Litter decomposition and Ectomycorrhiza in Amazonian

1. A comparison of litter decomposing and ectomycorrhizal Basidiomycetes in latosol­ terra-firme rain and whité podzol campinarana

Rolf Singer ( *) lzonete de Jesus da Silva Araujo (*)

Abstract lNTRODUCTION Application of a mycosociological method (adaptation of the Lange method) in Central lt had been assumed that ectomycorrhiza Amazonia produced the following results: In the in the neotropics ls restricted to 1) secondary­ white-sand podzol campinarana type of forests the forest and partially destroyed or damaged dominant trees are oblígatorily ectotrophically tropical and subtropical forests (cicatrizing mycorrhizal; litter is accumulatea as raw ), 2) to the natural vegetation above as a consequence of ectotroph dominance; fewer a certain altitude in the Andes and pre-Andine leaf inhabiting litter fungi occur in the dry as tropical-montane zone, 3) of intro­ well as the wet seasons tha..'1 are counted in the latosol terra-firme rain forest, and the fungi duced ectomycorrhizal trees, inoculated with of that category are most strongly represented eccomycorrh1za or carryng or ("F-dominance") by other here than in the with seeds or seedlings, 4) possible scattered terra-finne stands tested. The ectomycorrhizal trees occurrences restricted to certain genera of and !ungi are enumerated. On the other hand, in Cormophyta [Salíx was suggested), not being the terra-finne forest, ectotrophically mycorrhizal dominant in the tropical rain forest (Singer, !ungi did not occur in the test plots. The trees are 1963; Singer & Morello, 1960). This assumption, almost all non-ectomycorrhizal in primary terra­ firme forest; here, litter doE-s not appreciably if correct, would , mean that the neotropical accumulate as a deep raw humus layer because the humid lowland cannot be expected to produce considerably higher number o! leaf inhabiting litter anything in the way of a t rue ectotroph forest !ungi (ratios o! 4:1 to 4 .2:1 in favor cf terra-finne) excepting secondary forests (capoeira), plan­ and greater diversification (a larger number of tations and possibly forests containing species) is potentially capable o! reducing more scattered non-dominant ectotrophic elements. than the yearly leaf-fall. In this study, a group of !ungi was · mainly considered which is not This would mean that there is a basic differ­ represented in laboratory litter decomposition ence in the composition of the neotropical and experiments. However, a comparison with un­ the paleotropical lowland rain forests. published and published data shows that otir results However, recent observations by Kreisel satisfactorily match the experimental and phyto­ sociological data obtained both with other classes ( 1971) and Fiard (personal communication) o! microorganisms and wíth observations in other indicate that in the Gulf area certain types of regions. The quantity o! litter decomposing !ungi forest contain ectotrophically mycorrhizal in the folücolous group depends mainly on tne elements {Coccoloba in Cuba, Torrubía in amount o! precipitation during the last few days Martinique). before counting. This does not hold for all llgnicolous f ungi.. The reasons for this as well a.s Our own recent investigations in the Lower the mechanisms by which the ectomycorrhizae may Rio Negro region of Central Amazonia show. reduce litter decomposition rate:; and influence the thât certain vegetation types (campina, campi­ nutrient cycling patterns are disc-ussed. The most nar·ana, igapó) are rich in ectomycorrrhiza­ important genera of Basidiom,ycetes involved in forming fungi, e. g. (Singer, 1978a). litter decomposition in the Lower Rio Negro forest associations are enumerated. Possible economic Thus, in both hemispheres, certain tropical significance of introducing ectotrophs in the terra­ require for the formation of any kind of firme forest is indicated. forest the presence of ectomycorrhiza. Canse-

( • ) - Instituto Nacional de Pesquisas da Amazônia, Mall'aus .

ACTA AMAZONICA 9(1) : 25-41. 1979 -25 quently, the anectotrophic "hyiaea" is inter­ domycetes, Zygomycetes, etc., as well as mittent, with interspersed islands of ectotroph , Myxomycetes, and Actinomycetes. forests where climatic or edaphic (in Amazo­ worms, Arthropods, higher animais) under nia mainly the latter) conditions make it various conditions of tropical forests has, as impossible for anectotrophic trees to obtain far as we are aware, never been made, and sufficient mineral nutrition unless ectotrophs with the methods available, meets with some dominate to such a degree as to change the difficulties. microbiology of the completely and intro­ Under these circumstances it was felt that duce what has come to be cailed direct cycling a method had to be found that at least provides (Went & Stark, 1968) or "short-cycling" (Har­ quantitative data on the Basidiomycetes, their iey, 1977) of mineral nutrients. numbers, diversity, requirements and lhe proposal (Singer, 1964) to reclassify dependency on meteorological conditions, their the forest types of the world in such a way capacity of forming ectomycorrhiza, their fru­ that they are first and basically divided into iting periodicity, in fact ali data that could not two main groups [1) - ectotroph and anec­ be obtained in laboratory studies. This method totrophic forests - has been ignored by forest had already been introduced (Moser-method in ecologists, first because of misunderstandings , North, and South America; Lange­ with regard to the term "ectotroph" on the method in Europe) and had now to be adapted part o-f some mycorrhiza-speciaiists (Meyer, to the conditions of the lowland tropical rain 1973) and secondly because understandably forest. The method chosen - the Lange the mycological literature is not adequately methoci - was expected to provide the desired accessible to ali forest ecologists and phyto­ data and permit comparisons between the 2 sociologists ( ) • latosol -terra firme rain forest and the podzol The necessity to accept the importance ot white-sand campinarana . basidiomycetous components of the eco­ systems and the usefulness of terms de­ MATERIALS AND METHODS scribing unequivocally the -cormophyte symbiotic associations at the levei of the The Lange method ( 1948) was introduced individual (ectotroph) and the -fungus for the study of fungus sociology in Danish community (ectrotroph forest) has, in the Sphagneta whereby, in contrast to the Moser menntime, become ever more obvious and the method (1959), permanent 1x1 m squares present study wi 11 show that, without them, an were marked and fructifications periodic3lly undcrstanding of the phenomena observed is counted. In ou r case one 5x5 m square was nearly imposs1ble. marked in the primary latosol terra firme forest With regard to litter decomposition, the 30 km north of Manaus (immediately adjacent role of the Basidiomycetes is generally under­ to a hectare of a fully studied (Prance et. al., stood but rarely presented in quantitative form, 1976) forest reserve at EMBRAPA) and regu­ principally becauae earlicr investigators were larly observed (in 6-11 day intervals) 37 times hampered by the intricacies of the during a whole year. Furthermore two 5x1 m involved. On the other hand the experimental rectnngular test lots, one in latosol terra firme methods tend to minimize the part played by forest at km 45 of the Manaus-Caracaraí Road Basidiomycetes since in litter samples their and another immediately adjacent in the Re­ growth under laboratory conditions is sup­ serva Biológica de Campina INPA-SUFRAMA, pressed. A convincing study, or even estimate with three countings (two, at different seasons of the relative numbers and efficiency of litter of the year coordinated with countings, the decomposing organisms (Basidiomycetes, same day, in the latosol terra firme forest) . other Eu-Mycetes including Hypho-and En- The campinarana forest, the relatively most

( 1 ) - An ectotroph forest is one in which the dominant trees are obligatorily ectomycorrhizal. An anectotrophic forest is one in which the dominant trees are not obligatorily ectomycorrhizal. ( 2) - • Despite this massive documentation plant scientists commonly seem to little heed the phenomenon [mycor­ rhiza] and its implications unless they are studying mycorrhizae per se" J . M . Trappe & R. D. Fogel (1977).

