Mineral Nutrition and Die-Back in Terminalia Ivorensis A. Chev. in Ghana

Mineral nutrition and die-back in Terminalia ivorensis A. Chev. in Ghana

VICTOR K AGYEMAN* and E. Y. SAFOf

*Forestry Research Institute of Ghana and fDepartment of Crop Science, University of Science and Technology, P.O. Box 63, Kumasi, Ghana.

ABSTRACT. This investigation examined the hypothesis that nutrient deficiency is related to the die-back of Terminalia ivorensis. The study was conducted on three major soil groups in natural forest and T. ivorensis plantations. Five soil chemical factors, Total nitrogen, organic carbon, effective CEC, exchangeable calcium and magnesium, were positively related to die-back. Foliar nitrogen concentrations in trees suffering from die-back were almost 50% of those of healthy trees. The concentrations of magnesium in the leaves of T. ivorensis experiencing die-back were also low. Conversely, high concentrations of foliar calcium were associated with trees under stress. A highly significant relationship was observed between die-back ranks and leaf size.

KEY WORDS: die-back, Ghana, plantation, tropical forest, Terminalia ivorensis, soil chemical properties, foliar nutrient concentrations.

INTRODUCTION Terminalia ivorensis A. Chev. occurs naturally in a geographic region extending along the West African sub-region which receives between 1200 and 1800 mm rainfall per annum. The species is a strong light demander and must have overhead light for good early growth. It is not thought to be a long-lived tree (Taylor 1960). In Ghana, T. ivorensis is distributed throughout the forest zone, but achieves its greatest density in forest reserves within the south-east subtype of moist semi-deciduous forest (Hall & Swaine 1981). Terminalia ivorensis was the most popular tree for reforestation in Ghana during the period between 1950-1970. This is because it is fast growing, self- pruning, and has a straight bole and excellent form (Lamb & Ntima 1971). Nearly 100 different plantations of T. ivorensis totalling 2500 ha had been established on a wide range of sites at 28 locations/forest reserves scattered throughout Southern Ghana by 1970 (Canon 1979). It is estimated from the Forest Inventory Project data (unpublished) that by 1985 c. 3600 ha of T. ivorensis plantations had been established in the country. However, by 1975 about 34% of T. ivorensis plantations in Ghana had suffered die-back (Canon 1979). Cur- rent estimates from the Forestry Department of Ghana reveal that die-back

317 318 VICTOR K. AGYEMAN AND E. Y. SAFO has affected 50-60% of the plantations. Because of the die-back problem the establishment of the tree in plantations was virtually stopped in the 1980s. Die-back occurs throughout the entire West African region especially, Ghana and Cote d'lvoire where extensive plantations of the species exist. It is however, more common in the wet evergreen forests than other forest types (Canon 1979) and affects T. ivorensis plantations between the ages of 10-20 y. The disease is primarily characterized by the cessation of growth leading to deterioration over a period of time and ultimately death. The first obvious indicators of die-back are wilting and abnormally chlorotic and diminutive leaves (Ofosu-Asiedu & Canon 1976). Following leaf fall the branches and branchlets begin to die and the sapwood becomes stained. When an entire branch is dying back, branchlets at the extreme distal portion have smaller leaves and lose their leaves' faster than branchlets which are closer to the main branch. Malagnoux (1973) observed that growth cessation occurred 2y before the symptoms of the disease appeared. In a study of a 5-ha increment plot in a 30-y old plantation of T. ivorensis at Pra-Anum Forest Reserve in Ghana, Jones (1969) noted that almost all the trees died within 10 y after the inception of the disease in the plot. Several hypotheses have been put forward as to the possible cause of die- back. De Neef (1975) argued that die-back might be attributed to root competi- tion. Ofosu-Asiedu & Canon (1976) noted the frequent association of a fungus, the imperfect stage of Endothia species, with die-back. However, pathogenicity tests undertaken by Canon (1979) showed that the fungus was not the primary cause of die-back and only attacked trees which are already under extreme water and defoliation stress. Malagnoux (1973) noted that the disease was associated with the cerambycide beetle, Plocaederus viridipennis (Hope). How- ever, later studies by Brunck & Malagnoux (1976) showed that the Ceramby- cide beetle and other insects were strictly secondary pests which attacked trees already under stress through leaf defoliation. Other studies into the causes of die-back involving thinning (De Neef 1975), water stress (Canon 1979, Malagnoux 1973) and soil drainage (Canon 1979) were inconclusive. However, the results have led some workers (Bernhard-Reversat 1974, Brunck & Malagnoux 1976, Canon 1979) to suggest that mineral deficiency might be the cause of the disease. An earlier study by Canon (1979) revealed that the number and density of T. ivorensis trees in the natural forest was not significantly related to any geographic location or feature but was related to the great soil groups of Ghana as classified by Charter (Bramrner 1962). In order to investigate the relationship of soil chemical properties as well as foliar nutrient concentrations and die-back, this study was carried out on T. ivorensis growing on different soil types in Ghana. It is generally known that several conditions limit the effect- iveness of soil tests for evaluating the nutrient requirement of tree plants and Mineral nutrition and die-back in Terminalia 319 that any effective method of plant diagnosis for nutrient deficiency should include both soil and foliar analysis (Foth 1978, Lutz 1951).

