10
J. N. Am. Benthol. Soc., 2009, 28(2):416–425 Ó 2009 by The North American Benthological Society DOI: 10.1899/07–084.1 Published online: 7 April 2009 Aquatic fungi associated with decomposing Ficus sp. leaf litter in a neotropical stream Jose ´ Rinco ´n 1 AND Roberto Santelloco 2 Departamento de Biologı ´a, Facultad Experimental de Ciencias, Bloque A-2, Apartado 526, Universidad del Zulia, Maracaibo, Venezuela Abstract. Aquatic fungi are important decomposers of plant litter in temperate streams. However, these microorganisms have been poorly studied in tropical streams. We assessed the dynamics of aquatic hyphomycetes during the decomposition of Ficus sp. (Moraceae) leaves in an intermittent lowland stream of northwestern Venezuela. Our goals were to: 1) determine the composition of aquatic hyphomycetes during leaf decomposition, 2) assess the effect of different mesh sizes (i.e., coarse vs fine mesh) on assemblage composition and activity, and 3) assess the role of habitat (i.e., pools vs riffles) on fungal assemblages. Coarse- and fine-mesh litter bags were incubated in a pool and a riffle for 31 d. For each habitat and treatment, we determined physicochemical variables, sporulation activity, and the structure and composition of fungal assemblages. Leaf litter decomposition rates ranged from 0.058/d in fine-mesh bags in the riffle to 0.031/d in coarse-mesh bags in the pool. Decomposition rates were significantly influenced by habitat type, with the highest decomposition rates found in riffle habitats. Sporulation rates were significantly different between habitats but not between mesh sizes. The highest sporulation rate (399 spores mg 1 leaf dry mass d 1 ) and fungal diversity (16 spp.) was found in coarse-mesh bags in the riffle. Twenty- one fungal species were identified during the study. Anguillospora longissima and Lunuluspora curvula contributed up to 75% of the conidia produced in the coarse- and fine-mesh bags in the riffle, whereas Filosporella aquatica and Lemonniera terrestris accounted for 65 to 75% of the conidia produced in the coarse- and fine-mesh bags in the pool. In ordination space based on species composition, fungal assemblages formed 2 clear groups that corresponded to habitat type. A temporal change in fungal species composition was observed in riffle samples. Early succession assemblages (2–14 d) were characterized by the presence of A. longissima, L. curvula, and F. aquatica, whereas late assemblages (24–31 d) were dominated by Pyramidospora fluminea, Pyramidospora casuarinae, and unidentified sp 4. Overall, habitat type (pool or riffle) influenced sporulation rates and assemblage composition of aquatic hyphomycetes. Our study suggests that environmental factors associated with hydrology (e.g., stream velocity, width, depth) regulate fungal composition and activity and, hence, leaf litter decomposition in this tropical stream. Key words: tropical, decomposition, aquatic hyphomycetes, sporulation, intermittent stream. Aspects of fungal dynamics associated with leaf litter decomposition are well studied in temperate streams (e.g., Ba ¨ rlocher and Kendrick 1974, Suber- kropp and Klug 1976, Griffith and Perry 1994, Baldy et al. 1995, Gessner 1997, Grattan and Suberkropp 2001, Happala et al. 2001, Crenshaw and Vallet 2002, Hieber and Gessner 2002, Laitung et al. 2002, Gessner and Robinson 2003, Robinson and Gessner 2003), but less is known about the role of fungi during leaf litter decomposition in tropical streams (Mathuriau and Chauvet 2002). A few studies in tropical Asia and subtropical Africa have addressed colonization and diversity patterns of aquatic hyphomycetes during leaf decomposition in streams (Raviraja et al. 1996, 1998, Rajashekhar and Kaveriappa 2003, Abdel-Raheem 1997), and a few taxonomic studies are available for neotropical streams (Hudson and Ingold 1960, Betan- court and Caballero 1983, Betancourt et al. 1987, Justiniano and Betancourt 1989, Schoenlein-Crusius and Piccolo 2003). In Venezuela, initial taxonomic studies were published by Nilsson (1962), and more recent studies have been published by Smits et al. (2007) and Cressa and Smits (2007). To our knowledge, few studies have addressed patterns of aquatic 1 E-mail addresses: [email protected] 2 [email protected] 416

Aquatic fungi associated with decomposing Ficus sp. leaf litter in a neotropical stream

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J. N. Am. Benthol. Soc., 2009, 28(2):416–425� 2009 by The North American Benthological SocietyDOI: 10.1899/07–084.1Published online: 7 April 2009

Aquatic fungi associated with decomposing Ficus sp. leaf litterin a neotropical stream

Jose Rincon1AND Roberto Santelloco2

Departamento de Biologıa, Facultad Experimental de Ciencias, Bloque A-2, Apartado 526,Universidad del Zulia, Maracaibo, Venezuela

