Restoring Tropical Forests on Lands Mined for Bauxite: Examples from the Brazilian Amazon

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Ecological Engineering 17 (2001) 219–239 www.elsevier.com/locate/ecoleng

Restoring tropical forests on lands mined for bauxite: Examples from the Brazilian Amazon

John A. Parrotta a,*, Oliver H. Knowles b

a International Institute of Tropical Forestry, USDA Forest Ser6ice, P.O. Box 25000, Rı´o Piedras, PR 00928-5000, USA b C.P. 15, Santare´m, 68005.970 Para´, Brazil

Accepted 19 August 2000

Abstract

Restoring self-sustaining tropical forest ecosystems on surface mined sites is a formidable challenge that requires the integration of proven reclamation techniques and reforestation strategies appropriate to specific site conditions, including landscape biodiversity patterns. Restorationists working in most tropical settings are usually hampered by lack of basic information on the wide variety of native tree species that characterize the pre-disturbance forests, as well as insufficient understanding of the ecology of disturbance and natural recovery to design effective restoration programs. A notable exception to this is the forest restoration program developed since the early 1980s by a Brazilian bauxite mining company operating at Trombetas in Para´ State in central Amazonia. A systematic nursery and field research strategy was used to develop a reforestation program based on mixed plantings of more than 70 native old-growth forest tree species. This technique has been used to replant about 100 ha of deforested minelands each year over the past 15 years. Research in recent years has evaluated this approach and other, generally simpler, reforestation methods used at a smaller scale at this site. Post-plantation biodiversity development and other indicators of restoration success or sustainability were recorded. The results of these studies have shown the overwhelming importance of careful site preparation and topsoil handling/replacement practices in determining both future productivity and biodiversity of the redeveloping forests, irrespective of the complexity of the planting design used. The inclusion of a wide variety of forest species, particularly later successional species, was very important for long-range restoration owing to limitations on natural recovery processes that inhibit seed dispersal and subsequent colonization of many old-growth forest species. Many of the lessons learned at this site are applicable to improve the design of mineland rehabilitation and forest restoration programs worldwide. © 2001 Elsevier Science B.V. All rights reserved.

Keywords: Bauxite mine rehabilitation; Brazil; Natural regeneration; Plantations; Restoration; Soil seed bank; Succession; Tree life spans; Tropical forests

1. Introduction

* Corresponding author. Tel.: +1-787-7665335; Fax: +1- Surface mining in most tropical countries di- 787-7666263. E-mail address: [email protected] (J.A. Parrotta). rectly affects relatively small areas of forest com-

0925-8574/01/$ - see front matter © 2001 Elsevier Science B.V. All rights reserved. PII: S0925-8574(00)00141-5 220 J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 pared with forest cleared for agriculture, log- ing the forest cover destroyed at a rate of ging, hydroelectric and transportation projects approximately 100 ha year−1 during bauxite ore and other changes in land use. However, the extraction at Trombetas in western Para´ State off-site environmental impacts of surface mining (Knowles and Parrotta, 1995). The MRN mixed can be very extensive, due to erosion and runoff native species reforestation approach, involving resulting in siltation and deterioration of water careful site preparation (including topsoil re- quality in nearby rivers, lakes and reservoirs. To placement) and planting mixed stands of 80–100 avoid these adverse environmental impacts, ef- species of native forest species at a total cost of fective forest restoration on mined sites is re- approximately $2500 ha−1, has been the stan- quired. This requires careful planning and the dard reforestation technique used at the Trom- integration of mining and rehabilitation opera- betas mine since the mid-1980s. This more tions based on sound silvicultural and ecological sophisticated reforestation approach involving knowledge and principles (Bradshaw, 1987, mixed native species plantings has become the 1997). Proper site preparation, including mine- industry norm in response to Brazilian environ- site landscaping, topsoil handling and applica- mental legislation that now requires companies tion, and deep-ripping of compacted subsoil, has to restore, to the greatest extent feasible, the been shown to be an essential prerequisite for original vegetation destroyed during mining. good growth of planted tree species and vigor- At the Trombetas mine site, a number of re- ous natural regeneration of species from viable forestation methods, in addition to the standard seeds contained in forest topsoil (Tacey, 1979; mixed native species planting technique, were Tacey and Glossop, 1980; Fox, 1984; Ferraz, tested on a smaller scale during the 1980s. These 1993; Grant et al., 1996; Parrotta et al., 1997). included establishment of mixed species planta- In addition, silvicultural knowledge is required tions by direct seeding using mainly short-lived, to select species and establishment techniques native early successional trees, and mixed plant- appropriate to local site conditions and long- ings of mostly exotic species. Also present at range restoration objectives. In many tropical this site are small areas where: (1) the standard regions, including the Amazon basin, restora- mixed native species treatments were applied tionists lack basic, essential information on seed availability, propagation techniques, growth but, due to operational failures (inadequate top- rates and site adaptability for the hundreds of soil application), subsequent tree growth was candidate tree species present in natural forests greatly reduced; and (2) site preparation and (Knowles and Parrotta, 1995). topsoil replacement protocols were followed, but Forest restoration programs by mining com- where trees were not planted. The presence of panies in Brazil (Majer, 1992, 1996; Gaunt and these developing forest stands of similar age (9– Bliss, 1993; Knowles and Parrotta, 1995 ), Aus- 13 years) established using different methods, or tralia (Tacey, 1979) and other tropical countries treatments, provided a unique opportunity to have usually relied on planting of either native evaluate their relative value for forest restora- or exotic forest species to rapidly establish tree tion. Studies were therefore undertaken to com- cover on reclaimed mine sites and thereby facili- pare the structure, floristic composition, tate natural forest succession. In Brazil, prior to successional status and sustainability of these the early 1980s, bauxite mine rehabilitation pro- treatments with reference to the old-growth grams involved reforestation with fast-growing, forests surrounding the mine site. In this paper, exotic and native species such as Eucalyptus we will summarize the major results of these spp., Bracatinga scabrella and Australian Acacia studies, in the hope that they will be of use in spp. mine restoration programs elsewhere in the trop- Since 1979, the Brazilian mining company ics. Further details of these studies can be found Mineraçaõ Rio do Norte S.A. (MRN) has de- in Parrotta et al. (1997), Parrotta and Knowles veloped a reforestation program aimed at restor- (1999). J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 221