MATERIALS AND METHODS Study sites The study involved three major soil groups in the forest zone^of Ghana on which T. ivorensis grows extensively. These soils are classified locally as: (a) Forest ochrosols (luvisols, acrisols and cambisols (FAO-UNESCO 1974) or alfisols and ultisols (Soil Survey Staff 1975) ). (b) Forest ochrosol-oxysol integrades (ferralsols, acrisols and luvisols (FAO-UNESCO 1974) or oxisols, ultisols and alfisols (Soil Survey Staff 1975)). (c) Forest oxysols (ferralsols, gleysols and acrisols (FAO-UNESCO 1974) or oxisols, inceptisols and ultisols (Soil Survey Staff 1975)). The oxysols are highly leached and acidic with a very low nutrient status (Brammer 1962). The ochrosols are relatively well-drained, neutral to slightly acidic and better supplied with nutrients. There is no sharp boundary between the ochrosol and oxysol soil groups. The variation represents a continuum (Nye & Greenland 1960). Nine sites were chosen, three on each soil group. The three sites on each soil group were: (i) plantation with die-back; (ii) plantation without die-back; and (iii) natural forest. Details of the selected sites are shown in Table 1.

Table 1. Summary of sites sampled on three great soil groups in the forest zone of Ghana. Mean annual rainfall and mean daily temperature were taken over a period of 5 y.

LOCATION CLIMATE Lat. Long. Alt. Annual Daily (°'N) (0/W) (m) rainfall temp. SOIL GROUP' Reserve (mm) (°C) FOREST TYPE2 Ochrosol South 6 35 0 57 180 1490 27.3 Moist Formangsu semi-deciduous, S/E Subtype Jimira 6 30 1 54 190 1280 27.4 Moist semi-deciduous, N/W subtype Bobiri 6 38 1 16 150 1295 27.4 Moist semi-deciduous, N/W subtype

Ochrosol-Oxysol Denyau 6 02 1 47 80 1565 Moist evergreen Intergrade (2 sites) Tonton 6 04 2 05 90 1590 — Moist evergreen

Oxysol Nueng-North 5 09 2 01 40 1650 Wet evergreen (2 sites) Nueng-South 5 05 2 05 55 1650 — Wet evergreen ' After Brammer (1962) 2 After Hall & Swaine (1981) 320 VICTOR K. AGYEMAN AND E. Y. SAFO

In selecting the sites for sampling, conditions which might contribute to die-back or affect nutrient imbalance in the soil and foliage of trees were con- sidered. These were that: (a) fire should not have swept through the plantation after its establishment; (b) food crops should not have been cultivated on the land after its establishment, and (c) other tree species should not have been planted together with the Terminalia.

Plantation with die-back. On these sites, distinct phases of deterioration were identified as follows: (a) Trees completely dead with no leaves — Rank 1 (b) Trees with bark starting to peel off, some of the branches broken and with chlorotic and diminutive leaves (middle stage of die-back) — Rank 2 (c) Trees with bark and branches intact but having chlorotic and diminutive leaves (inception of die-back) — Rank 3 (d) Trees with healthy leaves — Rank 4 Two 1.0-ha plots were demarcated, each containing several patches of die-back and healthy trees for soil nutrient analyses. Within the two 1-ha plots in each soil group, 20 trees (five trees in each of the four ranks mentioned above) were chosen. Altogether 60 trees were chosen in plantations with die-back in the three soil groups.

Plantations without die-back. Since die-back patches appear to expand over time (Ofosu-Asiedu & Canon 1976) a plantation area without die-back which was almost of the same age (15-17 y) as the plantation experiencing die-back and occurring nearby in the same soil group was chosen as an example of T. ivorensis not currently at risk from die-back. A 1-ha plot was demarcated and five trees were chosen at random. A total of 15 trees were chosen in the three soil groups. These trees were designated as rank 5.

Site in the natural tropical forest. A total of 15 mature, healthy T. ivorensis trees (estimated to be over 100 y old) growing in the natural forest were chosen and designated rank 6. Five trees were chosen on each of the three soil groups. It was assumed that soil conditions under the trees were optimal for the growth of T. ivorensis since it had supported the trees to maturity.

Soil sampling and analysis To assess soil nutrient concentration, 270 soil samples were collected. Under each of the 90 trees, one soil sample was collected from each of three soil depths (0-20, 20-40 and 40-65 cm) at 1.5 m away from the tree. These depths were chosen based on the fact that young trees (those grown on a pulpwood rotation) need an effective rooting depth of only 40 cm, while old trees (those grown for timber) require about 65 cm effective rooting depth to achieve a plantation survival rate of 90% (Canon 1979). The soil samples were air-dried, crushed to pass through a 2-mm sieve and used for analyses. Soil analysis were Mineral nutrition and die-back in Terminalia 321 made in the Soil Science Laboratory of the University of Science and Techno- logy, Kumasi. The laboratory has been accepted and contracted by the Interna- tional Atomic Energy Agency (IAEA - Vienna) to carry out research into nitrogen fixation by trees. Soil total nitrogen was assessed by the Kjeldahl macro-digestion technique (Bremner 1965). Available phosphorus was determined using the Bray PI extraction procedure (Bray & Kurtz 1945). Soil pH was measured with a glass electrode and a soil-to-water ratio of 1 : 2.5. Exchangeable cations were extracted with 1.0 N neutral ammonium acetate solution (Thomas 1982). Pot- assium and sodium were determined using the flame photometer and calcium and magnesium using the EDTA compleximetric titration method. Exchange- able acidity (aluminium and hydrogen) was determined by the titration method after extraction with 1.0 N potassium chloride (Thomas 1982). Effective cation exchange capacity (CEC) is the sum of 1.0 N NH4OAc exchangeable bases plus 1.0 N KC1 exchangeable acidity. Water soluble sulphate-sulphur in the soil was measured turbidimetrically after extraction with water and charcoal (Wimberley 1968). Organic carbon (OC) and organic matter (OM) were determined by the standard Walkley-Black procedure (Allison 1965).