Abstract. Aquatic fungi are important decomposers of plant litter in temperate streams. However, thesemicroorganisms have been poorly studied in tropical streams. We assessed the dynamics of aquatichyphomycetes during the decomposition of Ficus sp. (Moraceae) leaves in an intermittent lowland stream ofnorthwestern Venezuela. Our goals were to: 1) determine the composition of aquatic hyphomycetes duringleaf decomposition, 2) assess the effect of different mesh sizes (i.e., coarse vs fine mesh) on assemblagecomposition and activity, and 3) assess the role of habitat (i.e., pools vs riffles) on fungal assemblages.Coarse- and fine-mesh litter bags were incubated in a pool and a riffle for 31 d. For each habitat andtreatment, we determined physicochemical variables, sporulation activity, and the structure andcomposition of fungal assemblages. Leaf litter decomposition rates ranged from 0.058/d in fine-mesh bagsin the riffle to 0.031/d in coarse-mesh bags in the pool. Decomposition rates were significantly influenced byhabitat type, with the highest decomposition rates found in riffle habitats. Sporulation rates weresignificantly different between habitats but not between mesh sizes. The highest sporulation rate (399 sporesmg�1 leaf dry mass d�1) and fungal diversity (16 spp.) was found in coarse-mesh bags in the riffle. Twenty-one fungal species were identified during the study. Anguillospora longissima and Lunuluspora curvulacontributed up to 75% of the conidia produced in the coarse- and fine-mesh bags in the riffle, whereasFilosporella aquatica and Lemonniera terrestris accounted for 65 to 75% of the conidia produced in the coarse-and fine-mesh bags in the pool. In ordination space based on species composition, fungal assemblagesformed 2 clear groups that corresponded to habitat type. A temporal change in fungal species compositionwas observed in riffle samples. Early succession assemblages (2–14 d) were characterized by the presence ofA. longissima, L. curvula, and F. aquatica, whereas late assemblages (24–31 d) were dominated byPyramidospora fluminea, Pyramidospora casuarinae, and unidentified sp 4. Overall, habitat type (pool or riffle)influenced sporulation rates and assemblage composition of aquatic hyphomycetes. Our study suggests thatenvironmental factors associated with hydrology (e.g., stream velocity, width, depth) regulate fungalcomposition and activity and, hence, leaf litter decomposition in this tropical stream.

Key words: tropical, decomposition, aquatic hyphomycetes, sporulation, intermittent stream.

Aspects of fungal dynamics associated with leaflitter decomposition are well studied in temperatestreams (e.g., Barlocher and Kendrick 1974, Suber-kropp and Klug 1976, Griffith and Perry 1994, Baldy etal. 1995, Gessner 1997, Grattan and Suberkropp 2001,Happala et al. 2001, Crenshaw and Vallet 2002, Hieberand Gessner 2002, Laitung et al. 2002, Gessner andRobinson 2003, Robinson and Gessner 2003), but less isknown about the role of fungi during leaf litterdecomposition in tropical streams (Mathuriau andChauvet 2002). A few studies in tropical Asia and

subtropical Africa have addressed colonization and

diversity patterns of aquatic hyphomycetes during leaf

decomposition in streams (Raviraja et al. 1996, 1998,

Rajashekhar and Kaveriappa 2003, Abdel-Raheem

1997), and a few taxonomic studies are available for

neotropical streams (Hudson and Ingold 1960, Betan-

court and Caballero 1983, Betancourt et al. 1987,

Justiniano and Betancourt 1989, Schoenlein-Crusius

and Piccolo 2003). In Venezuela, initial taxonomic

studies were published by Nilsson (1962), and more

recent studies have been published by Smits et al.

(2007) and Cressa and Smits (2007). To our knowledge,

few studies have addressed patterns of aquatic

1 E-mail addresses: [email protected] [email protected]

416

hyphomycetes associated with leaf litter decomposi-tion in neotropical streams (Mathuriau and Chauvet2002, Rincon et al. 2005).

Litter quality (i.e., lignin, secondary compounds,and nutrient content) (Abdel-Raheem 1997, Mathuriauand Chauvet 2002) and habitat type (Rincon et al.2005) influence biomass and colonization patterns ofaquatic hyphomycetes and leaf litter decomposition intropical streams. High fungal activity associated withleaf decomposition appears to be characteristic of leafprocessing in tropical streams (Mathuriau and Chau-vet 2002). Moreover, fungal colonization of decompos-ing leaves appears to affect shredder feedingpreferences in tropical streams, as it does in temperatestreams (Graca et al. 2001, Rincon and Martinez 2006).

