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Do indigenous browse trees influence chemical composition and in vitro dry matter digestibility of parasitic plants?
Animal Feed Science and Technology 115 (2004) 357–369
Do indigenous browse trees influence chemical composition and in vitro dry matter digestibility of parasitic plants? O.R. Madibela a,b,∗ , M. Letso b , B. Makoba a , O. Seitshiro a a
b
Sebele Station, Department of Agricultural Research, P/bag 0033, Gaborone, Botswana Department of Animal Science and Production, Botswana College of Agriculture, P/bag 0027, Gaborone, Botswana
Received 3 December 2002; received in revised form 2 February 2004; accepted 17 February 2004
Abstract This study examined the influence of nine browse trees on the chemical composition and in vitro dry matter (DM) digestibility (IVDMD) of parasitic plants (Tapinanthus lugardii, Erianthenum ngamicum, Viscum rotundifolium and Viscum verrucosum) found in Botswana. Browse trees did not have any effect (P > 0.05) on chemical composition and IVDMD of T. lugardii. Acid detergent fibre (ADF) in E. ngamicum was highest (P < 0.05) in samples harvested from Acacia fleckii (340.2 ± 13.1 g/kg DM) and was lowest (266.4 ± 32.1 g/kg DM) from those harvested from Acacia tortilis. V. verrucosum parasiting either A. tortilis or Dichrostacys cinerea had higher (P < 0.05) levels of crude protein (CP) (177.9±9.4 and 172.7±9.4 g/kg DM, respectively) than those parasiting Acacia robusta (140.6 ± 9.4 g/kg DM). Concentrations of calcium in V. verrucosum harvested from A. robusta were higher (P < 0.01; 20.6 ± 1.4 g/kg DM) than that from either A. tortilis (14.2 ± 1.4 g/kg DM) or D. cinerea (14.0 ± 1.4 g/kg DM). Phosphorous level of V. verrucosum was higher (P < 0.01) in samples from A. tortilis versus those from A. robusta and D. cinerea (2.1 ± 0.2 versus 1.3 ± 0.2 g/kg DM versus 1.3 ± 0.2 g/kg DM, respectively). Levels of CP of V. rotundifolium were higher (P < 0.001; 195.8 ± 10.5 g/kg DM) from samples from Boscia albitrunca and lowest (114.4 ± 10.5 g/kg DM) from those harvested from Maytenus senegalensis. V. rotundifolium parasiting Ziziphus mucronata had the highest (P < 0.05) phosphorous levels (2.0±0.1 g/kg DM) while that from B. albitrunca and M. senegalensis had the lowest concentrations (1.6 ± 0.1 and 1.5 ± 0.1 g/kg DM, respectively). Crude protein (182.6 ± 4.6 g/kg DM versus 161.3 ± 4.1 g/kg DM), calcium (Ca) (21.8 ± 0.7 g/kg DM versus 16.5 ± 0.7 g/kg DM) and neutral Abbreviations: ADF, acid detergent fibre; ADL, acid detergent lignin; Ca, calcium; CP, crude protein; NDF, neutral detergent fibre; NDIN, neutral detergent insoluble nitrogen; IVDMD, in vitro dry matter digestibility; P, phosphorous ∗ Corresponding author. Tel.: +267-3650100; fax: +267-3928753. E-mail address: [email protected] (O.R. Madibela). 0377-8401/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.anifeedsci.2004.02.004
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detergent insoluble nitrogen (NDIN) (11.5 ± 0.5 g/kg DM versus 7.5 ± 0.4 g/kg DM) were higher in browse trees than in parasitic plants. Plotting CP, Ca, P and IVDMD against months of January to June showed that nutrient contents of parasitic plants closely follow those of their host browse trees. There was a month effect for IVDMD, neutral detergent fibre (NDF), acid detergent lignin (ADL) (P < 0.05) and calcium (Ca) (P < 0.001), but not for acid detergent fibre (ADF), phosphorus (P), CP and NDIN (P > 0.05) within the parasitic plants. Browse trees appear to have some effect on the nutritive value of some parasitic plants. The parasitic plants with their associated browse trees may provide an alternative supply of nutrients to livestock when these are in short supply from natural forages. © 2004 Elsevier B.V. All rights reserved. Keywords: Parasitic plants; Browse trees; Chemical composition; In vitro dry matter digestibility
1. Introduction Mistletoes are common parasitic plants that attach themselves to branches of Acacia species, Boscia albitrunca, Ziziphus mucronata and other trees found in the semi-arid conditions of Botswana. These parasitic plants are sometimes specific to a host plant and/or locality. Their ultimate goal is to grow under conditions where they stand a best chance of establishment and survival (Visser, 1981). Due to the deep roots of browse trees, it is usually assumed that trees and shrubs can extract minerals from deep soils layers (Lukhule and van Ryssen, 2000) and it can therefore be hypothesised that some parasitic plants may maintain high nutritive value during the dry season. According to Press (1995), parasitic angiosperms can either be hemiparasites, with the ability to survive in the absence of their host during some part of their life cycle, or holoparasitic angiosperms that rely exclusively on the host for supplies of carbon and N. But most parasitic plants lie between the two extremes and may be capable of fixing atmospheric carbon dioxide, but relying on N from the heterotrophic supply. Since high protein browse trees have been recognised as important source of inexpensive protein to goats (Aganga and Monyatsiwa, 1999; Kabasa et al., 2000) it is important to determine if these browse trees influences the nutrient attributes of the parasitic plants. Deeni and Sadiq (2002) found that phytochemical substances of mistletoe plant Tapinanthus dodoneifolius were partly dependent on the host plant species. Parasitic plants form an alternative feed resource, which could increase both mineral and protein intake of ruminants. Previous studies (Madibela et al., 2000, 2002) have shown that parasitic plants growing on multipurpose trees in Botswana have higher crude protein (CP) and mineral levels than those expected in grasses. Smallholder farmers raising goats feed these plants during the dry season. However, they were also found to contain condensed tannins (Madibela et al., 2002) and their CP degradability varied, with T. lugardii and E. ngamicum having effective CP degradability of less than 50% (Madibela et al., 2003). It was hypothesised by Madibela et al. (2003), that factors such as tannins, seasonal variability and agronomic characteristic of the host browse plants may contribute to the differences in CP degradability of these plants. Madibela and Jansen (2003) have shown that V. verrucosum reduce faecal egg count in goats naturally infected by internal worms.
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Chemical composition of leaves from browse trees tend to vary very little within a season (Lukhule and van Ryssen, 2000) and it is likely that this characteristic would be conferred to the parasitic plants. The aim of the present study was to investigate the possible influence of browse trees on the nutritional attributes of parasitic plants.
