nutrient cycling in primary and old secondary rainforests

Applied Geography (1987), 7, 135-152

Nutrient cycling in primary and old secondary rainforests

John Proctor

Department of Biological Sciences, University of Stirling, Stirling FK9 4LA, Scotland

Abstract

The popular view of primary and old secondary tropical rainforests is that they occur on infertile soils, have most of the nutrients in the above-ground living matter, and maintain a high production by rapid and efficient nutrient cycling. This paradigm pervades much land use planning rationale in forested areas in the tropics.

In this paper, rainforest nutrient cycles are outlined and the methodological difficulties of work on them are emphasized. There is a shortage of information on nearly every aspect. It is concluded that the popular view is not fully justified even from the available data. Some rainforests occur on fertile soils with a high proportion of at least some nutrients below ground. In some cases there appears to be a substantial yearly loss of nutrients from the ecosystem and sometimes nutrient cycling is slow.

Rainforest nutrition is immensely complex and shows many differences from one area to another. It is concluded that much more research is necessary before useful generalizations are possible.

Introduction

There is a well-known notion (originated by Hardy 1936; Walter 1936; and Milne 1937) of tropical forests which occur on such nutrient-poor soils that most of the nutrients are in the living above-ground matter and which maintain a high production by exceptionally rapid and efficient nutrient cycling. However, the evidence on which these views might be sustained or rejected has been described as ‘woefully inadequate’ (Whitmore 1984). The aim of this paper is to present this evidence and to evaluate it. Nutrient cycling in forest plantations or young secondary forests is not discussed here, since these are aggrading systems with different cycling characteristics from those in mature steady-state forests.

The forest nutrient cycles are summarized in Fig. 1. The word nutrient is taken to mean all essential elemental constituents of the plants other than carbon, hydrogen and oxygen, but attention has been concentrated on nitrogen, phosphorus, potassium, calcium and magnesium because they are usually considered to be required in relatively large quantities. Nutrient cycling in forests must involve a complex set of direct and indirect feedbacks in which the soils influence vegetation and in which vegetation influences the soil. There is an interacting involvement of micro-organisms, vegetation and abiotic factors which has been well discussed by Coleman et al. (1983).

Nutrients enter the ecosystem with the rain, deposition of dust and aerosols, by fixation by micro-organisms (in the case of nitrogen) above and below ground, and (except for nitrogen) by weathering of the rock. The major above-ground pool of nutrients is the canopy (defined as the total plant community above the ground) and

0143-6228/87/020135-18 $03.00 0 1987 Butterworth & Co (Publishers) Ltd

136 Nutrient cycling in rainforests

EXCHANGE COMPLEXES

SOIL rock weathenng

.-___-____- --------- -\ T

nutrient losses in I \ watermovementsfromforest ,’

ROCK ‘.__________---___-I

Figure 1. Forest nutrient cycles.

there is a flow of nutrients from this to the forest floor in small and large litterfall and in throughfall and stemflow of rainwater, which usually becomes enriched by nutrients from leaves and bark. A proportion of the above-ground nutrients is in dead organic matter such as standing dead trees and small and large litter lying on the forest floor. Nutrients are gradually released from the dead matter by decomposition mediated by soil animals and micro-organisms. Decomposition is complex and can involve immobilization of nutrients as well as their release. Some of the immobilization involves a conversion of the litter to stable soil organic matter which in some cases (e.g. heath forests and peat-swamp forests) may hold nutrients indefinitely. Nutrients are taken up from the soil by roots (probably usually in association with mycorrhizal fungi) which provide a living below-ground pool and which export them to the canopy. The roots release nutrients to the soil as secretions and by the death and decomposition of their parts. Permanent loss of nutrients occurs through erosion, fires, loss in drainage water and in the case of nitrogen by abiotic or microbial denitrification. Some, particularly phosphorus, may effectively leave the system by conversion into insoluble inorganic forms within the soil. The task of understanding rainforest nutrient cycling is to measure the amounts of nutrients in the different pools and their flows into and out of the system and between the pools. No study has succeeded in examining all the flows and pools. There are immense difficulties at every stage, not the least of which is the intensive labour requirement.