Abiotic factors, such as water temperature, nutrientconcentrations, pH, and alkalinity, seem to affectfungal activity during leaf litter decomposition (Cha-mier 1992, Suberkropp and Chauvet 1995). The effectsof other factors, such as habitat type (riffles vs pools),on aquatic hyphomycete activity have been lessstudied. The roles of macroinvertebrates and fungiappear to change with habitat in temperate regions,and such changes have the potential to affect leaf litterdecomposition (Baldy et al. 2002, Langhans et al.2008). Pool–riffle sequences are particularly importantin intermittent streams where seasonal hydrologicalchanges can produce dramatic changes in somephysical and chemical variables affecting the streambiota (Rincon and Cressa 2000). In a temporaryMoroccan river, fungi were most active in springwhen water was constantly flowing and decomposi-tion was fastest (Maamri et al. 1998). Our understand-ing of the effects of stream habitat on fungal activity intropical streams is still very limited.

Little is known about how macroinvertebratespecies and aquatic fungal species interact to affectleaf litter processing rates. Differences in the feedingmode of macroinvertebrate species (e.g., scraping,shredding) might influence fungal colonization andleaf decomposition rates. Leaf decomposition rates canbe accelerated in the presence of macroinvertebratesbecause aquatic fungi can penetrate damaged leaftissue rapidly. We studied leaf decomposition in fine-and coarse-mesh leaf bags to assess the dynamics ofaquatic hyphomycetes in an intermittent neotropicalstream in northwestern Venezuela. Our goals were to:1) determine the composition of aquatic hyphomycetesduring leaf decomposition, 2) assess the effect ofdifferent mesh sizes (i.e., coarse vs fine mesh) onassemblage composition and activity, and 3) assess theeffect of habitat (i.e., pools vs riffles) on fungalassemblages.

Methods

Study site

We studied leaf litter decomposition in CarichuanoCreek, an intermittent 2nd-order stream in northwest-ern Venezuela (lat 10842 0–11808 0N, long 72842 0–728220W). The stream is in the northern foothills ofSierra de Perija (Estado Zulia, Venezuela), which is amajor structural component of the Venezuelan AndeanCordillera system. Carichuano Creek is a tributary ofthe Guasare River, which flows into Lago de Mara-caibo.

The stream drains a diverse tropical semideciduousdry forest, with ;17 to 20 plant species present in theriparian zone. Tabebuia rosea and Calliandra sp. aredominant in this area, and Anacardium excelsum, Cartansp., Luehea sp., Lecithis ollaria, Hura crepitans, Centro-lobium parense, Cecropia peltata, Guapira sp., Euphorbiacassearea, Ficus sp., and Inga spurea also are present(Cifuentes 2002). Catchment geology is dominated bylimestone, and streams have a characteristic waterchemistry classified as the bicarbonate–calcium type(152–320 mg/L CaCO3) (Cressa et al. 1993, Rincon andCressa 2000).

The study area has a mean annual rainfall of 1102 6

285 mm, and the annual average water temperature is27.78C. Two periods of rainfall, interspersed with dryerintervals of variable duration, occur each year (Espi-noza 1987). Typically, the 1st rainy period begins inApril and continues until June. A short dry periodfollows for 1 to 2 mo. The 2nd rainy period starts inSeptember and lasts until November or December, andis followed by another longer dry period (2 or 3 mo).Litterfall is strongly seasonal, with peaks at the end ofthe 2 dry periods (February and July) (JR, unpublisheddata). Water flow is not continuous during the dryseasons and isolated pools are common.

Leaf-litter decomposition experiment

Freshly fallen Ficus sp. (Moraceae) leaves with noindication of partial decomposition or fungal coloni-zation were collected from the riparian forest floor inJanuary 2004. Air-dried leaves were weighed into 3.06 0.1 g groups and enclosed in 15- 3 10-cm litter bags(240-lm [fine] and 5-mm [coarse] mesh). Litter bagswere anchored to the stream bottom with steel bars.

Leaf litter decomposition experiments were con-ducted from June to August 2004 (incubation periodsof 2, 7, 14, 24, and 31 d) in a riffle and a pool. Four leaflitter treatments were used: coarse mesh in riffle,coarse mesh in pool, fine mesh in riffle, and fine meshin pool. Five bags of each mesh size (coarse or fine)were retrieved from each habitat (riffle or pool) on

2009] 417AQUATIC FUNGI IN NEOTROPICAL STREAMS

each sampling date. An additional 20 bags were usedto evaluate handling losses. Leaf bags were transferredto plastic zip-lock bags and transported to thelaboratory in ice chests. In the laboratory, the bagswere disassembled, and leaves were washed gentlywith running tap water over a sieve (250 lm) toremove debris and invertebrates. On each samplingdate, the contents of 3 randomly selected bags (n ¼ 3)from each treatment were used to estimate leaf massloss; the contents of another 2 bags (n¼2) were used todetermine fungal spore production. Leaf mass loss wasestimated after drying the leaf litter at 608C for 48 h.