2. Materials and methods 2.1. Location of study The study was conducted at the Sebele Research Station situated at 24◦ 33 S and 25◦ 57 E at Gaborone, Botswana. It has an altitude of 994 m above sea level. The vegetation and the grass type was previously described by Madibela et al. (2000) as a mixture of Acacia savanna with broad-leaved middle layer trees like Combretum apiculatum and Burkea africana. Grass consists of species of intermediate forage value such as Eragrostis rigidior and E. lehmanmiana. Species, rated good in forage value include Panicum maximum, Digitaria milanjiana, Urochloa masambicensi and U. trichopus. Grasses of poor nutritional value are Aristida congesta and Melinis repens. The soil type of the area was classified by De Wit and Nachtergaele (1990) as moderately deep to very deep, imperfectly to moderately well drained, dark brown to red, sandy clay loams to clays. Sebele Station receives about 513.6 mm rainfall per annum and minimum and maximum daily temperature is 12.8 and 28.6 ◦ C, respectively. 2.2. Sampling Samples of first 15–20 cm leaves and stem of Tapinanthus lugardii, Erianthenum ngamicum, Viscum rotundifolium and V. Verrucosum were collected each month from January to June in 1999. January to March are the wet months and April to June are the dry months. Samples were placed in brown paper bags, oven dried at 60 ◦ C for 48 h and ground to pass a 2 mm screen. Host plants of the sampled parasitic plants were Acacia erubescens, A. fleckii, A. melifera, A. robusta, A. tortilis, B. albitrunca, Dichrostacys cinerea, Maytenus senegalensis and Z. mucronata. Samples were collected from different host plants, but kept separate according to the host plants. Care was taken to ensure that there was no cross-contamination between parasitic plant samples and host plant samples. The method for harvesting the parasitic plants has previously been described by Madibela et al. (2000). At the same time that parasitic plants were harvested, the leaves or terminal shoots (young leaf and stems) of host browse plants were also sampled, then oven dried at 60 ◦ C for 48 h and ground to pass a 2 mm screen. 2.3. Chemical analysis Chemical analysis was completed for neutral detergent fibre (NDF) acid detergent fibre (ADF), acid detergent lignin (ADL) (AOAC, 973.18, 1996). Sodium sulphite was used but not alpha amylase. Ash content was included for ADF. Neutral detergent fibre bound nitrogen (NDFIN) and N (a Kjeldahl method) were analysed (AOAC, 976.06, 1996). Calcium
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(Ca) was determined by atomic absorption spectrophotometry (AOAC 968.08, 1996), while phosphorous (P) was determined with a UV-Vis spectrophotometer (AOAC 965.17 1996). In vitro dry matter (DM) digestibility (IVDMD) was determined with the procedure by Tilley and Terry (1963), by incubating in a thermostatically controlled circulating water bath. 2.4. Statistical analysis General linear models (GLM) procedure of SAS (1990) was used to test effects of host browse plant, parasitic plant and months on chemical composition and IVDMD of the parasitic plants. Correlations between CP and NDIN, CP and ADF, CP and IVDMD were determined. Differences in chemical composition and IVDMD between browse trees, between parasitic plants and between months were tested for significance by a least significance differences (LSD) (Sokal and Rohlf (1969). Results are reported as mean ± standard error. 3. Results Browse trees did not have any effect (P > 0.05) on chemical composition and IVDMD of T. lugardii. ADF in E. ngamicum was highest (P < 0.05; 340.2 ± 13.1 g/kg DM) in samples (leaves and stems) harvested from A. fleckii and the lowest ADF (266.4 ± 32.1 g/kg DM) was from those harvested from A. tortilis (Table 1). Calcium level in samples of V. verrucosum harvested from A. robusta was higher (P < 0.01; 20.6 ± 1.4 g/kg DM) than those harvested from either A. tortilis (14.2 ± 1.4 g/kg DM) or D. cinerea (14.0 ± 1.4 g/kg DM). Samples from V. verrucosum parasiting A. tortilis and D. cinerea had high levels of CP (177.9 ± 9.4 and 172.7 ± 9.4 g/kg DM, respectively) than those parasiting A. robusta (140.6 ± 9.4). Interestingly, the browse tree A. robusta, had the least (114.7 ± 12.0 g/kg DM) amount of CP (Table 3). Calcium level in samples of V. verrucosum harvested from A. robusta were higher (P < 0.05; 20.6 ± 1.4 g/kg) than those harvested from either A. tortilis (14.2 ± 1.4 g/kg DM) or D. cinerea (14.0 ± 1.4 g/kg DM). Phosphorous level of V. verrucosum was high (P < 0.01) in samples from A. tortilis (2.1 ± 0.2 g/kg DM) as opposed to samples harvested from A. robusta and D. cinerea (1.3 ± 0.2 g/kg DM). Level of CP of V. rotundifolium was higher (P < 0.001; 195.8 ± 10.5 g/kg DM) from samples harvested from B. albitrunca and lowest (114.4 ± 10.5 g/kg DM) from those harvested from M. senegalensis. Phosphorous in leaves and stem of V. rotundifolium harvested from Z. mucronata was highest (P < 0.05; 2.0 ± 0.1 g/kg) and those from B. albitrunca and M. senegalensis were low (1.6 ± 0.1 and 1.5 ± 0.1 g/kg DM, respectively) (Table 1). The four parasitic plants had similar (P > 0.05) levels of CP, Ca, P, ADL and NDIN but differences (P < 0.001) were observed on ADF, NDF and IVDMD (Table 2). Month effects were observed for IVDMD, NDF, ADL (P < 0.05), Ca and NDIN (P < 0.01) but there was none (P > 0.05) for ADF, P and CP for the four parasitic plants. No interaction (P > 0.05) was observed between parasitic plants and month. A positive correlation was found between CP and NDIN (r = 0.43, P < 0.001) but none between IVDMD and CP (r = −0.068, P > 0.05). The nine browse trees showed differences in all parameters analysed for; CP, NDF, ADL, IVDMD (P < 0.001), ADF (P < 0.01) Ca, P and NDIN (P < 0.05) (Table 3). There was
Table 1 Effects of various browse trees on chemical composition (g/kg DM) and IVDMD (g/kg DM) of individual parasitic plants
CP Ca P ADF ADL NDF NDIN IVDMD
T. lugardii
E. ngamicum
A. erubescens
A. fleckii
A. melifera
A. tortilis
SL
A. erubescens
A. fleckii
A. melifera
A. tortilis
SL
164.4 ± 13.7 15.0 ± 2.4 1.5 ± 0.2 254.3 ± 16.5 132.1 ± 13.1 453.6 ± 24.0 7.3 ± 1.2 448.0 ± 31.9
155.6 ± 27.5 13.6 ± 4.8 1.4 ± 0.3 314.3 ± 33.1 160.0 ± 26.2 470.0 ± 47.9 10.9 ± 2.3 559.1 ± 63.7
166.9 ± 12.3 19.0 ± 2.1 1.7 ± 0.1 253.9 ± 14.8 130.7 ± 11.7 468.1 ± 21.4 8.4 ± 1.0 484.4 ± 28.5
144.3 ± 11.2 16.4 ± 1.9 1.4 ± 0.1 257.9 ± 13.5 118.7 ± 10.7 427.8 ± 19.6 7.2 ± 1.0 487.7 ± 26.0
NS NS NS NS NS NS NS NS
166.1 ± 9.5 16.7 ± 2.4 1.9 ± 0.1 331.5 ± 14.4 138.2 ± 22.4 544.2 ± 21.5 8.4 ± 1.2 475.6 ± 26.8
152.3 ± 8.7 18.9 ± 2.2 1.7 ± 0.1 340.2 ± 13.1 190.1 ± 20.4 526.9 ± 20.0 8.3 ± 1.2 497.6 ± 24.6
178.5 ± 8.7 18.4 ± 2.2 1.6 ± 0.1 292.6 ± 13.1 134.8 ± 20.4 485.5 ± 19.6 9.0 ± 1.1 487.5 ± 24.6
139.3 ± 21.3 22.7 ± 5.4 1.8 ± 0.2 266.4 ± 32.1 130.0 ± 50.0 484.7 ± 48.0 8.3 ± 2.6 583.1 ± 60.1
NS NS NS
SL
V. verrucosum A. robusta CP Ca P ADF ADL NDF NDIN IVDMD
140.6 ± 9.4 20.6 ± 1.4 1.3 ± 0.2 276.8 ± 12.2 142.8 ± 11.4 426.3 ± 13.7 6.1 ± 0.1 612.8 ± 28.3
∗
NS NS NS NS
V. rotundifolium A. tortilis 177.9 ± 9.4 14.2 ± 1.4 2.1 ± 0.2 281.8 ± 12.2 150.9 ± 11.4 445.4 ± 13.7 7.6 ± 0.1 554.6 ± 28.3
D. cinerea
SL
B. albitrunca
M. senegalensis
Z. Mucronata
172.7 ± 9.4 14.0 ± 1.4 1.3 ± 0.2 270.3 ± 12.2 132.2 ± 11.4 452.8 ± 13.7 9.6 ± 0.1 544.9 ± 28.3
∗
195.8 ± 10.5 9.5 ± 2.3 1.6 ± 0.1 281.6 ± 17.8 140.0 ± 23.8 428.8 ± 20.3 8.3 ± 1.2 558.4 ± 21.4
114.4 ± 10.5 18.3 ± 2.3 1.5 ± 0.1 294.5 ± 17.8 160.3 ± 23.8 422.0 ± 20.3 6.0 ± 1.2 586.8 ± 21.4
171.0 ± 10.5 14.8 ± 2.3 2.0 ± 0.1 280.0 ± 17.8 154.5 ± 23.8 431.5 ± 20.3 8.0 ± 1.2 538.2 ± 21.4
∗∗ ∗∗
NS NS NS NS NS
∗∗∗
NS ∗
NS NS NS NS NS
CP: crude protein, Ca: calcium, P: phosphorous, ADF: acid detergent fibre, ADL: acid detergent lignin, NDF: neutral detergent fibre, NDIN: neutral detergent insoluble nitrogen, IVDMD: in vitro dry matter digestibility, SL: significance level and NS: P > 0.05. ∗ P < 0.05. ∗∗ P < 0.01. ∗∗∗ P < 0.001.