2. Methods large terrestrial and arboreal mammals, bats and birds that play critical roles in forest succession. 2.1. Study location 2.2. Nati6e forest species propagation and The Trombetas bauxite mine is located in the performance assessment Saraca´-Taquera National Forest on an upland mesa (Saraca´ plateau) at an elevation of 180 m, 65 During the 1980s, 160 species of trees (from 42 km northwest of the town of Oriximina´and30 families) found in the old-growth forests sur- km south of the Trombetas River in western Para´ rounding the mine site were systematically evalu- State, Brazil (1°40%S, 56°27%W; Fig. 1). Mean an- ated to determine the most cost-effective methods nual rainfall at Porto Trombetas (1970–1994) is for their propagation and to assess their early 2185964 (S.E.) mm, with distinctly dry (winter) performance after planting at the mine site. This and wet (summer) seasons; mean monthly rainfall research program, described in detail in Knowles exceeds 100 mm in all months except July–Octo- and Parrotta (1995), involved evaluations of fruit- ber. The mean maximum and minimum tempera- ing phenology, seed viability, seed germination tures are, respectively, 34.6 and 19.9°C. Soils on treatments, propagation methods (direct seeding, the Saraca´ plateau are acidic yellow clay latosols use of stumped saplings, wildlings, and nursery- with a thin humus layer (Ferraz, 1993). The re- grown seedlings), and early survival and growth gional vegetation is evergreen equatorial moist during the ﬁrst 2 years after outplanting under forest, within which the forests occupying the operational conditions. upland mesas and surrounding slopes have average canopy heights of 20–35 m, with emergent 2.3. Reforestation treatments trees up to 45 m tall (Knowles and Parrotta, 1995, 1997). The forests surrounding the mine were, The study areas were located on the eastern until recently, largely inaccessible and undisturbed side of the Saraca´ plateau on sites mined between by hunting or forest clearing for the past 200–300 1982 and 1986, and next to undisturbed old- years. Consequently, wildlife diversity in the vicin- growth forest. For all treatments described in ity of the mine remains high and includes the Table 1 (with the exception of the mixed native species ‘failure’), the standard reclamation and site preparation sequence was followed, which includes leveling of the clay overburden, replacement of approximately 15 cm of topsoil and woody debris (removed from the site prior to mining and stockpiled for up to 6 months prior to application), deep-ripping of lines to a depth of 90 cm (1 m between lines), and planting along alter- nate rip lines at 2×2 m spacing (2500 trees ha−1) using seeds, stumped saplings and/or potted seedlings, depending on species and treatment.

2.4. Forest stand structure and ﬂoristics

Between 1995 and 1997, stand structure, ﬂoris- tic composition, and forest ﬂoor development were evaluated for all treatments and in old- growth forests on the Saraca´ plateau using repli- cated 10-m diameter circular plots (78.5 m2)asthe Fig. 1. Location of the study site. standard measuring unit. Due to stand area dif- 222 J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239

Table 1 Reforestation treatments studied at the Trombetas bauxite-mined site

Treatment Description Total Area Year established

Mixed native Mixed species plantings of ca. 70 native forest tree 100 ha 1985 species species of different successional stages (MNS) Mixed native As MNS, but poor survival (B25%) of planted treesSmall areas (B0.1 ha) in MNS 1985 speciesapparently due to inadequate site preparation, specifically treatment ‘failure’ insufficient topsoil application Mixed Mixed species plantings of Eucalyptus camaldulensis,2.0 ha 1987 commercial Eucalyptus citriodora, Eucalyptus pellita, Eucalyptus species torreliana, Eucalyptus urophylla, Acacia mangium and Sclerolobium paniculatum. Direct seedingMixed species plantings of 48 mainly short-lived native 17 ha 1986 forest taxa; mowed at 40 cm height to stimulate sprouting in 1987 Natural Regeneration initiated from seeds in applied topsoil Four sites, 0.3–1.0 ha each 1984–1987 regeneration ferences among treatments, the total sampling plot were recorded separately. Woody species area varied among treatments. Study plots were were also classified by their expected longevity, or located randomly within the study sites in the life span (B20, 20–40, 40–80, or \80 years), natural regeneration, mixed commercial species, based on Knowles’ long-term observations of the and mixed native species ‘failure’ treatments. In local tree flora, and their regeneration origin, i.e. the remaining two treatments (mixed native spe- whether they were planted or naturally regener- cies, direct seeding), these plots were established ated from either the applied soil seed bank or at varying distances from the intact old-growth subsequent inputs from surrounding natural forest along the edge of the plateau towards the forests. Canopy closure was estimated as the interior of the Saraca´ plateau, with plot centers at mean percentage crown cover measured with a 0, 10, 20, 40, 100, 250, 500 and 725 m along two spherical crown densiometer at 1 m from ground transects in the direct seeding stands and at 0, 10, level at four points located 3 m from plot centers 20, 40, 80, 160, 320 and 640 m along each of four (N, S, E, and W compass bearings). Litter and transects in the mixed native species stands. Old- humus depths were measured at ten randomly growth forest plots were located along two 100 m located points within each plot, with plot means transects in undisturbed forest areas in the general for each horizon used for subsequent analyses. vicinity of the restoration areas on the eastern side of the Saraca´ plateau, approximately 50 m from 2.5. Data analysis the plateau edge. Within each of the 78.5 m2 sample plots, a Numbers or individuals per square meter and complete inventory was made of all adult and basal area (for trees ]2 m tall) were calculated juvenile trees and shrubs, vines, herbs, and for all species in each treatment. Species richness grasses. For each of these floristic categories, the for each floristic category was expressed simply as total numbers of individuals (or clumps, for the number of species present per plot. Based on grasses) of each species were recorded. For trees the total plant species list for all plots in each and shrubs (including palms), height and stem treatment, Sorensen’s quotient of similarity (I) diameters (at 1.3 m=dbh) for trees ]2min was calculated for the tree flora to assess the height were also measured. Height and stem di- degree of similarity between restoration treat- ameter data for planted trees occurring in each ments and the old-growth forest. Mean canopy J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 223 closure, canopy height, tree basal area, litter and Evaluations of post-plantation adaptability and humus depth, plant density, and species richness early growth found that 37% of the 160 tree for woody species, vines, herbs and grasses were species studied were well adapted to the open site compared among treatments using unpaired two- conditions of the reforestation site, showing vigor- group t-tests. ous shoot growth and survival rates of ]75% during the first 2 years after planting. An additional 30 species (19%) were rated as ‘fair’, with 3. Results and discussion good shoot growth and survival rates of 50–75%; 3.1. Tree species propagation and performance these species prefer partial shading during the first year after planting, but grow vigorously under full The propagation methods tested by MRN for sun thereafter. The remaining 71 species (44%) 160 native tree species at the reclaimed mine site performed poorly during the first 2 years, with were, in order of increasing cost: direct seeding, survival rates B50% and stagnant shoot growth; planting of stumped saplings (i.e. saplings col- species in this group generally require shade, at lected from the wild whose tops and all but least during the first 2 years of their development, taproots are removed), wild seedlings, and nurs- and are recommended for enrichment plantings ery-grown seedlings. It was found that direct seed- beneath the closed canopy of plantations estab- ing was suitable (with survival rates ]75%) for lished using the better-adapted species, preferably 21% of the species studied; these species generally about 5 years after the initial plantings. Further had large seeds (\2 cm long and broad) that details on tree species propagation and early per- could be conveniently handled by planters in the formance after planting are provided in Knowles field. For an additional 13 species (8%), stumped and Parrotta (1995). saplings were the most economical and viable option. Of the remaining 113 tree species, 3.2. Influence of site preparation on forest wildlings collected from the surrounding old- de6elopment growth forests was the most cost-effective planting stock option for 78 species (49%), while only The importance of careful site preparation, par- 35 species, or 22% of the total, could not be ticularly topsoil handling, is evident when one propagated by these more economical means and compares the structural and floristic development required raising seedlings from seed in the 10 years after planting in sites at the Trombetas nursery. mine, where the mixed native species treatment The seeds of many tropical tree species require was applied with and without adequate topsoil mechanical or chemical scarification to speed their application during the site preparation phase. As germination. Pre-sowing treatments can, however, shown in Table 2, tree basal area, canopy height add significantly to the cost of nursery produc- and crown cover percentages were significantly tion. On an operational scale such as that prac- lower in the mixed native species treatment plots ticed by MRN at Trombetas, it is important to with inadequate topsoil application (MNS ‘fail- determine the least expensive methods for seed ure’) than in plots in which the prescribed site handling to minimize these expenses. Of the 160 preparation protocols were followed. In the for- native Amazonian tree species studied, however, mer plots, rates of litter accumulation and humus 71% were found to not require either method of development were relatively poor. Although the scarification to break seed dormancy. Twenty-one overall density of woody species in these areas percent required mechanical scarification and only was not significantly lower, individuals \2 m tall 7% required chemical scarification (soaking in were relatively uncommon. concentrated H2SO4). These findings were used to There were clear differences in the floristic rich- develop cost-effective strategies for planting stock ness of these sites, the MNS ‘failure’ plots having selection and, for nursery-grown seedlings, seed significantly fewer (approximately 50%) planted handling protocols. and naturally regenerated tree and shrub species 224 J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 tand C CD CD CD B B CD B B CD A AB D B D C 1.55 0 1.55 1.19 0.36 0.43 0.025 0 0.40 9–13 6.3 0.52 63.5 19.6 46.0 23.1 23.1 16.0 11.4 11.7 a te 1983–1987 regeneration -test). t 0.05, B P B A B B A A BC B CD B DE B AB B A B B C 0.50 6.9 0.52 3.04 2.93 0.54 1.14 0.18 3.47 0.82 1653.2 12 11.6 10.4 16.8 35.4 28.6 31.6 11.6 32.7 Direct seeding Natural D B D D B B B A BC A B A B E B C E C 8 0.16 5.7 1.32 0.15 1.04 0.28 0.34 1.16 1.18 9.8 1.17 5.5 59.8 17.4 24.9 42.7 12.3 17.5 11.4 628 1256 942 species BC C BC B C B A E C F C C E B C DE D 6 4.5 1.5 2.85 0.05 2.80 0.13 0.24 2.74 0 4.2 6.5 27.8 14.0 15.5 11.8 13.3 C BC B BC BC B B D CD B E B AB C A B C B 8.3 3.06 0.18 2.88 2.66 0.40 0.40 8.8 0.51 0.22 32 56.1 10.6 13.9 32.4 28.5 23.7 21.2 10 10 9 10 Mixed nativespecies (insufficient topsoil) Mixed commercial A A A B B E B A A A B A A A A A 5.47 0 5.47 5.04 0.43 0.48 0.17 0.36 0 ? 1985 1985 1987 1986 75.7 21.6 76.5 29.4 13.3 67.3 67.3 59.8 21.5 628 2512 471 ) 200? 2 d − \ Old-growth (‘primary’) forest ) ) I ( plot / ) 1 iduals m 6 − species 2 m tall2 m tall 2 m tall 2 m tall 2.75 14.6 ha ) . b 2 n B \ B \ no

