a incredsed about 5x m the cage blank as compared to the other treatments 340 partial cage (F19 4a)

Also, the medlan gram slze before I I 280 combustion (negatively correlated with the % of mud befo~ecombustion) underwent a significant exclusion 220 effect after 112 d of caging, showing a 1 5x decrease in the cages compared 160 to the partlal cage and blank treatments (Fig 4b) This effect was not found for median grain size after com- loo bustion and was therefore related to the muddy detritus fraction. 40 0 22 50 85 112 139 Procedural effect.As a result of the number of days after caglng cage and partial cage construction, the sediment underwent a salinity decrease Fig. 4. Exclusion effect (E: sign~f~canteffect with p < 0 05; f:factorial des~gn,m: between 0 and 22 d of (~i~,5a), mixed design) on (a) chlorophyll a concentration and (b) median grain size before combust~on Mean values and standard dev~ationsof the upper sllce (0to Both statistical designs (factorial and 2 cm) over time for the cage, partial cage, and blank treatment mixed) indicated a procedural treatment effect for pH, with a more acidic sediment in the blank units throughout the experiment (Fig. 5b). Biotic factors The median grain size after combustion (which is in general negatively correlated with the inorganic Exclusion effect.Cage amphipod densities exceeded muddy fraction) showed a decrease In the cages and those of partial cage and blank sediment from Day 85 partial cages as compared to the blanks. This led to a of the experiment onwards with a factor of 4 to 5. This procedural effect after 112 experimental days (Fig. 6). increase was confirmed by an overall significant exclu- A possible procedural impact on redox potential sion effect (Fig. ?a). could not be detected since practical problems made it The average individual amphipod length did not dif------1- r- --^r,.-- &L;, ~III~U>>;~L~: ..,,.,VUI;Ub!~ dnrizg the firs! 3 fer significirnt!;~ amclng treatm~nts (Fit 7h) periods. The density of insect larvae increased signif~cant- No effect.No clear effect was detected for all other ly after 85 d. A significant exclusion effect was de- variables (including the % of POM). tected after 85 and 139 d, cage densities reaching 5 Mar Ecol Prog Ser 136: 123-135, 1996

a. Salinity (psu) between the blank and partial cage treatment which was not detected before this period. As the ollgochaetes made up 94 % of the total macro-infaunal density, trends in the total community were inextricably linked with oligochaete trends (Fig 9b). No effect. Neither procedural nor exclusion effects were detected for polychaetes (Fig. lOa), macronematodes (Flg lob), gastropods and blank cnidarians...... DISCUSSION 10 0 22 50 85 112 139 number of days after caging Experimental design

The characteristics of the applied experimental design have been discussed by Schrijvers et al. (1995). All epibenthic fauna (>2 mm) was non-selectively excluded in this study and the most conspicuous observed effects are believed to result from the removal of the dominant epibenthos. Larger mesh sizes (above 2 mm) have been shown to reduce the exclusion effect (Reise 1977, 1978, Kneib & Stiven blank 1982) while a smaller mesh (<2 mm) . - ...... was expected to enhance fouling. I....J cage 1...... ~r (f + m) ...... 1...... 4 In analogous studies conducted in U temperate regions, where predation is 5.2 1 believed to be the driving force struc- 0 22 50 8 5 112 139 number of days after caaina- - turing endobenthic communities, significantly increasing macrobenthic Fig. 5. Procedural effect (PI: significant effect with p < 0.05,I f: factorial design, m: mixed desiclnl on (a) salinjty and (b] pH. Mean values and standard devia- densities near the sediment surface tions of the upper slice (0to 2 cm] over t&e for the cage, partial cage, and blank were the dominant exclusion effect treatment (Virnstein 1977, 1979, Holland et al. 1980). We therefore only analyzed the upper sediment layer. Moreover, sev- to 6x higher levels than in the other treatments eral trials revealed that less than 109'0 of the macro- (Fig. 8). fauna occurred deeper than 2 cm. Procedural effect. Already after 22 d, a significant With respect to the available literature, the following procedural effect was detected for oligochaete densi- should be taken into account: ties. This effect was repeated after 2 mo. The cage and (1) Most of the unsuccessful experiments (no effects partial cage densities slightly surpassed the blank den- or only procedural effects) have not been published. sity (Fig. 9a). This leads to wrong conclusions concerning experi- Table 1 shows the results of the Kruskal-Wallis and mental efficiency and benthic interaction levels (Hul- Median tests on the Tubificidae and Enchytraeidae berg & Oliver 1980, Connell 1983). densities for Periods 1. 2 and 5. Neither test detected (2) The influence of epibenthic predators or competi- any effect. Nevertheless, the Median test suggested a tors on infaunal density and diversity is bound to vary procedural effect for the Tubificidae after 112 caging with habitat, season, and succession phase. These fac- days: a significant difference (p < 0.05) was observed tors are usually not mentioned (Holland et al. 1980). Schrljvers et a1 Resource compet~tionIn a mangrove forest -