Spore production

Eight leaf discs were cut from the leaves in each bagwith a cork borer (1-cm diameter). Discs wereincubated in a 250-mL flask containing 100 mL ofautoclaved and filtered (0.45-lm pore size membranefilter) stream water and agitated in a shaker at 258C for72 h (slightly modified from Barlocher 2005). Theentire volume with suspended conidia was filteredthrough an 8-lm pore size membrane filter. The filterwas stained with cotton blue in lactophenol for 30 minat 408C, and the conidia trapped on the filter werecounted and identified at 4003 and 10003 magnifica-tions under a light microscope. Generally, the entiresurface of the filter was scanned and all conidia werecounted. If conidial densities were very high, 25randomly chosen microscope fields were scannedand conidia in these fields were counted. Aquatichyphomycetes species were identified with availablekeys for tropical areas (Marvanova 1997, Santos-Floresand Betancourt-Lopez 1997). Leaf discs were dried andweighed to measure the amount of leaf material andresults were expressed as conidia mg�1 leaf dry mass(DM) d�1.

Physicochemical variables

On each sampling date, temperature, conductivity,and pH were measured with field instruments (CheckMate 90; Corning, New York). Dissolved O2 (Winklermethod; Hauer and Hill 1996) was measured on 2water samples collected at ;60% depth from eachhabitat type. In addition, stream width, depth, andflow (Digimeter Model 9000; Scientific Instruments,Milwaukee, Wisconsin) were measured.

Data analysis

Percentage mass remaining through time was fit toan exponential model mt/m0 ¼ e�k t; where mt is themass remaining at time t, m0 is the initial mass, and k isthe decomposition rate coefficient (Boulton and Boon

1991). Differences in decomposition coefficients (de-termined from linear regression of ln[x]-transformeddata) between habitat types (pool and riffle) and meshsizes (coarse and fine) were tested using analysis ofcovariance (ANCOVA) in Prism 5.01 (GraphPadSoftware, San Diego, California). Slope estimates wereused to represent decomposition coefficients for eachtreatment and were compared with the Student–Newman–Keuls (SNK) multiple comparison method(a ¼ 0.05).

The effects of mesh size and habitat type onsporulation rates were determined with 2-way analy-sis of variance (ANOVA) (Sokal and Rohlf 1981). Datawere log(x þ 1)-transformed before analysis, and theanalysis was done with Statgraphics centurion XV(Statpoint Technologies Inc, Warrenton, Virginia).

Fungal assemblage composition in pools and riffleswere analyzed with nonmetric multidimensionalscaling (NMDS) in PRIMER (version 5.2.9; PRIMER-E, Plymouth, UK). NMDS is a procedure for plotting aset of assemblages in a space such that the distancesbetween assemblages correspond as closely as possibleto a given set of dissimilarities/similarities among theassemblages (Clark and Warwick 2001). Similaritiesbetween 2 assemblages were calculated with the Bray–Curtis similarity index. The abundance of each fungalspecies was 4th-root(x)-transformed before the similar-ities were calculated (Clark and Warwick 2001). Inaddition, a SIMPER routine (PRIMER-E) was done toinspect the contribution of individual species toaverage dissimilarity between groups.

Results

Physicochemical variables

Physicochemical variables varied slightly during thestudy period (Table 1). In the riffle, current velocityincreased steadily from day 2 to day 24, thendecreased sharply until day 31. In the pool, the current

TABLE 1. Values of physicochemical variables in riffle andpool habitats in Carichuano Creek, Venezuela, between Julyand August 2004.

Variable

Riffle Pool

Mean Range Mean Range

Temperature (8C) 28.3 27.6–29.6 28.4 27.6–29.0pH 8.0 7.95–8.02 8.0 7.99–8.06Dissolved O2 (mg/L) 9.5 8.9–10.5 9.8 8.7–10.4Conductivity (lS/cm) 580 562–590 555 447–607Depth (m) 0.23 0.20–0.30 0.42 0.38–0.46Width (m) 1.99 1.43–2.25 11.39 10.6–13.2Current velocity (m/s) 0.46 0.31–0.57 0.11 0.10–0.13

418 [Volume 28J. RINCON AND R. SANTELLOCO

velocity decreased slightly from day 2 to day 14, thenpeaked at day 24, and decreased by day 31. Streamwidth and depth were ;63 and 23, respectively,higher in the pool than in the riffle, but current velocitywas 43 higher in the riffle than in the pool (Table 1).Riffle and pool habitat did not differ in dissolved O2

concentration, pH, temperature, or conductivity.