John Proctor 137

Nutrient pools

Above-ground nutrients

The first problem in assessing above-ground nutrients is a general one of forest sampling. Rainforests are so rich in species (see, for example, Proctor et al. 1983) and there are such large interspecific differences in chemical composition (Grubb and Edwards 1982) that genuinely representative or replicate samples are difficult or impossible to obtain. There is also the cyclical phase of the samples to consider. Rainforests are a mosaic of different phases (pioneer, building, mature and degenerate) and again the question of representative sampling is posed. It is unfortunate that some reports of above-ground nutrient concentrations have not included details of the forest sample size (Table 1). Results for small samples can easily be biased because most of the nutrients are in the trunks of infrequent large trees. Some workers (Table 1) have based their data on sampled trees from no precise area; this method is likely to give different results from that where a delimited forest site was totally sampled.

It is important to note that several possible short-cut methods are prone to error. For example the chemical composition of leaves may (Tanner 1985) or may not (Grubb and Edwards 1982) be correlated with nutrients in wood. This means that leaves (which are relatively easy to collect) cannot be used as indicators of the nutrient status of whole ecosystems. Another difficulty is that heartwood has a different chemical composition from sapwood (Grubb and Edwards 1982) and this limits the use of tree corers since representative wood samples can best be obtained by the destructive and time consuming method of cutting discs or sectors from felled trees.

Tanner (1985) has pointed out the serious discrepancies that are likely to exist between published analyses. He quotes the work of La Bastide and Van Goor (1978) and Van Goor (1978) who sent identical leaf sub-samples to 21 laboratories for analysis and showed that for nitrogen the reported range of concentrations was 29 per cent of the mean; for phosphorus, 36 per cent; for magnesium, 45 per cent; for potassium, 83 per cent; for calcium, 85 per cent; and for sodium, 161 per cent. With unskilled analysts the discrepancy must be greater. Bearing in mind the above difficulties, it is clear that the results for above-ground nutrients in tropical forests (Table 1) must be interpreted with caution.

Estimates of nutrients in the small litter on the soil surface are relatively easily made provided that there are sufficient samples and care is taken with the definition of litter, as opposed to soil organic matter. Large litter (including fallen logs and standing dead trees) is difficult to sample because of its sporadic distribution. The litter data in Table 1 include both large and small litter and the reliability of many of the estimates is not high.

Below-ground nutrients

Roots are notoriously awkward to sample: their biomass varies with depth and the coarser roots, and perhaps the finer ones, are very patchy. They are difficult to dig up and clean satisfactorily. Roots seem likely to show interspecific differences in their nutrient concentrations (Grubb and Edwards 1982) and in this respect present similar sampling problems to those of the above-ground forest.

The measurement of inorganic nutrients in the soil involves the problem that the amounts estimated by chemical analysis are not necessarily a measure of those available to plants. The total amount will overestimate, and the available or


Table 1. The dry weights (tha- ‘) and nutrient contents

Dry weight N” Pb K‘ Ca Mg

434 424 201 63 82 55

8 21 18 58 0 17

77.1 80.5 69.1 1.4 4.0 6.2

Lowland forests Brazil (from Klinge 1976, based on felled plot of 0.2ha)

Above-ground plant parts 406 2430 59 Below-ground plant parts 61 558 6.9 Litte& 31 294 3.4 Soil (O-30cm) 4260 71 Above-ground plant parts/

Total (070) 32.2 42.1 Litter/Total (o/a) 3.9 2.4

Ghana (from Greenland and Kowal 1960, based on felled plot of 0.53 ha)

Above-ground plant parts 233 1690 112 753 Below-ground plant parts 54 326 24 143 Littere 74 264 20 46 Soil (O-30cm) 4950 13 649 Above-ground plant parts/

Total (Vo) 23.4 66.3 47.3 Litter/Total (oio) 3.7 11.8 2.9

Colombia (from Folster et al. 1976, based on extrapolations from sampled trees) Slope

Above-ground plant parts Litterf

Soil (O-50cm) Above-ground plant parts/

Total ((70) Litter/Total (070)

Terrace Above-ground plant parts Litterf Soil (O-50cm) Above-ground plant parts/

Total (Vo) Litter/Total (070)

Ivory Coast

326 1000 38 389 809 225 52 650 16 30 90 25

4830 205 176 1780 203

15.4 14.7 65.4 30.2 10.0 6.2 5.0 3.4

185 741 27 277 432 54 672 18 32 94

5350 254 119 31

11.0 9.0 64.7 77.6 9.9 6.0 7.5 16.9

2370 320 268 65 569 57

2580 295

41 .o 9.8

43.4 7.7

49.7 5.5

133 28 43

65.2 13.7

(from Bernhard-Reversat et al. 1978, based on extrapolations from sampled trees) Bancog