) ( 2 s Index of Similarity number of indi ’ ( c. c treatment ( / Calculated as the mean of plot averagesComparisons for with the surrounding five old-growth tallest trees forest. per See plot. Table 4 for list of tree and shrub species surveyed. A complete plant lists from old-growth fores Similar superscript letters (A, B, C, D, E) within a row indicate that means were not significantly different between treatments ( ‘Other’ species include those regenerating from the seed bank in applied soil or arising from seed inputs from surrounding old-growth forests. plots Planted Other Woody species, Woody species, Planted Other Woody species, Woody species, a b c d Number of sample 8 Species richness Woody species (all) 1.00 restoration treatments is available from the authors. Years since establishment Sample area (m Year established Table 2 Structural characteristics and tree species diversity inTreatment 9–13 year old reforestation plots and old-growth forest at the Trombetas bauxite-mined si Crown cover (%) Canopy height (m) Tree basal area (m Litter depth (mm) Humus depth (mm)Density Woody species (all) Vines GrassesHerbs MNS ‘failure’ Woody species (all) Sorensen 1.1 0.40 0.019 J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 225 in both the seedling (B2 m tall) and larger (\2 seed sizes between tree species regenerating in the m tall) size classes. As a result of poor perfor- reforestation area and those found in the old- mance of planted trees, the MNS ‘failure’ plots growth forest (Fig. 3) indicates that, while the tended to be dominated by persistent fire-prone smaller-seeded tree flora are already well repre- grasses and a very limited number of short-lived sented in the reforestation area, larger-seeded spe- early secondary forest species that can survive cies are less well represented. These include under such conditions. members of the most important tree families (in terms of dominance and ecological function) in 3.3. The role of landscape floristics and wildlife in the old-growth forest, i.e. Annonaceae, restoration processes Chrysobalanaceae, Lauraceae, Palmae and Sa- potaceae. Tree species from these families also In all of the plantation treatments studied, the tended to perform very poorly when planted un- total number of tree and shrub species present in der open conditions at this site (Knowles and study plots greatly exceeded the number of Parrotta, 1995). planted species. Regeneration from seeds in the applied topsoil and that resulting from seed inputs from nearby old-growth forest stands comprised between 70 and 83% of the total tree species richness, and 88–98% of the total numbers of seedlings and larger individuals in the study plots (Tables 2 and 4). Based on the authors’ knowledge of the seed viability, it was estimated that approximately 40% of the tree species regenerating in the study plots could have survived in the soil seed bank during the 6- to 12-month period between topsoil stockpiling and reapplication to the reforestation areas. The remainder of these species, up to 75 in the mixed native species treatment, were considered to be the result of post-plantation seed inputs, facilitated mainly by the birds, bats and terrestrial mammals that are the primary agents of seed dispersal in the upland forests of this region (Knowles and Parrotta, 1997; Parrotta et al. 1997). Tree species whose seeds are dispersed by wildlife were significantly more abundant in study plots located closer to the undisturbed forests surrounding the mine site than in those further from the old-growth forest edge. Although there was abundant colonization by woody forest species up to 640 m away from the old-growth forest edge in the mixed native species treatment, the density and diversity of colonizing species was Fig. 2. Relation between understory regeneration of woody inversely correlated with distance into the refor- old-growth forest colonists and distance from old-growth (‘pri- estation area (Fig. 2). mary’) forest in 10-year-old mixed native species plots at Trombetas bauxite mined site. (a) Plot distance from old- These results suggest that seed dispersal may be 2 B growth forest, y=0.69−0.24 log10 x (r =0.33, F=17.6; P limiting the process of tree flora enrichment 0.001). (b) Plot distance from old-growth forest, 2 B within the reforestation area. A comparison of y=18.8−4.96 log10 x (r =0.54, F=41.6, P 0.001). 226 J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 Tree longevity a vector class ?2 FaunaFauna 1 FaunaFauna 2 1 1 Fauna 2 WindFaunaFauna 4 2 1 XWind4 X Fauna 1 X Fauna 2 X XPWind4 X Wind Fauna 2 2 P X Wind 3 X X X X X X 3456 X PX P PX X X X PX P X P X P P X 12 X XPX X X XP X X X XPX XX XX X ´ preta ´ vermelho X ´ X Fauna 2 ´ P X Fauna 2 ´ ´rco amarelo X ´rco roxo X X Wind 4 Caju acuMuiracatiaraTapereba TatapiriricaEnvira ata X Envira pretaEnvira condeEnvira turı X X Fauna Fauna X P X X 4 2 FaunaPau d’a Fauna FaunaUruazeiro 2 2 1 Cajarana Envira taia Envira turı Common name TreatmentEnvira brancaEnvira jaca Seed dispersal AraracangaSorva Acariquara X branca XFel de veadoColhoes de bode Morototo FaunaParapara Pau d’a P 1 X Wind Fauna Fauna 4 3 1 Carapanauba sp. X sp. Muirajussara P X sp. sp. sp. X sp.sp. Envira bananinha X sp. Envira pindauba preta X X sp. X sp. sp. Envira pindauba amarela sp. Astronium lecointei Spondias mombin Rollinia Bocageopsis BORAGINACEAE Cordia alliodora ANACARDIACEAE Anacardium giganteum Tapirira guianensis Annona Guatteria Guatteria Bocageopsis Tabebuia serratifolia Unidentified Annona ambotay ANNONACEAE Guatteria Xylopia APOCYNACEAE ARALIACEAE Schlefflera morototoni BIGNONIACEAE Jacaranda copaia Tabebuia impetignosa Geissospermum Unidentified Bucheira X Wind 