26- Singer & Araujo thoroughly studied one in the Lower Rio Negro clays with exceptional temperaturas or air (Andcrson, 1978; Anderson et a/., 1975; Lis­ humidity measured were marked as such for bôa, 1975; Prar.ce, 1975) is located between later reference. The precipitation data for the the entrance to the Reserva and the transition test lot at EMBRAPA were obtained hom the to the more open, true campina-vegetation meteorological station of EMBRAPA (\ess than further east. In the following text we shall 1 km away) until October 1977, and from then refer to this lot and the corresponding cam­ on from that of Ducke Forest (INPA), little pinarana vegetation in other Rio Negro locali­ more than 3 km away. During this latter period ties as CR and to the latosol terra firme rain very minor rainfall may have been local, but forest as TF. any major rainfall and most minor ones were The fungi were counted accordlng to the sufficiently widespread so that the figures carpophores observed and were w ithout diffl­ registered at Ducke Forest should be con­ culty divrded into six main categories, viz. sidered valid for the test lot. those inhabiting dead dicotyledonous leaves The presence and distribution of ectotro­ (foliicolous), those inhabiting dead pieces of phically mycorrhizal fungi was determined by dicotyledonous wood and fallen branches and the following method: lnside the test plots sections of fallen tree trunks (lignicolous); intensive search was undertaken in order to those inhabiting monocotyledonous trash; detect 1) short suspected of being those growing on the basic mineral soil without ectomycorrhizal (these were preserved in recognizable orgMic tissue (terricolous); alcohol and tested anatomically), 2) carpo­ those growing in association with tree roots phores belonging to any of the genera known (ectomycorrhizal); those growing in associ­ to be ectomycorrhizal (the surrounding rootlets ation with algae (basidiolichens) . were then investigated as above) . This search In order to obtain data on a homogeneous for ectomycorrhizal fungi was not restricted to group of litter decomposing fungi, ali Dis­ the test lots but was extended to the whole comycetes and carpophore-producing Basidio­ surrounding area so far as it belonged to the mycetes were counted excepting the lignico­ same type of primary forest. The search lous category and the fungi associated with outside the test plots was supplemented by alg3e; in the lignicolous category Aphyllopho­ occasional observations and collections by A. rales were excluded. and in the ali but B. Anderson and T. V. St-John. Basidiolichens were excluded. The fungi counted are exactly those that are probably RESULTS overlooked in traditional phytosociological A. The lato sol terra firme forest (TF) - The work as well as in laboratory experiments. They Cormophyta individuais which contributed to were identified, as far as possible to the the litter of the TF test plot I (30 km N of species, and in ali cases to the genus; speci­ Manaus) and/or penetrated the lot which their mens of each species were deposited at the roots are the fottowing : HerbMium of INPA, Manaus. Araceae: Anthurium sp. The meteorological data corresponding to Bignoniaceae species a 1·, 2-, 3-, and 6-day period preceding the Bombacaceae: Probably Bombacopsis nervosa actual count (in the morning between 8AM and (Vitt.) Robyns 11 . 30 PM) were restricted to precipitatlon : Scleronema micr8nthum Ducke since in the ·interior of the foreot precise data Chrysobalanaceae: Licania sp. on soil temperature and humidity of the air Duckeodendraceae: Duckeodendron cestroides immediately above the soil were not available Kuhlm. and did not appear to influence fungus growth Euphorbiaceae: Mabea sp. equally in ali str~ta and substrata involved nor Lecythidaceae: Eschweilera sp. did they vary appreciably except as a functlon " : Corythophora rimosa W. Rodr. of precipitation. Wind velocity never reached Leguminosae (Caesalpinlaceae): Eperua sp. sufficient force or duration inside the forest " (Mimosaceae) : Pithecol!obium during the observation period. Nevertheless racemosum Ducke

Littcr decomposition ... -27 Melastomaceae: Miconia sp. Sterculiaceae: Theobroma sp. Meliaceae: Trichilia sp. In the test plot at km 30 (test area I) in TF, Moraceae: Brosimum sp. the year-round survey ot I itter decomposers Myristicaceae: Viro/a ? e/ongata Warb. yielded the results given in table I. species In the test plot at km 45 (test area 11) in TF, Palmae: Bactris sp. two surveys were made with the specific aim " : Astrocaryum acaule Mart. and A. sp. of comparing, under equal conditions, the Rubiaceae: ? Coussarea sp. survey of test area 111 on CR (see chapter B, Sapotaceae: Eremo/uma sp. below). This result can be found in table 111 . " : Pouteria sp. B. The campinarana (CÃ) - The Cormophyta The Cormophyta of the latosol TF test lot 11 whose roots crossed or entered test plot 111 in (km 45 of the road Manaus-Caracaraí) with CR or contributed to its litter are the following: roots reaching into and/or contributing to the Annonaceae: Annona nítida Mart. litter on the surface are the following : Apocynaceae: Tabernaemontana rupico/a Benth. Araceae: Phi/odendron sp. Guttiferae: Clusia sp. Burseraceae: Protium sp. Leguminosae (Caesalpiniaceae): A/dina hete­ Chrysobalanaceae: Licania /atifolia Benth. ex rophylla Spruce Hook. ex Benth. Parinari sp. : Swartzia do/ico- Leguminosae (Papilionaceae): Derris flor/bun- poda Cowan da Benth. Linaceae: Roucheria punctata Ducke Linaceae: Roucheria punctata Ducke Myrsinaceae: Conomorpha sp. Melastomaceae: Miconia sp. Myrtaceae: Myrcia servata McVaugh Myristicaceae: Viro/a sp. : Eugenia sp. Myrtaceae species Ochnaceae: Ouratea spruceana Eng/. Musaceae: Heliconia psittacorum L. f. Sapindaceae: Matayba opaca Radlk. Rubiaceae species (incl. Psychotria sp.) Simarubaceae: Simarouba amara Aubl. Sapotaceae species The surveys of the litter decomposing fungi of : Micropholis sp. test area 111 will be found in table 11. Table 111

TABLE 11- carpopllore count in plot UI. CR, carpophores per spccies (ca/sp.), and F-dominnnce - compared with a carpophore count in a Patagonian ectotroph forcst (Singer, 1971).

1. 2. 3. Nothofagetum Average 28 li 19'78 (maln 5 IV 1978 (main 10 VIII 1978 ( dry (N. pumilio> CR rai.ny season) rainy season) season) 1964 1) Foliic. l 33 25 8 22 20.9 Lignic. 11 11 8 10 5.1 Ectomyc. o 1 o 0.3 8.9 Total 44 37 16 32 39.2

Foliic. ca,tsp. 3.3 3.6 4 Lignic. ca;sp. 1.8 1.8 2 Folilc. F- .Myceoa osmundi- M.ycena osmundi- M.ycena microlcu. dominance cola var. (14) cola var. (16) ca (15.2) Lignic. F· llemimycena. Hem.imyccna. Crepidotus sphnc- dominance spec. 04) spec. (5) rosporus (6.6) 1l Doto here odJustcd to 5 m2 surfoce os used in plot 111.

28- Singer & Araujo shows the data obtained when test area 111 in nearly ali cases can be explained by some (CR) was compared wíth test plot 11 (TF) in special factors entering in specific surveys order to obtain, under equal meteorologicat such as exceptionally violent and abundant conditions comparable figures for both CR rainfall (which is contraproductive to fruiting and TF. especially during the "summer"; this does not necessarily mean that the mycelial activity C. Dependence of fungus growth on preclpl­ during such periods is diminished), possibly · tation - Our chart (fig. 1) clearly shows that also exceptionally high air humidity in the test there is a strong dependence of fungus growth, area (which is favorable for fructification) . as measured by carpophore production, on the There is also some influence of precipitation amounts of precipitation. There is no pro­ on the number of carpophores produced by portional rise of carpophore production but lignicolous and terricolous fungi but in this mostly an increase with higher, a decrease case the dependence is not, as in the foli­ with lower amounts of precipitation. The icolous fungi, primarily on the amount of clearest dependence can be demonstrated by rainfall during the preceding day, but on that the absolute number of carpophores and the of a longer period preceding the appearance of number of carpophores per species in the the carpophores. The reason for this will be foliicolous category (fig. 1) . There are even discussed in Critic. But dependence on here occasional irregularities which, however, avaílable humidity in and on the substratum

TABLE UI - Comparation dat.a on carpophore and species counts in adjacent CR (plot 111) and TF (plot 11) test areas.