Tree parameter measurements In an attempt to quantify the subjective deterioration assessment, a number of tree parameter (morphometric) measurements were made on trees from each of the rankings. Leaf size was measured by cutting down the lowest branch from the selected trees. Mean length and width of 20 randomly selected leaves found on the last branchlets (those closest to the main branch) were measured. These leaves according to Ofosu-Asiedu & Canon (1976), are larger than all other leaves. Tree height was measured with a clinometer and girth with a tape at 1.3 m.

Foliar sampling Foliar samples were collected from three trees randomly selected from each rank. A total of 45 trees (15 in each soil group) were assessed. Samples could not be collected from rank 1 because the trees were dead with no leaves. Terminalia ivorensis is deciduous, producing leaves between March-April and dropping leaves between January-February. Leaf material was collected at the end of the rainy season in July/August by which time the leaves are fully developed. Leaves therefore were all of even-a,ge.

Foliage analysis The foliar samples were oven-dried at 70 °C for 48 h ground in a mill using a sieve opening of 0.05 mm before total elemental analysis. Nitrogen was determined as described for soils. Phosphorus, potassium, calcium, magnesium and sulphur were determined after dry ashing in a muffle furnace at 450 °C for 322 VICTOR K. AGYEMAN AND E. Y. SAFO

8 h. After cooling, the ash was digested with 1.0 NHC1 on a hot plate. Phos- phorus was determined using the vanado-molybdate method (Association of Official Analytical Chemists 1970). For potassium, calcium and magnesium, the methods for soils were used. Sulphur was assessed turbidimetrically (Wimberley 1968). Reference samples of old and new leaves from healthy T. ivorensis trees in plantations were analysed at the Department of Biological Sciences of Manch- ester University. The mean foliar nitrogen concentration obtained in that laboratory was 26.6 mg g"1 for new leaves and 15.1 mgg"1 for old ones. The results were not significantly (P>0.05) different from the mean concentration of 28.0 mg g"1 for new and 17.2 mg g"1 for old leaves obtained at the Soil Sci- ence Laboratory of the University of Science and Technology.

RESULTS Leaf size and die-back The relationship between tree height, girth and leaf size and die-back ranks were examined with a view to developing a more accurate field assessment scheme for die-back ranks. For T. ivorensis trees between the ages of 15 and 17 y growing on all three soil groups the height and girth ranged from 28.9 to 35.6 m and 1.13 to 1.51 m respectively (Table 2). The growth variables (Table 2) were subjected to a two-way analysis of variance with die-back rank and soil type as the main factors (Table 3). Height and girth for trees of similar age were not significantly (P>0.05) related to die-back in the plantations (Table 3), even though growth cessation occurs 2 y before the symptoms of the disease appear. Leaf width ranged from 2.3 to 5.0 cm and leaf length from 6.9 to 13.2 cm (Table 2). Leaf length and leaf width were significantly (P<0.001) related to the levels of die-back (Table 3). Differences between the leaf sizes of healthy trees and those experiencing die- back were also significant (Table 3).

Soil depth and die-back The relationships between concentration of soil nitrogen, magnesium and calcium in each of the three soil depths, and die-back ranks in the forest Ochro- sol soil group (Figure 1) were similar. These relationships were also similar for all the three soil groups. This suggests that the influence of soil nutrients on die-back is independent of the depth in the soil from which the nutrients may be drawn. Therefore, only concentration of soil chemical properties in the 0-20 cm depth which showed pronounced relationships with die-back are presented and discussed in the following section.

Soil chemical properties and die-back The concentration of most soil chemical properties, with the exception of aluminium and hydrogen, were lower in the oxysols than the other soil groups Table 2. Mean height (Ht), girth (Gt), leaf length (Lt) and leaf width (Lw) for Terminalia ivorensis trees in the different die-back/tree ranks growing on fores t ochrosol, ochrosol-oxysol intergrade and oxysol soil groups. Tukey' s HSD tests for trees growing in plantations (ranks 1-5) are presente d as superscripted letters in each column: Values with the same letters in any one column are not significantly different. 1

Ochrosols Ochrosols-oxysols Oxysols Tree Tree Leaf Leaf Tree Tree Leaf Tree Tree Leaf Leaf Die-back Leaf Ht Gt Lt Lw Ht Gt Lt Lw Ht Gt Lt Lw rank Site (m) (cm) (cm) (cm) (cm) (cm) (cm) (cm) (cm) (cm) (cm) (cm) Plantation (die-back) 1 33.3 1.43 30.3 1.23 29.2 1.15 2 33.0 1.39 2.3" 31.2 1.20 7.3' 2.4" 31.5 1.18 6.9' 2.3* 7.6* b b 3 35.6 1.50 9.9" 3.3" 31.1 1.23 9.4" 3.4 30.3 1.13 9.2 3.1" 4 33.4 1.47 12.3" 4.6' 30.5 1.21 12.0° 4.2' 28.9 1.20 12.0' 4.0' 12.8b C Plantation (no die-back) ' 5 31.6 31.6 4.8' 31.0 1.17 12.9' 4.4° 29.8 1.16 12.4 4.0'

Natural forest 6 49.9 2.54 13.2 5.0 49.3 2.41 13.0 4.7 46.2 2.26 12.7 4.5 1 Where no small letters are shown in a column there are no significant differences 324 VICTOR K. AGYEMAN AND E. Y. SAFO

Table 3. Summary of analyses of variance for four Terminalia ivorensis tree parameters (meanisn Table 2). Sixty trees were used for height and girth while 45 trees were used for leaf length and width. Die-back Site Die-back x Site df F P df F P df F P Tree height 4 0.15 ns 2 3.29 * 8 0.24 ns girth 4 0.10 ns 2 18.43 ••* 8 0.24 ns length 3 11.17 »*• 2 0.19 ns 6 0.01 ns Leaf width 3 7.61 **• 2 0.58 ns 6 0.14 ns * P < 0.05; •*• P < 0.001; ns = not significant (P > 0.05)

