Most tadpoles are primarily herbivorous (ALFORD 1999) con-suming a wide variety of algal taxa as well as detritus, viruses, bacteria, protists, plant fragments, pollen grains, fungi, vari-ous kinds of small animals, anuran eggs, and other tadpoles (KUPFERBERGetal. 1994, HOFFetal. 1999).
Field studies of tadpole diets, including systematic and comparative evaluation of the food habits of tadpoles are rare (ALFORD 1999, HOFFetal. 1999) and few studies have detailed how food differences might influence community organization (DÍAZ-PANIAGUA 1985, INGER 1986, LAJMANOVICH 2000). As a conse-quence, little consensus exists regarding the occurrence of food partitioning and its role in the organization of tadpole com-munities. BELOVA (1964) observed that the diet of Ranaridibunda Pallas, 1771 (Ranidae) tadpoles collected from different bodies
of water was similar. HEYER (1973), JOHNSON (1991), SEALE & BECKVAR (1980) and LAJMANOVICH (1997) showed that tadpoles feed on what is available in their habitat. HEYER (1976) and LAJMANOVICH (2000) concluded that food plays no important role in habitat partitioning among species, whereas INGER (1986) observed that partition food was intertwined with distribution in space, and WASSERSUG (1980) suggested that differences in the internal oral characteristics may be related to preferences to different sizes of food particles in the microhabitats of tadpoles.
In the present study, we determined the diet of tadpoles of 13 anuran species in a temporary pond, southeastern Brazil. The patterns of breadth and overlap in food resource use were determined to analyze whether partitioning occurs and whether the degree of diet similarity is related to taxonomic affinity.
Denise de C. Rossa-Feres
1, Jorge Jim
2&
Mariluce Gonçalves Fonseca
31 Corresponding author. Departamento de Zoologia e Botânica, Universidade Estadual Paulista. Rua Cristovão Colombo
2265, 15054-000 São José do Rio Preto, São Paulo, Brasil. E-mail: denise@dzb.ibilce.unesp.br
2 Departamento de Zoologia, Universidade Estadual Paulista. Distrito de Rubião Júnior, 18618-000 Botucatu, São Paulo,
Brasil.
3 Departamento de Ciências Biológicas, Faculdades FAFIBE. Rua Orlando França de Carvalho 325, 14071-070 Bebedouro,
São Paulo, Brasil.
ABSTRACT. The diet of tadpoles of 13 anuran species was determined to verify whether food resource partition-ing occurs and whether the degree of diet similarity is related to taxonomic affinity. Tadpoles of all species studied were mainly herbivorous, except for these of Leptodactylusfuscus (Schneider, 1799) which were mycopha-gous. Although some species had exclusive items in their diet, most tadpole species ingested the same items, but differed in the amount of each item consumed. Two guilds were found: tadpoles that feed on diatoms on the pond bottom, and tadpoles that feed on Oedogonium Link, 1820 algae in midwater. Diet similarity was related to the taxonomic relationship, microhabitat and feeding behavior of tadpoles indicating that the community organization is complex and resulting from the interaction of several parameters.
KEY WORDS. Community ecology, food partitioning, microalgae.
RESUMO. Dieta dos girinos de um açude temporário no sudeste do Brasil (Amphibia, Anura). Determinou-se a dieta dos girinos de 13 espécies de anuros, com o objetivo de verificar se ocorre partilha de recursos alimentares e se o grau de similaridade na dieta é relacionado ao parentesco, inferido pela proximidade taxonômica. Os girinos de todas as espécies estudadas foram preponderantemente herbívoros, exceto os de Leptodactylusfuscus (Schneider, 1799) que foram micófagos. Embora algumas espécies tenham apresentado itens exclusivos em sua dieta, os girinos da maioria das espécies ingeriram os mesmos itens, diferindo na quantidade consumida de cada item. Duas guildas foram encontradas: girinos que se alimentam de diatomáceas no fundo do corpo d’água e girinos que se alimentam de algas do gênero Oedogonium Link, 1820 à meia-água. A similaridade na dieta foi relacionada à proximidade taxonômica, ao microhabitat e ao comportamento de alimentação, indicando que a organização desta comunidade é complexa e resultante da interação entre vários fatores.
MATERIAL AND METHO DS Study Site
Th is stu d y was con d u cted in an artificial, tem p orary p on d in a p a st u re in N o v a It a p irem a , D ist rict o f N o v a Alia n ça (21º11’S, 49º42’W ), St at e o f São Pau lo , Brazil. Th e p o n d , wit h clayey b o t t o m an d irregu lar sh ap e, m easu red ab o u t 54 x 22 m an d was 0.7 m d eep d u rin g t h e p erio d o f largest wat er vo lu m e. W at er p ersist ed fo r 5-7 m o n t h s/ year. Th e m argin s were co v-ered m ain ly wit h grasses (Po aceae an d Cyp eraceae) an d t h e a q u a t ic v e ge t a t io n c o n sist e d o f N y m p h e a c e a e , Po a c e a e , Cyp eraceae an d Po lygo n aceae. Th e clim at e o f t h e regio n is t ro p ical, wit h an an n u al rain fall ran gin g fro m 1,100-1,250 m m , 85% o f wh ich o ccu rred d u rin g t h e rain y seaso n fro m O ct o b er t o March (ARID & BARCHA 1973).
Analysis of gut contents of tadpoles
Th e t ad p o les were co llect ed at least o n ce a m o n t h fro m O ct o b er 1989 t o March 1995, b et ween 15:00 an d 19:00 h , wit h a fin e-m esh d ip n et (3 m m2) an d p reserved im m ed iat ely in 10% fo rm alin . Aft er id en t ificat io n , t h e an im als were st o red in 5% fo rm alin an d d ep o sit ed in t h e am p h ib ian co llect io n o f t h e Dep art am en t o d e Zo o lo gia e Bo t ân ica, Un iversid ad e Est ad u al Pau list a (UNESP), Cam p u s fro m São Jo sé d o Rio Pret o (DZSJRP 1 t o 128). Ad u lt s o f t h ese sp ecies were also d ep o sit ed in sam e co llect io n .
