Arboreal Legume Litter Nutrient Contribution to a Tropical Silvopasture

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Arboreal Legume Litter Nutrient Contribution to a Tropical Silvopasture
Article  in  Agronomy Journal · November 2016
DOI: 10.2134/agronj2016.02.0120
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Valéria X. O. Apolinário
Instituo agronomico de pernambuco
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José Carlos Batista Dubeux Jr.
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2478	 Agronomy	 Journa l 	 • 	 Volume	108 , 	 I s sue	6	 • 	 2016
Understanding soil–plant–atmosphere nutrient dynamics allows the design of appropriate pasture management procedures, to maintain soil fertility, 
ecosystem sustainability, and animal productivity. Th is knowl-
edge is especially important in tropical regions, where edapho-
climatic conditions oft en result in nutrient leaching and low 
soil fertility (Pinho et al., 2012). Introducing arboreal legumes 
into tropical pastures might contribute to maintaining soil fer-
tility through symbiotically fi xed N and to mitigate soil surface 
erosion through litter deposition. Arboreal legumes might also 
increase ruminant crude protein intake directly via legumes 
and indirectly through N-enriched associated grasses, (Paciullo 
et al., 2010; Freitas et al., 2011). Arboreal legumes can provide 
other environmental benefi ts such as C sequestration, slowing 
the increase of CO2 atmospheric concentration, a greenhouse 
gas (Pinho et al., 2012).
Legume tree litter cycles nutrients within the soil-plant-
animal complex. Its deposition provides thermo-insulation to 
the soil surface which mitigates erosion and evaporative soil 
moisture loss, which are important for seedling establishment 
and plant growth (Dubeux et al., 2006). Litter decomposition 
promotes mesofauna and microorganism growth and increased 
biodiversity. Decomposition is infl uenced not only by the litter 
chemical characteristics such as C/N, C/P, and lignin/N ratios 
(Heal et al.,1997), but also by other environmental factors, 
such as soil fertility and fertilization, microorganism activity 
and diversity and animal stocking rate (Dubeux et al., 2006). 
Legume litter has higher recycling rates than tropical grass due 
to its lower C/N ratio (Caldeira et al., 2013). Not all litter with 
high N concentration presents net N mineralization. Lignin > 
150 g kg–1 and polyphenol > 30 to 40 g kg–1 can result in net N 
immobilization (Palm et al., 1997).
Stable isotopes such as 15N has been used to assess symbiotic 
N2 fi xation by tree legumes in agroforestry systems (Boddey 
et al., 2000; Sierra et al., 2007; Apolinário et al., 2015). Major 
Arboreal	Legume	Litter	Nutrient	Contribution	
to	a	Tropical	Silvopasture
Valéria	Xavier	de	Oliveira	Apolinário,	José	Carlos	Batista	Dubeux,	Jr.,*	Mário	de	Andrade	Lira,	
Everardo	V.	S.	B.	Sampaio,	Silvânia	Oliveira	de	Amorim,	
Nalígia	Gomes	de	Miranda	e	Silva,	and	James	P.	Muir
Published in Agron. J. 108:2478–2484 (2016)
doi:10.2134/agronj2016.02.0120
Received 23 Feb. 2016
Accepted 18 Aug. 2016
Copyright © 2016 by the American Society of Agronomy
5585 Guilford Road, Madison, WI 53711 USA
All rights reserved
aBstract
Legumes contribute to pasture sustainability through sym-
biotic N2 fi xation, which may increase primary productivity 
and animal performance in low-input systems. Litterfall is the 
main way of cycling nutrients from tree legumes. We quanti-
fi ed gliricidia [Gliricidia sepium (Jacq.) Kunth ex Walp.]and 
sabiá (Mimosa caesalpiniifolia Benth) litter deposition, along 
two 336-d cycles, in a signalgrass (Brachiaria decumbens Stapf.) 
pasture. Litterfall was produced throughout the year but con-
centrated in the dry season. Sabiá produced slightly greater 
(P < 0.0001) litterfall amounts in the two cycles (10,790 kg ha–1) 
than gliricidia (10,420 kg ha–1) but the overall average N con-
centration of gliricidia (21.5 g kg–1) was greater than that of 
sabiá (18.8 g kg–1). Nitrogen amounts cycled through the litter 
were greater for gliricidia in both cycles (105 and 109 kg N ha–1) 
than for sabiá (87 and 98 kg N ha–1). Th e proportions of litter 
N that were derived from the atmosphere by symbiotic fi xation 
were similar (P ≥ 0.05) in both species (55%) and varied little 
along the two cycles. Lignin concentration, which infl uences 
decomposition, was similar in both species, averaging 238 and 
214 g kg–1 in the two cycles for gliricidia and 233 and 246 g kg–1
for sabiá. Greater N concentration, lower C/N ratio and lower 
lignin concentration indicate that gliricidia litter may have a 
faster cycling rate than sabiá litter. Sabiá could be a more prom-
ising species for soil cover and protection because of its slower 
litter decomposition rate.