Fig 6 Procedural effect (Pr signif~cant Medlan after combust~on(pm) effect with p < 0 05, f factorial design) on median gram s~zeafter combustion Mean 480 values and standard deviations of the upper shce (0 to 2 cm) over tlme for the 440 cage, partial cage and blank treatment 400

360 Experimental results 320

Environmental factors 280

Microalgae. The clear exclusion 240 effect on the chlorophyll a concentra- 200 tion is correlated with the density of microalgae in the sediment (Admiraal 160 l 1977, Gerdol & Hughes 1994a). The 0 22 50 85 112 139 number of days after caging

a. Arnphipod density (Grandidierella) (ind.lm2) increase possibly results from the exclusion of the microalgae feedlng partial cage epibenthos (Table 2). Microalgal growth can also be a response to a release of nutrients from previously deposited mud. However, this was not evident from our study. Sediment texture and detritus. Sev- eral studies showed that mud and detritus deposition can be due to procedural effects in exclusion cages (Virnstein 1977, Hulberg & Oliver 1980, Woodin 1981, Menge et al. 1986, Schrijvers et al. 1995), probably as a result of increased water stagnation. 0 22 50 85 112 139 This effect can possibly attract or repel number of days after caging certain infaunal species (Hulberg & Oliver 1980, Heip et al. 1985). In this b Average individual arnphipod length (mm) study, a decrease of the median grain size of the inorganic sediment fraction ...... indicated a shift to a slightly siltier con- part~alcage dition due to the cage construction (after 112 d). However, the exclusion effect on the median grain size before combustion (which is negatively correlated with the percentage of mud before combus-

Fig. 7 (a) Amphipod density and (b) avel- agn individual amphlpod length in the cage, partial cdge and blank treatment. Mean values and standard dev~diiol~soi ii~e upper slice (0 to 2 cm) over time. E: signifi- 0 2 2 50 85 112 139 cant exclusion effect with p < 0.05, f:factor- number of days after caging ial design, m: mixed design 130 Mar Ecol Prog Ser 136: 123-135, 1996

FI~8 Insect larvae dens~tyIn the cage, Insect larvae density (~nd/m2) part~al cage and blank treatment Mean values and standard deviations of the 2400 upper slice (0 to 2 cm) over time E slgn~fl- cant exclusion effect wlth p < 0 05, f facto-

r~aldesiqn, m mxed des~gn 11- blank partial cage - 1T ,,, 1 tion) suggests the muddy detritus to be marginally influenced by the 1200 exclusion. Physicochemical factors. It 1s obvious that the sediment of treatments P '0° and C became more humid through time than that of treatment B as a result of cage construction (PVC O plates and cover) (Table 3). This I I resulted in lower salinities. 0 22 50 85 112 139 number of days after caglng