Leaf litter decomposition

Loss of leaf litter mass was rapid during the first 2 dof immersion (40 and 17% for coarse- and fine-meshbags, respectively, in the riffle; 31 and 30% for coarse-and fine-mesh bags, respectively, in the pool; Fig. 1).After 7 and 14 d of immersion, leaf litter mass loss incoarse- and fine-mesh bags was higher in the pool thanin the riffle. After 24 and 31 d of immersion, leaf littermass loss was higher in the riffle than in the pool.

Decomposition rates (�k) ranged between 0.0585(fine mesh in the riffle) and 0.0313 (coarse mesh in thepool; Table 2), and differed significantly amongtreatments (ANCOVA; p , 0.001). Decomposition ratewas significantly affected by habitat type and meshsize, but not by their interaction (ANOVA; Table 3).Habitat type accounted for 20.9% and mesh sizeaccounted for 2.8% of the total variance. Decomposi-tion rates did not differ between coarse- and fine-meshbags in the pool or between coarse- and fine-meshbags in the riffle (SNK; Table 2, Fig. 2). Decompositionrates did not differ significantly between coarse-meshbags in the riffle and fine-mesh bags in the pool (SNK;Table 2, Fig. 2). Decomposition rates were significantly

faster in fine- and coarse-mesh bags in the riffle than incoarse-mesh bags in the pool.

Spore production

Spore production peaked after 14 d in the riffle (399and 383 conidia mg�1 DM d�1 in coarse- and fine-meshbags, respectively; Fig. 3A) and after 7 d in the pool(339 and 166 conidia mg�1 leaf DM d�1 in coarse- andfine-mesh bags, respectively; Fig. 3B). Spore produc-tion declined by the end of incubation in all treatmentsand habitats.

Sporulation rates were significantly higher in theriffle than in the pool (F ¼ 13.09, p ¼ 0.0010; Table 4).However, sporulation rates did not differ betweencoarse- and fine-mesh bags (F ¼ 4.12, p ¼ 0.0508), norwas the interaction term (mesh-size 3 habitat) statis-tically significant (F ¼ 0.44, p ¼ 0.5126; Table 4).

Fungal assemblages

Twenty-one taxa of aquatic hyphomycetes wereidentified from sporulating Ficus leaves in both riffleand pool habitat (Table 5). Anguillospora longissima andLunuluspora curvula contributed ;75% of conidiaproduced in the coarse- and fine-mesh bags in theriffle, whereas Filosporella aquatica and Lemonnieraterrestris contributed ;65 and ;75%, respectively, ofthe conidia produced in the coarse- and fine-mesh

FIG. 1. Mean (61 SE; n ¼ 3) percentage dry mass (DM)remaining of Ficus sp. leaves during decomposition in fine-and coarse-mesh litter bags in the riffle and pool ofCarichuano Creek, Venezuela.

TABLE 2. Mean (SE) leaf-litter decomposition rates (k) forFicus sp. leaves in coarse- (5 mm) and fine- (0.24 mm) meshbags incubated in the riffle and the pool of CarichuanoCreek, Venezuela. Treatments with the same letter were notsignificantly different on the basis of Student–Newman–Keuls (SNK) multiple comparison method (a ¼ 0.05).

Habitat Mesh k SNK grouping

Riffle Coarse �0.04693 (0.0045) acFine �0.05847 (0.0036) a

Pool Coarse �0.03132 (0.0037) bFine �0.03819 (0.0047) bc

TABLE 3. Results of 2-way analysis of variance for theeffects of habitat (riffle vs pool) and litter bag mesh size(coarse vs fine) on Ficus sp. leaf-litter decomposition rate (k).

Source dfSum ofsquares

Meansquare F-ratio p-value

Main effectsHabitat 1 0.0057 0.0057 19.06 ,0.0001Mesh size 1 0.0015 0.0015 5.01 0.0285Mesh size 3 habitat 1 0.0001 0.0001 0.32 0.5719

Residual 67 0.0201 0.0003Total (corrected) 70 0.0274

2009] 419AQUATIC FUNGI IN NEOTROPICAL STREAMS

bags in the pool (Table 5). Species richness was higherin coarse- (16) and fine-mesh (14) bags in the riffle thanin coarse- (9) and fine-mesh (5) bags in the pool.Conidia of Anguillospora crassa, Anguillospora gigantea,Heliscus tentaculus, Triscelophorus acuminatus, Campylo-spora filicladia, Flagellospora penicillioides, Flagellosporacurvula, Helicomyces sp., and 3 unidentified specieswere restricted to riffle samples, whereas L. terrestrisand 1 unidentified species were present only in poolsamples.