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Parameter
361
362
Plants
CP
Ca
P
ADF
ADL
NDF
NDIN
IVDMD
T. lugardii E. ngamicum V. verrucosum V. rotundifolium
156.0 ± 7.9 163.3 ± 8.2 163.7 ± 7.4 158.4 ± 6.9
16.6 ± 1.2 18.0 ± 1.2 16.2 ± 1.1 14.7 ± 1.0
1.5 ± 0.1 1.7 ± 0.1 1.5 ± 0.1 1.7 ± 0.9
256.7 ± 8.5 31.7 ± 8.8 276.3 ± 7.9 285.1 ± 7.4
125.6 ± 9.4 151.3 ± 9.8 141.9 ± 8.7 150.9 ± 8.2
453.2 ± 10.2 510.0 ± 10.6 441.5 ± 9.5 430.0 ± 9.0
8.0 ± 0.6 8.2 ± 0.6 7.8 ± 0.6 7.3 ± 0.5
474.6 ± 15.8 485.9 ± 16.4 570.8 ± 14.7 555.3 ± 13.7
Overall mean Level of significance
160.6 NS
16.5 NS
1.6 NS
285.5
144.6 NS
458.9
7.9 NS
527.1
∗∗∗
∗∗∗
∗∗∗
CP: crude protein, Ca: calcium, P: phosphorous, ADF: acid detergent fibre, ADL: acid detergent lignin, NDF: neutral acid detergent, NDIN: neutral detergent insoluble nitrogen, IVDMD: in vitro dry matter digestibility and NS: P > 0.05. ∗∗∗ P < 0.001
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Table 2 Mean chemical composition (g/kg DM) and IVDMD (g/kg DM) of four parasitic plants for the 6 months period
Browse tree
CP
Ca
P
ADF
ADL
NDF
NDIN
IVDMD
A. erubescens A. fleckii A. mellifera A. robusta A. tortilis B. albitrunca D. cinerea M. senegalensis Z. mucronata
203.5 ± 13.2 189.0 ± 11.1 213.3 ± 12.0 114.7 ± 12.0 212.0 ± 10.4 188.8 ± 12.0 186.5 ± 12.0 145.8 ± 12.0 200.8 ± 12.0
20.5 ± 2.6 22.3 ± 2.2 27.1 ± 2.4 18.4 ± 2.4 20.4 ± 2.1 20.2 ± 2.4 15.8 ± 2.4 27.9 ± 2.4 23.8 ± 2.4
1.1 ± 0.2 1.1 ± 0.2 1.2 ± 0.2 0.9 ± 0.2 1.5 ± 0.2 0.9 ± 0.2 1.2 ± 0.2 1.0 ± 0.2 1.8 ± 0.2
262.9 ± 19.7 271.8 ± 16.6 241.4 ± 17.8 311.8 ± 17.8 303.9 ± 15.6 298.9 ± 17.8 315.0 ± 17.8 243.2 ± 17.8 230.4 ± 17.8
87.8 ± 23.1 107.3 ± 19.4 106.4 ± 20.9 202.5 ± 20.9 192.0 ± 18.2 132.5 ± 20.9 195.2 ± 20.9 97.2 ± 20.9 109.4 ± 20.9
480.9 ± 14.6 489.0 ± 12.2 374.3 ± 13.2 452.7 ± 13.2 509.8 ± 11.5 442.3 ± 13.2 492.8 ± 13.2 386.3 ± 13.2 357.4 ± 13.2
14.7 ± 1.8 15.8 ± 1.5 8.3 ± 1.6 9.5 ± 1.6 11.9 ± 1.4 10.9 ± 1.6 12.3 ± 1.8 9.7 ± 1.6 11.9 ± 1.6
493.6 ± 35.9 500.7 ± 30.2 621.7 ± 32.4 340.8 ± 32.4 388.8 ± 33.7 583.8 ± 32.4 411.1 ± 32.4 735.6 ± 32.4 672.4 ± 32.4
Overall mean Level of significance
184.1
21.5
1.2
277.7
140.9
445.8
11.7
530.2
∗∗∗
∗
∗
∗∗
∗∗∗
∗∗∗
∗
∗∗∗
CP: crude protein, Ca: calcium, P: phosphorous, ADF: acid detergent fibre, ADL: acid detergent lignin, NDF: neutral acid detergent, NDIN: neutral detergent insoluble nitrogen and IVDMD: in vitro dry matter digestibility. ∗ P < 0.05. ∗∗ P < 0.01. ∗∗∗ P < 0.001.
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Table 3 Mean chemical composition (g/kg DM) and IVDMD (g/kg DM) of browse plants on which the parasitic plants attached
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a month effect for P (P < 0.05), Ca (P < 0.001), CP and IVDMD (P < 0.05) and none for NDF, ADL, ADF and NDIN (P > 0.05) for the browse plants. A negative correlation was observed between IVDMD and ADF (r = −0.50, P < 0.001) for the browse plants, while none was observed between CP and IVDMD (r = 0.14, P > 0.05), between NDIN and CP (r = 0.12, P > 0.05) and between CP and ADF (r = −0.05, P < 0.05). A comparison of leaves and stem between browse and parasitic plants showed that leaves from browse had higher (P < 0.001) CP (182.6±4.6 g/kg DM versus 161.3±4.1 g/kg DM), Ca (21.8±0.7 g/kg DM versus 16.5±0.7 g/kg DM), P (1.2±0.1 g/kg versus 1.6±0.1 g/kg) and NDIN (11.5±0.5 g/kg DM versus 7.5±0.4 g/kg DM). But no difference (P > 0.05) was found for ADF (271.6 ± 6.2 g/kg DM versus 284.0 ± 5.5 g/kg DM), ADL (134.5 ± 7.0 g/kg DM versus 143.5 ± 6.2 g/kg DM), NDF (439.5 ± 7.8 g/kg DM versus 458.9 ± 6.9 g/kg DM) and IVDMD (542.1 ± 14.9 versus. 518.8 ± 12.9 g/kg DM), respectively in leaves of browse plants and parasitic plants.
4. Discussion Observations from this study show that various browse host trees influence certain chemical attributes of some individual parasitic plants, but not IVDMD. The fact that Viscum species were the ones in which some of their nutritional attributes (especially CP) were influenced by browse may be indicative of a unique relationship between these plants and their hosts. V. verrucosum does not have leaves but V. rotundifolium has tiny leaves (Madibela et al., 2000) and may not be able to synthesis complex carbon molecules which E. ngamicum and T. lugardii were able to do due to the presence of leaves. Most parasitic plants are between being hemiparasitic and holoparasitic angiosperms and may be able to fix atmospheric carbon dioxide (Press, 1995). Differences were observed in CP, Ca and P levels of V. verrucosum and V. rotundifolium when these plants attached to different host plants. According to Press (1995), some mistletoes growing on different host species have foliar N concentrations directly related to that of its host species, as was found in the present study. For example, the parasitic plant Tapinanthus bangwensis was reported (Press, 1995; citing Steward and Orebamjo, 1980) to be able to reduce inorganic nitrate to amino acids and that nitrate reduction of the parasite differ between individuals parasitising different hosts. This was thought to be partly due to variation in the supply of nitrate from the host sap. Deeni and Sadiq (2002) also found that the presence or distribution of phytochemical substances in the leaves of African mistletoe, Tapinanthus dodneifolius, was partly dependent on the host plant species. In the present study, the supply of nutrients from the host did not affect structural components of plant cell wall. The fact that ADF, ADL, NDF, NDIN and IVDMD levels in parasitic plants were not influenced by differences in browse plants cannot not be explained. However, these parameters are structural components, and so are the least digestible, and we hypothesis that the host plants affect only the most digestible components of the parasitic plants. Contrary to Madibela et al. (2000), who found a positive correlation between IVDMD and CP, none was found for the parasitic plants in the present study. Browse trees appear to have some effects on the nutritive value of some parasitic plants. Parasitic plants that attached to browse tree with high CP, Ca, P, NDF and IVDMD also had high levels of these nutrients, albeit in lower levels than those of browse trees (Fig. 1). It was
Browse IVDMD P
CP Ca
IVDMD P
700
34.5 32.5 30.5
600
26.5 500
24.5 22.5 20.5
400
18.5 16.5 300
14.5 12.5 10.5
200
8.5 6.5
100
4.5 2.5
0
0.5 Jan
Feb
Mar
Apr
May
Months
Jun
Level of minerals (g/kg DM)
Level of DMD and CP (g/kg DM)
28.5
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CP Ca
Parasitic plants
Fig. 1. Nutritional attributes of browse trees and parasitic plants over a period of 6 months (n = 6). 365
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also observed that CP, Ca, P NDIN in browse trees were higher than that in parasitic plants. According to Press (1995; citing Bannister 1989), New Zealand non-mimic mistletoes generally have lower N concentrations than their host plants. The mimic types are said to have leaves with similar morphology to their hosts and also contain higher levels of N than non-mimics (Press, 1995). This strategy ensures that mimic mistletoes gain a selective advantage by not appearing distinct from their host and thus aim at reduced herbivory. Alternatively, non-mimics contain lower levels of N than their hosts and hence benefit by advertising the fact that their N level is low. Parasitic plants that attach on browse trees found in rangelands of Botswana are usually above the browse level of most browsing animals, except for bigger ungulates such as giraffes and elephants. As a result, they evolved having different leave morphology than their host trees, as they did not need to disguise their presences from herbivores in order to survive. In the present study, plotting CP, Ca, P and IVDMD against time (months) showed an interesting trend between the browse trees and parasitic plants (Fig. 1). The parasitic plants closely followed the pattern of the browse trees, except for Ca. In April there was a relatively large increase in Ca concentration of browse trees, that was not associated with a concomitant increase in Ca content of parasitic plants. April is the start of the dry period and it is not clear if a sudden moisture stress may have caused this effect. Unlike the study by Madibela et al. (2000), who found that the CP of parasitic plants increases from the wet months (January to March) to the dry month (May to June), in the present study CP varied little within the 6-month-sampling period. Crude protein averaged 160 g/kg and the phenomenon of nutrients varying less between seasons has been reported for browse trees (Lukhule and van Ryssen, 2000). Studies by Madibela et al. (2000, 2002, 2003) found differences in CP between parasitic plant species, whereas in the present study differences were not found. The mean level of CP of parasitic plants in the present study was higher than those of previous studies, but similar to a value of 160 g/kg reported by Madibela et al. (2003). Similar to previous studies, levels of Ca, P (Madibela et al., 2000, 2002) and of ADL (Madibela et al., 2000) were not affected by parasitic plant species in the present study. Levels of IVDMD was however higher, about 530 g/kg in the present study, than was previously found for the same plants by Madibela et al. (2000). The discrepancy between the studies cannot be explained except that probably the ratio of leaf to petioles in the edible samples used for the analysis (Abdulrazak et al., 2000) was different between the two studies. NDIN was not affected by parasitic plant species and was of the magnitude of 7.9 g/kg, suggesting that a portion of undegradable CP would escape rumen degradation and be available for post ruminal digestion. These plants have been reported to contain on average 57.0 g/kg condensed tannins (Madibela et al., 2002) and Reed (1986) found a high correlation between NDIN and insoluble proanthocyanidins, indicating the possible formation of tannin–protein complexes. This is consistent with positive correlation found between CP and NDIN in the present study. Some condensed tannins protect plant protein from digestion in the rumen. Subsequently the complex dissociates at abomasal pH providing amino acids for absorption in the small intestine (Waghorn et al., 1987, as cited by McSweeney et al., 1999). However, the benefits of the dissociated protein from the protein–tannins complex is not certain, because plant tannins contained in specific forage and browse plants can have positive or negative effects on N use, and overall livestock performance, depending on the types and concentration of tannins that are present in the diet (Turner, 2001).