a Oligochaete density (1ndlm2) Biotic factors 100000 Amphipod density. Gut content anal- 1I- blank part~alcage ysis of several individuals (N = 10) of 80000 /I I:: cage the genus Grandidierella (Schnjvers 1 unpubl.) revealed that detritus and small leaf particles, originating from the mangrove sediment, were dominant in the diet. The mangrove amphipod Parhyale hawaiensis was shown to consume large quantit~esof decomposing mangrove leaves (Poovachiranon et al. 1986).In general, crabs, amphipods, capitellid polychaetes and isopods seem to be breaking down mangrove 22 50 85 112 leaves in small particles, egesting it as number of days after caging plant detritus which thus becomes a food source for other species (Poova- b. Total macrobenthic density (~nd/mZ) chiranon et al. 1986, Camillen 1992). 120000 No microalgae were observed In the stomach of Crand~d~erellasp Gerdol & Hughes (1994b) found that mlcroalgae were not detectable in the gut of Coro- '. ' phlurn volutator, although this amphipod was shown to Ingest 4000 cells h-' and to significantly reduce diatom den- I

I sities Moreover, Pinckney & Sandulli t I

I Fig 9 (a) Oligochaete and (b) total macrobenthos density in the cage partial cage and blank treatment Mean values and standard deviations of the upper slice (0 to 2 cm) over time Pr s~gnLflcant procedural effect 0 22 50 85 112 139 with p < 0 05, f factonal des~gn,m muted number of days after caglng des~gn Schrijvers et al.: Resource competition in a mangrove forest 131

Table 1. Densities (ind. m ?) and results of the statistical Kruskal-Wallis and Median tests (with p < 0.05) for the oligochaete families Tubificidae and Enchytraeidae over 3 periods. B: blank, C: cage and P: partial cage. Bold indicates significance

Before caging 22 d after caging 112 d after caging Mean SD Mean SD Mean SD - - Tubificidae Blank 13040 2508 379 379 Cage 20421 828 6749 4517 Partial 26067 10581 2390 557 Kruskal-Walhs B=C/B=P/P=C B=C/B=P/P=C Median B+C/B=P/P=C B#C/B=P/P=C

Enchytraeidae Blank Cage Partial Kruskal-Wallis Median

a Polychaete density (ind./m2) (1990) refer to diatoms as an important food source for many amphipods. blank The exclusion effect on this genus partial cage I can possibly be related to 3 types of ..... 2400 l1.... I...... cage interactions: ,I: . (1) Predation on amphipods: Stom- ach analysis of the permanent epibenthos revealed little predatory evidence (Table 2). Possible predation by the visiting fauna might have been minor compared with the competitive influence of the permanent epifauna. (2)Competition for leaf material: The amphipod gut content analysis and the findings of Poovachiranon et al. (1986) and Camilleri (1992) suggest that re- 0 22 50 85 112 139 source competition for leaves is an ac- number of days after caging ceptable explanation for the exclusion effect which was found. The exclusion b Nematode density (ind/m2) of Sesarma meinerti, which mainly feeds on mangrove leaves (Table 2), 1- blank could have been the direct inducement partial cage 1 1 to the amphipods' increase in the cage. 1---- cage 1 I

On the other hand, Camilleri (1989) I argued that this resource competition for leaves and leaf particles may be facilitated by the availability of different particle sizes. Sesarma meinerti takes whole leaves and large particles while small shredders like amphipods are restricted to rather small particles. Moreover, the role of direct bacterial decomposition of the leaves could also I have gained in importance (Robertson 0 22 50 85 112 139 Q. nanini IQQQI .J. "U....,* Ad.,.,,. number of days after caging (3) Competition for microalgae and Fig. 10. (a) Polychaete and (b)nematode densities in the cage, partial cage and deposited food: The excluded epiben- blank treatment. Mean values and standard deviations of the upper slice (0 to thos was dominated by deposit and 2 cm) over time Mar Ecol Prog Ser 136: 123-135. 1996