Total above-ground biomass 513 1400 100 600 1200 Soil (O-50cm) 6150 190 120 150 Above-ground plant parts/

Total (070) 18.5 34.5 83.3 88.9

530 95

84.8

U Total N in all fractions b Total P in the Brazilian, Colombian, and both Venezuelan soils; acid-soluble in the Ghanaian and

Puerto Rican; assimilable P in the Ivory Coast soils, and fluoride-soluble P in the New Guinean soil c Exchangeable cations recorded for all soils except the Brazilian and Panamanian, for which total

contents are given d Includes the forest floor, fallen and standing dead trunks and branches, and epiphytic ‘soil’

John Proctor 139

(kgha-t) of four fractions in various tropical rainforests

Dry weight NO Pb Kc Ca

Yapor Total above-ground biomass 433 1000 70 350 1900 Soil (O-50cm) 2600 25 115 215 Above-ground plant parts/

Total (Oio) 27.8 73.7 75.3 89.8

Panama (from Golley et al. 1975, based on sampled plots of unspecified total area)

Above-ground plant parts 316 158 3020 3900 Below-ground plant partsh 11 - 6 81 208 Litter’ 5 - 2 21 128 Soil (O-30cm) - 22 353 22200 Above-ground plant parts/

Total (070) - 84.0 86.9 14.8 Litter/Total (070) 1.1 0.6 0.5

Venezuela (from Hase and Folster 1982, based on extrapolations from sampled trees)

Above-ground plant parts 398 1980 291 1820 3380 Litter/ 9 137 10 20 178 Soil (O-50cm) 3 930 2470 399 1680 Above-ground plant parts/

Total (oio) 32.7 10.5 81.3 64.5 Litter/Total (070) 2.3 0.4 0.9 3.4

Lower montane forests

New Guinea (from Edwards and Grubb 1982, based on felled plot of 0*04ha)

Above-ground plant parts 310 683 37 668 1270 Below-ground plant parts 40 137 6.4 186 333 Litterd 20.7 170 10 33 158 Soil (O-30cm) 19200 16 403 3750 Above-ground plant parts/

Total (oio) 3.4 53.3 51.8 23.0 Litter/Total (070) 0.8 14.4 2.6 2.9

Puerto Rico (calculated from a variety of sources by Edwards and Grubb 1982)

Mg

180 95

65.5

403 28 10

2260

14.9 0.4

313 30

393

42.5 4.1

187 61 28

682

19.5 2.9

Above-ground plant parts Below-ground plant parts Litter’ Soil (O-25 cm) Above-ground plant parts/

Total (070) Litter/Total (070)

197 814 43 517 894 340 78 300 16 230 300 85

6 126 - 1J 17 9 - 51 175 1780 460

39.1 56.0 29.9 38.0 - 0.1 0.6 1.0

Litter includes large dead wood Litter includes surface soil organic matter and dead wood Banco data combined for ‘plateau’ and ‘valley’ forest. No litter data given The data for roots are acknowledged to be gross underestimates Litter excludes dead wood K in litter thought to be improbably low


Table 1 (contd)

Dry weight NO J=‘b K’

Venezuela (from Grimm and Fassbender 1981a, based on felled plot of 0.25 ha)

Above-ground plant parts 348 875 52 1320 Below-ground plant parts 56 232 14 147 Litter’ 24 58 4 28 Soil (O-40cm) 3810 538 239 Above-ground plant parts/

Total (oio) 17.6 8.6 76.1 Litter/Total (oio) I.2 0.7 1.6

Upper montane forests Jamaica (from Tanner 1985, based on felled plot of 0.01 ha) Mor ridgeA

Above-ground plant parts 209 426 30 272 Below-ground plant parts 54 92 3 49 Soil (O-45 cm) 9000 130 Above-ground plant parts/

Total (070) 4.5 - 60.3 Mull ridge”

Above-ground plant parts 331 857 41 830 Soil (O-40cm) 7000 200 Above-ground plant parts/

Total (070) 10.9 - 80.6

Ca Mg

736 215 154 39 86 15

420 107

52.7 57.2 6.2 4.0

353 155 165 39 30 400

64.4 26.1

940 193 240 150

79.1 56.3

k No litter data given

exchangeable amount will underestimate what is available to plants in the long term. Different analytical methods, the use of total analyses by some authors and available analyses by others, and different sampled soil depths render published results difficult to compare.