(Table 4). The higher concentration of aluminium and hydrogen in the oxysols compared to the other two groups may have been due to the acidic nature of the soil. The data also show that most of the soil nutrient concentrations were higher in healthy plantations and the natural forest (die-back ranks 4-6) relat- ive to those experiencing die-back. The effective cation exchange capacity (CEC) involves the summation of exchangeable calcium, magnesium, potassium, sodium, aluminium and hydrogen. In the ochrosol soil group the mean effective CEC (index of nutrient availability) for natural forest and healthy plantations was 146 me kg"1 while that in die-back plantations was 75 me kg"1 (Table 4). In the oxysols the aver- age value for natural forest and healthy plantations was 48 me kg"1 while that for plantations with die-back was 33 me kg"1. The mean effective CEC value in the topsoil (0-20 cm) of the natural forest (rank 6) ranged over the three soils from 55 to 148 me kg"1. These values were higher than those under T. ivorensis plantations with and without die-back which ranged correspondingly from 40 to 74 me kg"1. This suggests that nutrient cycling may be more efficient in the natural forest than in T. ivorensis plantations. Soil variables (Table 4) were subjected to a two-way analysis of variance for factors die-back ranks and soil type (Table 5). Sodium (Na), potassium (K), aluminium (Al), hydrogen (H), available phosphorus (P), soluble sulphate- sulphur (Sol. SO4) and pH were not significant at P>0.05. However, total nitrogen (N), organic matter (OM) and effective CEC were significant for die-back ranks but not soils. Calcium (Ca) and magnesium (Mg) on the other hand showed significant differences for both die-back ranks and soils. Based on the results in Table 5, only mean values of total nitrogen, organic matter and effective CEC over the three soils for each die-back rank are presented in Table 6, while means of foliar nitrogen, calcium and magnesium concentrations for both soils and die-back ranks are presented in Table 7. To assess the relationship between die-back ranks and soil chemical factors in each of the soil groups, Kendall's tau-B rank correlations were performed using 15 trees for each of the six ranks (Table 8). This showed that the soil chemical properties which were related to die-back were similar in all the soil groups. Mineral nutrition and die-back in Terminalia 325

1.0 2.0 3.0 4.0 5.0 6.0 Die-back/Tree Ranks s100 I 50

125 i 0 1.0 2.0 3.0 4.0 5.0 6.0 Die-back/Tree Ranks s2.0 I1-5 I 1.0 -

j g0.5 OS § •1 1.0 2.0 3.0 4.0 5.0 6.0 Die-back/Tree Ranks

Figure 1. Mean nitrogen, calcium and magnesium concentration at 0-20 •, 20-40 • and 40-60 ^ cm soil depths beneath Terminalia ivorensis trees in six different die-back ranks. Means are the averages of five values. Bars show ± 1 standard error.

Foliar nutrient content and die-back The mean foliar nitrogen concentration of healthy trees are 14, 11 and 9 mg g"1 in the ochrosol, ochrosol-oxysol integrade and oxysol soil groups respectively (Table 7). These values were higher than the corresponding means of 5, 5 and 4 mg g"1 for trees experiencing die-back. Mean foliar nitrogen concentrations gradually increased with the health status of the trees from ranks 326 VICTOR K. AGYEMAN AND E. Y. SAFO

Table 4. Mean (± SE) chemical characteristics of soil (0—20 cm depth) under Terminalia ivorensis in plantations and natural forests: (a) ochrosol, (b) ochrosol-oxysol intergrade and (c) oxysol soil groups.

Sites Plantation Plantation with die-back without Natural Diseased trees Healthy trees die-back forests n 15 5 5 5 (a) Ochrosols

C(mgg-') 11.3 ±0.9 18.4 ±1.5 14.8 ±1.6 15.7 ±1.3 OM(mgg-') 19.5 ±1.5 13.7 ±2.9 25.5 ± 2.4 27.1 ±2.6 Total N (mg g"1) 1.0 ±0.1 1.4±0.1 1.5 ±0.1 1.5 ±0.1 pH 5.9 ±0.3 5.9 ±0.3 6.3 ± 0.2 5.9 ±0.1 Exchangeable cations (me kg"1) Ca 49.1 ±1.6 58.0 ±2.6 96.0 ± 3.9 91.0±3.2 Mg 10.7 ±1.3 19.0 ±2.1 40.0 ±4.1 48.0 ± 3.4 K 0.2 ±0.1 0.3 ± 0.0 0.5 ± 0.0 0.3 ± 0.0 Na 1.5 ±0.1 1.7±0.1 2.6 ±0.1 1.4±0.1 Al 1.9 ±0.2 1.8 ±0.8 1.8 ±0.9 6.4 ± 2.3 H 1.6 ±0.6 1.8 ±0.7 1.8 ±0.8 2.2 ±0.5 CEC (me kg"1) 67.0 ±3.6 81.9 ±6.8 143.0 ±4.2 148.0 ±6.8 Avail. P(mg kg"1) 10.4 ±1.1 10.0 ±1.3 9.2 ±1.0 12.7 ±1.7 Sol. SO, (mg kg'1) 10.8 ±1.3 16.2±2.1 14.0 ±1.6 12.8 ±1.8 (b) Ochrosols-oxysols