Table 2. Description of permanent and visltlng epibenthos excluded from the cages In the Avicennia marina zone studied (in terms of average densities, feeding behawour and habitat)

Epibenthic species Source Feeding behaviour Habitat Average density (ind. m-" (this study)

Cerithidea decollata Brown (1971) Non-selective deposit Frequently McIntosh (1984) feeding (detritus) on trees Dye & Lasiak (1987)

Dye & Lasiak (1987) Non-selective deposit feeding Sediment (inorganic parts, microalgae, dwelling bacteria, protozoans)

Cott (1929) Vegetarian Sediment 0 25 Emmerson & Omnivorous with preference dwelling (1 burrow m-') McGwynne (1992) for leaves (75% of diet) Steinke et al. (1993)

I Metopograprus thukuhar F. Dahdouh-Guebas et Omnivorous with preference Forest dweller al. (pets. cunu11.j for macroalgae and an~mal (trunk, roots, floor) McIntosh (1988) items (sometimes fresh leaves, seedlings, leaf litter and detritus)

Visiting fauna Herbivorous or carnivorous ? High tidal (only (unknown) during spring tides)

microalgae feeders (Table 2). In spite of the absence increased, the microalgal peak started to return to its of microalgae in their stomachs, the exclusion effect former level. In addition the indirect exclusion effect on amphipods was detected 1 mo after the detection on muddy detritus paralleled the exclusion effect on of a clear exclusion effect on the concentration of amphipods and the amphipods' stomachs contained a chlorophyll a. As soon as amphipod cage densities clear detrital fraction. This kind of competition is believed

Table 3 Qualltatlve observations (-: absent, +: present, k: intermediate) after be the determining 1 and 5 mo of caging with an evaluation of the procedure. B: blank, C: cage, Insect larvaedensity. According to P: partial cage O'Meara (1976), marine insect larvae

I I are basically omnivores (mainly Artefact After 1 mo caging After 5 mo caging Evaluati.on browsers and filter feeders). The B C P BCP resource competition hypothesis (as discussed for amphipods) would be Fouling - OK Shading - c procedural supported if most insect larvae found Sedimentation - OK were browsers abrading solid mater- Moisture - Procedural ial and manipulating and breaking Litter fall + OK down leaf and detritus particles. Epibenthos + 0 K However, most of the larvae in this study belonged to the Dolichopodi- dae family (B. Goddeeris pers. Table '.Effect size (f)per taxon with the 'between treatment' variance (MSef,,,,), comm.) whose members are preda- the 'error' vanance (MS,,,,,) and the estimated magn~tudeof treatments (qz)(cal- ceous and are frequently found In culated vla tables and formulas provlded by Cohen 1977) damp soil, sand and rotting wood in the intertidal zone (Smith 1989). Taxon Design MSelrect MSerror q2 f Power Examination of gut contents of the Dolichopodidae found in this study Polychaeta Factorial 3.48393 2.506394 0.07 0.274 11"h Mixed 3.48393 2.845246 0.04 0.05 5% revealed a high number of oligochaete setae. Nematoda Factorial Mixed O'Meara (1976) mentioned that fish and other insects were the main Schrijvers et al.: Resource colmpetition in a mangrove forest 133