It has long been recognized that rainforests occur over a wide range of soils. Proctor ef al. (1983: Table 10) have collated soil analyses from a range of rainforests and demonstrate that some are on nutrient-poor soils, others on nutrient-rich soils. This makes generalizations about rainforest soils difficult to sustain. For example, there is a frequently expressed view that Amazonian soils are unusually infertile, yet the data in Proctor et al. (1983) [and the analyses of Camargo and Falesi (1975) and Guerrero (1975)l do not support this for at least some of the soils of that region.

Table 1 summarizes soil data for those sites where there have been estimates of other nutrient pools. The results are for the upper horizons only, because these supply most of the nutrients since plant roots are probably usually concentrated there.

The distribution of nutrients between the different pools

Accepting that the data in Table 1 must be viewed with reservation, they can be used to test the idea that rainforest nutrients are largely above ground. The forest which comes closest to the conventional view is that investigated in Brazil by Klinge (1976), which has a high proportion of the total potassium, calcium and magnesium in the

John Proctor 141

above-ground biomass. Similarly high proportions elsewhere are less impressive because they are based on ‘available’ quantities of soil nutrients. In many cases a high proportion of the nutrients lies below the ground. This is always the case for nitrogen and often so for phosphorus, but raises the question of the true availability of these elements in the soil to plants. The proportion of nutrients in the litter on the forest floor is usually less than 10 per cent and in many cases less than 5 per cent of the total.

Nutrient flows

Ecosystem inputs

There are still few complete data sets on atmospheric influx. Some are collated in Table 2 and show considerable variation between nutrients and sites. The causes of inter-site variation include different amounts of precipitation and differing proximity to the sea, where onshore winds may enhance magnesium (as well as sodium) (Brasell and Sinclair 1983).

Atmospheric influx measurements are bedevilled by problems of contamination (including the growth of micro-organisms in stored samples) and the problems of adsorption of ions on to the sides of containers (Edwards 1982). A number of estimates are based on short-term studies and Kellman et al. (1982) have emphasized the difficulties of interpreting these. They found (for a seasonal area in Honduras)

Table 2. Annual input of elements in bulk precipitation measured in various tropical rainforest areas (kgha~‘yr’)

Location N P

Lowland forests Australia

Brazil Brazil Ghana

Ivory Coast Ivory Coast

Malaya Malaya Panama Papua Venezuela

Caatinga Caatinga Terra firme Terra firme

Lower montane forests New Guinea Puerto Rico

Venezuela

-

10 5.0

14

14 21.2

21.2 -

21.7

6.5

9.9

4 3 2.5

0.3 - 3.6 3 0.4 - 0.3 0.2 0.4 17.5 12.7 11.3

- 2.3

-

5.5

-

30 7

-

1.0 -

12.5 14 3.3 6.4 4.2 0.7 9.5 29.3 4.9 0.8 0 0.3

Brasell and Sinclair (1983) Anon. (1972) Brinkmann (1985) Nye and Greenland (1960) Servant et al. (1984) Bernhard-Reversat (1975) Kenworthy (197 1) Manokaran (1980) Golley et al. (1975) Turvey (1974)

24.8 23.4 27.0 3.4 Jordan et al. (1980) 16.7 - 16 - Jordan (1982) 24.9 24.6 28.4 3.5 Jordan et al. (1980) 26.9 11.6 11.6 3.0 Jordan (1982)

0.5 -

1.1

7.3 3.6 1.3 8.9 6.4 19.8

Edwards (1982) Clements and Colon (1975) Grimm and Fassbender (1981b)

2.6 5.6 5.2

K Ca Source


that 50 per cent of the annual input of each element was received on the following numbers of rain days (of a total of 170): nitrogen, 3; phosphorus, 9; potassium, 8; sodium, 5; calcium, 1, and magnesium, 1. Nutrient input in rainfall is likely to be fairly uneven in rainforest areas with more equable rainfall and may be greatly influenced by smoke from shifting agriculture or rarer events. Kellman et al. (1982) found evidence that volcanic activity 300km distant resulted in an increase in nutrient input even though their measurement site was well beyond the normal ash fall zone.

There are no rainforest measurements for soluble materials that are impacted upon plant surfaces as cloud droplets or dry aerosols and subsequently washed off by rainfall. The few data that are available on this phenomenon for temperate regions suggest that inputs received in this way may equal those received as bulk precipitation on horizontal surfaces (White and Turner 1970; Miller 1979a, 1979b; Miller and Miller 1980). The temporal variability of effective inputs to ecosystems by this pathway is likely to be high, especially during dry seasons when washoff by rainfall occurs infrequently.