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The nine host browse plants evaluated were found to differ in chemical composition and IVDMD, consistent with other studies (Sawe et al., 1998; Abdulrazak et al., 2000; Lukhule and van Ryssen, 2000). In the present study, CP content ranged from 146.0 to 213.0 g/kg DM. Calcium was relatively high, averaging 22 g/kg, and A. robusta had the highest level while B. albitrunca had the least level of Ca. Results from pasture clipping in Botswana over several years have shown that phosphorous rarely reaches 1.0 g/kg DM at any time of the year to satisfy the minimum levels required by livestock (APRU, 1980). In the present study, P levels in browse trees were 1.2 g/kg DM, indicating their potential in providing P to livestock. Abdulrazak et al. (2000) reported lower Ca and P levels for Acacia trees from Kenya than those found in the present study. The difference may be due to regional difference in soils and climatic conditions. Dicalcium phosphate is a common mineral supplement in Botswana, but the inaccessibility of the mineral lick to resource poor farmers means that their animals requirement for these minerals are often not met (Madibela et al., 2002). Calcium is associated with P metabolism of bones and Ca:P ratio of 2:1 is recommended (Abdulrazak et al., 2000). An average Ca:P ratio of 17.9:1 in browse tree was observed in the present study, indicating that if fed as the sole feed, browse trees provide an unbalanced source of these minerals. However, the usefulness of P would depend on its bioavailability to the animals, which was not determined in the present study. The ADF content of browse trees were similar to an average value (277.7 g/kg DM versus 287.8 g/kg DM) for leaves from indigenous fodder trees in South Africa reported by Lukhule and van Ryssen (2000). Differences were found in NDF, whereby levels were higher (445.8 g/kg DM versus 365.8 g/kg DM) than values reported for browse trees in South Africa by Lukhule and van Ryssen (2000). The high value of NDF found in the present study may be due to differences in the ratio of leaf to petioles in edible samples (Abdulrazak et al., 2000). Inclusion of woody twigs during sampling may explain this observation, since twigs contributes to higher NDF (Topps, 1992). Sixty-three percent of NDF was ADF, which indicates a high content of cellulose and lignin and low levels of hemicellulose. The higher (12.0 g/kg DM) amounts of NDIN found in browse trees than in parasitic plants probably suggest that a high level of undegradable CP would be unavailable to the host animal. This is likely to be the case with Acacia robusta and A. tortilis, which have lower IVDMD values than the mean (530 g/kg) by 18.9 and 14.1% units, respectively. The proportion of NDIN in browse trees in the present study was however lower than those of Acacia tree leaves from Kenya (Abdulrazak et al., 2000).
5. Conclusions Browse host plants influence CP, Ca, P only in V. verrucosum and V. rotundifolium. This effect may be due to variation in nutrient supply by the host browse plants or the fact that the Viscum species do not have leaves, while E. ngamicum and T. lugardii do and were able to synthesis complex carbon molecules. The levels of CP, P and IVDMD of parasitic plants followed the same pattern as that of browse over the 6-month-sampling period. Browse trees however, had high levels of CP, Ca, P and NDIN. The diversity of browse trees and parasitic plants, and their associated high nutritive value warrant their use as supplements for livestock by resource poor farmers who cannot access commercial feed supplements.
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Acknowledgements The authors would like to recognize input by staff at Feed and Plants Laboratory of Department of Agriculture Research (DAR). The authors would also like to recognize Drs. J. Macala (DAR) and U.J. Omphile (Botswana college of Agriculture) for critiquing the manuscript. J. Makore is acknowledged for helping with statistical analysis. References Abdulrazak, S.A., Fujihara, T., Ondiek, J.K., Ørskov, E.R., 2000. Nutritive evaluation of some Acacia trees leaves from Kenya. Anim. Feed Sci. Technol. 85, 89–98. Aganga, A.A., Monyatsiwa, C.B., 1999. Use of browse (Terminalia serecia, Combretum apiculatum or Eulea schimperi) as supplement for growing Tswana goats. Trop. Anim. Health Prod. 31, 295– 305. AOAC, 1996. Official Methods of Analysis. Association of Official Analytical Chemists, Washington, DC. APRU, 1980. APRU (Animal Production Research Unit), 1980. Handbook on Beef Production and Range Management in Botswana. Government Printers, Gaborone. Deeni, Y.Y., Sadiq, N.M., 2002. Antimicrobial properties and phytochemical constituents of leaves of African mistletoe (Tapinanthus dodoneifolius (DC) Danser) (Loranthaceae): an ethnomedicinal plant of Hausaland, Northern Nigeria. J. Ethnopharmacol. 83, 235–240. De Wit, P.V., Nachtergaele, F.O., 1990. Explanatory note on the soil mapping of the Republic of Botswana. FAO/UNDP/Government of Botswana. Soil Mapping and Advisory Services Project (FAO/BOT/85/011). Field Document 30. Kabasa, J.D., Opuda-Asido, J., ter Meulen, U., 2000. The effect of oral administration of polyethylene Glycol on faecal helminth egg counts in pregnant goats grazed on browse containing tannins. Trop. Anim. Health Prod. 32, 73–86. Lukhule, M.S., van Ryssen, J.B.J., 2000. The chemical composition of leaves from indigenous fodder trees in South Africa. S. Afr. J. Anim. Sci. 30 (Suppl. 1), 72–73. Madibela, O.R., Boitumelo, W.S., Letso, M., 2000. Chemical composition and in vitro dry matter digestibility of four parasitic plants (Tapinanthus lugardii, Erianthenum ngamicum, Viscum rotundifolium and Viscum verrucosum) in Botswana. Anim. Feed Sci. Technol. 84, 97–106. Madibela, O.R., Letso, M., Boitumelo, W.S., Masedi, M., Alton, K., 2002. Chemical composition of four parasitic plants harvested over a period of 6 months from two sites in Botswana. Anim. Feed Sci. Technol. 95, 159– 167. Madibela, O.R., Mabutho, S., Sebolai, B., 2003. Dry matter and crude protein degradability of four parasitic plants (mistletoes) associated with browse trees in Botswana. Trop. Anim. Health Prod. 35, 365–372. Madibela, O.R., Jansen, K., 2003. The use of indigenous parasitic plant (Viscum verrocosum) in reducing faecal egg counts in female Tswana goats. Livestock Res. Rural Dev. 15 (9) http://www.cipav.org.co/lrrd/lrrd15/9/ madi159.htm. McSweeney, C.S., Dalrymple, B.P., Gobius, K.S., Kennedy, P.M., Krause, D.O., Mackie, R.I., Xue, G.P., 1999. The application of rumen biotechnology to improve the nutritive value of fibrous feedstuffs: pre- and post ingestion. Livestock Prod. Sci. 59, 265–283. Press, M.C., 1995. Carbon and nitrogen relations. In: Press, M.C., Graves, J.C. (Eds.), Parasitic Plants. Chapman and Hall, London, pp. 110–112. Reed, J.D., 1986. Relations among soluble phenolics, insoluble proanthocyanidins and fibre in East African browse species. J. Range Manage. 39, 5–7. SAS Institute Inc., 1990. SAS User’s Guide. Statistics Version 6. SAS Institute Inc., Cary, NC, USA. Sawe, J.J., Tuitoek, J.K., Ottaro, J.M., 1998. Evaluation of common tree leaves or pods as supplements for goats on range area of Kenya. Small Rumin. Res. 28, 31–37. Sokal, R.R., Rohlf, F.J., 1969. Biometry. The Principles and Practice of Statistics in Biological Research, second ed. p. 244.