predators on insect larvae. Still, no larvivorous fishes 1979) and in mudflats (Reise 1978) polychaetes reacted have been described for the studied area (J. Mees pers. positively to epibenthic exclusion. comm.). Some studies have shown the number of meioben- Oligochaete and total densities. Both densities were thic nematodes to double in the cage sediment in con- closely linked since oligochaetes made up the largest trast with the control cages after 2 mo of epibenthic part of the total infaunal macrobenthos. exclusion (Relse 1979, Schrijvers et al. 1995). The Procedural effects on oligochaetes have been docu- macronematodes in our study all belonged to the fam- mented before and are thought to be a result of sedi- ily of Oncholaimidae. These are believed to be scav- ment modification caused by the cage construction engers with a very broad diet that stimulate bacterial (Hulberg & Oliver 1980, Hall et a1 1990a). The pro- and fungal metabolism by decomposing organic mat- cedural effect in our study could possibly be linked ter (Lopez et al. 1979, Jensen 1987). This alternative with changes in environmental factors due to cage feeding behaviour could possibly have kept this group construction: from being influenced by resource competition. (1) Salinity. It has been stated that this factor is cru- The absence of significant effects for polychaetes cial in determining oligochaete distribution (Giere and nematodes possibly results from the efficiency of 1980, Giere & Pfannkuche 1982). This holds especially the experimental design to detect effects. Parameters for salinity of tropical, intertidal areas where 40 psu is significance levels (0.05),effect sizes (f),and the num- the upper tolerance limit for oligochaetes (Giere & ber of treatment groups (18) resulted in power levels of Pfannkuche 1982). 8 % for polychaetes and 5 % for nematodes (average (2) pH: Tolerance experiments (Giere 1977 In Giere power for factorial and mixed design) (Hall et al. & Pfannkuche 1982) showed that extreme alkalinities 1990b).The effect size (f) per taxon (Table 4) was cal- (exceeding 9) in combination with high salinities and culated via the ANOVA variances, the number of temperatures could cause a deterioration of viability in degrees of freedom (10), of groups (18), and of repli- interstitial tubificids. No such conditions were fo.und in cates within a group (3).The power levels point to the this experiment. chance of avoiding a type I1 error (l -P)and were cal- (3) Light intensity: The shadow caused by the con- culated via the power table provided by Cohen (1977). struction cover could possibly have induced an upward The low levels could possibly result in an undetectable vertical migration of littoral, negative1.y phototactic influence. oligochaetes (Giere & Pfannkuche 1982). (4) Mud: The decrease in grain size could have influenced habitat selection. However, this is more relevant CONCLUSION in mesopsammic forms for which interstitial space is a crucial condition for life (Giere & Pfannkuche 1982). Oligochaete, polychaete and macro-nematode den- Nevertheless, most studies concentrating on oligo- sities were not positively affected after epibenthic chaete densities in temperate areas found successful excluslon. The positive exclusion effect on the amphi- exclusion effects. It is usually concluded that these pod community seems to point to a resource competi- effects are a result of predation exclusion (Reise 1977, tion with the dominant epibenthos for microalgae, 1978, Kneib & Stiven 1982, Connell 1983, Gee et al. muddy detritus and, possibly, for leaves. No driving 1985). The only experimental study dealing with force for the conspicuous positive exclusion effect on oligochaetes of mangrove sediments was that of Schrij- insect larvae could be found. However, in this case too, vers et al. (1995), which indicated that meiobenthic predatory exclusion is believed to be unimportant. oligochaetes are influenced by competition with the Therefore, the predation hypothesis is thought to be deposit-feeding epibenthos rather than by predation. minor as an interaction between the epibenthos and The slight increase of the oligochaete density in the macrobenthic infauna under the Avicennia marina cage after 112 d (which was not statistically significant) stand studied. A resource competitive effect caused by could also be a response to the indirect excluslon effect the permanent epibenthos is found to be more conspic- on the muddy detritus. The most important dietary uous. The questlon whether epibenthic predation on item for interstitial tubificids and enchytraeids is endobenthos from this high intertidal mangrove forest believed to be organic matter (detritus) enriched with floor is present or absent remains to be answered. bacteria (Giere & Pfannkuche 1982). Polychaete and nematode densities. As found for Acknowledgements. Financlal support was given by the meioberithlc pc!ychzc:cs $2 a Ceficps mangrove FKFO-programme 32.0043.88 and 32.0009.92 of the Belgian !?p! National Fund for Sclentltlc Kesearcn and rile ice~lyd-Eeiyium sediment (Schrijvers et al. 1995), macro-polychaetes Project in Marine Sciences In cooperation with the EC project did not show an exclusion effect. However, In other 'Dynam~csand Assessment of the Mangrove Ecosystem in experimental studies in seagrass beds (Reise 1978, Kenya' The work was performed at the Kenya Marine and 134 Mar Ecol Prog Ser