In a p revio u s an alysis was o b served t h at t h e m an ico t t o glan d u lare o f t ad p o les was u su ally em p t y an d t h at fo o d co n -t en -t d id n o -t vary in q u an -t i-t y o r co m p o si-t io n alo n g -t h e in -t es-t in e. Th u s, we ju ses-t an alyzed es-t h e co n es-t en es-t o f es-t h e firses-t cen es-t im ees-t er o f t h e in t est in e o f five in d ivid u als o f each sp ecies, in d evelo p -m en t al st ages 35-38 o f GO SNER (1960). Th is p art o f t h e gu t was rem oved an d its con ten t was h om ogen ized in 160 µ l of Tran seau so lu t io n (BICUDO & BICUDO 1970). Fo u r sem ip erm an en t slid es were m o u n t ed fo r each t ad p o le, wit h 40 µ l o f t h is so lu t io n . In t wo slid es, t h e fo o d it em s were id en t ified an d co u n t ed in t h e en t ire area co vered b y t h e co verslip (324 m m2) at 200x m agn i-ficat io n . In t h e o t h er t wo slid es, t h e size o f t h e fo o d it em s was m easu red wit h a grid calib rat ed fo r t h e o b ject ive o f t h e m icro -sco p e at 160x m agn ificat io n . Th e algae were id en t ified t o ge-n u s acco rd ige-n g t o BICUDO & BICUDO (1970) age-n d t h eir m icro h ab i-t ai-t was d efin ed o n i-t h e b asis o f i-t h eir m o rp h o lo gy. Th o se wii-t h an y at t ach m en t st ru ct u res were co n sid ered p erip h yt ic an d t h e rem ain in g were p lan kt o n ic. Th e p o sit io n o f t h e t ad p o les in t h e wat er co lu m n was d et erm in ed b y d irect o b servat io n , an d d erived fro m m icro h ab it at o f t h e in gest ed algae, an d t h e t ad -p o les were co n sid ered b en t h ic o r n ekt o n ic m id wat er.
Diet d iversit y was calcu lat ed fo r each sp ecies b y t h e Sh -an n o n -W ien er in d ex (H’) -an d t h e b read t h o f t h e n ich e fo r t h e t yp es o f fo o d it em s in gest ed was calcu lat ed b y Levin s’ m easu re (B) (KREBS 1999). Th e n ich e o verlap was calcu lat ed b y t h e sim i-larit y in d ex o f Mo risit a-Ho rn (CH) fo r t h e t yp e (freq u en cy o f in gest io n o f each algal gen u s) an d size (freq u en cy o f in gest io n o f each size cat ego ry o f algae) grad ien t o f t h e fo o d it em s. O
ver-lap valu es were co n sid ered h igh wh en su rp assin g CH = 0.50. Clu st er an alysis was ap p lied t o t h e sim ilarit y m at rix o b t ain ed b y t h e u n weigh t ed m ean m et h o d (KREBS 1999).
Species
W e an alyzed t h e gu t co n t en t o f t ad p o les o f t h e fo llo w -in g 1 3 sp ecies: Bufo sch n eideri W ern er, 1 8 9 4 (Bu fo n id a e); El a ch i s t ocl ei s ov a l i s ( Sc h n e i d e r , 1 7 9 9 ) ( M i c r o h y l i d a e ) ; Leptodactylus fuscus (Sch n eid er, 1799), L. podicipin us (C o p e, 1 8 6 2 ), Ph ysalaem u s cen t ralis Bo k e r m a n n , 1 9 6 2 , P. cu vieri Fit zin ger, 1 8 2 6 , P. fuscom aculatus (St ein d a ch n er, 1 8 6 4 ), P. nattereri (St ein d ach n er, 1 8 6 3 ) (Lep t o d act ylid ae); Hyla n an a Bo u len ger, 1889, Phrynohyas venulosa (Lau ren t i, 1768), S. fusco-m argin atus (A. Lu t z, 1 9 2 5 ), Scin ax fuscovarius (A. Lu t z, 1 9 2 5 ), an d S. sim ilis (C o ch ran , 1 9 5 2 ) (H ylid ae). Rep ro d u ct ive ad u lt s o f b o t h Hyla n an a Bo u len ger, 1889 an d H. san born i Sch m id t , 1 9 4 4 w ere fo u n d , b u t b ecau se t ad p o les o f t h ese sp ecies co u ld n o t b e d ist in gu ish ed , t h ey were lu m p ed t o get h er as Hyla nana. Scin ax fuscom argin atus t ad p o les w ere rare an d t h e d iet o f o n ly o n e in d ivid u al is d escrib ed h ere. Six sp ecies fo rm p airs o f t axo -n o m ically relat ed sp ecies (Ph ysalaem us cuvieri a-n d P. ce-n tralis; P. n attereri a n d P. fuscom aculatus; Scin ax fuscovarius a n d S. sim ilis).
Du rin g a five-year st u d y, t h e t ad p o les o f t h ese 13 sp ecies co exist ed d u rin g so m e p erio d in each year. Sin ce t h e p o o l is t em p o rary an d accu m u lat es o n ly rain wat er, it is assu m ed t h at reso u rce availab ilit y ch an ged yearly wit h in a n arro w b read t h . Th u s, t o ch aract erize t h e d iet o f t ad p o les, t h e gu t co n t en t s were an alyzed in in d ivid u als co llect ed d u rin g t h eir m o d al p erio d o f o ccu rren ce an d in t h e years wh en t h ey were m o st ab u n d an t (Tab. I). Besid es, t o m in im ize t h e risk o f co n fo u n d in g d ifferen ces b et weifferen d ays (INGER 1986), gu t co n t ifferen t s o f p airs o f t axo -n o m ically relat ed t ad p o les were a-n alyzed fro m sp ecim e-n s co l-lect ed o n t h e sam e d ay.
Table I. Dates of tadpole collection from a tem porary pond in Nova Itapirem a, São Paulo, Brazil.
Species Date
Hyla nana 25 Jan 90
Physalaemus centralis 7 M arch 90
Physalaemus cuvieri 7 M arch 90
Scinax fuscomarginatus 7 M arch 90
Scinax fuscovarius 20 Dec 90
Scinax similis 20 Dec 90
Bufo schneider 20 Dec 90
Physalaemus nattereri 29 Nov 94
Physalaemus fuscomaculatus 29 Nov 94
Leptodactylus fuscus 29 Nov 94
Leptodactylus podicipinus 29 Nov 94
Elachistocleis ovalis 29 Nov 94
RESULTS Spectrum of food items
Th e t ad p o le d iet s co n sist ed m o st ly o f m icro algae, al-t h o u gh fragm en al-t s o f h igh er p lan al-t s (m ain ly leaves o f Po aceae an d Cyp eraceae), fu n gal h yp h ae (m ain ly Deu t ero m yco t in a), Sarco m ast igo p h o ra, C ilio p h o ra, Ro t ifera, N em at o d a, Tard i-grad a, an d Cru st acea were also fo u n d (Tab . II). Micro algae b e-lo n gin g t o 44 gen era were id en t ified , d iat o m s (Bacillario p h y-ceae) rep resen t ed 8-54% o f t h e d iet o f t ad p o les o f 13 sp ecies reco rd ed in t h e t em p o rary p o n d (Tab s III an d IV).