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Tilley, J.M.A., Terry, R.A., 1963. A two-stage technique for the in vitro digestion of forages. J. Br. Grassl. Soc. 18, 104–111. Topps, J.H., 1992. Potential, composition and use of legume shrubs and trees as fodder for livestock in the tropics (a review). J. Agric. Sci. (Cambridge) 118, 1–8. Turner, K.E., 2001. Tannins and protein utilization relationships in small ruminant grazing and browsing systems. J. Anim. Sci. 79 (Suppl. 2), 27 (abstract). Visser, J., 1981. South African parasitic flowering plants. Juta and Company Limited, Cape Town.
Do indigenous browse trees influence chemical composition and in vitro dry matter digestibility of parasitic plants? O.R. Madibela a,b,∗ , M. Letso b , B. Makoba a , O. Seitshiro a a
b
Sebele Station, Department of Agricultural Research, P/bag 0033, Gaborone, Botswana Department of Animal Science and Production, Botswana College of Agriculture, P/bag 0027, Gaborone, Botswana
Received 3 December 2002; received in revised form 2 February 2004; accepted 17 February 2004
Abstract This study examined the influence of nine browse trees on the chemical composition and in vitro dry matter (DM) digestibility (IVDMD) of parasitic plants (Tapinanthus lugardii, Erianthenum ngamicum, Viscum rotundifolium and Viscum verrucosum) found in Botswana. Browse trees did not have any effect (P > 0.05) on chemical composition and IVDMD of T. lugardii. Acid detergent fibre (ADF) in E. ngamicum was highest (P < 0.05) in samples harvested from Acacia fleckii (340.2 ± 13.1 g/kg DM) and was lowest (266.4 ± 32.1 g/kg DM) from those harvested from Acacia tortilis. V. verrucosum parasiting either A. tortilis or Dichrostacys cinerea had higher (P < 0.05) levels of crude protein (CP) (177.9±9.4 and 172.7±9.4 g/kg DM, respectively) than those parasiting Acacia robusta (140.6 ± 9.4 g/kg DM). Concentrations of calcium in V. verrucosum harvested from A. robusta were higher (P < 0.01; 20.6 ± 1.4 g/kg DM) than that from either A. tortilis (14.2 ± 1.4 g/kg DM) or D. cinerea (14.0 ± 1.4 g/kg DM). Phosphorous level of V. verrucosum was higher (P < 0.01) in samples from A. tortilis versus those from A. robusta and D. cinerea (2.1 ± 0.2 versus 1.3 ± 0.2 g/kg DM versus 1.3 ± 0.2 g/kg DM, respectively). Levels of CP of V. rotundifolium were higher (P < 0.001; 195.8 ± 10.5 g/kg DM) from samples from Boscia albitrunca and lowest (114.4 ± 10.5 g/kg DM) from those harvested from Maytenus senegalensis. V. rotundifolium parasiting Ziziphus mucronata had the highest (P < 0.05) phosphorous levels (2.0±0.1 g/kg DM) while that from B. albitrunca and M. senegalensis had the lowest concentrations (1.6 ± 0.1 and 1.5 ± 0.1 g/kg DM, respectively). Crude protein (182.6 ± 4.6 g/kg DM versus 161.3 ± 4.1 g/kg DM), calcium (Ca) (21.8 ± 0.7 g/kg DM versus 16.5 ± 0.7 g/kg DM) and neutral Abbreviations: ADF, acid detergent fibre; ADL, acid detergent lignin; Ca, calcium; CP, crude protein; NDF, neutral detergent fibre; NDIN, neutral detergent insoluble nitrogen; IVDMD, in vitro dry matter digestibility; P, phosphorous ∗ Corresponding author. Tel.: +267-3650100; fax: +267-3928753. E-mail address: [email protected] (O.R. Madibela). 0377-8401/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.anifeedsci.2004.02.004
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detergent insoluble nitrogen (NDIN) (11.5 ± 0.5 g/kg DM versus 7.5 ± 0.4 g/kg DM) were higher in browse trees than in parasitic plants. Plotting CP, Ca, P and IVDMD against months of January to June showed that nutrient contents of parasitic plants closely follow those of their host browse trees. There was a month effect for IVDMD, neutral detergent fibre (NDF), acid detergent lignin (ADL) (P < 0.05) and calcium (Ca) (P < 0.001), but not for acid detergent fibre (ADF), phosphorus (P), CP and NDIN (P > 0.05) within the parasitic plants. Browse trees appear to have some effect on the nutritive value of some parasitic plants. The parasitic plants with their associated browse trees may provide an alternative supply of nutrients to livestock when these are in short supply from natural forages. © 2004 Elsevier B.V. All rights reserved. Keywords: Parasitic plants; Browse trees; Chemical composition; In vitro dry matter digestibility
1. Introduction Mistletoes are common parasitic plants that attach themselves to branches of Acacia species, Boscia albitrunca, Ziziphus mucronata and other trees found in the semi-arid conditions of Botswana. These parasitic plants are sometimes specific to a host plant and/or locality. Their ultimate goal is to grow under conditions where they stand a best chance of establishment and survival (Visser, 1981). Due to the deep roots of browse trees, it is usually assumed that trees and shrubs can extract minerals from deep soils layers (Lukhule and van Ryssen, 2000) and it can therefore be hypothesised that some parasitic plants may maintain high nutritive value during the dry season. According to Press (1995), parasitic angiosperms can either be hemiparasites, with the ability to survive in the absence of their host during some part of their life cycle, or holoparasitic angiosperms that rely exclusively on the host for supplies of carbon and N. But most parasitic plants lie between the two extremes and may be capable of fixing atmospheric carbon dioxide, but relying on N from the heterotrophic supply. Since high protein browse trees have been recognised as important source of inexpensive protein to goats (Aganga and Monyatsiwa, 1999; Kabasa et al., 2000) it is important to determine if these browse trees influences the nutrient attributes of the parasitic plants. Deeni and Sadiq (2002) found that phytochemical substances of mistletoe plant Tapinanthus dodoneifolius were partly dependent on the host plant species. Parasitic plants form an alternative feed resource, which could increase both mineral and protein intake of ruminants. Previous studies (Madibela et al., 2000, 2002) have shown that parasitic plants growing on multipurpose trees in Botswana have higher crude protein (CP) and mineral levels than those expected in grasses. Smallholder farmers raising goats feed these plants during the dry season. However, they were also found to contain condensed tannins (Madibela et al., 2002) and their CP degradability varied, with T. lugardii and E. ngamicum having effective CP degradability of less than 50% (Madibela et al., 2003). It was hypothesised by Madibela et al. (2003), that factors such as tannins, seasonal variability and agronomic characteristic of the host browse plants may contribute to the differences in CP degradability of these plants. Madibela and Jansen (2003) have shown that V. verrucosum reduce faecal egg count in goats naturally infected by internal worms.
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Chemical composition of leaves from browse trees tend to vary very little within a season (Lukhule and van Ryssen, 2000) and it is likely that this characteristic would be conferred to the parasitic plants. The aim of the present study was to investigate the possible influence of browse trees on the nutritional attributes of parasitic plants.