A further unknown concerns the efficiency of uptake of nutrients from atmospheric sources, since sporadic heavy rainfall may largely flow from the ecosystem. The soil moisture storage capacity, the frequency and magnitude of precipitation and influx of nutrients, and differing abilities of species to take up nutrients are all likely to be involved. It is likely that epiphytes play a major role in atmospheric nutrient capture and this has been reviewed by Benzing (1983).

There are virtually no data on inputs of nutrients from rock weathering into natural rainforest systems although Bruijnzeel (1983) has shown this source to be important in his work on forest plantations in Java. Baillie and Ashton (1983) provided indirect evidence which suggested that substantial quantities of nutrients may be supplied by rock weathering to undisturbed rainforest. They observed that ‘reserve’ (i.e. hydrochloric acid extractable) quantities of elements correlated better than exchangeable quantities with an ordination of a large number of plots in Sarawak dipterocarp forests. This led to their suggestion that the less labile forms ot elements may be supplied by rock weathering and influence vegetation composition.

Nitrogen input by biological fixation is not properly quantified for any tropical forest but must often be the principal means by which nitrogen is added. The identity of the organisms responsible for the nitrogen fixation is not known with certainty. Sylvester-Bradley et al. (1980) estimated that annual nitrogen inputs to Amazonian rainforests via noduled legumes are c. 1 .5-2.5 kgham I in forests on oxisols, c. 20 kgha- I in campina vegetation on ultisols, and over 240 kg ham I on fertile ‘varzea’ soils. Nitrogen fixation by blue-green algae and non-symbiotic soil bacteria is probably usually at low rates but good data are lacking. Collins (1983) has discussed nitrogen fixation by the bacteria in termite guts but the total quantities fixed by this method must be small.

Ecosystem nutrient loss

Estimates of nutrient loss from rainforests are very difficult. Two methods have been used: measurements of nutrients in stream flow and lysimetry. The first method depends on finding sites where streams emerge from clearly defined watersheds over- lying impermeable strata. The method has been used in the classic temperate forest studies at Hubbard Brook, USA (Likens 1985) and there are smaller-scale examples in the tropics by Kenworthy (1971) and Turvey (1974). Even assuming that good sites can be found, streamwater analyses may not account for the removal of particulate matter (including large and small litter as well as soil particles). Dudgeon (1984) has

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Table 4. Amounts (kgha- ’ yr ‘) of elements in rainfall, canopy enrichment (throughfall minus rainfall), stemflow (where data are available), litterfall and total [rainfall, canopy enrichment (and stemflow) and litterfalll for tropical forests

N P K Ca Location

Lowland forest

Australia Site 1 Rainfall

Enrichment Litterfall Total

Site 2 Rainfall Enrichment Litterfall Total

Brazil Rainfall Enrichment Litterfall Stemflow Total

Ghana Rainfall Enrichment Litterfall Total

Ivory Coast Banco, Rainfall

Plateau Enrichment Litterfall Total

Banco, Rainfall Valley Enrichment

Litterfall Total

Yap0 Rainfall Enrichment Litterfall Total

Panama Rainfall Enrichment Litterfall Total

Lower rnontane forest

New Guinea Rainfall Enrichment Litterfall Total

Puerto Rico Rainfall Enrichment Litterfall Stemflow Total

Mg Source

4 121 64

192

4 93 56

144

3 47

211 268

2 Brasell and Sinclair 23 (1983) 29 62

3 Brasell and Sinclair 18 (1983) 36 50

0.2 Brinkmann (1985) 6.6

14.5 2.1

23.3

53 171 198

0.3 10.2 18.2 5.8

34.5

12 29

206 247

0.4 0.5 2.1 0.6 3.6

0.41 3.7 7.3

11.4

2; 105

15 145

14 12.3

200 226.3

-

18 220

68 306

11 18 45 74

7 34 51 92

7 41 36 86

7 16 23 46

5 10 22 37

Nye (1961)

21.2 2.3 58.8 -0.1

170 8 250 10.2

21.2 2.3 59.8 7.5

158 14 239 23.8

21.2 2.3 11.8 3.7

113 4 146 10

5.5 59.5 28 93

5.5 169.5 81

261

5.5 82.5 26

114

9 50

129 188

30 9

61 100

30 17 85

132

30

Bernhard-Reversat (1975)



Golley et al. (1975)