Differences in conidial composition between coarse-and fine-mesh bags were small in both the riffle andthe pool (Table 5). In the riffle, A. longissima andLunuluspora curvula dominated both coarse- and fine-mesh bags, although some additional less-abundantspecies (,1% of total conidial production) werepresent (Pyramidospora casuarinae, T. acuminatus, F.curvula, and 1 unidentified species). In the pool,Filosporella aquatica and Lemonniera terrestris dominatedboth coarse- and fine-mesh bags. Three species(Campylospora chaetocladia, Lunuluspora cymbiformis,and P. casuarinae) were found in coarse-mesh bags inthe pool.

Spatial variation of aquatic fungal communities

NMDS ordination of fungal samples indicatedseparation of pool and riffle assemblages on axis 1(Fig. 4). Only 4 samples (2 replicates from day 2 coarse-mesh bags, 1 replicate from day 24 coarse-mesh bags,and 1 replicate from day 7 fine-mesh bags) from thepool grouped with samples from the riffle. No rifflesamples grouped with pool samples. In the riffle,samples from coarse-mesh bags tended to group to the

right and above samples from fine-mesh bags. Thespecies that contributed most to the separation of pooland riffle samples were A. longissima (22%), Lunulu-spora curvula (16.5%), F. aquatica (12.2%), and Pyramido-spora fluminea (11.9%).

Assemblage composition did not appear to varytemporally in the pool samples, but assemblagecomposition in riffle samples showed a temporal trendon axis 2 (Fig. 4). Two assemblages were defined for

FIG. 2. Mean (61 SE; n¼ 3) leaf decomposition rates (�k)of Ficus sp. leaves during decomposition in fine- and coarse-mesh litter bags in the riffle and pool of Carichuano Creek,Venezuela. Treatments with the same letter were notsignificantly different on the basis of Student–Newman–Keuls (SNK) multiple comparison method (a ¼ 0.05).

FIG. 3. Mean (range) rate of conidia production on Ficussp. leaves during decomposition in fine- and coarse-meshlitter bags in the riffle (A) and pool (B) of Carichuano Creek,Venezuela.

TABLE 4. Results of 2-way analysis of variance for theeffects of habitat (riffle vs pool) and litter bag mesh size(coarse vs fine) on conidia production during decompositionof Ficus sp. in Carichuano Creek.

Source dfSum ofsquares

Meansquare F-ratio p-value

Main effectsHabitat 1 2.05 2.05 13.09 0.0010Mesh size 1 0.64 0.64 4.12 0.0508Mesh size 3 habitat 1 0.07 0.07 0.44 0.5126Residual 32 5.01 0.16Total (corrected) 35 7.56

420 [Volume 28J. RINCON AND R. SANTELLOCO

riffle samples: early (days 2–14) and late (days 24–31).Early assemblages often were dominated by A. longis-sima, L. curvula, and F. aquatica, whereas late assem-blages often were dominated by P. casuarinae, P.fluminea, and unidentified sp. 4.

Discussion

Leaf decomposition

Ficus leaves decomposed rapidly in both riffle andpool habitats of this intermittent stream. Decomposi-tion rates were comparable with those reported forFicus benghalensis in southern India (Raviraja et al.1998), Ficus insipida in Costa Rica (Rosemond et al.1998), Croton in the Colombian Andes (Mathuriau andChauvet 2002), and Hura crepitans in mid-northVenezuela (Abelho et al. 2005). In contrast, Protiumbrasiliense leaves in a tropical Cerrado stream in Brazil(Goncalves et al. 2007) and 3 species (Myrsineguianensis, Cupania latifolia, and Nectandra lineatifolia)in a headwater stream of Colombian Andes (Chara etal. 2007) had slower decomposition rates than wereobserved for Ficus in our study. Ficus decompositionrates in our study were considerably higher than thoseof Anacardium excelsum in the same stream (Rincon etal. 2005). This difference might be a consequence ofdifferences in the chemical composition of Ficus andAnacardium leaves (Rincon and Martinez 2006). Ana-cardium leaves have high lignin and total polyphenols,whereas Ficus leaves have low lignin and polyphenols.Content of lignin and total polyphenols are goodpredictors of leaf litter decomposition rates (Campbelland Fuchshuber 1995, Ostrofsky 1997, Gessner andChauvet 1994).

TABLE 5. Relative abundance (%) of identified and unidentified taxa of aquatic hyphomycetes sporulating on Ficus leaves incoarse- and fine-mesh bags incubated in the riffle and the pool of Carichuano Creek, Venezuela.