2. Materials and methods 2.1. Location of study The study was conducted at the Sebele Research Station situated at 24◦ 33 S and 25◦ 57 E at Gaborone, Botswana. It has an altitude of 994 m above sea level. The vegetation and the grass type was previously described by Madibela et al. (2000) as a mixture of Acacia savanna with broad-leaved middle layer trees like Combretum apiculatum and Burkea africana. Grass consists of species of intermediate forage value such as Eragrostis rigidior and E. lehmanmiana. Species, rated good in forage value include Panicum maximum, Digitaria milanjiana, Urochloa masambicensi and U. trichopus. Grasses of poor nutritional value are Aristida congesta and Melinis repens. The soil type of the area was classified by De Wit and Nachtergaele (1990) as moderately deep to very deep, imperfectly to moderately well drained, dark brown to red, sandy clay loams to clays. Sebele Station receives about 513.6 mm rainfall per annum and minimum and maximum daily temperature is 12.8 and 28.6 ◦ C, respectively. 2.2. Sampling Samples of first 15–20 cm leaves and stem of Tapinanthus lugardii, Erianthenum ngamicum, Viscum rotundifolium and V. Verrucosum were collected each month from January to June in 1999. January to March are the wet months and April to June are the dry months. Samples were placed in brown paper bags, oven dried at 60 ◦ C for 48 h and ground to pass a 2 mm screen. Host plants of the sampled parasitic plants were Acacia erubescens, A. fleckii, A. melifera, A. robusta, A. tortilis, B. albitrunca, Dichrostacys cinerea, Maytenus senegalensis and Z. mucronata. Samples were collected from different host plants, but kept separate according to the host plants. Care was taken to ensure that there was no cross-contamination between parasitic plant samples and host plant samples. The method for harvesting the parasitic plants has previously been described by Madibela et al. (2000). At the same time that parasitic plants were harvested, the leaves or terminal shoots (young leaf and stems) of host browse plants were also sampled, then oven dried at 60 ◦ C for 48 h and ground to pass a 2 mm screen. 2.3. Chemical analysis Chemical analysis was completed for neutral detergent fibre (NDF) acid detergent fibre (ADF), acid detergent lignin (ADL) (AOAC, 973.18, 1996). Sodium sulphite was used but not alpha amylase. Ash content was included for ADF. Neutral detergent fibre bound nitrogen (NDFIN) and N (a Kjeldahl method) were analysed (AOAC, 976.06, 1996). Calcium
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(Ca) was determined by atomic absorption spectrophotometry (AOAC 968.08, 1996), while phosphorous (P) was determined with a UV-Vis spectrophotometer (AOAC 965.17 1996). In vitro dry matter (DM) digestibility (IVDMD) was determined with the procedure by Tilley and Terry (1963), by incubating in a thermostatically controlled circulating water bath. 2.4. Statistical analysis General linear models (GLM) procedure of SAS (1990) was used to test effects of host browse plant, parasitic plant and months on chemical composition and IVDMD of the parasitic plants. Correlations between CP and NDIN, CP and ADF, CP and IVDMD were determined. Differences in chemical composition and IVDMD between browse trees, between parasitic plants and between months were tested for significance by a least significance differences (LSD) (Sokal and Rohlf (1969). Results are reported as mean ± standard error. 3. Results Browse trees did not have any effect (P > 0.05) on chemical composition and IVDMD of T. lugardii. ADF in E. ngamicum was highest (P < 0.05; 340.2 ± 13.1 g/kg DM) in samples (leaves and stems) harvested from A. fleckii and the lowest ADF (266.4 ± 32.1 g/kg DM) was from those harvested from A. tortilis (Table 1). Calcium level in samples of V. verrucosum harvested from A. robusta was higher (P < 0.01; 20.6 ± 1.4 g/kg DM) than those harvested from either A. tortilis (14.2 ± 1.4 g/kg DM) or D. cinerea (14.0 ± 1.4 g/kg DM). Samples from V. verrucosum parasiting A. tortilis and D. cinerea had high levels of CP (177.9 ± 9.4 and 172.7 ± 9.4 g/kg DM, respectively) than those parasiting A. robusta (140.6 ± 9.4). Interestingly, the browse tree A. robusta, had the least (114.7 ± 12.0 g/kg DM) amount of CP (Table 3). Calcium level in samples of V. verrucosum harvested from A. robusta were higher (P < 0.05; 20.6 ± 1.4 g/kg) than those harvested from either A. tortilis (14.2 ± 1.4 g/kg DM) or D. cinerea (14.0 ± 1.4 g/kg DM). Phosphorous level of V. verrucosum was high (P < 0.01) in samples from A. tortilis (2.1 ± 0.2 g/kg DM) as opposed to samples harvested from A. robusta and D. cinerea (1.3 ± 0.2 g/kg DM). Level of CP of V. rotundifolium was higher (P < 0.001; 195.8 ± 10.5 g/kg DM) from samples harvested from B. albitrunca and lowest (114.4 ± 10.5 g/kg DM) from those harvested from M. senegalensis. Phosphorous in leaves and stem of V. rotundifolium harvested from Z. mucronata was highest (P < 0.05; 2.0 ± 0.1 g/kg) and those from B. albitrunca and M. senegalensis were low (1.6 ± 0.1 and 1.5 ± 0.1 g/kg DM, respectively) (Table 1). The four parasitic plants had similar (P > 0.05) levels of CP, Ca, P, ADL and NDIN but differences (P < 0.001) were observed on ADF, NDF and IVDMD (Table 2). Month effects were observed for IVDMD, NDF, ADL (P < 0.05), Ca and NDIN (P < 0.01) but there was none (P > 0.05) for ADF, P and CP for the four parasitic plants. No interaction (P > 0.05) was observed between parasitic plants and month. A positive correlation was found between CP and NDIN (r = 0.43, P < 0.001) but none between IVDMD and CP (r = −0.068, P > 0.05). The nine browse trees showed differences in all parameters analysed for; CP, NDF, ADL, IVDMD (P < 0.001), ADF (P < 0.01) Ca, P and NDIN (P < 0.05) (Table 3). There was
Table 1 Effects of various browse trees on chemical composition (g/kg DM) and IVDMD (g/kg DM) of individual parasitic plants
CP Ca P ADF ADL NDF NDIN IVDMD
T. lugardii
E. ngamicum
A. erubescens
A. fleckii
A. melifera
A. tortilis
SL
A. erubescens
A. fleckii
A. melifera
A. tortilis
SL
164.4 ± 13.7 15.0 ± 2.4 1.5 ± 0.2 254.3 ± 16.5 132.1 ± 13.1 453.6 ± 24.0 7.3 ± 1.2 448.0 ± 31.9
155.6 ± 27.5 13.6 ± 4.8 1.4 ± 0.3 314.3 ± 33.1 160.0 ± 26.2 470.0 ± 47.9 10.9 ± 2.3 559.1 ± 63.7
166.9 ± 12.3 19.0 ± 2.1 1.7 ± 0.1 253.9 ± 14.8 130.7 ± 11.7 468.1 ± 21.4 8.4 ± 1.0 484.4 ± 28.5
144.3 ± 11.2 16.4 ± 1.9 1.4 ± 0.1 257.9 ± 13.5 118.7 ± 10.7 427.8 ± 19.6 7.2 ± 1.0 487.7 ± 26.0
NS NS NS NS NS NS NS NS
166.1 ± 9.5 16.7 ± 2.4 1.9 ± 0.1 331.5 ± 14.4 138.2 ± 22.4 544.2 ± 21.5 8.4 ± 1.2 475.6 ± 26.8
152.3 ± 8.7 18.9 ± 2.2 1.7 ± 0.1 340.2 ± 13.1 190.1 ± 20.4 526.9 ± 20.0 8.3 ± 1.2 497.6 ± 24.6
178.5 ± 8.7 18.4 ± 2.2 1.6 ± 0.1 292.6 ± 13.1 134.8 ± 20.4 485.5 ± 19.6 9.0 ± 1.1 487.5 ± 24.6
139.3 ± 21.3 22.7 ± 5.4 1.8 ± 0.2 266.4 ± 32.1 130.0 ± 50.0 484.7 ± 48.0 8.3 ± 2.6 583.1 ± 60.1
NS NS NS
SL
V. verrucosum A. robusta CP Ca P ADF ADL NDF NDIN IVDMD
140.6 ± 9.4 20.6 ± 1.4 1.3 ± 0.2 276.8 ± 12.2 142.8 ± 11.4 426.3 ± 13.7 6.1 ± 0.1 612.8 ± 28.3
∗
NS NS NS NS
V. rotundifolium A. tortilis 177.9 ± 9.4 14.2 ± 1.4 2.1 ± 0.2 281.8 ± 12.2 150.9 ± 11.4 445.4 ± 13.7 7.6 ± 0.1 554.6 ± 28.3
D. cinerea
SL
B. albitrunca
M. senegalensis
Z. Mucronata
172.7 ± 9.4 14.0 ± 1.4 1.3 ± 0.2 270.3 ± 12.2 132.2 ± 11.4 452.8 ± 13.7 9.6 ± 0.1 544.9 ± 28.3
∗
195.8 ± 10.5 9.5 ± 2.3 1.6 ± 0.1 281.6 ± 17.8 140.0 ± 23.8 428.8 ± 20.3 8.3 ± 1.2 558.4 ± 21.4
114.4 ± 10.5 18.3 ± 2.3 1.5 ± 0.1 294.5 ± 17.8 160.3 ± 23.8 422.0 ± 20.3 6.0 ± 1.2 586.8 ± 21.4
171.0 ± 10.5 14.8 ± 2.3 2.0 ± 0.1 280.0 ± 17.8 154.5 ± 23.8 431.5 ± 20.3 8.0 ± 1.2 538.2 ± 21.4
∗∗ ∗∗
NS NS NS NS NS
∗∗∗
NS ∗
NS NS NS NS NS
CP: crude protein, Ca: calcium, P: phosphorous, ADF: acid detergent fibre, ADL: acid detergent lignin, NDF: neutral detergent fibre, NDIN: neutral detergent insoluble nitrogen, IVDMD: in vitro dry matter digestibility, SL: significance level and NS: P > 0.05. ∗ P < 0.05. ∗∗ P < 0.01. ∗∗∗ P < 0.001.