C(mgg-) 10.8 ±0.5 17.1 ±4.7 13.6 ±3.3 18.4 ±3.1 0M(mgg-') 18.6 ±0.4 29.5 ± 6.4 23.4 ±5.2 31.7±4.9 Total N(mgg-') 0.8 ±0.1 1.2 ±0.3 1.5 ±0.4 2.3 ± 0.6 pH 4.8 ±0.4 4.7 ± 0.4 4.8 ±0.3 5.0 ± 0.3 Exchangeable cations (me kg"1) Ca 13.2 ±3.4 16.0 ±4.8 17.0 ±5.2 32.0 ±7.5 Mg 4.1 ±1.2 6.0 ±1.5 6.0 ±1.4 13.0 ±7.5 K 0.6 ±0.1 2.1 ±0.1 • 2.0 ±0.1 0.6 ± 0.0 Na 0.3 ±0.1 0.4±0.1 0.3 ±0.1 2.0 ±0.1 Al 8.7 ± 2.4 13.8 ±4.3 14.9 ±4.0 5.6 ±4.9 H 3.9 ±1.8 5.2±1.1 3.5 ±1.1 11.2 ±3.3 CEC (me kg"1) 29.9 ±3.5 43.5 ±5.5 39.2 ±3.3 70.1 ±4.0 Avail. P (mg kg"1) 10.9 ±1.1 12.2 ±1.5 11.5 ±2.9 5.7 ±2.1 Sol. SO4(mgkg-') 10.7 ±1.9 10.4 ±2.4 16.4 ±2.8 13.4 ±1.5 (c) Oxysols

C(mgg-') 10.4 ±0.6 13.5 ±0.4 13.9±1.0 15.8 ±1.4 OM (mg g"1) 17.9 ±0.4 23.3 ±0.7 24.0 ± 0.7 27.2 ±1.0 Total N(mgg-') 0.8 ±0.0 1.1 ±0.0 1.2 ±0.0 1.5 ±0.0 pH 4.3 ±0.0 4.5 ±0.0 4.5 ± 0.0 4.3 ±0.1 Exchangeable cations (me kg"1) Ca 6.5 ± 0.6 14.8 ±1.0 16.5 ±0.8 25.6 ±1.1 Mg 4.6 ± 0.5 5.8 ±0.8 6.2 ±0.7 10.2 ±0.1 K 0.7 ±0.1 0.8 ±0.1 0.9 ± 0.0 1.5 ±0.1 Na 1.3 ±0.2 I.I ±0.2 1.2 ±0.5 1.2 ±0.4 Al 12.6 ±0.9 7.6 ±1.4 8.4 ±1.4 10.0 ±1.2 H 4.1 ±0.3 5.6 ±0.3 5.8 ±0.4 9.0 ± 0.4 CEC (me kg'1) 31.3 ±2.5 35.7 ±3.5 39.0 ± 3.2 55.4 ± 3.4 Avail. P(mg kg"') 24.2 ±1.2 24.6 ±1.2 16.8 ±1.5 9.6 ± 1.2 Sol. SO4 (Mg kg"') 6.8 ±0.8 7.2 ±1.0 7.9 ± 0.8 10.4 ±0.8 Mineral nutrition and die-back in Terminalia 327

Table 5. F-values' and levels of significance2, using a two-way analysis of variance to test the relationships between (a) soil chemical properties and (b) foliar nutrient concentration and die-back in Terminalia ivorensis on three different soil groups. The analysis used results from 90 trees for soils (6 ranks) and 45 trees for foliar nutrients (5 ranks). [Rank 1 trees were leafless and could therefore not be sampled for foliar analysis].

Dieback Soil group Die-back x Soil group F P F P F P (a) Soils

OM 17.63 »»• 2.52 ns 1.67 ns Total N 22.84 •*• 4.05 * 2.68 ** PH 1.45 ns 125.29 *** 1.09 ns Ca 37.88 *** 538.80 **• 11.44 *** Mg 32.82 •** 170.99 *•• 19.75 *** Na 1.91 ns 2.26 ns 1.72 ns K 1.50 ns 3.34 * 1.38 ns Al 2.14 ns 2.57 ns 1.54 ns H 1.97 ns 2.82 ns 1.27 ns CEC 2.43 * 4.08 * 1.86 ns Avail. P 2.26 ns 2.46 2.01 * Sol. SO, 2.21 ns 3.21 * 0.68 ns (b) Foliar nutrients

N 975.68 *** 156.96 *** 50.45 *** Ca 50.90 *•• 46.16 **• 4.32 ** Mg 5.63 ** 3.21 * 1.66 ns P 1.22 ns 67.12 *•* 6.08 *** K 2.46 ns 28.45 *»• 1.96 ns S 0.31 ns 33.50 *** 0.43 ns ' df [die-back (soils)] = 5; df [die-back (foliar nutrients)] = 4; df [soil group] = 2; df [error (soil group)] = 72; df [error (foliar nutrients)] = 31 2 • P < 0.05, "PS 0.01, •*• P £ 0.001, ns = not significant (P > 0.05)

Table 6. Mean (± SE) organic matter (OM), total nitrogen (N) and effective cation exchange capacity (CEC) under 90 trees of Terminalia ivorensis in six die-back ranks.

Die-back rank OM(mgg-') N(mgr') CEC (me kg"') 1 18.0 ±0.96 0.86 ± 0.04 43.3 ± 4.95 2 18.1 ±1.13 0.86 ±0.03 41.0 ±5.20 3 18.7 ±1.42 0.98 ± 0.05 43.9 ±4.73 4 28.2 ±1.39 1.25 ±0.08 54.0 ± 5.54 5 25.5 ±1.72 1.33 ±0.07 74.9± 13.17 6 28.7 ± 1.04 1.78±0.16 90.5111.57

2 to 5 in the three soil groups (Table 7). Foliar nutrient concentrations were not obtained for die-back rank 1 since the trees were leafless. Two-way analysis of variance (Table 5) for mean foliar nutrient concentrations of all the three soil groups combined show that foliar nitrogen concentration was significantly higher in healthy trees than in those experiencing die-back. Mean foliar nitrogen concentration in mature healthy trees from the natural forest was 7 mg g"1 for the three soils, which was lower than the corresponding mean of 13 mg g"1 observed for healthy plantation trees (ranks 4-5). 328 VICTOR K. AGYEMAN AND E. Y. SAFO

Foliar calcium concentrations for mature T. ivorensis trees found in the natural forest averaged 13 mgg"1 in the three soil groups. This value is significantly lower than the corresponding mean of 18 mgg"1 observed for healthy trees (ranks 4—5) growing in the plantations (Tables 7). Mean foliar magnesium concentration in trees experiencing die-back was significantly (P<0.001) lower than that in healthy trees (Table 5). However, mean foliar phosphorus, potassium and sulphur concentrations in healthy trees experiencing no die-back were not significantly (P>0.05) different from those in trees experiencing die-back (Table 5).