105 140

29 37

240 306

0.6 8.6

10.2

6.5 0.53 23.1 2.0 91 5.1

120 7.6

7.3 3.6 1.3 Edwards (1982) 63 ‘8 15.4 9.6 28 95 19 99 114 30

8.9 6.4 19.8 Clements and Colon 79 25.8 47.5 (1975)

7.0 81.8 10.2 3.8 1.2 1.6

98.7 115.2 79.1

John Proctor 145

Table 4 (contd)

Location N P K Ca Mg Source

Venezuela Rainfall 9.9 1.1 2.6 5.6 5.2 Fassbender and Enrichment 8.5 1.4 69.7 6.9 3.3 Grimm (1981) and Litterfall 69.1 4.0 33.1 43.1 14.4 Grimm and Stemflow 0.06 0.02 1.0 0.12 0.04 Fassbender (1981b) Total 87.6 6.5 106.4 55.7 22.9

given an account of various processes in tropical streams which help return forest nutrients lost in them. Lysimetry involves collecting soil water draining by gravity (zero-tension lysimetry) or by suction (tension lysimetry). With both methods there are problems of adequate replication in heterogeneous soils. The relevance and relative merits of tension and zero-tension lysimetry are controversial and Russell and Ewe1 (1985) have made a recent contribution to the discussion.

There are few studies (Tables 2 and 3) which have combined analyses of precipitation with those of drainage water. The data are sparse and show no general picture of nutrient conservation. In some cases there is a substantial annual net loss of nutrients.

Losses of nitrogen by denitrification and volatilization of ammonia are not quantified for rainforests. Servant et a/. (1984) have estimated that about 15 per cent of the nitrogen mineralized annually in the soils of some rainforest areas in the Ivory Coast escapes into the atmosphere.

Cycling of nutrients within ecosystems

It is useful to recognize two kinds of mineral turnover in rainforests: one is a fairly rapid cycle in small litterfall, throughfall and stemflow. The other is a slower cycle of nutrients incorporated into large woody parts, which follows the regeneration phase of the vegetation. Obviously the two processes are not separate and the distinction is somewhat arbitrary.

Relatively rapid nutrient cycling. Measurements of small litterfall are theoretically straightforward but there are many pitfalls. Proctor (1983) has critically reviewed the methodology and has pointed out the difficulties with trap size and replication, sample size within the forest, length of the measurement period, length of period between samples, and the definition of the litterfall size fractions. Proctor (1984) has summarized the information on small litterfall. The recorded amounts of small litterfall in studies from lowland rainforests vary from 3.4 t ha- I yr- I [in the Western Chats in India (Rai and Proctor 1986)] to 15.1 t ha - I yr - 1 in a Rhizophora mangrove in Malaya [Sasekumar and Loi (in Proctor 1984)]. Nutrient contents of small litterfall vary greatly and the following ranges (in kg ha- I yr- i) have been recorded (calculated from Proctor 1984: Table 7): nitrogen, 8-223; phosphorus, O-4-18.2; potassium, 1 .O-100; calcium 7.7-372; magnesium 1.1-64.

Throughfall is the rain which falls through the canopy; stemflow is the rainwater which is channelled down the stems. There is a comprehensive review of forest


throughfall and stemflow in Parker (1983). Both throughfall and stemflow leach nutrients from the surfaces of the plants as part of the cycle within the ecosystem. The extent to which minerals are leached from a forest canopy depends on such factors as temperature, rainfall, the residence time of water on leaves and the leaf area index. Throughfall and stemflow will also wash off insect frass, fixed nitrogen from the phyllosphere, and allochthonous nutrients. Nutrients may also be lost by absorption into leaves and aerial roots and adsorption on to plant surfaces. In general there is an enrichment of throughfall but Jordan et ul. (1980) have reported substantial reductions in concentrations (in throughfall compared with rainfall) of phosphorus, calcium and sulphur for two Amazonian rainforests. There are substantial differences amongst the nitrogen enrichment values. It seems likely that these involve different amounts of nitrogen fixation on the leaf surfaces or possibly in the rain collectors. Edwards (1982) claims that nitrogen is not readily leached from leaves.