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Parameter
361
362
Plants
CP
Ca
P
ADF
ADL
NDF
NDIN
IVDMD
T. lugardii E. ngamicum V. verrucosum V. rotundifolium
156.0 ± 7.9 163.3 ± 8.2 163.7 ± 7.4 158.4 ± 6.9
16.6 ± 1.2 18.0 ± 1.2 16.2 ± 1.1 14.7 ± 1.0
1.5 ± 0.1 1.7 ± 0.1 1.5 ± 0.1 1.7 ± 0.9
256.7 ± 8.5 31.7 ± 8.8 276.3 ± 7.9 285.1 ± 7.4
125.6 ± 9.4 151.3 ± 9.8 141.9 ± 8.7 150.9 ± 8.2
453.2 ± 10.2 510.0 ± 10.6 441.5 ± 9.5 430.0 ± 9.0
8.0 ± 0.6 8.2 ± 0.6 7.8 ± 0.6 7.3 ± 0.5
474.6 ± 15.8 485.9 ± 16.4 570.8 ± 14.7 555.3 ± 13.7
Overall mean Level of significance
160.6 NS
16.5 NS
1.6 NS
285.5
144.6 NS
458.9
7.9 NS
527.1
∗∗∗
∗∗∗
∗∗∗
CP: crude protein, Ca: calcium, P: phosphorous, ADF: acid detergent fibre, ADL: acid detergent lignin, NDF: neutral acid detergent, NDIN: neutral detergent insoluble nitrogen, IVDMD: in vitro dry matter digestibility and NS: P > 0.05. ∗∗∗ P < 0.001
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Table 2 Mean chemical composition (g/kg DM) and IVDMD (g/kg DM) of four parasitic plants for the 6 months period
Browse tree
CP
Ca
P
ADF
ADL
NDF
NDIN
IVDMD
A. erubescens A. fleckii A. mellifera A. robusta A. tortilis B. albitrunca D. cinerea M. senegalensis Z. mucronata
203.5 ± 13.2 189.0 ± 11.1 213.3 ± 12.0 114.7 ± 12.0 212.0 ± 10.4 188.8 ± 12.0 186.5 ± 12.0 145.8 ± 12.0 200.8 ± 12.0
20.5 ± 2.6 22.3 ± 2.2 27.1 ± 2.4 18.4 ± 2.4 20.4 ± 2.1 20.2 ± 2.4 15.8 ± 2.4 27.9 ± 2.4 23.8 ± 2.4
1.1 ± 0.2 1.1 ± 0.2 1.2 ± 0.2 0.9 ± 0.2 1.5 ± 0.2 0.9 ± 0.2 1.2 ± 0.2 1.0 ± 0.2 1.8 ± 0.2
262.9 ± 19.7 271.8 ± 16.6 241.4 ± 17.8 311.8 ± 17.8 303.9 ± 15.6 298.9 ± 17.8 315.0 ± 17.8 243.2 ± 17.8 230.4 ± 17.8
87.8 ± 23.1 107.3 ± 19.4 106.4 ± 20.9 202.5 ± 20.9 192.0 ± 18.2 132.5 ± 20.9 195.2 ± 20.9 97.2 ± 20.9 109.4 ± 20.9
480.9 ± 14.6 489.0 ± 12.2 374.3 ± 13.2 452.7 ± 13.2 509.8 ± 11.5 442.3 ± 13.2 492.8 ± 13.2 386.3 ± 13.2 357.4 ± 13.2
14.7 ± 1.8 15.8 ± 1.5 8.3 ± 1.6 9.5 ± 1.6 11.9 ± 1.4 10.9 ± 1.6 12.3 ± 1.8 9.7 ± 1.6 11.9 ± 1.6
493.6 ± 35.9 500.7 ± 30.2 621.7 ± 32.4 340.8 ± 32.4 388.8 ± 33.7 583.8 ± 32.4 411.1 ± 32.4 735.6 ± 32.4 672.4 ± 32.4
Overall mean Level of significance
184.1
21.5
1.2
277.7
140.9
445.8
11.7
530.2
∗∗∗
∗
∗
∗∗
∗∗∗
∗∗∗
∗
∗∗∗
CP: crude protein, Ca: calcium, P: phosphorous, ADF: acid detergent fibre, ADL: acid detergent lignin, NDF: neutral acid detergent, NDIN: neutral detergent insoluble nitrogen and IVDMD: in vitro dry matter digestibility. ∗ P < 0.05. ∗∗ P < 0.01. ∗∗∗ P < 0.001.
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Table 3 Mean chemical composition (g/kg DM) and IVDMD (g/kg DM) of browse plants on which the parasitic plants attached
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a month effect for P (P < 0.05), Ca (P < 0.001), CP and IVDMD (P < 0.05) and none for NDF, ADL, ADF and NDIN (P > 0.05) for the browse plants. A negative correlation was observed between IVDMD and ADF (r = −0.50, P < 0.001) for the browse plants, while none was observed between CP and IVDMD (r = 0.14, P > 0.05), between NDIN and CP (r = 0.12, P > 0.05) and between CP and ADF (r = −0.05, P < 0.05). A comparison of leaves and stem between browse and parasitic plants showed that leaves from browse had higher (P < 0.001) CP (182.6±4.6 g/kg DM versus 161.3±4.1 g/kg DM), Ca (21.8±0.7 g/kg DM versus 16.5±0.7 g/kg DM), P (1.2±0.1 g/kg versus 1.6±0.1 g/kg) and NDIN (11.5±0.5 g/kg DM versus 7.5±0.4 g/kg DM). But no difference (P > 0.05) was found for ADF (271.6 ± 6.2 g/kg DM versus 284.0 ± 5.5 g/kg DM), ADL (134.5 ± 7.0 g/kg DM versus 143.5 ± 6.2 g/kg DM), NDF (439.5 ± 7.8 g/kg DM versus 458.9 ± 6.9 g/kg DM) and IVDMD (542.1 ± 14.9 versus. 518.8 ± 12.9 g/kg DM), respectively in leaves of browse plants and parasitic plants.
4. Discussion Observations from this study show that various browse host trees influence certain chemical attributes of some individual parasitic plants, but not IVDMD. The fact that Viscum species were the ones in which some of their nutritional attributes (especially CP) were influenced by browse may be indicative of a unique relationship between these plants and their hosts. V. verrucosum does not have leaves but V. rotundifolium has tiny leaves (Madibela et al., 2000) and may not be able to synthesis complex carbon molecules which E. ngamicum and T. lugardii were able to do due to the presence of leaves. Most parasitic plants are between being hemiparasitic and holoparasitic angiosperms and may be able to fix atmospheric carbon dioxide (Press, 1995). Differences were observed in CP, Ca and P levels of V. verrucosum and V. rotundifolium when these plants attached to different host plants. According to Press (1995), some mistletoes growing on different host species have foliar N concentrations directly related to that of its host species, as was found in the present study. For example, the parasitic plant Tapinanthus bangwensis was reported (Press, 1995; citing Steward and Orebamjo, 1980) to be able to reduce inorganic nitrate to amino acids and that nitrate reduction of the parasite differ between individuals parasitising different hosts. This was thought to be partly due to variation in the supply of nitrate from the host sap. Deeni and Sadiq (2002) also found that the presence or distribution of phytochemical substances in the leaves of African mistletoe, Tapinanthus dodneifolius, was partly dependent on the host plant species. In the present study, the supply of nutrients from the host did not affect structural components of plant cell wall. The fact that ADF, ADL, NDF, NDIN and IVDMD levels in parasitic plants were not influenced by differences in browse plants cannot not be explained. However, these parameters are structural components, and so are the least digestible, and we hypothesis that the host plants affect only the most digestible components of the parasitic plants. Contrary to Madibela et al. (2000), who found a positive correlation between IVDMD and CP, none was found for the parasitic plants in the present study. Browse trees appear to have some effects on the nutritive value of some parasitic plants. Parasitic plants that attached to browse tree with high CP, Ca, P, NDF and IVDMD also had high levels of these nutrients, albeit in lower levels than those of browse trees (Fig. 1). It was
Browse IVDMD P
CP Ca
IVDMD P
700
34.5 32.5 30.5
600
26.5 500
24.5 22.5 20.5
400
18.5 16.5 300
14.5 12.5 10.5
200
8.5 6.5
100
4.5 2.5
0
0.5 Jan
Feb
Mar
Apr
May
Months
Jun
Level of minerals (g/kg DM)
Level of DMD and CP (g/kg DM)
28.5
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CP Ca
Parasitic plants
Fig. 1. Nutritional attributes of browse trees and parasitic plants over a period of 6 months (n = 6). 365
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also observed that CP, Ca, P NDIN in browse trees were higher than that in parasitic plants. According to Press (1995; citing Bannister 1989), New Zealand non-mimic mistletoes generally have lower N concentrations than their host plants. The mimic types are said to have leaves with similar morphology to their hosts and also contain higher levels of N than non-mimics (Press, 1995). This strategy ensures that mimic mistletoes gain a selective advantage by not appearing distinct from their host and thus aim at reduced herbivory. Alternatively, non-mimics contain lower levels of N than their hosts and hence benefit by advertising the fact that their N level is low. Parasitic plants that attach on browse trees found in rangelands of Botswana are usually above the browse level of most browsing animals, except for bigger ungulates such as giraffes and elephants. As a result, they evolved having different leave morphology than their host trees, as they did not need to disguise their presences from herbivores in order to survive. In the present study, plotting CP, Ca, P and IVDMD against time (months) showed an interesting trend between the browse trees and parasitic plants (Fig. 1). The parasitic plants closely followed the pattern of the browse trees, except for Ca. In April there was a relatively large increase in Ca concentration of browse trees, that was not associated with a concomitant increase in Ca content of parasitic plants. April is the start of the dry period and it is not clear if a sudden moisture stress may have caused this effect. Unlike the study by Madibela et al. (2000), who found that the CP of parasitic plants increases from the wet months (January to March) to the dry month (May to June), in the present study CP varied little within the 6-month-sampling period. Crude protein averaged 160 g/kg and the phenomenon of nutrients varying less between seasons has been reported for browse trees (Lukhule and van Ryssen, 2000). Studies by Madibela et al. (2000, 2002, 2003) found differences in CP between parasitic plant species, whereas in the present study differences were not found. The mean level of CP of parasitic plants in the present study was higher than those of previous studies, but similar to a value of 160 g/kg reported by Madibela et al. (2003). Similar to previous studies, levels of Ca, P (Madibela et al., 2000, 2002) and of ADL (Madibela et al., 2000) were not affected by parasitic plant species in the present study. Levels of IVDMD was however higher, about 530 g/kg in the present study, than was previously found for the same plants by Madibela et al. (2000). The discrepancy between the studies cannot be explained except that probably the ratio of leaf to petioles in the edible samples used for the analysis (Abdulrazak et al., 2000) was different between the two studies. NDIN was not affected by parasitic plant species and was of the magnitude of 7.9 g/kg, suggesting that a portion of undegradable CP would escape rumen degradation and be available for post ruminal digestion. These plants have been reported to contain on average 57.0 g/kg condensed tannins (Madibela et al., 2002) and Reed (1986) found a high correlation between NDIN and insoluble proanthocyanidins, indicating the possible formation of tannin–protein complexes. This is consistent with positive correlation found between CP and NDIN in the present study. Some condensed tannins protect plant protein from digestion in the rumen. Subsequently the complex dissociates at abomasal pH providing amino acids for absorption in the small intestine (Waghorn et al., 1987, as cited by McSweeney et al., 1999). However, the benefits of the dissociated protein from the protein–tannins complex is not certain, because plant tannins contained in specific forage and browse plants can have positive or negative effects on N use, and overall livestock performance, depending on the types and concentration of tannins that are present in the diet (Turner, 2001).