CR TF TF CR TF CR/TF ~ CR CRj TF CRj TF S IV 78 S IV 78 S IV 78 10 VIII 78 10 VIII 78 10 VIII 78 X X :x - Total, carp. 36 163 1:4.5 16 40 1:2.5 52 203 1:3.9 , species 13 17 6 1~ carpJspecies 2.8 9.6 2.7 3.1

I Foliicol. carp. 25 106 1:4.2 8 32 1:4.0 33 138 1:4.2 , species 7 8 2 , 8 carp./sp. 3.6 4 , 13.3 4 % of Total 69.45 64.98 50 82.5

Folücol + Terric. ca. 25 107 1:4.3 8 3~ 1:4.13 33 140 1:4.2 , sp. 7 9 2 9 ," , ca/sp. 3.6 11.9 4 3.7 , % of Total 69.45 65.03 50 82.5

Lignicol. carp. 11 54 1:4.9 8 1 1:0.88 19 71 1:3 .7 .. species 6 '1 4 4 , .carpJsp. 1.83 7.71 2 1. 75 , % of Total 30.56 33.1 50 17.5

Terricol. carp. o 1.0 0:1 o 1.0 0:1 o 2 0:2 Mycorrhizal carp. 1 o 1:0 o o 0:0 1 o 1:0 Dominant species % of Total 44.4° 22.7+ 22.5+

( • ) Myccna osmundlcola ( +l M)·ccna polyadclpho

LiHer decomposition ... -29 190 0 180

170 • _. _ f CIS X lO -0- Fo CA; 2 160 · -- PREC. PREV. OAY IN mm 0

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·~ la() 0 0 0 _..., 120 ( I lj' I l i I I I 110 I 1\ I 0 I I I I 0 ' I I' I ,, . ' 100 ' I \ ' li 11 ' ' 0 I I ' I I " I I /' I \ I 1 ' ' -e ( I'

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40 0 o 30

20 lO ~/ o I 2 3 • S 6 1 8 g 10 11 12 13 1t IS 16 17 11 I' 20 21 ll l3 H 25 26 l7 28 ~? 3 0 Cll 3Z 33 J

Fig. 1 - COmpanson of prccipitation during the day previous to counting date :md fruiting ( folücolou~ carpophorcs - Fo Ca, and foliicolous carpophores per species - Fc/s) in TF.

3 is quite obvious inasmuch as during the driest D. F - dominance ( ) - This h as been es­ periods of the year there is also a decrease in tablished at every single survey date for the carpophore production in ali categories. On the two most important categories (foliicolous other handl one of the interesting results of a and lignicolous) . Excepting those surveys that year-round survey is the observation that in produced such a small number of carpophores ali test areas there is even in relatively dry in either of the categories that the data could perioas of the year, interrupted In 1977 (as in not be considered statistically significant, many years) by a short secondary rainy season, there was a certain consistency in the F-domi· never a complete stop of carpophore pro­ nance of Mycena polyade/pha in TF and M. duction which means that the mycelial in ali osmundicola in CR, each species being most categoriesl continue their activity without commonly encountered and most evenly dis­ interruption, even though in summer to a lesser tributed in the respective test areas, and thcir 'degree and with the participation af species total numbers in ali surveys to·gether being normally not fruiting in the main rainy season. higher than those of other species. Ou r data

( 3) - We use, to be precise, the term F (ruitíng)-domlnan ce for the dominance in numbers and density. determined by the carpophores rather than by the extenslon o f the mycelia in a given tungus associatlon. F-dominance ls not an ldentlcal but an analogous term compared to the term domlnance o f Cormophyta In pfiy"tosociology.

30- Singer & Araujo show that F-dominance is not constant during which macromorphologically and anatomically different periods of the year (different proved to be ectomycorrhizal belonged to a • aspects "). in different forest communities liana (Gnetum sp.) which is (TF and CR) cf. fig. 2 and table I . certainly not dominant, but on the contrary, scattered to rather rare in TF . The other E. Presence and absence of ectotrophic found to be ectomycorrhizal belonged to Neea mycorrhizae - Our study shows that ectomy­ 4 sp. ( ) • These data lndicate that TF is, although corrhizae are present in the test area in CR, scattered ectomycorrhizae occur, not an absent in the test areas in TF. The negative ectotroph forest but an anectotrophic forest. result in the larger test area I (TF) suggests that TF does not contain ectotroph elements The characteristic, bright yellow clamp­ but a search through the entire I ha stand bearing, mycelium farming the ectonwcorrhiza produced in two cases roots with ectomycorrhi­ in Gnetum .sp., first collected by T. V. St-John, za and in two more cases carpophores of was subsequently also discovered in CR, and genera believed to be generally ectomycorrhi­ tentéltively identified as belonging to Sclero­ zal ( craseoderma Bas and Russulv derma slnnamariense Mont.. Only physiological puiggarii (Speg.) Sing.) . Onc of the roots studies can determine whether this is a

ISO ·-MY<:ENA POLVADE~LPHA

14 0 ----- M. XANTHDPHYllA X S

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120

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$0 • :• I I ti 'I 1 I I I I I I I I ,I I 1·- I I Í' lO ·, , I I I I ' I ' · . I I I ,, \ I I I ' \ ,\ I I \ . I, ' I \ · - f \ ' I 'I ' I O I 2 :1 4 5 6 1 11 ' 10 11 12 13 1+ 15 16 17 18 I 9 20 Zl 22 23 2'1' 25 26 27 28 29 30 :SI 32 33 3~ 35 36 31

F!g. 2 - Number of carpophores of two representativa species of foliicoious !ungi durlng 37 count.s in TF (for correspondlng meteorological data compare fig. 1 and table I).

( 4) - Neea (Nyctagln-acae) forms clcatrlzlng mycorrhlza where root-damage occurs, especlally In secondary latosol forests.