The proportion of rain in throughfall and stemflow varies with the duration and intensity of rainfall. Kenworthy (1971) found that in a Malayan forest 4.5 mm of rain was needed before there was any throughfall. Such rain is said to be intercepted by the canopy and evaporates directly from the leaves. At the other extreme, 99 per cent of a single heavy storm was throughfall at another site in Malaya (Manokaran 1979). Averaged over a long term it seems that 66-86 per cent of precipitation forms throughfall in tropical forests: examples include a site in Uganda, 66 per cent (Hopkins 1960); in Ghana, 84 per cent (Nye 1961); in Puerto Rico, 70 per cent (Jordan 1970); in Malaya, 78 per cent (Manokaran 1979); in New Guinea, 68 per cent (Edwards 1982); and for two sites in Australia, 76 per cent and 86 per cent (Brasell and Sinclair 1983). Stemflow is a minor component overall being 1 per cent of rainfall in New Guinea (Edwards 1982), Pasoh (Manokaran 1979), and Venezuela (Grimm and Fassbender 1981 b), although Raich (1983) has reported that it was 9 per cent of the rainfall at La Selva, Costa Rica.

Table 4 summarizes data for situations where small litterfall and throughfall measurements have been made simultaneously. The relative importance of these pathways varies from element to element and from site to site. In general, potassium has a faster circulation in throughfall, whilst the other elements have a faster circulation in litterfall.

The elements in litterfall are less mobile than those in throughfall and they are not immediately available for redistribution within the ecosystem. There are important factors in the pattern of the availability and cycling of each element such as the proportion of the input that is derived from litterfall, the seasonal distribution of litterfall, and the rate of loss of each element from litterfall on the forest floor. The last involves the process of decomposition by which organic matter is broken down to release the nutrients (and carbon dioxide). The breakdown is mediated by animals, fungi and bacteria and involves an initial mechanical phase of breaking into smaller pieces followed by chemical action.

A common misconception is that decomposition in tropical forests is invariably rapid. Anderson and Swift (1983) have critically discussed this idea and described many of the complexities. They have shown that decomposition rates in tropical forests may be fast or relatively slow.

The three most widely used measures of litter decomposition are soil respiration, litterfall/forest floor litter quotients (kt_ values) and direct measurements of weight losses from litterbags. It is now accepted that soil respiration measurements cannot be used as a measure of decomposer activity because there is a lack of quantification of the root respiration components. Provided that the same components of the

John Proctor 147

Table 5. Litterfall, forest floor litter and turnover coefficients (kL) for a range of tropical forests

Lowland rain forest Brazil

Leaves

Ghana Leaves

Ivory Coast Banco

(Plateau) Leaves Yap0

(Plateau) Leaves

Malaya Pasoh

Leaves Penang

Leaves

Panama Leaves

Sarawak Alluvial

forest Leaves Dipterocarp

forest Leaves Heath forest

Leaves Forest over

limestone Leaves

Lower montane forest

Turnover coefficient Forest floor (kr)

Litterfall litter _~ (tha-‘yr-‘) (tha-t) Leaves Small litter

7.6 7.2 6.1 4.0

9.7 4.9 7.4 3.0

8.2

6.6

10.6 3.2 6.3 I.7 7.5 7.7 5.4 5.1

13.3 11.2 7.0 2.8

9.4 5.5 6.6 3.8 7.7 5.9 5.4 3.2 8.1 6.1 5.6 3.9

10.4 7.1 7.3 4.2

2.5

I.8

I.5

2.5

3.3

3.6

3.6

I.1

2.6

I.8

I.7

I.4

I.7

New Guinea 6.8-7.6 6.1-7.7

Puerto Rico Leaves 4.8 5.1 0.9

Upper montane forest

Source

1.1 Klinge (1973)

2.0 John (1973)

Bernhard (1970)

3.3

I.0

I.2

Ogawa (1978), Y oda ( 1978) Gong and Ong (1983)

1.N.HealeyandM.J. Swift (unpublished)

I.7

I.3

Anderson et al. (1983)

I.3

I.5

1.0-1.4 Edwards (1977)

Wiegert (1970)

Jamaica Leaves 4.9-5.5 8.1-11.7 0.5-0.7 Tanner (1981)

Nofe: Values are for total small litter (i.e. leaves, fruits, twigs and small branches, generally less than 2.5-5cm in diameter, but size often undefined), except where leaves are specified

litterfall and forest floor litter are compared, k, values are useful. Unfortunately, many of the older studies have lumped forest floor litter with total soil organic matter and this results in spuriously low k, values. The interpretation of weight losses from litterbags is difficult because the bags introduce a series of artefacts by excluding some animals and altering the moisture regime of the litter.