Th ree it em s were fo u n d in t h e d iet o f all sp ecies: d ia-t o m s (Bacillario p h yceae), Oedogonium (O ed o go n iaceae) an d Trachelom onas (Eu glen aceae). O n t h e o t h er h an d , fift eeen it em s were rare an d fo u n d in t h e in t est in es o f o n ly o n e sp ecies (Tabs III an d IV). Th e sam e o ccu rred wit h o t h er fo u r it em s, t h at were fo u n d in a n o t ab le am o u n t (> 5 % ): Lyngbya Agard h , 1 8 2 4 (O scillat o riaceae) in Physalaem us cuvieri; Sorastrum Ku t zin g, 1845 (Hyd ro d ict yaceae), Scenedesm us Meyen , 1829 (Scen ed es-m a cea e) a n d Lepocin clis Pert y, 1 8 4 9 (Eu glen a cea e) in Bufo schneideri (Tab s III an d IV).
Diet diversity and similarity
Tad p o les o f seven sp ecies (Physalaem us centralis, P. cuvieri, P. fuscom aculatus, P. nattereri, Leptodactylus fuscus, L. podicipinus, an d Bufo schneideri) o ccu rred o n t h e p o n d b o t t o m , an d t ad -p o les o f Scinax fuscovarius, S. sim ilis an d Phrynohyas venulosa o ccu rred in t h e m id wat er. Excep t fo r Bufo schneideri an d Phry-nohyas ven ulosa t ad p o les, w h ich in gest ed large am o u n t s o f p lan kt o n ic algae, t h e rem ain in g t ad p o les m ain ly in gest ed p e-rip h yt ic algae (Fig. 1).
Th e m em b ers o f each sp ecies p air – Physalaem us cuvieri an d P. centralis, P. nattereri an d P. fuscom aculatus, Scinax fusco-varius an d S. sim ilis – were sim ilar in d iet co m p o sit io n (Fig. 2), wit h o n ly 4-6 it em s n o t sh ared (Tab. III). Am o n g Leptodactylus fuscus an d L. podicipinus, co n gen eric sp ecies, b u t b elo n gin g t o d ifferen t sp ecies gro u p s, t h e d iet d iffered at least in t erm s o f t h e m o st ab u n d an t it em (Tab . IV). Fo r t h e rem ain in g sp ecies, t h ere were 8-10 it em s n o t sh ared (Tab . IV). Ho wever, so m e o f t h ese sp ecies h ad d iet s sim ilar t o sp ecies b elo n gin g t o t h e t h ree t axo n o m ically relat ed p airs (e.g. Leptodactylus podicipinus wit h Physalaem us centralis; Elachistocleis ovalis wit h P. nattereri; Tabs III an d IV). Sim ilarit y an alysis d em o n st rat ed t wo m ajo r sp e-cies clu st ers wit h o verlap valu es h igh er t h an 0.70 (Fig. 3): (1) sev en sp ecies w h ich in gest ed m a in ly d ia t o m s (Ba cilla rio -p h yceae) an d (2) t wo t axo n o m ically relat ed s-p ecies (Scinax fuscovarius an d S. sim ilis) wh ich in gest ed m ain ly algae o f t h e gen u s Oedogonium . Th ree sp ecies wit h d ifferen t d iet s d o n o t
Figure 1. Percentage of food item s of planktonic and periphytic habits in the diet of tadpoles of the three pairs of taxonom ically related species (A) and of the other six species (B) in the tem po-rary pond of N ova Itapirem a, São Paulo.
Planktonic algae Periphytic algae Unidentified items 0
20 40 60 80 100
Pcu Pce Pn Pfm Sfu Ssi
0 20 40 60 80 100
Bp Eo Lfu Lp Pv Hn
A
B
Table II. Categories of food item s ingested and their percent frequencies (%) in the diet of tadpoles of 13 species. (Bs) Bufoschneider, (Eo) Elachistocleis ovalis, (Hns) Hyla nana, (Lfu) Leptodactylus fuscus, (Lp) L. podicipinus, (Pce) Physalaemus centralis, (Pcu) P. cuvieri, (Pfm )
P. fuscomaculatus, (Pn) P. nattereri, (Pv) Phrynohyas venulosa, (Sfu) S. fuscovarius, (Ssi) S. similis, (Sfm ) Scinax fuscomarginatus. Except for
S. fuscomarginatus (with only one specim en exam ined), five specim ens of each species were exam ined. (UN I) Unidentified item . Food item s Bs Eo Hn Lfu Lp Pce Pcu Pfm Pn Pv Sfu Ssi Sfm M icroalgae 90.05 72.03 17.87 33.35 79.32 94.21 95.04 77.35 81.84 69.87 59.64 84.54 95.39 Fungus 0.72 1.10 0.28 34.60 3.60 1.14 1.20 8.97 4.99 2.94 0.61 0.85 – Fragm ents of angiosperm s 3.48 2.06 0.37 13.35 9.06 0.33 – 4.09 7.74 5.87 5.60 7.00 0.28 Sarcom astigophora 0.74 6.67 0.27 4.66 5.38 2.33 3.00 0.98 1.11 5.38 2.75 1.43 0.14 Ciliophora 0.09 0.11 0.02 1.97 0.21 – – 0.17 0.09 2.07 – 1.83 – Rotifera 2.90 5.23 0.57 5.05 1.62 0.11 0.02 2.89 2.01 13.07 1.00 3.35 0.55 N em atoda 0.17 0.22 – 1.15 0.26 1.18 0.34 0.52 0.24 – 1.00 0.20 0.14 Tardigrada 0.08 – – 0.70 0.06 – – – 0.71 0.05 0.06 0.05 –
Acari – – – 0.14 – – – 0.05 0.03 – – – –
N em atocera, larvae – – – – – – 0.03 – – – – – –
Crustacea 0.36 7.98 0.14 3.40 0.44 0.67 0.52 2.72 1.63 0.28 1.00 1.53 0.48
UN I 1 – 4.64 72.54 – – – – – – – – – –
0 10 20 30 40 50 60
Bacil Oscil Phac Trach Lyng Clost Oed P.cuvieri P.centralis
0 10 20 30 40 50 60
Bacil Oed Fhp Trach Fung Anab P.nattereri P.fuscomaculatus
0 10 20 30 40 50 60
Bacil Oed Trach Eug Clost Fhp S.fuscovarius S.similis
0 10 20 30 40 50 60
Bacil Fung Oscil Phac Fhp Rot Trach L.fuscus L. podicipinus
n n
n n
Figure 2. Five m ost abundant food item s of each species of taxo-nom ically related pairs and of the congenerics Lept odact ylusfuscus
and L. podicipinus. (Anab) Anabaena, (Bacil) Bacillariophyceae, (Clost) Clost erium, (Eug) Euglena, (Fhp) fragm ent of a higher plant, (Fung) Fungal hyphae, (Lyng) Lyngbya, (Oed) Oedogonium, (Oscil)
Oscillat oria, (Phac) Phacus, (Rot) Rotifera, (Trach) Trachelomonas.