Litter decomposition ... - 31 mutualistic or a pseudomycorrhizal relation­ • Amanita xerocybe Bas ship but the apparently constant associat ion Bolete/lus ananas (Curt.) Murr. var. minar Gnetum/ Basidiomycete sp. in primary forest ined. (type variety widespread) suggests the former. On the other hand, in *Cantharellus guyanensis Mont. (widespread) the CR and shaded campina, obligatory Cortínarius (subgenus ) sp. ectomycorrhizae are not an isolated occurrence Cortinarius (subgenus Telamonia), four but are represented by numerous obligatorily species, collections B 11021, B 11026, ectomycorrhizal mycelia and carpophores, B 11026a, B 11313. connected with severa! tree species ali through Craterel/us orinocensis Pat. & Gaill. the area and are particularly and specifically (widespread) present on the dominant trees (Aidina hetero­ Fistuline/la campinaranae Sing. phylla Spr. ex Benth. and probably also other *Hebelomina amazonensis Sing. ined Leguminosae such as some Swartzia and lnocybe (subgenus lnocybe) sp. ·Eperua spp. as well as Sapotaceae, specifi­ amazoniensis Sing. ined. cally Glycoxy/on inophyllum (Mart. ex Miq.) Lactarius annulifer Sing. ined. Ducke) . The ectotrophic element is also repre· Lactarius brasi/iensis Sing. ined. sented in test area 111 (CR) and is abundantly * Lactarius reticulatus (Berk.) Sing. lalso in present in other campinarana forests along the igapó). road to Caracaraí (km 114-5, km 125) which Lactarius venezuelanus Dennis (widespread) belong to the same general type of ectotroph Phyllobolites miniatus (Rick) Sing. forest although they may well be described as (widespread). different subassociations or associations ot Phylloporus gymnocystis Sing. ined. the campinarana type because they are flo­ Porphyrellus olivaceus Sing. ined. ristically and in soil characteristics somewhat ? orinocensis Pat. (widespread) different from the area 111. A list of the fungus Russula puiggarii (Speg.) Sing. (widespread, components of ectotrophs observed in ali . cam­ also in igapó and secondary forest - only pinarana forests investigated is given below facultatively mycorrhizal) (those with asterisk (*) demonstrably linked *Russula nanei/a Sing. with Leguminosae or Sapotaceae; the rest *Russula pachycystis Sing. expected to be ectomycorrhizal because of Strobi/omyces pauper Sing. ined. taxonomic position and occurrence restricted *Tylopilus arenarius Sing. & I. Araujo to campina, campinarana and black-water inun­ Tylopi/us potamogeton Sing. & I. Araujo (also . dable forests subject to inundation (igapó) in campina and igapó) . and growing under Leguminosae and Sapota- • Xerocomus amazonicus Sing. & I. Araujo ceae, or because they were demonstrably Xerocomus aff. brasí/iensis (Rick) Sing. linked with or Psychotria roots}: * Xerocomus g/obulifer Sing. ined. Xerocomus scrobiculatus Sing. ined. GASTEROMYCETES: The seemingly small representation (little over 1% of the carpophores counted and Mycelium, ectomycorrhizal with Gnetum cf. scarcely 3% of the species observed) of the paniculatum Spr. (also in TF) . Scleroderma 36 species enumerated above within the test sinnamariense Mont.. area 111 is obviously not due to the scarcity of the total since everywhere including APHYLLOPHORALES: test area 111 ectomycorrhizal shortroots were Sarcodon atroviddis (Morg.) Banker numerous (although in obligatory as well as (widespread). cicatrizing mycorrhizae we find the root system of a·n individual ectotroph of Amazonian prima­ ·ry as well as secondary forest is not con- AGARICALES: sistently shortroot-like) . The reason for the

f: Amanita campinaranae Bas scathered fruiting may be attributed to three Amanita sulcatíssima Bas (widespread) factors: (1) ectomycorrhizal fungi produce,

Singer & Araujo 32- especially in the tropical rain forest, much Dr. K. Dumont who (personal communication) larger carpophores than most litter fungi; in finds a much stronger rep1·esentation of the tcst area 111, one carpophore of Xerocomus Discomycetes in general in the tropical-mon­ amazonicus equals, by dry weight as well as tane forests and in the lowland forests closer by volume, the sum of ali other carpophores to the Andine chains as well as in the sub­ collected and counted that day; (2) the corre­ tropical forests. Likewise Gasteromycetes and sponding volume of substratum reached by the Aphyllophorales, although often encountered: hyphae of the individual mycelíum of the represent a definite minority among the litter carpophore of an ectomycorrhizal fungus decomposing foliicolous fungi. carpophore is considerably larger than that of Among the terrestrial fungi, the genera the non-mycorrhizal species (since there is an Lepicta, Rhodophyllus, , Conocybe, obvious proportional relation between the mass Callistodermatium are prominent. lt is re­ of the carpophores and the extension of the markable that in Amazonia in general, hypo­ mycelium); (3) the observations in campina­ geous fungi and "secotiaceous" Basidiomyce­ rana as well as in other ectotroph forests tes are so poorly represented that until now (Lange, 1948; Singer, 1971) show that ecto­ not one specimen has come to our attention . myccrrrizal fungi do not fruit - as many Among the Basidiolichens, only one species, saprophytes do - continuously or in a suc­ Multic/avula sp. is common. cession of "flushes" - but appear solitarily or in small groups at longer intervals ali We have not counted and incorporated in through the rainy season, especially at the our charts the insect-parasites (Ciavicipitales beginning and towards the end of the rainy and Deuteromycetes) and endotrophically season , because the living root, their carbohy­ mycorrhizal Basidiomycetes (orchid mycorrhi­ drate source, is continually available during zae) and Zygomycetes (VA-mycorrhiza). Ali the whole year and independent of the con­ three categorias do, however, occur in ali test ditions modifying their capacity of producing areas, in varlable numbers and different enzymatic cellulose breakdown. specialization (see Discussion) . In the lignicolous group, the genera most F. ldentity of the fungi observed and their frequently founú are aside frcrm, again Mycena, ecological specialization - A list of ali the Marasmius, Hemimycena, Marasmiellus, Hy­ species occurring, the quantity observed in dropus the tollowing: Lactocollybia, Gerrone­ each survey in test areas I, 11 , and 111 has, with ma, Collybia, Polyporus, Pyrrhog/ossum, Stlg­ the exception of the ectotroph-forming species, matolemma. While we did not take into con­ thus far not been completed. These data as sideration any non-Agaricales in this category, well as the data available on host specia­ it should be noted that the number ot aphyllo­ lization are now being collected for the second phoraceous lignicolous species in TF was as part ot this pape r. For the purpose of the a whole lower than that of the Agaricales, with present part they are not essential . lt may the exception of such prominent species as however be mentioned here that the genera Amauroderma sp. and Caripia montagnei observed most commonly in the foliicolous (Berk.) O. K., the latter also very common in ~ategory are : TF and CR. This is in contrast to the promi­ TF test areas: Myceng, Marasmlus, Hemimyce­ nence of lignicolous Aphyllophorales in freshly na, Marasmiellus, 'Gioiocephala, Hydropus. cut or bumed primary as well as in secondary CR test area: Mycena, Marasmius, Hemimyce­ forests, on construction wood, lumber piles, na, Marasmlellus, Hygrotrama, Clavulinopsis. fences, etc. Althouyh we have registered in the foli­ Specialization is generally high as far as icolous category a wide spectrum of fungus habitat categorias (foliicolous, lignicolous, famílias, it is remarkable that the Agaricales etc.) were concerned, and we found no diffi­ are most strong\y represented. Helotiales culty in classifying the Basidiomycetes in were poorly and Pezizales very poorly repre­ habitat-groups. This is not only interesting but sented. This observation is corroborated by also fortunate insofar as it permits precise