V.X.O. Apolinario and M.A. Lira, Inst. Agronômico de Pernambuco, 
Av. General San Martin, 1371, Bongi, Recife, PE 50761-000 Brazil; 
J.C.B. Dubeux, Jr., Univ. of Florida, North Florida Research and 
Education Center, 3925 Highway 71, Marianna, FL 32446; E.V.S.B. 
Sampaio, Univ. Federal de Pernambuco, Av. Prof. Moraes Rego, 1235, 
Cid. Universitária, Recife – PE, Brazil 50670-901; S.O. de Amorim 
and N.G.M. Silva, Univ. Federal Rural de Pernambuco, Rua Dom 
Manoel de Medeiros, SN, Dois Irmaos, Recife 52171-900 Brazil; J.P. 
Muir, Texas A&M AgriLife Research, 1229 N. U.S. Highway 281, 
Stephenville, TX 76401. Part of a doctoral dissertation fi nanced by 
CNPq and FACEPE, and supported by the Pernambuco Agricultural 
Inst. (IPA) and Federal Rural Univ. of Pernambuco (UFRPE) Brazil. 
*Corresponding author (dubeux@ufl .edu).
Abbreviations: BNF, biological nitrogen fi xation.
core ideas
•	 Litter deposition was an important pathway of N return in 
warm-climate silvopasture systems.
•	 Tree legumes added signifi cant amounts of biological nitrogen 
fi xation to silvopasture systems.
•	 Gliricidia litter presented better quality than Mimosa litter.
•	 Proportion of litter N derived from atmosphere was signifi cant.
 soil fertility & croP nutrition
Published November 3, 2016
Agronomy	 Journa l 	 • 	 Volume	108,	 Issue	6	 • 	 2016	 2479
limitations to assess biological nitrogen fixation (BNF) in 
woody perennials include: (i) plant-to-plant variation; (ii) 
long-term, perennial nature of growth and seasonal changes 
in patterns of N assimilation; (iii) logistics of harvesting trees 
(Boddey et al., 2000). Gathumbi et al. (2002) assessed BNF 
by tree legumes using the natural abundance method. They 
observed that most tree/shrub legumes showed no 15N dis-
crimination during BNF, however, significant discrimination 
occurred during translocation from roots to shoots. They con-
cluded that the natural δ15N abundance method is a useful tool 
for estimating the amount of N derived from BNF.
Nitrogen transfer from tree legumes to the companion grass 
is a key aspect of the N cycle in agroforestry systems (Sierra 
et al., 2007). Tree legumes might transfer fixed atmospheric-
N2 by litter fall, root exudates, or cattle excreta, benefiting 
the companion signalgrass. Trannin et al. (2000) assessed N 
transfer from an herbaceous legume (Stylosanthes guianensis 
‘Mineirão’) to signalgrass. The main pathway of belowground 
N transfer from the legume to the grass occurred via decompo-
sition of roots rather than via root exudates or direct mycorrhi-
zal hyphae transfer. In a multispecies grassland, Pirhofer-Walzl 
et al. (2012) observed that grasses having fibrous roots received 
greater amounts of N from legumes than dicotyledoneous 
plants which generally have tap roots. Therefore, addition 
of tree legumes are expected to enhance the N cycling and 
improve productivity of signalgrass pastures. In the current 
study, the tree legumes were established on a degraded area 
of signalgrass, with declining productivity and low soil fertil-
ity. The strategy is to enhance nutrient cycling and recover 
degraded signalgrass pastures by adding tree legumes.