Figure 3. Clusters of species, indicating those w ith sim ilarity higher t han CH = 0.70 in the com position of the diet. For abbreviations
see t able II.
Table III. Abundance (m ean ± standard deviation, n = 5) of the food item s found in the gut content of tadpoles of the three pairs of taxonom ically related species in the tem porary pond of Nova Itapirem a, São Paulo. The m ost abundant item s for each species are in bold; (FA) fragm ent of angiosperm s; (UNI) unidentified item .
Food item s P. cuvieri P. centralis P. nattereri P. fuscomaculatus S. fuscovarius S. similis
Cyanophyta
Anabaena 5.70 ± 8.06 – – 8.76 ± 9.77 3.86 ± 8.63 –
Chroococcus 0.23 ± 0.38 0.07 ± 0.16 0.06 ± 0.09 0.05 ± 0.10 0.23 ± 0.21 0.50 ± 0.64
Lyngbya 6.25 ± 8.60 0.88 ± 0.85 – – 0.25 ± 0.30 0.15 ± 0.34
Oscillatoria 9.40 ± 5.71 12.34 ± 13.55 1.19 ± 0.58 5.56 ± 3.67 3.25 ± 1.76 3.40 ± 3.00
Spirulina 0.10 ± 0.12 – – – 0.04 ± 0.10 –
Cyanophyceae (UNI) 0.10 ± 0.15 0.11 ± 0.12 – – – –
Chlorophyta
Actinotaenium 0.25 ± 0.17 1.02 ± 1.15 – – – –
Ankistrodesmus – 0.04 ± 0.05 0.49 ± 0.16 1.02 ± 0.73 – –
Cladophora – – 0.72 ± 1.61 – – –
Chlorococcum 1.70 ± 1.10 1.28 ± 0.90 – – – –
Closterium 2.90 ± 1.70 5.02 ± 2.89 4.41 ± 1.94 2.86 ± 1.58 6.0 ± 3.50 2.70 ± 1.20
Coelastrum – – 0.16 ± 0.23 0.54 ± 0.56 0.35 ± 0.80 –
Cosmarium 1.35 ± 1.85 3.57 ± 1.07 – 0.25 ± 0.35 3.00 ± 2.56 3.61 ± 2.81
Desmidium 0.74 ± 0.87 2.18 ± 2.32 – – – –
Euastrum 0.26 ± 0.13 0.67 ± 0.61 – – 1.07 ± 1.16 0.32 ± 0.43
Gonatozygon 0.34 ± 0.47 1.25 ± 2.42 – – – –
M esotaenium – 0.09 ± 0.20 – – – –
M icrasterias 0.40 ± 0.36 0.51 ± 1.03 – – – –
Oedogonium 3.00 ± 2.30 3.78 ± 1.28 11.86 ± 7.26 15.53 ± 14.33 29.00 ± 24.24 38.80 ± 22.0
Oocystis 0.76 ± 0.51 0.89 ± 0.76 0.23 ± 0.17 0.63 ± 0.73 0.50 ± 0.72 1.00 ± 0.85
Pediastrum – 0.02 ± 0.05 – – – –
Pleurotaenium – 0.04 ± 0.10 – – 0.10 ± 0.20 0.12 ± 0.27
Continues
Pce
Pcu
Lp
Pn
Eo
Pfm
Bs
Sfu
Ssi
Lfu
Pv
Hns
1 0.957 0.805 0.652 0.499 0.346 0.194 0.042 0 1
b elo n g t o eit h er clu st er: Hyla nana, Phrynohyas venulosa an d Leptodactylus fuscus.
Th e d iversit y an d n ich e bread t h o f t h e fo o d t yp e in gest ed were h igh (H’ > 0.95 an d B > 4.0, resp ect ively) fo r m o st o f t h e sp ecies (Tab . V). Nich e o verlap was h igh (CH > 0.60) fo r 42.4% o f t h e 66 p o ssib le co m b in at io n s o f sp ecies p airs (Tab. VI). Hyla nana t ad p o les, wh ich m ain ly in gest ed an u n id en t ified it em
resem blin g in sh ap e t o m em bers o f Bacillario p h yceae, Leptodac-tylus fuscus tad p oles, wh ich were p rep on d eran tly m ycop h agou s, an d Phrynohyas venulosa t ad p o les, wh ich m ain ly co n su m ed p lan kt o n ic algae, were t h e o n ly o n es p resen t in g lo w n ich e o verlap wit h t h e rem ain in g sp ecies. Th e h igh est o verlap o c-cu rred b et ween Physalaem us centralis an d P. c-cuvieri (Tab. VI).
Th e t ad p o les in gest ed it em s ran gin g in size fro m
10-Table III. Continued.
Food item s P. cuvieri P. centralis P. nattereri P. fuscomaculatus S. fuscovarius S. similis
Chlorophyta (cont.)