Fisheries Research Institute in Mombasa (Dr E. Okemwa) and Gerdol V, Hughes RG (1994b) Feeding behaviour and dlet of at the Section of Marine Biology in Gent. Julius Okondo. Ann Corophlum volutator in an estuary in southeastern Eng- Vanreusel, Jan Mees, Steven Degraer and Sandra Vanhove land. Mar Ecol Prog Ser 114:103-108 offered valuable comments on earlier versions of the manu- Giere 0 (1980) Tolerance and preference reactions of marine script. The help of the technical staff of the Institute of 2001- Oligochaeta in relation to their distribution. In: Brinkhurst ogy and the K.M.F.R.I. was indispensable to the sampling and RO. Cook DG (eds) Aquatic oligochaete biology. Plenum sample processing (special thanks to M. Beghyn, M. Publishing Corporation, New York, p 385-409 Bruyneel, G. De Smet, W. Gyselinck, N. Lefevre, A. Ototo, D. Giere 0. Pfannkuche 0 (1982) Biology and ecology of marine Schram, J. Van de Velde, D. Van Gansbeke, A, Van Kenhove, Oligochaeta, a review. Oceanogr Mar B~olA Rev 20: A. Vierstraete, and the people of Gazi). The first author 173-308 acknowledges a grant from the Belgian National Fund for Sci- Hall SJ, Raffaelli D, Basford DJ, Roberston MR (1990a) The entific Research (N F W 0.) importance of flatfish predation and disturbance on marine benthos: an experiment with dab Linianda limanda (L.).J Exp Mar Biol Ecol 1.36:65-76 LITERATURE CITED Hall SJ. Raffaelli D, Robertson MR (1990b) The role of the predatory crab, Liocarcinus depurator, in a marine food Admiraal W (1977) Influence of llght and temperature on the web. J Anim Ecol59:421-438 growth rate of estuanne benthic diatoms in culture. Mar Help C, Vincx M, Vrancken G (1985) The ecology of marlne Biol39:l-9 nematodes. Oceanogr Mar Biol A Rev 23:399-489 Alongi DM (1989) The role of soft-bottom benthic communi- Hoffman JA, Katz J, Bertness MD (1984) Fiddler crab deposit- ties in tropical mangrove and coral reef ecosystems. Rev feeding and meiofaunal abundance in salt marsh habitats. Aquat Sci 1:243-280 J Exp Mar Biol Ecol82:161-174 Bell SS ji980j Meiofauna-macrofauna interactions in a high Holland AF, Mountford NK, Hiegel MH, Kaumeyer KR, salt marsh habitat. Ecol Monogr 50:487-505 Mihursky JA (1980) Influence of predation on infaunal Brown DS (1971) Ecology of Gastropoda in a South African abundance in Upper Chesapeake Bay, IJSA. Mar Biol57: mangrove swamp. Proc Malac Soc Lond 39:263-278 221-235 Camilleri J (1989) Leaf choice by crustaceans in a mangrove Holme NA, Mclntyre AD (1984) Methods for the study of forest In Queensland. Mar Biol 102:453-459 marine benthos. Blackwell Scientific Publications, London Camilleri JC (1992) Leaf-lltter processing by invertebrates in Hulberg WL, Oliver JS (1980) Caging manipulations in a mangrove forest in Queensland. Mar Biol 114:139-145 marine soft-bottom communities: Importance of animal Cohen J (1977) Statlstlcal power analysis for the behavioural interactions or sedimentary hab~tatmodificat~ons Can J sciences Academic Press, New York Flsh Aquat Sci 37:1130-1139 Connell JH (1983)On the prevalence and relative importance Hurlbert SH (1984) Pseudoreplication and the deslgn of eco- of interspecific competition: evidence from field expen- logical field experiments. Ecol Monogr 54:187-211 ments. Am Nat 