Table 5 collates k, values from asnumber of tropical forests and shows that for most the litter turnover takes less than a year (i.e. k = 1). However, there is a wide range (1.1-3.3) and some are within the values exhibited by temperate forests (0.4-l 04). Results for litterbag studies (Table 6) have shown a similarly large


Table 6. Percentage weight losses from leaves in litterbag studies made in tropical forests

Bag mesh

Lowland forests

Brazil Ivory Coast Nigeria Panama

Sarawak

Lower rnontane forest

New Guinea

Upper montane forest

Jamaica

(> 10mm) (<2mm)

35-80 153-212

219-548 150-352 120-183

52-61 53-65

26-95 Edwards (1977)

27-96 Tanner (1981)

Source

lrmler and Furch (1980) Bernhard-Reversat (1972) Madge (I 965) 1. N. Healey and M. J. Swift (unpublished) Anderson et al. (1983)

No/e: Studies were carried out over differing periods of’ time and the results are expressed a, per cent yr-’

variation and overlap with the rates observed in temperate studies. The causes of the variation in decomposition rates are to be sought in the nature of the decompose1 community (the animals and the micro-organisms); the characteristics of the organic matter which determine its degradability (resource quality) and the physicochemical environment. The relative importance of these variables is different from site to site and from resource to resource (leaves, wood, fruits, etc.). The release of nutrients from decomposing material is not simple and it is probably commonplace for them to be temporarily removed from other sources by avid uptake by micro-organisms on substrates where nutrients are limiting. Anderson et ul. (1983) have given examples ot different rates of nutrient release during decomposition of leaves in litterbags.

A Gdespread generalization about rainforests is ‘direct nutrient cycling’, which was proposed by Went and Stark (1968a,b). This idea envisages that mycorrhizal fungi cycle nutrients by breaking down organic matter and transporting the nutrients directly to the host trees. ‘Direct nutrient cycling’ has been critically discussed by Janos (1983), who has pointed out that whilst it is known for some orchid species, it remains unproven for tropical trees since their fungi apparently lack the enzymis capability to break down litter. This is not to say that mycorrhizas are unimportant in mineral nutrient cycles. They are undoubtedly efficient at ion uptake e\;en if exoenzymes of other micro-organisms break down the organic matter.

Kelati\v/J S/OH, ttutrirnt c;vcli~~g. There is little information on the slower cycle of nutrients because we know 1i:tle of forest gl-owth rates in general and sampling large dead trunks is dift’icult. Even rates of large branch fall are little known. Brasell and Sinclair (1983) have made an estimate of the elements circulated in large branch fall and their results, which they admit are not reliable, at least indicate that substantial quantities of nutrients may move by this pathway.

Tanner (1985) estimated stem nutrient contents and combined these with earlier measurements of growth increments (Tanner 1980) to make a useful preliminary calculation of the nutrients required to make one year’s trunk growth increment in ‘mar ridge’ and ‘well-developed mull ridge’ upper montane forest in .Jamaica. On the ‘mor ridge’ the following were required (in kgha ‘year I); nitrogen, 0.75;

John Proctor 149

phosphorus, 0.055; potassium, 0.5; calcium, 0.7 and magnesium, 0.3. On the ‘well- developed mull ridge’ the requirements were: nitrogen, 2.3; phosphorus, O-11; potassium, 2.3; calcium, 2.6 and magnesium, 0.5. These values are less than 2.5 per cent of the instantaneously extractable nitrogen and exchangeable potassium, calcium and magnesium. Tanner had no measure of soil phosphorus. Tanner (1985) discusses the shortcomings of the estimates but it seems reasonable to conclude that relatively small quantities of nutrients are immobilized in new wood each year in his forests. A similar conclusion was reached for lowland forests in the Ivory Coast by Bernhard-Reversat et a/. (1978) although their methods are described in less detail.

Also included in the slower cycle of nutrients are those nutrients which are incorporated into stable soil organic matter. These are slowly released by decomposition and the rate has been usefully quantified for nitrogen by De Rham (1970), Tanner (1977), Lamb (1980), Robertson (1984) and Vitousek et al. (1983).

Conclusion

Nutrient cycling in little disturbed tropical rainforests is immensely complicated and so far we have nothing more than glimpses at some aspects of the process in a few of them. The assumptions which are often held have been shown to be based on insufficient evidence and there is a need for much more research into the nutrition of rainforests if we are to evaluate the consequences of their destruction and the best methods by which they can be managed for sustained production.

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(Revised manuscript received 14 July 1986)

nutrient cycling in primary and old secondary rainforests

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