2 Duguetia riparia Duguetia Aspidospermum exalatum Aspidospermum Couma guianensis Geissospermum sericeum Tabernaemontana Table 4 Tree and shrub species surveyed in old-growthScientific forests name and in 9- to 12-year-old restoration treatments at the Trombetas bauxite mine site Aspidospermum oblongum J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 227 Tree longevity Seed dispersal vectorFauna class 2 FaunaFaunaFaunaFauna 3 Fauna 2 1 4 4 Fauna 1 Fauna Fauna 1 X Fauna 1 56 X X Fauna 2 X Fauna 3 X X Fauna 1 X X Fauna 1 XXP XX Fauna 4 X P P PX PX XX XX XP XP XP 1234 X X X X X X XX X X XX X XPX X ńdio X P X ´ ´ X X Fauna 3 ´deanta Breu pretoBreu sucurubaCupiubaPajura Castanha de galinhaCaraiperana P X X X XCuiarana Fauna Fauna X X Fauna 4 3 Fauna 3 P 3 Fauna 4 Common name Treatment Pajura MacucuCaripe de vidro Fauna 2 Breu brancoBreu vermelho X X X X FaunaCuiaranazinhaArara-mira 2 X Fauna Fauna 4 2 CaquiUrucuranaCaxixa X X X Fauna Fauna 4 3 Seringa itauba X Fauna 3 Taquari Boleira X Fauna 2 ) sp. spp. Pau de ı sp. sp. sp. Continued ia sp. sp. Breu amarelo X spp. sp. sp. Jequitaia X 6 cf. micrantha sp. sp. Macucu vermelho Fauna 2 sp. sp. Caripe sp. Pau gaviota X sp. sp. Clusia X X X X eiba 6 ea guianensis 6 Trattinnickia rhoifolia CELASTRACEAE Goupia glabra Couepia bracteosa CHRYSOBALANACAEAE Scientific name Protium Tetragastris panamensis Couepia longipendunculo Couepia Hirtella Hirtella Licania Licania Clusia COMBRETACEAE Buchena Licania BURSERACEAE Licania Licania CLUSIACEAE Unidentified CONNARACEAE Hemicrepidospermum rhoifolium Protium apiculatum Connarus Connarus EBENACEAE Unidentified Diospyros ELAEOCARPACEAE Sloanea EUPHORBIACEAE Conce Table 4 ( Croton He Mabea Joannesia princips 228 J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 Tree longevity vectorFauna class 1 Fauna 2 FaunaFauna 2 3 FaunaFauna 3 3 Fauna Fauna 3 Fauna 3 X Fauna 3 X X X Fauna 1 P X Fauna 3 X XX Fauna Fauna 2 3 P Fauna 4 X X X X X X 3456 X X X PX P PX XX X X X X P 12 X X Treatment Seed dispersal X XXX XPX XXX X X X X XX XX X X X X XX ´ ´ X X Fauna 3 ´ preta ´ X Fauna 3 â X X X ˆco P Wind 4 ´ X X Fauna 3 ćo CaferanaCanela de velha X Fauna Fauna 1 1 Common name Pau jacare Lacre marrom Lacre branco X X Fauna 1 Lacre vermelhoUchi coro Uchi pucuAchua X X X Fauna 1 Uchi morcegoLouro amarelo X X Fauna Fauna 3 3 Louro pucherinLouro rosaLouro precioso Itauba amarela X X X Fauna Fauna 2 3 Louro vermelhoLouro canela Louro prataLouro abacate X X X Fauna Fauna Fauna 4 3 2 Louro branco Louro chumboCastanha do Para Taurı Fauna 3 Matamata ) sp. Jarana X sp. Matamata sp. iflora Permollis 6 sp. sp. sp. Continued sp. Bacuri mirim Fauna 2 sp. sp. Louro pequeno X sp. Louro preto sp. sp. Louro fofo X sp. cf. FLACOURTIACEAE Casearia Casearia Casearia Scientific name Laetia procera GUTTIFERAE Platonia Vismia guianensis Vismia cayennensis Vismia HUMIRIACEAE Duckesia sericea Endopleura uchi Sacoglottis mattogrossensis Vantanea paraensis LAURACEAE Aniba hostmaniana Aniba par Table 4 ( Aniba Aniba Aniba Mezilaurus itauba Nectandra rosa Ocotea fragrantissima Ocotea guianensis Ocotea myriantha Ocotea Ocotea Ocotea Cariniana micrantha Unidentified LECYTHIDACEAE Bertholletia excelsa Eschweilera Eschweilera Holopyxidium J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 229 Tree longevity vector class FaunaFauna 2 2 WindWind 2 Wind 3 4 XWind3 56 PX Fauna Fauna 3 2 P X Fauna 1 PWind1 PX X Fauna Fauna 3 3 PPP X FaunaX XX X WindX Fauna 1 Fauna Fauna 4 Fauna 4 1 2 1 X P P X X P Fauna 1 X X X Wind 3 X PX X P X PX XX X X X X X P P XP X 1234 X X XX X XPX X XX XX ´PX ´ grande t.f. P Fauna 2 ´ peq. t.f. ´ dos campos´ pitomba P X Wind Wind 1 2 ´ vermelho ´ pororoca Fauna 4 ´ X Fauna 4 ´ vermelha X ´ veluda´ grande X X Fauna 1 ´ branca´ xixica ´ cipo´ escamosa ´ guariba´ dura X X X X X Fauna Fauna Fauna 1 1 1 Faveira timboranaAngelim rajadoFaveira dentinha X X X Wind Fauna 3 4 Common nameFaveira marimarı Treatment Seed dispersal Leucaena Albizia falcataFaveira arara tucupı Faveira japacamim Faveira bolotaFaveira arara II P X P X Wind Fauna Fauna 1 3 3 Jutaı Inga Inga Jutaı Mulateiro CoataquicauaTachı Tachı Acacia auriculiformis Acacia mangium XCarolina X Cedrorana Angelim pedraFaveira timborilFaveira de roscaInga Inga Inga Inga X Inga P P X P P Fauna ? Fauna 1 3 2 Tachı Tachi preto folha miuda ) onia 6 eolens sp. P 6 sp. X Continued sp. Faveira rabo de arara sp.sp. Cassia piolho Faveira marimarı P sp. sp. Inga sp. sp. sp.sp. Inga Parkia Piptadenia sua Pithecellobium racemosum Pithecellobium LEGUMINOSAE-CAESALPINIOIDEAE Parkia pendula Parkia ulei Leucaena leucocephala Paraserianthes falcataria Parkia oppositifolia Scientific name Cassia spruceana Cassia Cassia Inga Inga Parkia gigantocarpa Dialium guianensis Peltogyne paniculata Sclerolobium paniculatum Acacia mangium Enterolobium schomburgkii Inga obtusata Inga Adenanthera pa Inga falcisti Inga Hymenaea courbaril Peltogyne paradoxa Sclerolobium melanocarpum Tachigali myrmecophylla Acacia auriculiformis Cedralinga catanaeformis Dinizia excelsa Enterolobium maximum Inga alba Inga Inga Tachigali LEGUMINOSAE-MIMOSOIDEAE Table 4 ( 230 J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 Tree longevity class WindFauna 3 1 vector ?3 WindFaunaFauna 2 2 3 Fauna 3 Fauna 4 Fauna 3 Fauna 2 XWind3 X Fauna 1 56 P XX? 2 Fauna 2 X FaunaX X 3 Fauna 1 X X Fauna 1 P X Fauna 4 X Fauna 4 X X X X X X X X X X X P P X X P P P P P X X PX P P PX X P X XP X Treatment1234 XX Seed dispersal X X XPX XX XX XX X X ´Wind2 ´ ´ X Fauna 3 ´ do Para ´ba da terra firme Wind 3 ´rosa´ P ´ba X Fauna 3 ´ da terra firme õ de negro X ´ da mata P X Fauna 2 ´ Fauna 1 ¸a ´ba X ća ´ba XXX Fauna 1 Sucupira amarela Sucupira pretaJacaranda P Wind 3 Palheteira Faveira