COMPARISON OF RESULTS WITH OTHER SOIL AND FOLIAR NUTRIENT CONCENTRATION DATA Soil nutrients Mean nitrogen concentrations in soils under plantations and the natural forest were 1.2 and 1.8 mgg"1 respectively (Table 4). These results are similar to the 0.9 mg g"1 observed 3 y after a forest had been converted into a cocoa plantation and the 1.6 mg g"1 noted for soils under natural forests (Maclean & Wasowicz 1950). Results of mean soil nitrogen concentration by other workers, for example the 0.14 mgg"1 in a pine forest in the semi-deciduous ecological zone (Asiamah 1973) and the 0.20 mgg"1 under cocoa plantations (Ahenkorah et al. 1986) show similar trends. Exchangeable calcium and magnesium concentrations for all the soil groups (plantations and natural forest; Table 4) are comparable with data reported by Nye & Greenland (1960) who found calcium levels of 7.40 to 84.0 me kg"1 and magnesium levels of 6.2 to 28.0 me kg"1 for some Ghana forest soils. The level of calcium was two to three times greater than magnesium. Ahn (1958) also reported Ca : Mg ratio of between 2.22 and 3.78 for soils in the forest zone

Table 7. Mean foliar nitrogen, calcium and magnesium concentrations (mg g"') in five die-back ranks of Tcminalia ivorensis on ochrosols, ochrosol-oxysol intergrade and oxysols. (Rank I trees were leafless.)

Plantation Plantation Natural with die-back without die-back forest Rank: 2 3 4 5 6 Nitrogen Ochrosols 4.30 6.40 10.70 22.20 7.40 Intergrade 4.10 5.30 10.20 16.40 7.30 Oxysols 3.90 4.10 8.20 12.10 6.80

Calcium Ochrosols 12.40 14.87 17.67 21.80 16.33 Intergrade 7.07 10.67 16.07 16.33 11.20 Oxysols 10.93 14.70 14.40 16.00 12.30

Magnesium Ochrosols 4.97 4.90 5.93 6.07 5.87 Intergrade 4.63 4.87 6.00 7.27 4.57 Oxysols 3.33 5.57 4.93 5.37 4.73 Mineral nutrition and die-back in Terminalia 329

Table 8. Coefficients of correlation (Kendall's tau) between (a) soil chemical properties, and (b) foliar nutrient concentrations, and die-back ranks for trees of Terminalia ivorensis on each of three soil groups.

Ochrosols- Combined Ochrosols oxysols Oxysols groups (a) Soils n 30 30 30 90 OM 0.382** 0.502** 0.673** 0.443** Total N 0.719** 0.652** 0.634** 0.621** PH 0.016 0.151 0.129 0.038 Ca 0.564** 0.580** 0.563** 0.289** Mg 0.709** 0.587** 0.588** 0.397** Na 0.122 0.120 0.061 0.141 K 0.143 0.120 0.133 0.130 Al 0.145 0.161 -0.199 0.031 H 0.106 0.146 0.217 0.127 CEC 0.549** 0.741** 0.441** 0.360** Avail. P 0.088 -0.147 -0.575** -0.185* Sol. SO4 0.126 0.134 0.165 0.104

(b) Foliar nutrients n 15 15 15 45 N 0.564** 0.561** 0.522** 0.025 Ca 0.535** 0.455* 0.206 -0.106 Mg 0.411* 0.436* 0.389* -0.101 K 0.052 0.156 -0.185 -0.233 P -0.249 -0.134 0.104 -0.610** S -0.125 0.094 0.101 0.064 * PS 0.05, •• 0.01 of Ghana. Calcium formed about 45 to 70% of the effective CEC in the soils under T. ivorensis plantations. The mean values for available phosphorus over the three soil groups ranged from 5.7 to 24.6 mg kg"1. This range is within the 0.8 to 25.0 mg kg"' observed by Oteng & Acquaye (1971) for 48 representative soil series of Ghana and the 0.5 to 67.0 mg kg"1 reported by Safo & Sekou (1976) for four forest soils of Ghana. The mean sulphate sulphur values which ranged from 6.8 to 16.4 mg kg"1 (Table 4) are similar to the 3.25 to 23.35 mg kg"1 obtained by Safo & Sekou (1976) and the 3.0 to 22.0 mg kg"1 reported by Acquaye & Kang (1987) for 48 surface soils (0-22 cm) of Ghana.