IJtter decomposition ... -33 separate counting for each category and reasons. In the fungi this situation is ex­ reveé:ls a specific pattern of behavior of each pressed by the fact that terricolous fungi are, category with regard to mycelial deveiopment, if not abundantly or consistently, but un­ carpophore production, dependence on precipi­ doubtedly present as a definite category in the tation, etc. The relatively high percentage of TF while what may come closest to this habitat lignicolous fungi in the tropics has been indi­ group in CR may be termed humicolous. cated before (Watling, 1977). lt is also oovious Humicolous mycelia are found in the \ower in our tables where the lignicolaus carpopho­ stratum where sand particles are mixed with res comprise one quarter to one half of the alread deformed or small fragments of rotting total in CR while more or less one eight af the leaves or pieces of wood, recognizable as such carpophores are lignicolous in the corre­ but not further identifiable. We registered such sponding (i. e. ectotroph) forests of the fungi as foliicolous respectively lignicolous . temperate zone of South America (Singer, The lack of exposed earth in CR also explains 1971; Singer & Moser, 1965). Only very few the absence ·or scarcity of basidiolichens . species are both lignicolous and foliicoious. lt is also well established (Anderson, 1978) Mycena po/yadelpha, occurring predominantly that the number of species of phanerogams is on Jeaves, grows also occasionally on small smaller in the white sand stands than in the pieces of dicotyledonous wood. Mycena os­ terra firme forests which also finds its ex­ mundJco/a (sensu lato) occurs frequently on pression in the enumeration (see Results) both Jeaves and wood, but may be a hetero­ of host species in the test lots in TF geneus taxon since populations vary in minar anci in CR. In TF it is impossible to find any anatomical and pigment characters, yet only single species or even gemus that may qualify one character combination is found in each, as dominant and only a group of tree species either foliicolous or lignicolous population. This treated as a unit may be termed leading since observation was also made by A. H. Smith their combined individual representations are ( 1947) . In contrast to a statement by Watling most numerous and produce the largest (1977) we know of no example where a biornass, root extension, and litter in a given saprophytic speceis, terricolous in the temper­ stand of primary forest. In CR, on the other ate zones, would be lignicolous in the tropics. hand, dominant species may be determined An exception ta this rule may be seen in the (Prance et. ai., 1976). The average height of fact that ectotrophically mycorrhizal fungi the trees is greater in TF than in CR, and partly which are only exceptionally lignicolous in as a consequence of this but also because of a temperate zones very frequently ascend on different pattern of leaf shedding, the number standlng living or dead trunks in the neotropics. of leaves shec! during one year is apparently However, their established or assumed ecto­ smaller in CR than in TF. Less leaf shedding trophy suggests that the mycelium, at least in per surface unit compnred with greater litter its mycorrhizal state, penetrates the soil under­ accumulation in CR thê.n in TF is remarkable neath so that it is in contact with the roots. and can only be attributed to a lesser degree of activity of litter decomposing fungi in CR COMPARISON BETWEEN TF AND CR than in TF . A. Habitat - lt is well known (Prance et ai., Furthermore, the floristic composition of 1976; Singer, 1978) that the litter in the white­ campinarana-type forest and latosol terra firme sand stands of forest accumulates to form a forests is different (Prance et a!., 1976), as is deep, soft layer not exposing the mineral soil also shown in the enumerations of species whereas in the clay soils of terra firme forests influencing the substartum in the three test no such accumulations of litter and raw humus plots (see above) . While there is a small occur and the mineral soil is exposed over number of species common to both commu­ large areas or merely covered by freshly fallen nities. the majority of the species is specific leaves; an accumulation of leaves and wood for one or the other community, and the occurs only in some depressions or other number of genera common to both is relatively restricted places for purely mechanical smat:.

34- Singer & Araujo B. Quantitativa differences in the TF and CR (Singer, 1978a and 1978b). This involves a litter decomposing fungi (saprophytes) - A different type of N and P cycling (Went & comparison between our tables and particularly Stark, 1968) and to a certain degree also C a glance at tab\e 111 which reflects our counts cycling (Lundeberg, 1970). and will inevitably under equal meteorological and seasonal con­ express itself in the characteristics of litter ditit'ns in both TF and and CR shows significant and soil (Harley, 1975). diffrerences, whereby the fructlfication (and E. Distribution patterns of the mycoflora ôf therefore the number of active mycelia) is TF and CR - In previous studies by the senior indeed considerl'lbly smaller in CR than in TF. author it has been stated (Singer, 1971; Singer Consequently the rate of decomposition ob­ & Moser, 1965) that in ectotroph forests a served in CR, can be satisfactorily explained by smaller percentage of the observed fungi is this observation regardless of the accessory subcosmopolitan or widespread (in the sense role other decomposers may or may not play that these species occur also outside their (see Discussion) . communities and over an extensiva area) than A further difference, perhaps of lesser in the anectotrophic forests. We csnnot com­ signiíicance, is the fact that during transition pare the percentage figures obtained in the from rainy to dry season the lignicolous com­ papers quoted and in unpublished surveys In ponent of the litter decomposers increases in the Andine Alneta and adjacent anectotrophic CR while in TF it decreases in percentage forests with precise figures resulting from the exc~!pt in cases where the carpophore pro­ present study while the identification of many duction is too small to be statistically signifi­ species is still pending (see Results) . cant (see table I) . The dominant species in TF belong no doubt in their majority to the widespread type (and C. Comparison of neotropical ectotroph forests are ditferent from those of CR), and the list of and ectotroph forests of the south-temperate the ectomycorrhizal species of the campinara­ zone - A previous study of the macro-fungi na shows only 34.3% occurring also outside of the Patagonian Nothofagetum (Singer, 1971; the Rio Negro campinas, where severa! of Singer & Moser, 1965) permits a comparison these accompany their host tree (e. gr. Aldina during the time of maximal fructification of a hetcrophylla) no further than into the black­ temperate with a neotropical ectotroph-doml­ water igapós or the secondary or destroyed nated forest (CR) . lf the data on the former forests of Amazonia. Only two of these species 2 are sdjusted to equal surface (5m ) the figures are common to CR and TF. Some of the species for total carpophore production and for foli­ are much more closely related to paleotropical icolous fungi are remarkably close in both species than to either temperate or neotropical communities. A lower percentage of carpo­ species, particularly Strobi/omyces pauper (the phorcs in the lignicolous category in the genus Strobilomyces is new for South America, Nothofagus forest corresponds to the generally but is well represented in Africa) . However, lower number of lignicolous fungl in temperate even in the TF there are severa! examples of as compared to tropical forests, an the higher genera restricted to Amazonia and the pa­ number of ectomycorrhizal Basidiomycetes in leotropics (e. g. Podabrel/a}. the Nothofagetum (N. pumilio) is easily ex­ plained by the (a) shorter fructification period DISCUSSION and (b) higher density of the ectotrophically myccrrhizal trees in the Nothofagus pumilio From the results here reported it can be forests. deduced that in test plots I and 11 (TF) the litter decomposíng fungi are much more D. Ectotroph dominance - As pointed out in numerous than in plot 111 (CR) or in Patagonlan lntroduction and above, CR differs basically ectotroph forests. The proportion of litter from TF in that the former, according to defi­ decomposers measured by carpophore nition, is a typical ectotroph forest, the latter numbers on equal surface in TF and CR an anectotrophic forest as had been anticipated respectlvely varies between 1 : 3. 7 and 1 : 4.2.