camuze Faveira pituı Andira-uchi Fauna 4 Common name Faveira mapuchiqui Mututı Corac Pitaı Maramara branca Tento Tento monocor vermelhoMacacau Faveira amargosa Muricı Mirixı PMuu SapateiroMaramara preta Fauna 3 X X X X Fauna Fauna 1 1 Cumaru Cumaru Angelim da mataAngelim aroeira P X XMuirau Wind Wind 4 4 Andiroba Jatoa brancaJatau Capitiu Fauna 2 ) sp. sp. Nitida sp. sp. cf. sp. spp. Gombeira X Continued sp. sp. sp. sp. Miconia arbusto X sp. sp. Jatoa vermelha X Bowdichia Bowdichia Clitoria racemosa Andira retusa Stryphnodendron pulcherrimum Stryphnodendron UnidentifiedLEGUMINOSAE-PAPILIONOIDEAE Faveira mucuna Scientific name Unidentified Pterocarpus rohrii Swartzia corrugata Swartzia polyphylla Swartzia Platymiscium duckei Vatairea sericea Belucia dichotoma Miconia longifolia Miconia Ormosia MALPIGHIACEAE Ormosia discolor Byrsonima Byrsonima MELASTOMATACEAE Miconia Dalbergia spruceana Dipteryx odorata Hymenolobium Miconia Dipteryx magnifica Hymenolobium excelsum Mouriri plasscharti MELIACEAE Carapa guianensis MONIMIACEAE Siparuna amazonica Guarea Guarea Trichilia lecointei Table 4 ( J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 231 Tree longevity Wind 2 Fauna Fauna 2 WindWind 2 2 vector class Fauna 2 FaunaFauna 1 1 X Fauna 2 X XX Fauna Fauna 3 1 P Fauna 1 XXX Fauna Fauna 4 1 X Fauna 1 P P P P X X 3456 X X X X XX XX X X X X X XX 12 XX X XX XXX XX X XX XX X ¸ai X ˆra P Fauna 1 ´ X X Fauna 1 ¸a Fauna 1 ¸a pe UccubaranaUcuuba pretaUcuuba vermelhaEucalyptus camaldulensisEucalyptus citriodora Eucalyptus pellitaEucalyptus torreliana X X X P Fauna Fauna Wind Wind 3 3 2 2 Muiratinga amarela Fauna 3 Muiratinga preta MiurapinimaImbaubarana Eucalyptus urophylla PixunaMurta Fauna 3 X X X Fauna Fauna 1 2 Janita Guariuba Apui X Fauna 2 Common nameAmapa doceMuirapirangaImbauba Treatment X Seed dispersal P X X Fauna Fauna 4 1 Goiaba Arac Palmeira mumbaca Palmeira murumuru X X Fauna 2 Arac AcariquaraPalmeira jacitaraPalmeira ac Palmeira paxiuba X Fauna 2 ) a 6 sp. sp. Continued sp. spp. sp. sp. sp. Joao mole X Eucalyptus citriodora Eucalyptus pellita MYRISTICACEAE Iryanthera sagotiana Virola multicostata Virola MYRTACEAE Eucalyptus camaldulensis Eucalyptus torreliana Olmedia perebaea Noyera mollis Pourouma Eucalyptus urophylla Piratinera guianensis Myrcia Myrcia fallax Psidium guaja Ficus MORACEAE Brosimum lactescens Clarisia racemosa Brosimum potabile Scientific name Brosimum rubescens Cecropia Psidium Psidium guianensis NYCTAGINACEAE Astrocaryum munbaca Astrocaryum murumuru Neea OLACACEAE Minquartia guianensis PALMAE Desmoncus polycanthos Euterpe oleracea Iriatella setigera Table 4 ( 232 J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 Tree longevity class vector FaunaWindFauna 2 Fauna 4 Fauna 3 1 2 Fauna 2 Fauna 3 FaunaFaunaFaunaFaunaFauna 3 3 3 2 3 Fauna 3 XX Fauna Fauna 2 2 X?X 2 Fauna 1 56 X Fauna 1 X X Fauna 1 X Fauna 3 X X XX P X X XX Treatment1234 X Seed dispersal X X X X XX X XX X X X X X X XXX X X X X 1 X Wind 1 ´ c ´ Palmeira pataua Palmeira bacaba X P X Fauna 2 Common name Palmeira bacaba-ı Palmeira marajaPalmeira tucumaGenipapo P Fauna Fauna 2 2 Palmeira ubim Faieira PuruiPau de remo X X X Fauna 2 Erva de rato vermelhoPau para tudo P X Fauna 1 Pitomba da mata X Abiurana vermelha Fauna 3 Abiurana barriguca Fauna 3 MaparajubaAbiurana rosadinha Abiurana arrepiadu X Fauna Fauna 4 3 Abiurana cutite X Abiurana amarela AbiuranaAbiurana moraicica Abiurana folha grande X Fauna Fauna 3 3 Abiurana casca fina Fauna 3 ) ii sp. Abiurana casca grossa X 6 sp. Tamanqueira sp.sp. Erva de rato amarelo X Continued spp. sp. sp. sp. Jessenia bataua Oenocarpus bacaba Scientific name Oenocarpus minor Unidentified Palmeira pinaupira X Unidentified Unidentified Duroia Genipa americana Unidentified Roupala RUBIACEAE PROTEACEAE Duroia Palicourea Palicourea Unidentified RUTACEAE Spathelia excelsa Zanthoxylum SAPINDACEAE Talisia cupularis Unidentified SAPOTACEAE Chrysophyllum prieurii Chrysophyllum Lucuma dissepala Manilkara amazonica Micropholis guianensis Pouteria kruko Table 4 ( Radlkofarella macrocarpa Unidentified Abiurana folha comprida X Pouteria trilocularis Unidentified Pouteria Unidentified Unidentified Abiurana ajara Unidentified Unidentified Abiurana X X J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 233 (MNS) Tree longevity , average expected life vector class Wind 3 Fauna 2 ?2 ?1 ?1 ?2 ?1 ? ?2 X Fauna 1 X X X XX Fauna Fauna 3 1 X XX XX Fauna Fauna Fauna 1 1 1 XWind2 XXX ? 1 X 3456 X X X Fauna 2 X X X XX 12 X XXX X X X XX XXXX X 80 years. \ ´ ¸oita cavalo Marupa Common name Treatment Seed dispersal CacauranaPente de macaco X X P Ac Curumin Lantana Acariquarana QuarubaranaQuaruba rosa Pau de rego Papo de mutum Jameca Pau tucandeiraUnknown species Wind 4 ? ? 1 1 Muiranta ) estris 6 icata 6 20 years; 2, 20–40 years; 3, 40–80 years; 4, Continued B sp. Jacamin branco X X sp. Jacamin preto Treatment: P, Planted species; X, natural regeneration from soil seed bank or external sources. 1, Native old-growth forest; 2, mixed native species a STERCULIACEAE Simarouba amara SIMARUBIACEAE Theobroma syl Scientific name TILIACEAE Apeiba echinata Lueheopsis di ULMACEAE plantation; 3, MNS ‘failure’;span: 4, 1, mixed commercial species plantation; 5, direct seeding plantation; 6, natural regeneration. Tree longevity class Trema micrantha VERBENACEAE VIOLACEAE Lantana camara Rinorea guianense Rinorea Table 4 ( Rinorea VOCHYSIACEAE Erisma uncinatum Unidentified families Unidentified Vochysia obscura UnidentifiedUnidentifiedUnidentified Unidentified UnidentifiedUnidentified UnidentifiedUnidentified Acariquarana Canela brava Olho de veado Tapioca X X X X X P Unidentified 234 J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239