Taxon

Riffle Pool

Coarse mesh Fine mesh Coarse mesh Fine mesh

Anguillospora crassa Ingold 2.0 1.9 — —Anguillospora gigantea Ranzoni 1.0 0.9 — —Anguillospora longissima Ingold 47.1 54.8 7.7 2.1Campylospora chaetocladia Ranzoni 3.3 1.4 0.6 —Campylospora filicladia Nawawi 1.6 — — —Clavariopsis azlanii Nawawi 1.3 1.4 — —Filosporella aquatica Nawawi 6.5 1.4 36.9 37.5Flagellospora curvula Ingold 1.0 — — —Flagellospora penicillioides Ingold 1.3 2.9 — —Heliscus tentaculus Umphlett 0.3 0.5 — —Helicomyces sp. — 0.5 — —Lemonniera terrestris Tubaki — — 26.2 37.5Lunulospora curvula Ingold 28.4 22.4 12.5 8.3Lunulospora cymbiformis Miura 2.0 1.4 3.6 —Pyramidospora casuarinae Nilsson 0.3 — 1.8 —Pyramidospora fluminea Miura and Kudo 3.3 9.1 7.7 14.6Triscelophorus acuminatus Nawawi 0.3 — — —Unidentified sp.1 — — 1.8 —Unidentified sp. 2 0.3 — —Unidentified sp. 3 — 0.5 — —Unidentified sp. 4 — 0.5 — —Total number of species 16 14 9 5

FIG. 4. Nonmetric multidimensional scaling ordinationplot for fungal assemblage composition on Ficus sp. leavesduring decomposition in coarse- and fine-mesh bags placedin a pool and riffle in Carichuano Creek, Venezuela. Sampleswere collected on days 2, 7, 14, 24, and 31 after deploymentof the bags. Points within ellipses labeled Pool or Rifflerepresent samples from those respective habitats unlessotherwise labeled.

2009] 421AQUATIC FUNGI IN NEOTROPICAL STREAMS

Decomposition rates were not affected by mesh sizewithin a habitat. This result indicates that macroin-vertebrates, particularly shredders, played a minorrole in decomposition, as has been reported for sometropical streams (Mathuriau and Chauvet 2002, Want-zen and Wagner 2006, Goncalves et al. 2006, 2007). Incontrast, shredders have been associated with differ-ences in decomposition rates of leaves in bags withdifferent mesh sizes in other tropical streams (Cheshireet al. 2005, Chara et al. 2007). Scarcity of shreddersmight be a biogeographical rather than a latitudinalissue (Cheshire et al. 2005). The high abundance ofshredders in Colombian Andean streams (Chara et al.2007) contrasts with the low abundance of shreddersin lowland tropical streams (Dobson et al. 2002,Mathuriau and Chauvet 2002, Wantzen and Wagner2006).

Differences in current velocity between pool andriffle habitats might partially explain the differences indecomposition rates in our study. Current velocity inriffles can accelerate decomposition by increasingphysical fragmentation, improving the transport andcolonization of fungal species, and supplying dis-solved O2 and nutrients to microbial communities.Differences in sporulation activity between habitatsappear to support this idea. Rincon et al. (2005)attributed differences in decomposition rates of A.excelsum between pools and riffles in CarichuanoCreek to current velocity. Langhans et al. (2008)suggested that current velocity promoted faster leach-ing and fragmentation and, hence, faster leaf litterdecomposition in river channels than in ponds in thefloodplain of the Tagliamento River (Italy). In contrast,decomposition rates did not differ significantly be-tween main stem and floodplain ponds of the GaronneRiver system in France, and fungal production wassimilar between the 2 sites (Baldy et al. 2002). Baldy etal. (2002) suggested that fungi might be importantagents of litter decomposition in standing water bodiesof fluvial systems when the physicochemical condi-tions are favorable to aquatic hyphomycetes.

Sporulation rates and activity of aquatic hyphomycetes

Habitat type influenced fungal activity, assemblagecomposition, and decomposition rates of Ficus sp. inCarichuano Creek. Sporulation rates in our study werewithin the range reported in other tropical andtemperate studies (Mathuriau and Chauvet 2002, Gulisand Suberkropp 2003, Rincon et al. 2005, Ferreira andGraca 2006). Early sporulation rates similar to those inour study have been reported for other fast-decom-posing leaf species in tropical (Mathuriau and Chauvet2002) and temperate streams (Gessner et al. 1993,

Gessner 1997). This result is consistent with the strongrelationship between the maximum sporulation rateand the decay coefficients for 7 deciduous leaf species(Gessner and Chauvet 1994).

In our study, current velocity and turbulent condi-tions in riffles provided favorable conditions foraquatic hyphomycetes activity. Sporulation rate onFicus leaves was greater in the riffle than in the poolhabitat, a result similar to that reported for sporulationrates on A. excelsum leaves in Carichuano Creek(Rincon et al. 2005). In a fluvial system in France,sporulation activity was highest in the main channeland very low in the floodplain pond (Baldy et al. 2002).Fungal biomass was highest in the river channel andlowest in ponds of a riverine floodplain in Italy(Langhans et al. 2008). In addition, Maamri et al.(1999) reported a lower fungal biomass in a pool than ariffle during leaf decay in an intermittent stream inNorth Africa. Fungal activity and biomass might belimited by low turbulence and oxygenation in pools(Barlocher 1985, Chamier 1987, Suberkropp 1992,Abdel-Raheem 1997).