Foliar nutrients The foliar nutrient concentration observed in T. ivorensis trees (Table 7) are compared mostly to those of other tropical timber trees in this section. The mean foliar nitrogen concentration of 1'3.3 mg g"1 for healthy T. ivorensis trees in plantations (Table 7) are comparable to the concentrations of 16.1 mgg"1 for Khaya ivorensis A. Chev. and 13.8 mgg"1 for Tieghemella heckilli Pierre. (Drechsel & Zech 1991). The range of concentrations is however, lower than the 20-28 mgg"1 for ElaeisguineensisJacq. (Okoye 1980). The mean foliar calcium concentrations in mature T. ivorensis trees which ranged from 11.2-16.33 mgg"1 are similar to that of 6.2-12.4 mg g~" for 17- 330 VICTOR K. AGYEMAN AND E. Y. SAFO

23 year old stand of T. ivorensis; 5-15 mgg"1 for Tieghemella heckilli (Drechsel & Zech 1991); 13-15 mgg"1 for Gmelina arborea Roxb. (Evans 1986). The mean foliar calcium concentration of 10.2 mgg"1 for Militia regia A. Chev. (Sharma 1983) and 14.0 mg g"1 for 9-mo old T. ivorensis trees (Aluko & Aduayi 1983) are also comparable to the observed values in the natural forest. The mean foliar calcium concentration in trees experiencing die-back was however, higher than the concentrations observed by (Aluko & Aduayi 1983, Drechsel & Zech 1991, Sharma 1983) for young and old trees of T. ivorensis. Foliar magnesium concentration in T. ivorensis which ranged between 3.3 and 7.3 mg g"1 (Table 7) was similar to the 4.0-6.3 mg g~l reported for Pinus elliottii Engelm. (Van Lear & Smith 1972). However, the range of concentrations is higher than the 1.8-3.1 mgg"1 forLophira lanceolata Van Tiegh.; 1.7-2.9 mgg"1 for Tarrietia utilis Spraque. (Drechsel & Zech 1991). The concentration of foliar phosphorus in T. ivorensis was comparable to the 1.3-1.4 mg g"1 reported for Entandrophragma utile Dawe & Sprague and the 1.1- 1.3 mg g"1 for T. ivorensis (Drechsel & Zech 1991).

DISCUSSION Die-back is not related to either tree height or girth (Table 3) in an even-aged plantation. This is because seemingly healthy trees in plantations experiencing die-back may have ceased growing. Malagnoux (1973) observed that growth cessation occurred 2 y before symptoms of the disease appeared. It is important to note that all classes of trees in an even-aged plantation are affected by die-back. Leaf-size is however, related to die-back (Table 3). Leaf size of some trees are also affected by light (Went 1941), water (Salisbury & Ross 1992) and nutrient stress (Allaway 1957). Tree height, girth and leaf size were significantly different for site (Table 3). These parameters for T. ivorensis trees growing on the ochrosol soil group were higher probably because the ochrosols are relatively more fertile than the other soil groups. The oxysols are acidic and less fertile and may account for the fact that the incidence of die-back occurs more extensively (lower plantation survival rate) on this soil group than the other soil groups (Canon 1979). The significant values of the soil group and die-back interaction (Table 5) for most of the nutrients suggest that plants are more likely to be healthy in the soil group with the highest nutrient concentrations. This is supported by Canon (1979) who observed that the ochrosols and integrade soils are especially suitable for the survival of T. ivorensis to maturity. Most of the soil nutrient concentrations were about 60% lower under trees experiencing die-back than in healthy plantations and the natural forest (Table 4). This indicates that most of the soil nutrient concentrations may be growth limiting and therefore related to die-back. The soil chemical properties which Mineral nutrition and die-back in Terminalia 331 may influence die-back are total nitrogen, organic matter, effective cation exchange capacity, exchangeable calcium and magnesium (Table 5).

Nitrogen and organic matter The concentrations of total nitrogen in the soil under T. ivorensis plantations are lower than that of the natural forest. Total nitrogen and organic matter decrease as die-back/tree rank decreases (healthy to dying trees). This suggests that total nitrogen and organic matter concentrations may be related to the incidence of die-back. This is perhaps related to the observation by Bernhard- Reversat (1974) that mineralisation of nitrogen in the litter of T. ivorensis is slow. Nitrogen deficiency may cause chlorosis and diminutive leaf size in plants (Fitzpatrick 1986, Lutz 1951, Wilde 1958). These symptoms are associated with die-back (Ofosu-Asiedu & Canon 1976). However, the observed nutrient concentrations of soils beneath severely affected trees which is about 60% of healthy trees do not seem low enough to indicate a deficiency. The differences are however, large enough to show that nitrogen may be related to die-back. Foliar nitrogen concentration in plantation trees suffering from die-back was almost 50% of that of healthy trees. Generally the available nutrient content in the soil is related to nutrient concentration of plants (Jones 1982), especially the nitrogen content of forest tree leaves (Lutz 1951). Therefore, the low concentration of foliar nitrogen in plants under stress may be related to the low total nitrogen concentration beneath T. ivorensis trees suffering from die-back. Plants under stress of any kind may have reduced nitrogen concentration (Tisdale et al. 1985) because of retranslocation of the nutrient from older leaves to younger ones (Raitio 1991). Supplying nitrogen to such a plant may initially stimulate growth to an extent which lowers further its concentration in the leaves by a dilution effect (Webster & Wilson 1966). The deterioration of the young growing tips, before the mature parts of the crown, observed in T. ivorensis trees experiencing die-back (Ofosu-Asiedu & Canon 1976) may be due to the dilution effect of nutrient concentrations in the upper part of the crown. The foliar nitrogen concentrations found in the natural forest were significantly lower than that in the plantations (Table 7). The concentration of nitrogen was expected to be higher in trees found in the natural forest compared with plantations on similar soil types, due to the rapid turnover of nitrogen under the forest vegetation of Ghana (Nye & Stephens 1962). However, the lower foliar nutrient concentration recorded in the natural forest may have been influenced by the comparatively higher, light environment from which samples were'collected (Acquaye 1964). This is because T. ivorensis is an emer- gent tree (Hall & Swaine 1981) in the natural forest. Foliar samples were collected from the lowest branch of the selected trees. Lower concentration of nutrients in even-aged leaves may also be found in comparatively older plots compared with correspondingly younger ones in some species (Chijicke 1980). 332 VICTOR K. AGYEMAN AND E. Y. SAFO