122(5):661-695 Hutchings P, Saenger P (1987) Ecology of mangroves Univer- Cott HB (1929) Observations on the natural history of the s~tyof Queensland Press, St Lucla, Australia land-crab Sesarma meinerti, from Beira, with special ref- Jensen P (1987) Feeding ecology of free-living aquatic nema- erence to the theory of warning colours. Proc 2001 Soc todes. Mar Ecol Prog Ser 35187-196 Lond 46:679-692 Knelb RT, Stiven AE (1982) Benthic invertebrate responses to Day JH (1967) A monograph on the Polychaeta of Southern size and density manipulations of the common murnmi- Africa, Part I. Errantia. Trustees of the British Museum chog, Fundulus heteroclitus, in an intertidal salt marsh. (Natural History), London Ecology 63(3):1518-1532 Dittman S (1993) Impact of foraging soldiercrabs (Decapoda: Lopez G, Riemann F, Schrage M (1979) Feeding biology of the Mictyridae) on meiofauna in a tropical tidal flat. Rev Biol brackish-tvater oncholaimid nematode Adoncholaimus Trop 41 (3).627-637 thalassophygas. Mar Biol54:311-318 Dye AH, Laslak TA (1986) Microbenthos, rneiobenthos and Mantoura RFC, Llewellyn CA (1983) The rapid determination fiddler crabs. trophic interactions in a tropical mangrove of algal chlorophyll and carotenoid plgments and their sediment. Mar Ecol Prog Ser 32:259-264 breakdown products in natural waters by reverse-phase Dye AH, Laslak TA (1987) Assimilation efficiencies of flddler high performance liquid chromatography. Analyt Chim crabs and deposlt-feeding gastropods from troplcal man- Acta 151.:297-314 grove sedlments. Comp Biochem Physiol 87A(2):341-344 Marinelli RL, Coull BC (1987) Structural complexity and juve- Emmerson WD, McGwynne LE (1992) Feeding and ass~rnila- nlle fish predation on melobenthos: an experimental tion of mangrove leaves by the crab Sesarma meinerti approach. J Exp Mar Biol Ecol 108.67-81 de Man in relation to leaf litter production in Mgazana, McIntosh DJ (1984) Ecology and productivity of Malaysian a warm-temperate southern African mangrove swamp. mangrove crab populations (Decapoda: Brachyura). Proc J Exp Mar Biol Ecol 157(1):41-53 Asian Symp Mangrove Environ, Res Manag 1:354-377 Federle TW. Livingston RJ. Meeter DA, White DC (19831 Mod- McIntosh DJ (1988) The ecology and physiology of ifications of estuarine sedimentary microbiota by exclusion decapods of mangrove swamps. Symp Zoo1 Soc Lond 59: of epibenthic predators. J Exp Mar Biol Ecol73:81-94 315-341 Gee JM, Warwick RM, Davey JT, George CL (1985) Field Menge BA. Lubchenco J, Ashkenas RL (1986) Experimental experiments on the role of epibenthic predators in deter- separation of consumers on sessil prey in the low zone of a mining prey densities in an estuarine mudflat. Estuar rocky shore in the Bay of Panama: direct and indirect con- Coast Shelf Sci 21:429-448 sequences of food web complexity. J Exp Mar Biol Ecol Gerdol V, Hughes RG (1994a) Effect of Corophium volutator 100:225-269 on the abundance of benthic diatoms, bactena and sedi- O'Meara, GF (1976) Saltmarsh mosquitoes (Dlptera: Culici- ment stab~l~tyin two estuaries in southeastern England dae). In: Cheng L (ed)Manne insects North-Holland Pub- Mar Ecol Prog Ser 114:109-115 lishing Company, Amsterdam, p 303-333 Schrljvers et a1 . Resource corn petltlon In a mangrove forest 135