3.4. Effect of o6erstory composition on forest structure and ﬂoristic di6ersity

3.4.1. Forest co6er and tree density Forest canopy cover, tree basal area, litter and humus depths were broadly similar among the mixed native species, mixed commercial species, direct seeding and natural regeneration treatments, although distinctly dissimilar to those of the old-growth forest (Table 2). Average crown cover ranged from 53 to 64% and tree basal area from 13.9 to 24.9 m2 ha−1 among restoration treatments, as compared with 76% and 77 m2 ha−1 in the old-growth forest. These values were Fig. 3. Distribution of average seed lengths for tree species highest in the mixed commercial species and low- found in 10-year-old mixed native species plantations and nearby old-growth (‘primary’) forests at the Trombetas baux- est in the mixed native species treatment. Mean ite mine site. Figures above bars indicate the percentages of canopy heights were significantly greater in the species in each size class in the plantations relative to the old-growth forest (21.691.5 m) and mixed com- old-growth forest. mercial species treatment (17.490.9 m) than in the other three treatments (range of means, 10.4– 11.7 m). Litter accumulation was significantly In the forests of the Trombetas region, as in greater in the mixed commercial species and natu- other moist tropical forests, larger-seeded species ral regeneration treatments (range of mean litter generally depend on a variety of bird and mam- depths, 43–46 mm) than in the direct seeding, mal species for their dispersal. Previous surveys of mixed native species and old-growth forest stands wildlife in the reforestation areas at this site (Pe- (range of means, 29–33 mm). Average humus dreira Gonzaga, 1991; Parrotta et al., 1997; Wun- depths ranged from 5.7 mm in the mixed commer- derle, 1997) suggest that the regeneration of cial species stands to 13.3 mm in the old-growth large-seeded tree species is limited by the relative forest; treatment differences were significant only scarcity in these developing forest stands of these between these extremes. important seed dispersers, i.e., birds such as The density of both planted and naturally regenerated woody species was lower in all restora- curassows, toucans, toucanets, and aracaris, ter- tion treatments than in the old-growth forest restrial mammals such as deer, agouti, tapir and (Table 2). Planted trees comprised 5.6–15% of the opossum, and primates. Assuming that the total among the plantation treatments, the re- restoration treatment stands continue to develop mainder arising either from soil seedbank regener- both structurally and floristically, larger-seeded ation, subsequent seed inputs from surrounding species from presently under-represented families old-growth forest areas and, for a small number may eventually become established as conditions of species, regeneration from planted trees. become more favorable for a greater diversity of Seedlings (individuals B2 m tall) comprised 77– seed-dispersing birds and mammals, as well as for 87% of the total woody species density among seed germination and seedling growth. Nonethe- restoration treatments and 92% in the old-growth less, it is recommended that restoration managers forest. The average density of larger stems (]2m at this site carry out understory enrichment plant- tall) ranged from 0.28 to 0.54 individuals per ings of these generally shade-demanding species square meter among restoration treatments and when the planted trees are sufficiently tall to was significantly higher in the direct seeding treat- permit easy access, usually about 5 years after ment than in the other restoration treatments or planting. the old-growth forest. J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 235