Scenedesmus 0.30 ± 0.10 0.57 ± 0.29 – 0.08 ± 0.11 0.61 ± 0.40 0.15 ± 0.34
Selenastrum 0.03 ± 0.06 0.02 ± 0.05 – – – –
Sorastrum 0.03 ± 0.06 0.15 ± 0.20 0.05 ± 0.12 0.08 ± 0.11 – –
Sphaerocystis – 0.08 ± 0.08 0.55 ± 0.36 0.70 ± 0.78 1.10 ± 1.73 0.70 ± 0.62
Spirogyra 2.84 ± 2.05 2.58 ± 1.11 – – – –
Staurastrum 0.80 ± 0.14 0.86 ± 0.33 0.08 ± 0.11 0.09 ± 0.13 – 0.16 ± 0.24
Staurodesmus 0.07 ± 0.12 0.02 ± 0.05 – – – –
Xantidium – 0.02 ± 0.05 – – – –
Chlorophyceae (UN I) 0.33 ± 0.46 – – – – –
Bacillariophyta 36.05 ± 13.70 40.83 ± 7.98 54.45 ± 10.67 32.29 ± 8.91 22.21 ± 11.66 13.63 ± 8.00 Euglenophyta
Eudorina 0.51 ± 0.61 1.19 ± 0.91 0.03 ± 0.08 – – –
Euglena 2.60 ± 1.33 3.25 ± 2.77 0.93 ± 0.60 1.34 ± 0.42 7.0 ± 2.00 5.45 ± 2.23
Lepocinclis 0.66 ± 0.40 1.54 ± 0.65 0.03 ± 0.08 0.14 ± 0.21 0.21 ± 0.40 –
Phacus 8.77 ± 9.25 2.25 ± 0.95 0.33 ± 0.12 0.56 ± 0.33 1.35 ± 0.70 0.70 ± 1.30
Strombomonas 0.03 ± 0.06 0.08 ± 0.11 0.03 ± 0.07 – – –
Trachelomonas 8.52 ± 2.61 7.18 ± 3.23 6.84 ± 5.98 7.87 ± 5.19 8.34 ± 10.43 13.0 ± 16.28 Chrysophyta
Dinobryon – – – – 0.17 ± 0.40 0.15 ± 0.34
Dinophyta
Goniaulax 0.02 ± 0.04 0.03 ± 0.06 – – – –
Fungus 1.20 ± 0.87 1.14 ± 0.24 4.99 ± 2.88 8.97 ± 11.51 0.61 ± 0.51 0.85 ± 0.67 FA – 0.33 ± 0.41 7.74 ± 5.53 4.09 ± 1.70 5.60 ± 6.40 7.00 ± 10.00 Thecam aeba 3.0 ± 1.36 2.33 ± 1.60 1.11 ± 1.04 2.83 ± 2.79 2.75 ± 2.13 1.43 ± 1.04
Ciliophora – – 0.09 ± 0.20 0.17 ± 0.22 – 1.83 ± 3.00
Rotifera 0.02 ± 0.04 0.11 ± 0.16 2.01 ± 1.31 2.89 ± 1.54 1.00 ± 0.64 3.35 ± 3.43 Nem atoda 0.34 ± 0.44 1.18 ± 1.97 0.24 ± 0.25 0.52 ± 0.79 1.00 ± 2.00 0.20 ± 0.33 Tardigrada – – 0.71 ± 1.16 0.98 ± 0.96 0.06 ± 0.14 0.05 ± 0.11
Acari – – 0.03 ± 0.07 0.05 ± 0.10 – –
Diptera (larvae) 0.03 ± 0.06 – – – – –
Copepoda – 0.05 ± 0.11 – – – –
Ostracoda 0.12 ± 0.20 0.12 ± 0.13 – – – –
Crustacea (UN I) 0.40 ± 0.17 0.50 ± 0.35 0.44 ± 0.35 2.72 ± 2.87 1.00 ± 0.32 1.53 ± 1.20
Table IV. Abundance (m ean ± standard deviation, n = 5) of the food item s found in the gut content of tadpoles of seven species in the tem porary pond of N ova Itapirem a, São Paulo. The m ost abundant item s for each species are in bold; (*) description of the diet of one individual; (FA) fragm ent of angiosperm s; (UNI) unidentified item .
Food item s L. fuscus L. podicipinus B. schneider P. venulosa E. ovalis Hyla nana *S. fuscomarginatus
Cyanophyta
Anabaena 0.18 ±0.42 0.22 ±0.36 – – 0.64 ±0.77 – 0.07
Chroococcus – 0.08 ±0.19 – – – – –
Oscillatoria 1.13 ±1.56 10.89 ±8.33 0.59 ±0.69 0.05 ±0.09 2.05 ±0.83 – 0.07
Spirulina – – – – 0.40 ±0.50 – –
Chlorophyta
Ankistrodesmus 1.09 ±1.95 0.52 ±0.27 0.84 ±0.80 0.06 ±0.11 – 0.06 ±0.08 0.14
Chaetophora – 0.23 ±0.36 - – – – –
Closterium 2.29 ±1.41 4.30 ±1.11 1.05 ±1.74 2.04 ±0.47 8.45 ±1.51 1.10 ±1.07 6.40
Coelastrum 0.37 ±0.84 0.20 ±0.19 1.17 ±1.11 0.34 ±0.43 – – 39.19
Cosmarium 0.13 ±0.28 0.18 ±0.24 0.95 ±0.47 – 0.04 ±0.08 0.22 ±0.07 7.10
Cruciginea – – 1.37 ±0.66 – – – 0.14
Desmidium – – – – – – 0.21
Dictyosphaerium – – 0.25 ±0.34 – 0.06 ±0.12 – 4.30
Euastrum – – 0.65 ±0.43 0.06 ±0.11 – 0.11 ±0.15 1.00
Gonatozygon – – – – – – 7.83
M ougeotia – – – – – – 0.14
Oedogonium 1.94 ±1.93 3.77 ±2.84 3.43 ±3.23 12.57 ±6.30 2.30 ±1.05 0.40 ±0.22 2.60
Oocystis 0.13 ±0.29 0.20 ±0.28 0.16 ±0.15 0.30 ±0.29 0.64 ±0.50 0.04 ±0.08 0.35
Scenedesmus – – 6.23 ±3.14 0.06 ±0.11 0.06 ±0.13 – 0.14
Sorastrum – 0.06 ±0.14 7.21 ±2.37 – 0.06 ±0.13 – –
Sphaerocystis 0.12 ±0.28 0.36 ±0.30 0.10 ±0.14 0.05 ±0.09 – – –
Staurodesmus – – 0.15 ±0.34 – – – 0.14
Bacillariophyta 8.81 ±5.06 37.46 ±10.27 27.56 ±7.0 8.24 ±0.53 45.57 ±7.40 8.17 ±4.20 3.20
Euglenophyta
Eudorina 0.73 ±0.70 0.20 ±0.19 – 0.37 ±0.39 0.18 ±0.17 – 5.00
Euglena 1.61 ±0.36 2.06 ±1.21 3.32 ±1.37 1.73 ±0.92 0.37 ±0.39 0.09 ±0.11 2.60
Lepocinclis – – 9.66 ±3.87 0.89 ±0.84 0.25 ±0.46 0.02 ±0.05 –
Phacus 0.89 ±1.01 6.00 ±3.47 7.61 ±1.94 2.21 ±1.42 1.50 ±0.50 0.29 ±0.24 0.28
Trachelomonas 15.54 ±1.91 12.51 ±6.25 18.70 ±4.74 40.75 ±8.23 8.82 ±4.12 6.97 ±5.04 3.81
Chrysophyta
Dinobryon – 0.08 ±0.19 – – – – –
Dinophyta
Glenodinium – – 0.06 ±0.13 – – – 0.14