Rank 6 comprises mature trees probably over 100 y while rank 1 to 5 are made up of younger trees (15-17 y). Organic matter contributes immensely to the availability of nutrients already in the soil (Agboola & Corey 1973) and may influence die-back through its soil buffering effects (Russel 1973) or as the repository for most of the soil nitrogen. Both nitrogen and organic matter could be added to soils in plantations experiencing die-back. Calcium and magnesium Calcium is relatively abundant in soils and rarely limits crop production (Tisdale et al. 1985). However, it was significantly correlated with die-back in T. ivorensis (Table 8). The symptoms of die-back observed by Ofosu-Asiedu & Canon (1976), that terminal buds, younger leaves and branchlets of T. ivorensis trees experiencing die-back deteriorate at the tips and margins and fall off before older leaves and branchlets, seem to suggest a deficiency of calcium. Calcium is not moved from old to new leaves in plants under stress (Fitzpatrick 1986) and its deficiency is associated with growing tip deformity (Russel 1973). However, the concentration of calcium beneath trees experiencing die-back (Table 7) is such that a deficiency of calcium is not likely to result unless the concentration of exchangeable sodium is high (Ramzam 1968). The mean concentration of exchangeable sodium (0.78 me kg"1) is not so high as to affect the absorption of calcium leading to a deficiency of the nutrient in plantations. The range of foliar calcium in T. ivorensis trees growing in plantations was higher than that in most tropical West African trees. This may be due to the high concentration of calcium found in trees under stress growing in plantations. For most healthy trees, foliar nitrogen has the highest concentration followed by potassium (Chijicke 1980). Healthy T. ivorensis trees (rank 5) followed this trend. However, the highest concentration of foliar nutrients in T. ivorensis trees experiencing die-back was calcium followed by nitrogen and potassium. This may be due to retranslocation of mobile nutrients (nitrogen, phosphorus and potassium) from older leaves to younger ones (Raitio 1991) in trees experiencing die-back. This results in a higher concentration of highly immobile nutrients like calcium (Marschner 1986) in older leaves. Calcium is absorbed passively and is independent of plant metabolic activity (Mengel & Kirkby 1982) and therefore its concentration in leaves tends to increase with stress (Hoyle 1965). This may probably account for the high concentration of calcium in plantation grown trees experiencing die-back compared to healthy naturally growing trees. The relatively high concentration of calcium in some healthy trees compared to those experiencing die-back in plantations suggests that these seemingly healthy trees may be under stress. This can be attributed to the fact that the symptoms of die-back become evid- ent two years after its inception (Malagnoux 1973). Therefore seemingly healthy trees, growing in plantations, with high concentrations of foliar calcium (higher than those experiencing die-back) may be under stress and may ultimately die. This would be in accordance with the observation by Jones (1969) Mineral nutrition and die-back in Terminalia 333 that all the healthy trees in a T. ivorensis plantation experiencing die-back died within 10 y after the inception of the disease. The association of the high concentration of foliar calcium with die-back can be further explained using data of the oxysol soil group. In those soils with a relatively low range of exchangeable calcium (7-26 me kg"1), compared to the ochrosol-oxysol (13-32 me kg"1) and ochrosol (49-96 mg kg"1) soil groups (Table 4), foliar calcium was not significantly related to die-back (Table 8). Soil and foliar magnesium concentrations correlated with die-back (Table 8). The relatively low concentration of foliar magnesium observed in trees experiencing die-back may have been influenced by the following factors: The high concentration of calcium may have affected the uptake and translocation of magnesium, especially to the upper plant parts (Embleton 1966, Schimansky 1981). The relatively low concentration of foliar nitrogen in trees experiencing die-back may have reduced the uptake of magnesium due to the synergistic effect of nitrogen on magnesium (Wallace 1952). The low uptake of magnesium (Mengel & Kirkby 1982) and nitrogen (Oren et al. 1988) caused by increased concentration of aluminium (Grime 1983) and leaching of cations from the soil (Oren et al. 1988) may explain the high incidence of die-back in the oxysols compared with the other soil groups.

Other nutrients Aluminium, hydrogen and pH affect the acidity of soils and consequently the availability of plant nutrients. Plants grown in strongly acid soils are often nutrient deficient (Tisdale et al. 1985). However, these three soil chemical factors did not show any significant correlation to die-back in T. ivorensis.

Conclusions The results lend support to the hypothesis that plant nutrition is one of the most important factors influencing die-back. Healthy trees in plantations and the natural forests were found in soils with a relatively higher nutrient content than those experiencing die-back. The soil chemical properties which influence die-back are total nitrogen, organic matter, exchangeable calcium and effective CEC. The organic matter may influence die-back through its soil buffering effects or as the repository for most of the soil nitrogen. Both nitrogen and organic matter could be added to the soil to combat die-back. Effective CEC comprises a group of exchangeable cations including calcium. Effective CEC is therefore, not easy to apply as a single entity or in the form of fertilizers and therefore would be difficult to manipulate to combat die-back. It is recommended that further investigations to examine the effect of soil calcium content on die-back should be carried out. Fertilizer (especially nitrogen) trials should be conducted on plantations experiencing die-back to assess its effects on survival rate. 334 VICTOR K. AGYEMAN AND E. Y. SAFO

ACKNOWLEDGEMENTS The authors are grateful to the Sigma Xi Committee of Grants-in-Aid of Research (USA) and the Forest Research Institute of Ghana for sponsoring this project. The suggestions of Mr J. G. K. Owusu and Drs Albert Ofosu- Asiedu, Mike Swaine, Jill Thompson and Prof. David Newbery are greatly appreciated. The assistance of Dr Malcolm Press in analysing the reference samples is acknowledged.

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Accepted 22 August 1996