3.4.2. Tree species richness species in the direct seeding, and 73 species in the Tree species richness varied greatly among mixed native species treatments. treatments. The total numbers of woody species The mixed native species, direct seeding and recorded were 157 in the old-growth forest (repre- natural regeneration treatments contained 55– senting 39 families), 141 species from 38 families 90% of the total number of species and 82–97% in the mixed native species treatment, 47 species of the total number of families found in the (from 22 families) in the mixed native species old-growth forest plots. The restoration treat- ‘failure’ plots, 40 species (from 21 families) in the ments exhibited a low to moderate degree of mixed commercial species treatment, 117 in the floristic similarity to the original old-growth direct seeding treatment (from 37 families), and 86 forest, as measured by Sorensen’s quotient of species (from 32 families) in the natural regenera- similarity (I), which ranged from a low of 0.16 (in tion treatment (Fig. 4). These totals include the mixed commercial species treatment) to 0.50– planted species, i.e. 7, 42 and 73 in the mixed 0.51 (in the direct seeding and mixed native spe- commercial species, direct seeding, and mixed na- cies treatments) (Table 2). Although most of the tive species treatments, respectively. If planted families present in the old-growth forest tree flora species were discounted, the species–area relation- were represented in the natural regeneration, di- ships presented in Fig. 4 would appear similar for rect seeding and mixed native species treatments, all but the mixed commercial species stands and certain important families, including Annonaceae, the mixed native species ‘failure’, which contain a Chrysobalanaceae, Lauraceae, Palmae and Sa- smaller number of tree and shrub species than the potaceae were, in general, very poorly represented other treatments. in all restoration treatments, as already discussed. Discounting tree seedlings (individuals B2m These general trends are supported by analyses tall), total tree species richness varied consider- of plot-based (equal area) measurements of spe- ably among treatments and between restoration cies richness (Table 2). The average numbers of tree and shrub species per plot were significantly treatments and the old-growth forest. The old- different among treatments, and increased two- growth forest plots contained a total of 88 tree fold from the mixed native species ‘failure’ and species with individuals \2 m in height as com- mixed commercial species to the direct seeding pared with 19 species in the mixed commercial treatments, with intermediate values in the natural species, 37 species in the natural regeneration, 27 regeneration and mixed native species treatments. In the old-growth forest, mean tree and shrub species richness was 67.3 species/plot, more than twice that of the direct seeding treatment. Planted species comprised up to one-third of the total in the mixed commercial species, direct seeding and mixed native species treatments. Tree seedling and sapling (individuals B2 m tall) species richness was significantly different among all restoration treatments, and ranged from an average of 9.8 species/plot in the mixed commercial species treatment to 31.6 species/plot in the direct seeding treatment. The old-growth forest plots had a significantly larger number of species in this size class (mean, 59.892.6 species/plot) than all Fig. 4. Species–area relationships for tree, shrub and palm restoration treatments. Woody species richness species in restoration treatments and old-growth (‘primary’) ] forest. Treatment descriptions are provided in the text; ‘MNS’ for larger individuals ( 2 m tall) was very similar refers to the mixed native species treatment, the standard among restoration treatments (range of means, reforestation practice at the Trombetas mine site. 11.4–14.6 species/plot) but was significantly lower 236 J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239

Table 3 Stand basal area distributions in 9- to 13-year-old restoration treatments and old-growth forest at the Trombetas bauxite mine sitea

TreatmentDominant tree species Family %BA Longevity (years)

Natural regeneration Cecropia sp. Moraceae 29.6 B20 Byrsonima sp. Malpighiaceae 12.6 20–40 Vismia guianensis Guttiferae 7.7 B20 33 other species 50.1 Mixed commercial species Eucalyptus pellita Myrtaceae 22.6 20–40 Sclerolobium paniculatum Leguminosae (C) 21.4 B20 Acacia mangium Leguminosae (M) 20.2 B20 16 other species 35.8 Direct seedingSclerolobium paniculatum Leguminosae (C) 53.9 B20 41 other species 46.1 Mixed native speciesCroton sp. Euphorbiaceae 12.9 B20 Joannesia princips Euphorbiaceae 10.8 20–40 Bellucia dichotoma Melastomataceae 8.7 B20 Parkia gigantocarpa Leguminosae (M) 8.6 40–80 Bysonima sp. Malpighiaceae 8.4 20–40 66 other species 50.6 Mixed native species (insufﬁcient topsoil)Vismia spp. (3) Guttiferae 32.1 B20 Joannesia princips Euphorbiaceae 19.2 20–40 18 other species 48.7 Old-growth forestBrosimum rubescens Moraceae 14.3 \80 Astrocaryum murumuru Palmae 11.4 20–40 Unidentiﬁed Palmae 10.6 20–40 Endopleura uchi Humiriaceae 8.9 40–80 Virola sp. Myristicaceae 5.9 40–80 151 other species 48.9

a Dominant species comprising approximately 50% of total basal area listed individually. than in the old-growth forest (mean, 21.591.9 native species ‘failure’, three species of Vismia and species/plot). J. princips comprised 51% of the total basal area. The old-growth forest plots were dominated by a 3.4.3. Tree species dominance very different suite of tree species, with 75% of the There were marked differences among treat- total basal area represented by species either rare ments in tree species dominance, as measured by or absent from the restoration plots, including basal area percentages (Table 3). In the natural Brosimum rubescens, Astrocaryum murumuru and regeneration treatment, the pioneer species Ce- other palms, Endopleura uchi, Virola sp., and Nec- cropia sp., Byrsonima sp., and Vismia guianensis tandra rosa, which collectively comprised 57% of together comprised 50% of the total basal area. In the total. Among restoration treatments, the the mixed commercial species treatment, the mixed native species plots more closely resembled planted species Eucalyptus pellita, Sclerolobium the old-growth forest in that they exhibited much paniculatum, and Acacia mangium comprised 64% less marked patterns of dominance by fewer tree of the total basal area. In the direct seeding species than the other restoration treatments. treatment, the dominant species was S. paniculatum, with 54% of the total basal area. In the 3.4.4. Tree species life spans mixed native species treatment, five species: Cro- Categorizing tree species by their expected aver- ton sp., Joanesia princips, Bellucia dichotoma, age life spans, differences among treatments are Parkia gigantocarpa,andByrsonima sp. com- apparent (Fig. 5). For all treatments, the propor- prised 49% of the total basal area. In the mixed tions of species and total basal area decrease from J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 237 younger to older tree life span classes, in contrast cies with expected life spans \40 years comprise to the old-growth forest, where very short-lived 0.5% of total basal area. The direct seeding treat- (B20 years) species are both less numerous and ment is also dominated by short-lived trees, with dominant than longer-lived (20–40 or 40–80 88% of the total basal area comprised of species years) species. The percentage of species with with life spans B20 years, and relatively poor \ expected life spans \40 years is lowest in the representation by trees with life spans 40 years, mixed commercial species treatment (23%), inter- which comprise 2.6% of the total basal area. The mediate in the natural regeneration treatment natural regeneration treatment was also dominated by short-lived species, although longer-lived (35%) and highest in the direct seeding and mixed (\40 years) taxa contributed significantly to total native species treatments (43%). In the old-growth basal area (21%). The most even life-span distri- forest, such longer-lived species comprised 44% of bution of tree species and total basal area is found the total. in the mixed native species treatment. In these Treatment differences in basal area distribu- stands, very short-lived (B20 years) tree species tions followed similar but more pronounced comprise 45% of the total basal area, and long- trends. In the mixed commercial species, tree spe- lived species (\40 years) 23% of total basal area. In the old-growth forest, very short-lived trees comprised only 6.1% of the total basal area, the remaining basal area distributed among species with expected life spans of 20–40 years (37%), 40–80 years (33%) and \80 years (24%). The lesser degree of dominance by shorter-lived tree species, particularly those with expected life spans of less than 20 years, in the mixed native species treatment relative to other plantation treatments suggests that these stands are at a lower risk of arrested succession in the near future. Elsewhere at the Trombetas mine site and in other mine rehabilitation areas in the tropics, the authors have observed the senescence and prema- ture mortality of planted early successional native tree species and short-lived exotic timber species such as eucalyptus and A. mangium. Under these conditions, in the absence of vigorous under- growth comprised of longer-lived native forest trees, such stands are very often subject to rapid invasion by persistent, fire-prone grasses that are known to severely slow, or even preclude, natural forest succession (Uhl and Jordan, 1984; Uhl et al., 1988; Nepstad et al., 1991; Parrotta, 1993; Aide et al., 1995). This risk appears to be mini- mized in the mixed native species plantation areas Fig. 5. Expected longevity of planted and naturally regenerat- that predominate at the Trombetas mine site. In ing tree species in old-growth forest and 9- to 13-year-old spite of their relatively low productivity at this age reforestation area study plots at the Trombetas bauxite mine compared with that of the other treatments stud- 2 site. (a) Total numbers of tree species; (b) stem basal area (m ied, the mixed native species plantation approach ha−1) for trees ]2 m in height. PF, Old-growth (‘primary’) forest; MNS, mixed native species treatment; MCS, mixed adopted by MRN and other mining companies in commercial species treatment; DS, direct seeding treatment; the region offers the best hope for long-term NR, natural regeneration treatment (topsoil application only). forest restoration success. 238 J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239