LlUor docomposltlon ... -35 These figures explain to a large degree the Sinner & Singh, 1971) are ectomycorrhizal, accumulation of litter in CR and in the Pata· with Boletaceae. Russuloceae, Amanitaceae gonian forest and its rapid turnover in TF, but and other ectomycorrhizal fungi present in in order to be generalized our results must be abundance. Consequently, and Janzen makes compared with those obtained on the activities of a point of it, these paleotropical com­ of other litter-decomposing organisms of the munities belong, althrough to different as­ same or comparable forest communities. Dr. sociations. in the group of white-sand or black· H. Lieth has kindly permitted us to quote his vvater forest communities and are eco'logically report (1978) . still unpublished as this is comparable with our campinarana, and igapó, written, on the data obtained by B. Katz with having ali the main characterist ics of thcse litter samples collected by H. lieth in San viz. those indicated in the compárison be­ Carlos, Venezuela at two different localities, tween TF and CR, A. Jazen and some one characterized as groundwater podzol and ather observers are particularly impressed the other as latosol. These may be assumed by the • scleromorphism " or • sclero­ to correspond respectively to CR and TF. Katz phylly" (undoubtedly a useful mechanism of was able to isolate a total of 67 (surface nutrient conservation in the living plant) and lltter), 61 (root zone litter), and 39 (below root abundance of "secondary substances " (poly­ zone litter) Deutromycetes isolates in latosol phenols, alkaloids) in these forest com­ and 12 respectively 8 respectively 8 such mumlies , whcreas mycologists are impressed i sol ates in the podzol zone. As for bacteria, by what we consider the most important yeasts and "Phycomycetes ". the correspond i ng common denominator, viz the fact that ali the figures are 41, 43, 23 in latosol and 33, 44, 48 nutrient-poor white-sand and black-wat er in podzol. Since Katz's mioroorganisms of forests we know are typical ectotroph forests. surface lit:ter + root-zone correspond to the Both these observations - scleromorphism foliicolous fungi counted by us, we find for ali with toxic substances in the litter and ec­ microorganisms observed in these zones tomycorrhiza predominance - have been (Jan· (ages), (and including the two Basidiomycetes, zen, 1974; Singer, 1978b) considered to be, one Ascomycetes and 5 Mycelia sterilia) a to· either one or the other, the main reason for the tal of 220 isolates in latosol and 111 isolates in litter accumulation in CR and similar stands. podzol. This proportion become.s even more Prance et a/. (1976) observed in a 10 x 80 m significant when we compare the Fungi lm­ lot of TF immediately adjacent to our test plot perfecti alone ( 132 vs. 26). i. e. there is a ratio among the 29 tree individuais with 15 em or ot 5 : 1 . These rations correspond very favora­ more diameter, as many as 15 with latex or bly to ours on foiiicolous Higher Fungi (see phenolic substances, i. e. over 50 % . Whatever table 111). and appear to confirm the appli· the corresponding percentage in CR might be, cability of our method as well as the general it is hard to imagine that it might be responsi· value of the resulting data for not merely one ble for a reduction of litter decomposing fungi single group of tungi but for the sum of ali to a quarter of those in TF. There is no proof litter fungi. On the other hand the animal of a negative influence of these secondary communities, especially insects, playing a substances in the litter upon the fungi and positive role in litter decomposition, are ac­ other microorganisms decomposing it and even cording to Janzen (1974) reduced in numbers less so on fungus growth in general ; on the and variety in the tropical nutrient-poor white contrary, the regular and abundant de­ sand soils. velopment of mycorrhizal fungi shows that at Janzen (1974) made many observations in least these - Zygo-and Basidiomycetes - paleotropical white sand forests, particularly are not affected and that many or most litter­ . -dominated "Ones. Although decomposing fungi appear to be perfectly he quotes Brunig and Stark for the trequence adapted to develop and assimilate normally on of "mycorrhizae" in tropical podzols, he does freshly fallen CR litter as well as on living and not seem to be aware that trees of this tamily, dead woody substrata. On the contrary. a pQrticularly Shorea (Bakshi, 1974; Singer, 1971; tannin-rich zone underneath the mantle in the

36- Singcr & Araujo roots of ectomycorrhizal trees seems to be The notion that scleromorphic formations, normal and even characteristic for most short­ admittedly abundant in ectotroph forests, may roots (Bakshi, 1974; Bowen, 1973). Capacity have a decisive influence on the rate of litter to form tannin-rich tissue appears to be a decomposition has obviously arisen from the condition rather than a hidrance for the es­ field and laboratory experiments (Cromack Jr. tablishment of functioning ectotrophs. Thus & Monk, 1975; Oaubenmire & Prusso, 1963; the ultimate cause of the reduced activity of Melin, 1930; Shanks & Olson, 1961) referring· litter decompO'sers in the ectotroph forest is to differences in decomposition rates in vari­ - if secondary substances play any rôle at ali ous species of trees, components of temperate - the selective capacity of certain tree forests in North America. As ide from still species to form ectotrophic mycorrhiza. In unsolved difficulties related to methods and arder to uphold the toxicity hypothesis one techniques it must be remembered that in the would have to believe (and has believed, cf. temperate ectotroph forest different elements Janzen, 1974) that the decomposers can attack may well show different decomposition rates the litter only after it has been leached out but that these data cannot apply to a compari­ and its toxicity correspondlingly reduced. Our son of a tropical anectotrophic with a tropical own observations here reported, and those of ectotroph-forest, both with a much higher others (Lieth, 1978) show that the uppermost diversity of litter origin and litter character­ recently fallen litter is the one richest in istics, with a larger number of presumably observable, active and isolable fungi even adapted forms of litter-decomposing mlcro­ when freshly fallen sclerophyll-leaves have organisms, much longer yearly periods of anti-leAching shingle-like arrangement (Herre­ activity and a sharply differing extent of ra et a!., 1978). Furthermore, if the leaching ectomycorrhizal development. of the litter by rainfall were responsible for An alternativa mechanism, which may well the softening and detoxication of the sub­ be mainly responsible for the reduced litter stratum, and thus the accessibility of the decomposition in the campinarana stands, has material for fungus attack, the number of first been suggested by Harley (1975 and mycelia in the upper, freshest, litter layer 1977) . lt is the on ly one that has been ex­ would be much less drastically reduced during perimentally confirmed (Gadgil & Gadgil, 1971) the period of little or no precipitation in the by showing that in the absence of ectomy­ &nectotrophic forest (terra firme) than in the corrhizal () roots, litter decomposition was ectotroph forest (campinarana) . This is not signiflcantly higher during a 12 months period the case as becomes evident O'n table 111. than in a plot where the roots were left We do not question the statements (Jan­ intact. Harley's hypothesis would attribute zen, 1974) emphasizing the scarcity of assimi­ this to "short cycling" of nutrients, mineral Jable non-toxic nutrition in the black-water and nutrients in the first place (but possibly also white-sand communities when applied to ani­ competition for sources by that minority mais, and particularly arthropods. This seems of ectomycorrhizal fungi which are capable of to be confirmed by recent authors who ob­ utilizing the of the sub­ served a relatively small ( 1 - 2%) leaf are a stratum), thus depriving the entire population consumed by insects (Herrera et a!., 1978). of the saprophytic fungi living in soil and litter lt is not quite clear whether the many insects of an essential part of the available N and P feeding. on fungus mycelium and carpophores compounds. reduce or increase (by dissemination) In the lower layer of the litter another the overall litter decomposition by fungi, and factor may also to a variable degree be re­ whether litter reduction by animais (wlth sponsible for the smaller number of saprophy­ smaller communíties and, it seems. smaller tes. The exudates originating from ectotrophl­ average size of individuais) as a whole ls a cally mycorrhizal fungi and/or from other lesser factor in the ectotroph forests than in fungous elements of the frequently the anectotrophic forests of Central Amazonia include antibiotics which may selectively influ­ (cf. Fittkau & Klinge, 1973; Schubart, 1977). ence the populatlons of soil microorganlsms