Orth RJ (1977) The importance of sediment stability in sea- Smith KGV (1989) An introduction to the immature stages of grass communities. In: Coull BC (ed) Ecology of manne British flies: Diptera larvae, with notes on eggs, puparia benthos. University of South Carolina Press, Columbia, and pupae. In: Dolling WR. Askew RR (eds) Handbooks p 281-300 for the identification of British insects, Vol 10, Part 14. Pinckney J, Sandulli R (1990) Spatlal autocorrelation analysis Royal Entomological Society of London, London of meiofaunal and microalgal populatlons on an intertidal Steinke TD, Rajh A, Holland AJ (1993) The feeding behavlour sandflat: scale linkage between consumers and resources. of the red mangrove crab Sesarrna rnejnerti de Man. 1887 Estuar Coast Shelf Sci 30:341-353 (Crustacea: Uccdpoda Grapsidae) and its effect on the Platt HM, Warwick RM (1988) Freeliving marine nematodes, degradation of mangrove leaf litter. S Afr J Mar Sci 13: Part 11. British chromadorids. In: Kermack DM, Barnes 151-160 RSK (eds) Synopses of the British fauna, no. 38. EJ Brill & Tietjen JH, Alongi DM (1990) Population growth and effects W Backhuys, Leiden of nematodes on nutrient regeneration and bacteria asso- Poovachiranon S, Boto K, Duke N (1986) Food preference ciated with mangrove detritus from northeastern Queens- studies and ingestion rate measurements of the mangrove land (Australia). Mar Ecol Prog Ser 68:169-179 amphlpod Parhyale hawaiensls (Dana). J Exp Mar Biol Virnstein RW (1977) The importance of predation by crabs Ecol 98:129-140 and fishes on benthic infauna In Chesapeake Bay. Ecology Reise K (1977)Predator exclusion experlrnents in an intertidal 58:1199-1217 mud flat. Helgolander Wiss Meeresunters 30:263-271 Vlrnsteln RW (1978)Predator caging experiments in soft sed- Reise K (1978) Experiments on epibenthic predation in the ~ments:caution advised. In. Wiley ML (ed)Estuarine inter- Wadden Sea. Helgolander Wiss Meeresunters 31:55-101 actions. Academic Press, New York, p 261-273 Reise K (1979) Moderate predation on meiofauna of the mac- Virnstein RW (1979) Predation on estuarine infauna: response robenthos of the Wadden Sea. Helgolander Wiss Meeres- patterns of component species. Estuaries 2(2):69-86 unters 32:453-465 Woodin SA (1981) Disturbance and community structure in a Reise K (1985) Tidal flat ecology - an experimental approach shallow water sand flat. Ecology 62(4):1052-1066 to species interactions. Springer-Verlag, Heidelberg Young DK,Buzas MA, Young MW (1976) Species densities of Robertson AI, Daniel PA (1989) The Influence of crabs on lit- macrobenthos associated with seagrasses: a field experi- ter processing in high intertidal mangrove forests in tropi- mental study of predation J Mar Res 34:57?-592 cal Australia. Oecologia ?8:191-198 Young DK, Young MW (1977) Community structure of the Schr~jversJ, Okondo J, Steyaert M, Vlncx M (1995) Influence rnacrobenthos associated wlth seagrass of the Indian River of epibenthos on meiobenthos of the Cenops tagal man- estuary, Florida. In: Coull BC (ed) Ecology of marine grove sediment at Gazi Bay, Kenya. Mar Ecol Prog Ser benthos. University of South Carolina Press, Columbia, 128:247-259 p 359-382

This article was submitted to the editor Manuscript first received: June 12, 1995 Revised version accepted: January 8, 1996