Fungus 34.60 ±9.40 3.60 ±2.95 0.72 ±0.69 2.94 ±2.96 1.10 ±0.63 0.28 ±0.26 –
FA 13.35 ±4.25 9.06 ±6.80 3.48 ±0.86 5.87 ±0.63 2.06 ±2.70 0.37 ±0.32 0.28
Thecam aeba 4.66 ±3.93 5.38 ±3.47 0.74 ±0.50 5.38 ±0.69 6.67 ±2.32 0.27 ±0.26 0.14
Ciliophora 1.97 ±2.35 0.21 ±0.21 0.09 ±0.13 2.07 ±2.66 0.11 ±0.25 0.02 ±0.05 –
Baccilario p h yceae, were fo u n d alive an d u n d am aged in t h e in -t es-t in al co n -t en -t s o f Derm a-tono-tus m uelleri (Bo e-t -t ger, 1885) an d Elachistocleis bicolor (Gu érin Mén eville, 1838) tad p oles (ECHEVERRÍA & CONFORTI 2000). On th e oth er h an d , stu d ies h ave d em on strated t h at ep ip h yt ic d iat o m s an d cyan o bact erial en d o sym bio n t s en -h an ce gro wt -h , d evelo p m en t , an d su rvival o f Hyla regilla (Baird & G irard , 1 8 5 2 ) (H ylid ae) t ad p o les (KU PFERBERG et al. 1 9 9 4 , KUPFERBERG 1997a) an d t h at co m p et it io n bet ween t ad p o les o f Rana catesbeiana Sh aw, 1802 an d R. boylii Baird , 1854 (Ran id ae) ap p eared t o be m ed iat ed by algal reso u rces (KUPFERBERG 1997b). Th e d etection of Ciliop h ora an d oth er soft-bod ied an im als, su ch as Tard igrad a an d Ro t ifera in t h e in t est in es, is an im p o rt an t fin d in g becau se few st u d ies h ave d et ect ed so ft bo d ied o rgan -ism s o r bact eria, an d t h ey co u ld be t h e real so u rce o f n u t rien t s fo r t ad p o les (INGER 1986, HO FF et al. 1999). Acco rd in g HO FF et al. (1999), t h e co n t ribu t io n o f t h ese sm all it em s t o t ad p o le d iet s rem ain s u n st u d ied in n at u re, an d t h at p art o f t h e m at erial t h at a t ad p o le in gest s t h at is act u ally d igest ed is n o t kn o wn .
Th e u n id en t ified it em s fo u n d in Hyla nana gu t co n t en t s are sim ilar in sh ap e t o m em b ers o f Bacillario p h yceae, b u t it s id en t ificat io n was im p o ssib le, b ecau se n o reco gn izab le st ru c-t u re was fo u n d . LAJMANO VICH ec-t al. (2000) su ggesc-t ed c-t h ac-t Hyla nana t ad p o les h ave a d et rit ivo ro u s d iet , rich in o rgan ic m at t er in d eco m p o sit io n . Th u s, t h ese u n id en t ified it em s m ay b e silica fru st u le o f p art ially d eco m p o sed Bacillario p h yceae.
Th e d at a o b t ain ed su ggest t h e o ccu rren ce o f fo o d selec-t io n , selec-t h aselec-t resu lselec-t s in selec-t h e in gesselec-t io n o f d ifferen selec-t p ro p o rselec-t io n s o f t h e fo o d it em s availab le in t h e h ab it at rat h er t h an in d ifferen t d iet co m p o sit io n s. In ch o ice exp erim en t s, KUPFERBERG (1997a) sh o wed t h at t ad p o les fo raged select ively o n t h e algal fo o d s t h at p ro m o t ed m o st rap id gro wt h an d d evelo p m en t .
DUELLMAN & TRUEB (1986) co m m en t ed t h at fo o d p art it io n -in g am o n g an u ran t ad p o les is cau sed b y d ifferen ces -in t h e ab il-it y o f t h e vario u s sp ecies t o in gest p art icles o f varyin g sizes an d also t o t h e p o sit io n t h ey o ccu p y in t h e wat er co lu m n , a co n seq u en ce o f m o rp h o lo gical ad ap t at io n s fo r t h e exp lo it a-t io n o f sp ecific m icro h ab ia-t aa-t s. Th e h igh n ich e o verlap o b served
Table V. Breadth (B = Levins' m easure) and diversity (H' = Shannon-Wiener index) of the diet of tadpoles in the tem porary pond of Nova Itapirem a, São Paulo.
Species B H'
Physalaemus cuvieri 4.80 1.00
Physalaemus centralis 3.71 0.93
Physalaemus nattereri 2.84 0.83
Physalaemus fuscomaculatus 5.74 1.00
Scinax fuscovarius 5.45 1.00
Scinax similis 4.47 0.96
Leptodactylus fuscus 4.91 0.97
Leptodactylus podicipinus 4.97 0.99
Bufo schneider 5.99 1.00
Phrynohyas venulosa 4.37 0.96
Elachistocleis ovalis 3.70 0.93
Hyla nana 1.80 0.58
1,550 µ m , b u t at least 52% o f t h e it em s were 10-100 µ m in len gt h (Tab . VII). Nich e o verlap b ased o n t h e size o f fo o d p ar-t icles was h igh (CH > 0.54) fo r 92.4% o f t h e 66 p o ssib le co m b i-n at io i-n s o f sp ecies p airs (Tab. VI).