4. Conclusions on seed-dispersing wildlife, mainly bats, birds and terrestrial mammals. The conservation status of the surrounding old-growth forest 1. With a modest but timely investment in re- and an effective ban on hunting greatly facili- search, mining companies can develop an effi- tated this process. Restoration managers need cient, cost-effective system for selecting and to be cognizant of the critical role of wildlife in propagating a wide array of native tropical forest re-development, actively encourage forest trees about which basic silvicultural wildlife conservation in the surrounding land- knowledge is lacking, and thereby successfully scape, and design restoration treatments that establish highly diversified mixed native spe- will provide suitable habitats for a variety of cies plantations on an operational scale. target wildlife species. 2. Careful site preparation practices, particularly 6. In the 10-year-old mixed native species planta- judicious topsoil handling and reapplication tions, the density and diversity of colonizing prior to tree planting, are essential for the primary forest trees was significantly (and pos- establishment of forest cover, elimination of itively) affected by the proximity to seed competing grasses, and acceleration of natural sources in the surrounding old-growth forest. forest succession on reclaimed bauxite mine Many large-seeded tree species and others that sites in Amazonia. are considered important components of the 3. In addition to the mixed native species planta- region’s old-growth forests performed poorly tion approach (the standard reforestation tech- when planted under open conditions and were nique at the Trombetas mine site), alternative apparently not colonizing the site due to natu- plantation treatments and reliance on natural ral seed dispersal limitations and/or seed and regeneration from applied topsoil were found seedling mortality when they did arrive. For to be effective in re-establishing forest cover these species, restoration managers are advised and facilitating regeneration of a large number to carry out enrichment plantings in the un- of native forest species during the first 9–13 derstory of established plantations to ensure years. Among treatments, stand basal areas at their successful re-introduction. this age ranged from 18 to 33% of that in the 7. The results of our studies at the MRN bauxite surrounding old-growth forest. mine site at Trombetas strongly suggest that 4. Although the less expensive alternatives (com- the current reforestation practices will eventu- mercial species plantings, direct seeding, and ally be successful in meeting the long-term reliance solely on natural regeneration from goal of restoring the complex Amazonian applied topsoil) were more productive (greater ‘terra firme’ forest ecosystem destroyed by basal area development) than the mixed native mining. These findings defy the assumptions of species treatment, they were generally less well some restorationists that high-diversity forest developed in terms of floristic biodiversity. systems cannot be successfully established Due to their relatively high degree of domi- through high-diversity planting schemes (Dob- nance by short-lived exotic or native tree spe- son et al., 1997). cies, and somewhat less well-developed understory tree flora, the risk of early canopy mortality and subsequent re-invasion by Acknowledgements highly competitive, fire-prone grasses is poten- tially much greater in these stands than in the This work was conducted in cooperation with mixed native species treatment. the University of Puerto Rico and supported in 5. Floristic enrichment of the reforestation areas part by a grant from the World Bank to the through natural regeneration of ‘colonizing’ International Institute of Tropical Forestry, tree species (i.e. those not planted or present in USDA Forest Service (Research Support Budget the applied soil seed bank) is largely dependent Grant RPO c680-05: ‘The catalytic effect of tree J.A. Parrotta, O.H. Knowles / Ecological Engineering 17 (2001) 219–239 239 plantings on the rehabilitation of native forest Knowles, O.H., Parrotta, J.A., 1997. Phenological observa- biodiversity on degraded tropical lands’). The au- tions and tree seed characteristics in an equatorial moist thors thank Mineraçaõ Rio do Norte for permitting forest at Trombetas, Para´ State, Brazil. In: Lieth, H., Schwartz, M.D. (Eds.), Phenology in Seasonal Climates access to the reforestation area for research pur- I. Backhuys, Leiden, pp. 67–84. poses and offer special thanks to Sr Pedro Ferreira Majer, J.D., 1992. Ant recolonisation of rehabilitated baux- for his special expertise and assistance in identifying ite mines of Poços de Caldas, Brazil. J. Trop. Ecol. 8, trees and seedlings in the field. The authors also 97–108. thank Daniel Janzen and an anonymous reviewer Majer, J.D., 1996. Ant recolonization of rehabilitated bauxite mines at Trombetas, Para´, Brazil. J. Trop. Ecol. 12, for their helpful comments and suggestions on an 257–273. earlier version of this paper. Nepstad, D., Uhl, C., Serraõ, E.A., 1991. Recuperation of a degraded Amazonian landscape: forest recovery and agri- cultural restoration. Ambio 20, 248–255. References Parrotta, J.A., 1993. Secondary forest regeneration on degraded tropical lands: the role of plantations as ‘foster ecosystems’. In: Lieth, H., Lohmann, M. (Eds.), Restora- Aide, T.M., Zimmerman, J.K., Herrara, L., Rosario, M., 1995. Forest recovery in abandoned tropical pastures in tion of Tropical Forest Ecosystems. Kluwer Academic, Puerto Rico. For. Ecol. 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