Litter dccOm!Josition ... -37 far beyond the rhizosphere proper although endomycorrhiz3 are quantitatively equally they will hardly affect the microflora of the represented in campinarana and terra firme most recent litter layer above the root levei. forestsl their impactl although certainly sig­ nificant for the physiology of the individual Whatever the quantitatively most important tree associated with it (cf. i. a. Daft & mechanism of limiting the activity of saprophy­ Hacskaylol 1977). cannot be more than ac­ tes in the campinarana may bel it is obvious cessory on soil and litter of the ectotroph that it is basically the dominance of the fcrest when compared with the impact of ec­ ectotroph that is required for its functioning. tomycorrhiza. The biomass and enormous Consequently I we assume the causal sequence extension (cf. Burgess & Nicholasl 1961; of the phenomenon to be as follows: Oligo­ Trappe & Fogel, 1977) of the mycelial hyphae trophyl leading to ectotroph dominancel leading ectomycorrhizae cannot be matched by VA to raw humus accumulation. mycorrhizael while is too A recent study (Herrera et a/. , 1978) using habitat-restricted to greatly influence the soil clippings of fresh leaves superimposed on and litter formation. Unfortunatelyl not only in growing rootlets demonstrates transference of the tropicsl but also in tempcrate regionsl P from the leaves to the rootlets in Jaboratory there é!re few data permitting a quantitativa comparison of extension and biomass of these conditions. The authorsl unfortunately I do not identify the type of the forest community or the three types of mycorrhizae. Those - perhaps fungus but its origin in the Upper Rio Negro not fully representativa - estimates availablc to us suggest a ratio of over a million to onc region and the dominance of Epcrua leucantha 1 the description of the soil as oligotrophic and in terms of ectomycorrhizal sclerotia versus the fungus mycelium as septate make it VA-sporocarps in tempcrate forests (Gõbll virtually certain that the phenomenon de­ 1965; Kessler & Blankl 1972; Trappe & Fogell scribed refers to an ectotrophically mycorrhizal 1977). fungus in an ectotroph forest of the igapó or The influence of -fixing bacteria campinarana type. At any rate we h ave ex­ has still to be determined. Considering the perimental evidence of direct cycling of P. importance of leguminosous trees in neo­ This would be exceptional in the latosol terra communities, one would obvi­ firme forest where mineral nutrient absorption ously wish to supplement mycorrhiza studies by the feeder roots seems to be basically with quantitativa, comparativa studies on sufficient for nutrient conservation in a virtu­ nitrogen fixing systems in campinarana and ally closed cycling systeml but it isl on the terra firme vegetation. But nodules are practi­ basis of our observations of identified ec­ cally absent in TF (Rosemary S. Bradley, tomycorrhizal partnersl characteristic for the personal communication) . Ncither Singer Amazonian ectotroph forests. (1978b) nor Herrera et ai. (1978, 1978a) have We are not in a position to introduce a missed the significance of their respectiva comparativa study on the relativa importance data with regard to the detcrioration of tropical of endotrophic mycorrhizae in the forest and soils when the primary forest communities under consideration. Orchid my­ is partially or totally destroyed (cf. Schubart, corrhizae (Basidiomycetes) do occur in both 1977). Once we understand thc decisiva rôle TF and CR. So do VA mycorrhizae according of ectomycorrhiza in the poor white-sand soils, to data kindly supplied by Dr. T. St-John in we cannot but wonder whether introduction of both campinarana and terra firme forest ectotrophs previous to forest removal will not although the dominant tree species in the test permit the format~on of a deep raw humus area TF are either devoid of them or have them layer even in the latosol forest and thus lend only sporadically (personal communicationl a higher degree of stability to the soils after and communicéltion at the Second North Amerl­ cutting by increasing resistence to the develop­ can Mycorrhiza Conference Athensl August ment of an unfavorable soil microflora and 1977) . Even assuming that both types of erosion.

38- Singer & Araujo CRITIC within the substratum rather than the precipi­ tation even if a six day period previous to the In the hands of specialists, our relatively counting date is considered. Furthermore, the simple methods produce fairly constant, relia­ respective species were not restricted to the ble results, matching other available quanti­ primary latosol terra firme forest but occurred tativa data which seem to be consistent with likewise in other communities, i. e. forming accepted theory. They reveal however no part of the chRracteristic dead-wood mycoflora· consistent behavior in the phenology of which appears after falling and persists in the lignicolous Agélricales, terricolous basidioli­ secondary forest, joining there such charac­ chens and fungi decomposing monocatyledo­ teristic species as Schizophyllum comune, nous litter and give no clue as to the conditions Pycnoporus sanguineus, Pleurotus hirtus, Panus necessary for their develapment insofar as it crinitus, P. rudis, P. badius, some species of appears different from that of the foliicolous Gymnopilus and Marasmiellus. On the other fungi. In the case of the monocot litter, the hand, species growing on small fragments of reason may perhaps be the relatively smaller dead woody matter mixed into the litter had amount of litter derived from Monocotyledones fewer carpophores per species at a given time and a different leaf shedding rhythm of these and showed a fruiting pattern similar to that . The behavior of the Basidiolichens on of the other litter fungi. In future assays, it our plots is erratic because we have here a should probably be decided to either exclude different and largely self-contained association the trunk-and iog-inhabiting fungi altogether, which requires a separata study. What is or, if their particular rôle and fruiting pattern remarkable in this case is that they appear to is considered essential for the study, they be linked with a special habitat - raised or should be separnted into a special category. denuded (by vertebrate activity ?) mineral soil lt is difficult to decide just where the limit of - and that they appear in large quantities but s:.~bstratum volume should be set; this limit erratically during certain periods of the rainy miaht be at the point where substratum size season. While their appearence is most begins to be little influenced by externai noticc?.ble in one restricted locality, they are humidity, i.e. does not dry out or become totally absent in similar in other wetted thoroughly at the same rate as the rest localities where they have been observed o f the lltter. before. The limited time necessary for their development suggests the possibility that there ACKNOWLEDGMENTS might be some insufficiently explored phe­ nomenon at hand which we may call micro­ The authors wish to thank ali colleagues migrction. and co-workers at INPA who have helped Another problem, more important for the collecting fungi, identifying plants, discussing present study, is that of the lignicolous group various aspects of our problems and critically of fungi. In test area I, we have counted in the reaàing the manuscript. Our gratitude is also same (lignicolous) category, ali Agaricales due to the Director of INPA, Dr. W. E. Kerr, growing on dead wood, including those ap­ Dr. H. Si ali, Dr. A. E. Schultes of Harvard pearing on one rotting tree trunk (Eschwei/era) University and Dr. F. Ehrendorfer, of the crossing part of the test plot (no such trunks Botanical lnstitute of the University Vienna · were pr.esent on test areas 11 and 111) . Ali the Austria for stimulating discussions and en­ high counts of lignicolous fungi in test area I couragement, and to Dr. C. Bas for identl· were due to mass fructifications on the fication of the Amanitaceae. Eschweilera trunk. Here, the various mycelia at work are more extensiva, apparently Resumo compatible with each other within the sub­ stratum but with a specific, limited fruiting A aplicação de um método micossociológico periodicity which depends on the degree and (adaptação do método de Lange) na Amazônia Cen­ duration af availability of a water surplus tral produziu os seguintes resultados: Na. camptna-