DISCUSSIO N Diet, microhabitat and feeding behavior
Acco rd in g t o ALFO RD (1999), relat ively lit t le in fo rm at io n is available o n t h e d iet s o f t ad p o les an d field st u d ies o f t ad p o les d iet are n o t co m m o n . Man y in gest ed it em s p ass u n d am aged t h ro u gh t h e gu t , wh ile o t h er so ft -bo d ied o rgan ism s an d bact e-ria are n o t d et ect ed (HO FF et al. 1999). In t h is st u d y, so m e o f t h e algae were fo u n d bro ken an d wit h o u t an y o rgan elles in t h e gu t o f t h e t ad p o les, bu t it is n o t kn o wn if t h e t ad p o les d igest ed t h ese algae, becau se t h ey d o n o t h ave cellu lase fo r d igest in g p lan t m at erials (HO FF et al. 1999). Eu glen o id s, alo n g wit h sev-e r a l s p sev-e c i sev-e s o f C h l o r o p h y c sev-e a sev-e , D i n o p h y c sev-e a sev-e a n d
Table IV. Continued.
Food item s L. fuscus L. podicipinus B. schneider P. venulosa E. ovalis Hyla nana *S. fuscomarginatus
Rotifera 5.05 ±4.68 1.62 ±0.78 2.90 ±1.51 13.10 ±10.8 5.23 ±2.53 0.57 ±0.20 0.55
Nem atoda 1.15 ±0.36 0.26 ±0.38 0.17 ±0.26 – 0.22 ±0.30 – 0.14
Tardigrada 0.70 ±0.46 0.06 ±0.13 0.08 ±0.12 0.05 ±0.09 – – –
Acari 0.14 ±0.31 – – – – – –
Copepoda – – – – 0.06 ±0.13 – –
Ostracoda – – – – 1.80 ±3.70 – –
Crustacea (UN I) 3.40 ±2.40 0.44 ±0.61 0.36 ±0.26 0.28 ±0.48 6.12 ±5.70 0.14 ±0.14 0.48
UN I 1 – – – 0.05 ±0.09 4.64 ±2.38 72.54 ±6.74 –
in t h e p resen t st u d y d em o n st rat es t h at p art icle size is n o t a crit eriu m d u e t o wh ich fo o d select io n o ccu rs. Acco rd in g ALFO RD (1999), sp ecies d iffer in t h eir filt rat io n rat es an d ab ilit ies t o in gest p art icles o f d ifferen t sizes, b u t m o st are very efficien t at ext ract in g a wid e variet y o f p art icle sizes fro m t h e in co m in g wat er. In co n t rast , t h e in flu en ce o f t h e m icro h ab it at o n t h e p art it io n in g o f fo o d reso u rces was d em o n st rat ed b y sim ilarit y an alysis wh ich d ivid ed t h e t ad p o les in t o t wo cat ego ries: t h o se t h at m ain ly in gest ed d iat o m s an d t h o se t h at p referred algae o f t h e gen u s Oedogonium . Th e first gro u p co n t ain s bo t h t axo n o m cally relat ed sp ecies an d sp ecies b elo n gin g t o d ifferen t fam i-lies, all o f t h em o ccu rrin g o n t h e b o t t o m o f t h e p o n d . Th e seco n d co n sist ed o f t wo t axo n o m ically relat ed sp ecies, Scinax fuscovarius an d S. sim ilis, wh ich o ccu rred at t h e m id wat er level. DÍAZPANIAGUA (1985), also d et ect ed t wo clu st ers in a co m m u n it y o f five an u ran sp ecies in so u t h west ern Sp ain : b o t t o m t ad
-p o les wh ich m ain ly in gest ed d et rit u s an d -p eri-p h yt ic algae an d m id wat er t ad p o les wh ich m ain ly in gest ed p h an ero gam s o r p h yt o p lan kt o n . Th is au t h o r p ro p o sed t h at a large p ro p o rt io n o f p erip h yt ic algae in d icat es t h at t h e t ad p o les are bo t t o m d well-ers. In o u r st u d y area, m o st d iat o m s b elo n g t o t h e p erip h yt o n co m m u n it y (O . Necch i Jr., p ers. co m m .), in d icat in g t h at t h e t ad p o les o f t h e first clu st er m ain ly feed d iat o m s as a co n se-q u en ce o f o ccu p yin g t h e sam e m icro h ab it at .
Ho wever, m icro h abit at p art it io n in g alo n e d o es n o t fu lly exp lain t h e t wo clu st ers, becau se Phrynohyas venulosa t ad p o les, alth ou gh occu rrin g in m id water, p resen ted a d ifferen t d iet com p ared t o t h e rem ain in g t ad p o les t h at o ccu p ied t h e sam e m icro -h abit at . P-hryno-hyas venulosa t ad p o les in gest ed Trac-helom onas, a p lan kt o n ic alga, wh ereas Scinax fuscovarius an d S. sim ilis tad -p o les scra-p e su rfaces fo r fo o d , a fact wh ich ex-p lain s t h e large am ou n ts of Oedogonium – a sp ecies th at grows on leaves of aq u atic
Table VI. Niche overlap for the type and size (in bold) of the food item s ingested by tadpoles in the tem porary pond of Nova Itapirem a, São Paulo. For abbreviations see table II.
Hn Pce Pcu Pn Pfm Lfu Lp Sfu Ssi Eo Bs Pv
Hn – 0.54 0.59 0.35 0.55 0.54 0.46 0.51 0.46 0.63 0.32 0.57
Pce 0.11 – 0.99 0.94 0.99 0.98 0.96 0.97 0.98 0.99 0.90 0.98
Pcu 0.10 0.96 – 0.91 0.99 0.99 0.94 0.97 0.97 0.99 0.87 0.99
Pn 0.11 0.90 0.85 – 0.90 0.88 0.99 0.86 0.91 0.92 0.99 0.86
Pfm 0.09 0.87 0.87 0.86 – 1.00 0.92 0.98 0.98 0.98 0.85 0.99
Lfu 0.06 0.28 0.29 0.26 0.29 – 0.90 0.99 0.98 0.97 0.83 0.99
Lp 0.11 0.94 0.93 0.85 0.82 0.47 – 0.87 0.91 0.95 0.98 0.89
Sfu 0.07 0.67 0.66 0.70 0.86 0.25 0.60 – 0.99 0.95 0.80 0.99
Ssi 0.06 0.45 0.43 0.52 0.69 0.23 0.40 0.93 – 0.95 0.85 0.98
Eo 0.20 0.93 0.89 0.92 0.82 0.34 0.92 0.60 0.37 – 0.89 0.97
Bs 0.11 0.78 0.85 0.72 0.72 0.41 0.84 0.56 0.40 0.78 – 0.81
Pv 0.10 0.33 0.37 0.29 0.35 0.52 0.50 0.31 0.35 0.40 0.64 –
Table VII. Size categories (length in µm ) of the food item s consum ed and their percent frequencies in the diet of five tadpoles from 13 species. For abbreviations see table II.