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The nine host browse plants evaluated were found to differ in chemical composition and IVDMD, consistent with other studies (Sawe et al., 1998; Abdulrazak et al., 2000; Lukhule and van Ryssen, 2000). In the present study, CP content ranged from 146.0 to 213.0 g/kg DM. Calcium was relatively high, averaging 22 g/kg, and A. robusta had the highest level while B. albitrunca had the least level of Ca. Results from pasture clipping in Botswana over several years have shown that phosphorous rarely reaches 1.0 g/kg DM at any time of the year to satisfy the minimum levels required by livestock (APRU, 1980). In the present study, P levels in browse trees were 1.2 g/kg DM, indicating their potential in providing P to livestock. Abdulrazak et al. (2000) reported lower Ca and P levels for Acacia trees from Kenya than those found in the present study. The difference may be due to regional difference in soils and climatic conditions. Dicalcium phosphate is a common mineral supplement in Botswana, but the inaccessibility of the mineral lick to resource poor farmers means that their animals requirement for these minerals are often not met (Madibela et al., 2002). Calcium is associated with P metabolism of bones and Ca:P ratio of 2:1 is recommended (Abdulrazak et al., 2000). An average Ca:P ratio of 17.9:1 in browse tree was observed in the present study, indicating that if fed as the sole feed, browse trees provide an unbalanced source of these minerals. However, the usefulness of P would depend on its bioavailability to the animals, which was not determined in the present study. The ADF content of browse trees were similar to an average value (277.7 g/kg DM versus 287.8 g/kg DM) for leaves from indigenous fodder trees in South Africa reported by Lukhule and van Ryssen (2000). Differences were found in NDF, whereby levels were higher (445.8 g/kg DM versus 365.8 g/kg DM) than values reported for browse trees in South Africa by Lukhule and van Ryssen (2000). The high value of NDF found in the present study may be due to differences in the ratio of leaf to petioles in edible samples (Abdulrazak et al., 2000). Inclusion of woody twigs during sampling may explain this observation, since twigs contributes to higher NDF (Topps, 1992). Sixty-three percent of NDF was ADF, which indicates a high content of cellulose and lignin and low levels of hemicellulose. The higher (12.0 g/kg DM) amounts of NDIN found in browse trees than in parasitic plants probably suggest that a high level of undegradable CP would be unavailable to the host animal. This is likely to be the case with Acacia robusta and A. tortilis, which have lower IVDMD values than the mean (530 g/kg) by 18.9 and 14.1% units, respectively. The proportion of NDIN in browse trees in the present study was however lower than those of Acacia tree leaves from Kenya (Abdulrazak et al., 2000).
5. Conclusions Browse host plants influence CP, Ca, P only in V. verrucosum and V. rotundifolium. This effect may be due to variation in nutrient supply by the host browse plants or the fact that the Viscum species do not have leaves, while E. ngamicum and T. lugardii do and were able to synthesis complex carbon molecules. The levels of CP, P and IVDMD of parasitic plants followed the same pattern as that of browse over the 6-month-sampling period. Browse trees however, had high levels of CP, Ca, P and NDIN. The diversity of browse trees and parasitic plants, and their associated high nutritive value warrant their use as supplements for livestock by resource poor farmers who cannot access commercial feed supplements.
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Acknowledgements The authors would like to recognize input by staff at Feed and Plants Laboratory of Department of Agriculture Research (DAR). The authors would also like to recognize Drs. J. Macala (DAR) and U.J. Omphile (Botswana college of Agriculture) for critiquing the manuscript. J. Makore is acknowledged for helping with statistical analysis. References Abdulrazak, S.A., Fujihara, T., Ondiek, J.K., Ørskov, E.R., 2000. Nutritive evaluation of some Acacia trees leaves from Kenya. Anim. Feed Sci. Technol. 85, 89–98. Aganga, A.A., Monyatsiwa, C.B., 1999. Use of browse (Terminalia serecia, Combretum apiculatum or Eulea schimperi) as supplement for growing Tswana goats. Trop. Anim. Health Prod. 31, 295– 305. AOAC, 1996. Official Methods of Analysis. Association of Official Analytical Chemists, Washington, DC. APRU, 1980. APRU (Animal Production Research Unit), 1980. Handbook on Beef Production and Range Management in Botswana. Government Printers, Gaborone. Deeni, Y.Y., Sadiq, N.M., 2002. Antimicrobial properties and phytochemical constituents of leaves of African mistletoe (Tapinanthus dodoneifolius (DC) Danser) (Loranthaceae): an ethnomedicinal plant of Hausaland, Northern Nigeria. J. Ethnopharmacol. 83, 235–240. De Wit, P.V., Nachtergaele, F.O., 1990. Explanatory note on the soil mapping of the Republic of Botswana. FAO/UNDP/Government of Botswana. Soil Mapping and Advisory Services Project (FAO/BOT/85/011). Field Document 30. Kabasa, J.D., Opuda-Asido, J., ter Meulen, U., 2000. The effect of oral administration of polyethylene Glycol on faecal helminth egg counts in pregnant goats grazed on browse containing tannins. Trop. Anim. Health Prod. 32, 73–86. Lukhule, M.S., van Ryssen, J.B.J., 2000. The chemical composition of leaves from indigenous fodder trees in South Africa. S. Afr. J. Anim. Sci. 30 (Suppl. 1), 72–73. Madibela, O.R., Boitumelo, W.S., Letso, M., 2000. Chemical composition and in vitro dry matter digestibility of four parasitic plants (Tapinanthus lugardii, Erianthenum ngamicum, Viscum rotundifolium and Viscum verrucosum) in Botswana. Anim. Feed Sci. Technol. 84, 97–106. Madibela, O.R., Letso, M., Boitumelo, W.S., Masedi, M., Alton, K., 2002. Chemical composition of four parasitic plants harvested over a period of 6 months from two sites in Botswana. Anim. Feed Sci. Technol. 95, 159– 167. Madibela, O.R., Mabutho, S., Sebolai, B., 2003. Dry matter and crude protein degradability of four parasitic plants (mistletoes) associated with browse trees in Botswana. Trop. Anim. Health Prod. 35, 365–372. Madibela, O.R., Jansen, K., 2003. The use of indigenous parasitic plant (Viscum verrocosum) in reducing faecal egg counts in female Tswana goats. Livestock Res. Rural Dev. 15 (9) http://www.cipav.org.co/lrrd/lrrd15/9/ madi159.htm. McSweeney, C.S., Dalrymple, B.P., Gobius, K.S., Kennedy, P.M., Krause, D.O., Mackie, R.I., Xue, G.P., 1999. The application of rumen biotechnology to improve the nutritive value of fibrous feedstuffs: pre- and post ingestion. Livestock Prod. Sci. 59, 265–283. Press, M.C., 1995. Carbon and nitrogen relations. In: Press, M.C., Graves, J.C. (Eds.), Parasitic Plants. Chapman and Hall, London, pp. 110–112. Reed, J.D., 1986. Relations among soluble phenolics, insoluble proanthocyanidins and fibre in East African browse species. J. Range Manage. 39, 5–7. SAS Institute Inc., 1990. SAS User’s Guide. Statistics Version 6. SAS Institute Inc., Cary, NC, USA. Sawe, J.J., Tuitoek, J.K., Ottaro, J.M., 1998. Evaluation of common tree leaves or pods as supplements for goats on range area of Kenya. Small Rumin. Res. 28, 31–37. Sokal, R.R., Rohlf, F.J., 1969. Biometry. The Principles and Practice of Statistics in Biological Research, second ed. p. 244.
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