Litter decomposition ... -39 rana, tipo de floresta sobre podzol de areia branca, BOWI!N, G.D. as árvores dominantes são, obrtgatonamente, ecto· 1973 - Mineral nutrition of P-ctomycorrhizae in troficamente micorrizais; a liteira é acumulada co­ G.C. Marks & T.T. Kozlowski (eds), mo humus em conseqüência àa dominância de Ectomycorrhlzae, Academic Press, New ectótro!os; tanto na estação seca bem como na York (p. 151-205). úmida, o número de !olhas habitadas por fungos da BURGI!SS, A. & NICHOLAS, D .F. liteira é menor do que o número encontrado na 1961 - The use of soil sections in studying the floresta úmida de terra firme sobre latossol e os amount of fungai hyphae in soil. Soil fungos dessa categoria são aqui, mais fortemente Sei., 92 : 25-29. representados ("F-dominância") por outras espé­ cies do que nas áreas testadas de terra firme. As C~tOMACK JR., K. & MONK, C.D. 1975 - Litter production, decomposition, and árvores ectomicorrizais e fungos são enumerados. nutrient cycling in a mixed. hardwood Por outro lado, na floresta de terra firme, não ocor­ reram fungos ectotroficamente micorrizais nas áreas watershed :md a White Pine watershed in F. G. Howell; J. B. Gentry & M. H. testadas. Na floresta primária de terra firme, qua.. Smilh (eds) ERDA Symposium series se todas as árvores não são ectomicorrizais; a li· teira não é apreciavelmente acumulada como uma (p. 609·624). camada profunda de humus porque o considerável DAFT, M .J. & HACSK.AYLO, E. número de fungos habitantes das folhas da liteira 1977 - Growth of endomycorrhizal and non­ (relação de 4:1 a 4.2:1 em favor da terra firme) e mycorrhizal Red M;::ple seedlings in a grande diversidade (um grande número de espé­ sand and anthracite ~poil. Forest Sei., cies) permitem que a decomposição seja, potencial­ 23: 207-216. mente, maior do que a quantidade de !olhas que DAUUENMIIU:., R. & PRUSSO, D.C. cai anualmente. Neste estudo, um grupo de fungos 1963 - Studies o! the decomposition rate or que não é representado em experimentos de decom­ tree litter. , 44 : 589·5!>2 . posição da liteira em laboratório. !oi principalmen­ FrrrKAu, E.J. & KLINGE, H. te enfocado. Contudo, uma comparação com dados 1973 - On biomass and trophic structure or publicados e não publicados mostra que os nossos the Central Amazonian . Bio. resultados igualaram satisfatoriamente os dados tropica, 5: 2-14. obtidos com outras classes de microrganismos e observações em outras regiões. No grupo !olícola, a GAOOIL, R.L. & GADGIL, G.D. quantidade de fungos decompositores da liteira de­ 1971 - Mycorrhiza and litter decomposition. pende, principalmente, da precipitação durante os Nature, 233: 133. dias anteriores à contagem. Isto não é válido para GouL, F. todos os fungos lignfcolas. As razões para isso, bem 1965 - Mykorrhizauntersuchungen in eincm como o mecanismo pelo qual os fungos ectomicor­ subalpinen Fichtenwald. Mitt. Forstl. rizais podem reduzir a taxa de decomposição da Bundcsversuchsanstalt Mariabrunn 66 : liteira e influenciar os padrões dos ciclos de nu­ 173-195. trientes, são discutidos. Os mrus importantes gê­ HARLEY, J.L. neros de Basidiomycetes envolvidos na decomposi­ 1975 - Problems oí mycotrophy in Sanders, ção da litcira nas associações florestais do baixo F.E.T., B. Mosse & P.B.H. Tinker, rio Negro são enumerados. A possível significação Endomycorrhizae. Lc:ndon 1975, (p. econômica de introdução de ectótro!os na floresta 1-5). de terra firme é indicada. 1977 - Banquet address, Thírd North Ameri­ can Con!erence on Mycorrhizae (distri­ buted by D. H. Marx, 1978). LlTERATURE HEAAERA, R.; JORDAN, C.F.; KLlNoé, H. & MloDlNA, E. ANDERSON, A.B. 1978 - Amazon ecosystems, their structure and functioning with particular emphasis on 1978 - Aspectos floristicos P fitogeográficos de campinas e campinaranas na Amazônia nutricnts. Interciencia, 3 : 223-231. Central. Thesis. HERRERA, R.; MERIDA, T.; STARK, N. & JoRDAN, C.F. ANDERSON, A.B.; PAANCE, G.T. & ALBUQUERQUE, B.W. DE 1978a-Direct transfer from leaf 1975 - Estudos sobre a. vegetação das Campi­ litter to roots. Naturwissenschaften, 65: nas Amazônicas. IH Acta A.Inallonica, 208. 5(3) : 225-246. J ANZEN, D.H. BAKsHr, B. K. 1974 - Tropical blackwater rívers, anima1s and 1974 - Mycorrhiza. and its role in , p. mast fruiting by Dipterocarpaceae. Bio. 1-89. Dehra Dun. tropica, 6 : 69-103.

40- Singer & Araujo Kt:SSLER, K.J. & BLANX, R.W. SINOER, R. 1972 - sporocarps associated with 1963 - Der Ektotroph, seine Deflnition, geogra.. sugar ma.ple. Mycologla, 64 : 634-638. phische Verbreltung und Bedeutung in der ForsWkologie in Mycocrrhlza, I<.REJSEL, H. Internationales Mykorrhizasymposium 1971 - Biologische Rundschau. 9 : 97. Weimar, 1960, p. 223-231. LANOE, M. 1964 - Areal und ôkologie des Ektotrophs in 1948 - The Agarlcs of Maglemose. Dansk Bot SUdamerlka. Zeltschr f. Pllk., 30 : 8-14. Ark. 13 . 1971 - Forest mycology and forest communities in South America II in E. Hacskaylo LIETB, H.H. (ed) Mycorrhizae. Us Governrnent 1978 - Interim report for travei grant NSF Printing Offlce Washington (p. 204-215). (unpublished, recleved 1978). 1978a-Notes on Bolete taxonomy II. Persoonia, l!SBÔA, p . L . 9:421438. 1975 - Estudos sobre a vegetação das campi­ 1978b- Origins of the deficiency of Amazonian nas amazônicas. II. Ac ta Amazonica, soils - a new approach. Ac ta Amazotú­ 5(3) : 211-223. ca, 8(2).

LUNDEBERO, G. STNOI!R, R. & MORI!LLO, J. H. 1970 - Utilization of variou::; nitrogen sources, 1960 - Ectotrophic tree mycorrhiza and forcst in particular bound soil nitrogen, by communities. Ecology, 41 : 549·551. mycorrhlzal !ungi. f-tudla Florestalia SINoER, R. & Mosn, M . Sueciaca, 79 : 1-95. 1965 - Forest Mycology and forest communities MELJN, E. in South America.. Mycopathologia et 1930 - Biological decomposition of some types Mycologi.a Applicata., 26 : 129-191 . of litter from Americ~n forests. Ecology, SINOER, R. & SINGH, B. 11 : 72-101. 1971 - Two new ectotroph-forming boletes. MEYER, F .H. Mycopathologia et 1\'t.ycologia Appllcata, 1973 - Dintribution of eetomycorrhiza.e in 43: 25-33. native and manmadc forests in G.C. SMrrH, A.H. Marks & T.T. Kozlowski (eds), Ectomy­ 1947 - North American Spec:es of Mycena. Ánn corrhlzae. Academic Press, New York Arbor, Mich. (p. 79·105). TRAPPE, J.M. & FOGEL, R.D. MosER, M. 1977 - Ecosystematic functions o! mycon·hlzae 1959 - Piiz und Ba.um. SchwE'iz. Zeitschr. Piizk. in Forest Service USDA, A synthesis o! 37: 52. plant-associated processes, Range Sei. P'RA.Nce, G . T. Dep. Sei. Ser. 26, Colorado State 1975 - Estudos sobre a. vegetação das campi­ University, Fort Collins (p. 205-214). nas amazônicas. I . Ac ta Amazonica, WATLINO, R. 5(3) : 207-209. 1977 - An analysis of the taxonomic characters PRA.NcE, G.T.; ROoRtoues, W.A. & SILVA, M.F. DA used in defining the species of the in H. Clemençon (ed.). The 19'!6 - Inventário florestal de um hectare de species concept in Hymenomycetes. J . terra firme km 30 da Estrada Ma.naus­ Cramer, Vaduz (p. 11-53, espccially p . Itacoatiara. Acta Arnazonlca, 6(1) : 9-35. 49-50). SctruBART, H.O.R. WENT, F.W. & STARJC, N. 1977 - Critérios ecológicos para o desenvolvi· 1968 - Mycorrhiza. Bio-Sci., 18: 1035-1039. menta agrlcola das terras firmes da Amazônia. Acta Arnazonica, 7(4) : 559-567.

StiANKS, R.E. & ÜLSON, J.S. 1961 - First year breakdown of leaf litter from North American forests. Ecology, 11: 72-101. (Aceito para pub!lcação em 31110/ 78)

IJtter decomposltlon ... -41