Length of item s Bs Eo Hn Lfu Lp Pce Pcu Pfm Pn Pv Sfu Ssi Sfm 10-50 72.2 46.8 9.4 38.0 61.0 42.3 42.0 40.6 63.2 35.5 33.3 37.1 92.00 60-100 14.8 31.7 75.4 22.8 23.0 22.2 26.5 24.3 14.6 24.1 19.2 16.5 2.18 110-150 5.1 9.0 1.3 15.3 4.5 8.1 10.9 15.1 5.1 13.2 12.7 9.5 2.20 160-200 1.5 3.1 8.5 7.5 1.9 5.0 5.2 4.1 5.2 5.7 6.20 6.2 1.50 210-250 1.2 2.5 2.2 3.7 1.5 1.7 2.1 3.8 2.7 4.0 5.80 5.8 0.80 260-300 0.8 2.4 2.2 1.9 0.7 2.2 1.5 2.1 1.3 4.0 2.90 3.7 0.30 310-350 0.3 1.7 0.3 1.0 1.1 1.7 1.6 1.3 1.8 2.5 2.90 3.5 0.20 360-400 0.4 0.8 0.1 1.4 1.0 2.1 0.6 2.0 1.4 1.9 1.50 2.4 0.10 410-450 0.7 0.1 0.2 1.2 0.5 2.3 1.8 0.7 0.6 1.2 2.70 2.3 0.30
m acro p h yt es an d o t h er p lan t s (PRESCO TT 1984) – in it s d iet . Fu r-t h erm o re, Bufo schneideri r-t ad p o les, d esp ir-t e sh o win g a m o rp h o l-o gy l-o f t yp ical bl-o t t l-o m d wellers, were l-o bserved swim m in g n ear t h e su rface u p sid e d o wn , esp ecially at n igh t . Th is beh avio r m ay exp lain t h e p rep o n d eran ce o f p lan kt o n ic algae in t h eir d iet . Leptodactylus fuscus tad p oles, d esp ite bein g typ ical bottom d well-ers (ALTIG & JOHNSTON 1986), co n su m ed a d iet t h at d iffered fro m t h o se o f all o t h er t ad p o les. Th ese d at a d em o n st rat e t h at fo o d p art it io n in g is relat ed n o t o n ly t o t h e o ccu p at io n o f d ifferen t m icro h abit at s, bu t also t o t h e feed in g beh avio r o f t h e t ad p o les. Th e im p o rt an ce o f fo o d p art it io n in g in t h e o rgan izat io n of tad p ole com m u n ities is con troversial. HEYER (1974) an d LAJMA-NO VICH (1997, 2000) claim ed t h at sp ace an d t im e were m u ch m o re im p o rt an t t h an fo o d p art it io n in g, wh ereas DÍAZ-PANIAGUA (1985) d ist in gu ish ed t wo t ad p o le clu st ers o n t h e b asis o f d iet t yp e, m icro h abit at an d m o rp h o lo gy. INGER (1986) o bserved t h at t h e d ifferen t feed in g m o d es o f t ad p o les are relat ed t o m icro h ab it at d ist rib u t io n an d t o so m e o f t h e d ifferen ces in d iet co m -p o sit io n . In t h e -p resen t st u d y, t h e lo w feed in g o verla-p am o n g t h e sp ecies sh o ws t h at fo o d p art it io n in g was a fact o r t h at co n -t rib u -t ed -t o -t ad p o le segrega-t io n , esp ecially o f -t h o se b elo n gin g t o d ifferen t gen era, wh ich o ccu p ied d ifferen t m icro h abit at s an d p resen t ed d ifferen t feed in g b eh avio rs.
Similarity of diets of related species
Am o n g t ad p o les o f Physalaem us Fit zin ger, 1826, o n e sp e-cies o f each t axo n o m ically relat ed p air t en d ed t o p resen t great er n ich e b read t h . Th u s, P. cuvieri an d P. fuscom aculatus h ad m o re d iversified d iet co m p ared wit h P. centralis an d P. nattereri. In co n t rast , t h e n ich e b read t h o f Scinax fuscovarius an d S. sim ilis t ad p o les was sim ilar in t h e variet y o f it em s. Nich e o verlap in fo o d t yp e was h igh er am o n g P. cuvieri an d P. centralis an d am o n g S. fuscovarius an d S. sim ilis, wh ich p resen t ed a lo wer d ifferen ce in n ich e b read t h . Th is su ggest s t h at n ich e o verlap m ay b e great er am o n g m o re gen eralist sp ecies.
In t h e t h ree p airs o f t axo n o m ically relat ed sp ecies, n ich e o verlap p in g was h igh (CH > 0.50). Excep t fo r Physalaem us cen-tralis an d P. cuvieri, h owever, som e n on -con gen eric sp ecies (e.g., P. cen t ralis a n d Lept odact ylu s podicipin u s; P. cuvieri an d L. podicipinus) sh o wed eq u al o r h igh er o verlap . Th ese d at a sh o w t h at t h e sim ilarit y o f t h e t ad p o le d iet can n o t be exp lain ed sim p ly by t h e t axo n o m ic p ro xim it y. Th is d o es n o t m ean t h at t axo -n o m ic p ro xim it y, a h ist o rical fact o r, was -n o t im p o rt a-n t i-n t h e com m u n ity stu d ied , bu t con tem p orary factors, sp ecifically feed in g beh avio r an d m icro h abit at u se, also in flu en ced t h e u se p at -t ern o f fo o d reso u rces. Th ese d a-t a d em o n s-t ra-t e -t h a-t -t h e o rgan i-zat io n o f t h is co m m u n it y is co m p lex an d resu lt s fro m t h e in t er-act io n o f several fer-act o rs.
ACKNO WLEDGMENTS
W e t h an k O rlan d o Necch i Jr. an d Lu ís Hen riq u e Bran co fo r t rain in g an d h elp wit h algal id en t ificat io n , an d valu ab le in fo rm at io n ab o u t algal m icro h ab it at , an d Fran cisco Lan gean i,
all o f UNESP, S.J. d o Rio Pret o , fo r crit ical review o f t h e m an u -scrip t . Nelso n Bern ard i an d Pat ricia Toth reviewed En glish . Th is st u d y w as p art ially su p p o rt ed b y research gran t s fro m t h e Fu n d ação d e Am p aro à Pesq u isa d o Est ad o d e São Pau lo – FAPESP (p ro cesses 01/ 07944-7 an d 01/ 13341-3).
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