Fungal assemblages

The fungal assemblage on Ficus leaves in Carichua-no Creek was similar to that found in other tropicalstudies (Santos-Flores and Betancourt-Lopez 1997,Mathuriau and Chauvet 2002, Rincon et al. 2005).Species richness in our study (21 species) was nearly23 greater than previous reports of aquatic hyphomy-cetes for Venezuela (11 species; Nilsson 1962), but only;½ of the number (50 species) reported by Smits et al.(2007) from 7 streams in Venezuela. All speciesidentified in our study were included in a recentcompilation made for South America (Schoenlein-Crusius and Piccolo 2003). However, the fact that wewere unable to identify 4 species with available keysindicates the need for more surveys and taxonomicalstudies to improve our knowledge of neotropicalfungi.

Sporulating fungal assemblages differed betweenriffle and pool habitat. Higher species richness ofconidia in the riffle than in the pool suggests thatconditions for reproduction of aquatic hyphomycetesare better in riffles than in pools. Fungal assemblagesin the riffle were dominated by A. longissima and L.curvula. Lunuluspora curvula is a widespread speciescommonly found during the summer in temperatestreams (Webster and Descals 1981). This species alsois commonly reported as a dominant species oftropical (Justiniano and Betancourt 1989, Mathuriauand Chauvet 2002) and subtropical streams (Abdel-Raheem 1997). Anguillospora longissima is a widespread

422 [Volume 28J. RINCON AND R. SANTELLOCO

species commonly found in tropical (Schoenlein-Crusius and Piccolo 2003) and temperate (Websterand Descals 1981) streams. Different species (Filospo-rella aquatica and Lemonniera terrestris) were dominantin the pool, a result that might indicate habitatpreferences by the aquatic fungi. Filosporella aquaticaand L. terrestris have a typical tropical distribution butalso can be found in fungal assemblages in temperatelowland rivers (Marvanova 1997, Santos-Flores andBetancourt-Lopez 1997).

Successional patterns in fungal development, suchas the pattern observed in the riffle in our study, havebeen reported previously, but to our knowledge, oursis the first study to assess temporal dynamic patternsin fungal assemblage composition in a neotropicalstream. Fungal succession moved through 3 stages andwas coupled with the dynamics of leaf mass loss in atemperate stream in France (Gessner et al. 1993). In ourstudy, Lunuluspora curvula, A. longissima, and F.aquatica were associated with the early stage ofcolonization, whereas P. casuarinae, P. fluminea, andunidentified sp. 4 were associated with the advancedstages of decay. Changes in nutritional and chemicalvalues of leaves might promote changes in speciesassemblages during leaf decomposition (Arsuffi andSuberkropp 1984).

Changes in water temperature can influence tempo-ral changes in fungal assemblages in subtropicalstreams (Abdel-Raheem 1997). However, water tem-perature was constant during our study, and thus, wasunlikely to have influenced fungal assemblage com-position in Carichuano Creek. In our study, streamflow varied considerably during the experiment, andenvironmental factors associated with changes inhydrological conditions (e.g., stream velocity, width,and depth) could have affected fungal assemblages.Goncalves et al. (2006) attributed low microbialcolonization in Mediterranean streams to flow-relatedconditions. In addition, Maamri et al. (1998, 1999,2001) showed that fungal assemblages changed duringthe flow transition from wet to dry period in anintermittent stream in Morocco (North Africa). Theintermittent character of Carichuano Creek makeshydrology a critical driver of physical, chemical, andbiological processes (Rincon and Cressa 2000). A betterunderstanding is needed of the responses of fungalcommunities to hydrological changes and their impli-cations for decomposition rates.

Acknowledgements

Our work was funded by the Fondo Nacional deCiencia, Tecnologıa e Innovacion de la RepublicaBolivariana de Venezuela (FONACIT) (grant no. S1-

2002000392). We thank Jeimmy Uzcategui and MarioNava for field assistance. We also thank Luz Boyeroand Alonso Ramırez for their kind invitation to theTropical Session at the annual meeting of the NorthAmerican Benthological Society in Anchorage, Alaska,USA. We thank Felix Barlocher for his comments onearlier versions of the manuscript. Several anonymousreferees provided useful comments on earlier versionsof the manuscript, which are much appreciated.

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Received: 23 July 2007Accepted: 17 November 2008

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