In spite of the increasing importance of arboreal legumes in 
silvopastoral systems of tropical regions (Paciullo et al., 2011), 
few reports have been published reporting the amounts of 
nutrients that are recycled though their litterfall (Leόn and 
Osorio, 2014). There is even less information available on how 
much N derived via symbiotic fixation is incorporated into the 
soil and eventually transferred to the grass plants in the pasture 
(Xavier et al., 2014). Considering this scarcity of information 
and to better understand the incorporation and recycling of N 
by tree legumes in a tropical silvopastoral system, we measured 
litterfall of two tree legume species in a signalgrass pasture, 
along 2 yr, in Pernambuco, Brazil, determining incorporation 
of atmospheric N by the 15N natural abundance technique.
Material and Methods
site description
Litterfall measurements were performed from April 2012 
to March 2014, in an experiment previously established 
at Itambé Experiment Station, Pernambuco State, Brazil, 
located at 7°23¢ S, 35°10¢ W, with an average altitude of 
189 m. Average annual rainfall is 1200 mm and temperature 
25°C (Beltrão et al., 2005). Rainfall was recorded during the 
experimental period (Fig. 1). The soil in the area is classified 
as an Ultissol (red-yellow dystrophic Argissol according to 
the Brazilian Soil Classification). Soil analyses of samples 
collected from the top 0 to 20 cm of the experimental area, 
according to the EMBRAPA (2009) methods, showed: 
pH (water– 1:2.5) = 5.4; Mehlich-1 P = 3.2 g m–3; Na+ = 
1 molc m
–3; K+ = 17 molc m
–3; Mg2+ = 20 molc m
–3; Ca2+ = 
33 molc m
–3; Al+3 = 2 molc m
–3; H + Al = 65 molc m
–3; and 
organic matter = 43.1 g kg–1. Prior to the establishment of the 
experiment, the area received 100 kg ha–1 of P2O5 ha
–1 as triple 
super phosphate and 120 kg ha–1 of K2O as potassium chloride.
The experiment had been set up in 2008 (Apolinário et al., 
2015) as a randomized block design with plots, replicated four 
times, planted with gliricidia or sabiá trees, in an already estab-
lished pasture of signalgrass. In each 33 by 20 m plot the trees 
were planted in three double rows spaced 10 by 1 by 0.5 m, ori-
ented in the North–South direction (Fig. 2). The signalgrass 
occupied the space between the double rows as described by 
Silva et al. (2013). In 2012, when the current study started, 
the arboreal legumes had an average height slightly above 
5 m (Apolinário et al., 2015). Every 6 mo the blocks were 
mob grazed, using crossbred 5/8 Holstein/zebu cattle as put-
and-take animals, which were introduced to pastures when 
the sward height reached 50 cm and taken off at 10 to 15 cm 
stubble height (Apolinário et al., 2015).
Litter deposition was collected every 28 d, for 24 cycles, 
from trays 0.25 m2, made of a wooden frame covered with 
nylon mesh, following the methods described by Bruce and 
Ebersohn (1982) and modified by Dubeux et al. (2006). Forty 
trays (sampling unit) were placed per plot, in five positions in 
relation to the tree trunks, with eight replications within each 
plot: 0.5, 1.0, 1.5, 2.0 and 3.0 m distant from the trunk bases. 
The litter of all distances of each replicate was pooled together 
and weighed and a representative subsample was weighed, dried 
at 55°C in a forced-air oven and weighed again to determine 
Fig.	1.	Monthly	rainfall	at	the	Itambé	Experiment	Station	during	the	trial	(April	2012–March	2014);	Itambé,	Pernambuco	State,	Brazil.
2480	 Agronomy	 Journa l 	 • 	 Volume	108,	 Issue	6	 • 	 2016
ash-free dry biomassas described by AOAC (2007). Acid deter-
gent fiber (ADF) and lignin were determined as described by 
Van Soest et al. (1991), using an autoclave, according to Pell 
and Schofiel (1993).
Part of the subsample was used to determine C, N and 15N 
by mass spectrophotometry with a Vario Micro Cube (CHNS 
analyzer using the Dumas dry combustion method; Elementar, 
Hanau, Germany) interfaced with an ISOPRIME 100 Isotope 
Ratio Mass Spectrometer (Elementar, Manchester, UK). Values 
were expressed as d units, defined as the difference per one 
thousand (0) of 15N abundance in the sample relative to the 
standard (atmospheric N2), by the equation:
( )15 RsampleN ‰ =1000 × 1
Rstandard
d  - 
 
where Rsample and Rstandard are the 15N/14N ratios of the 
litter sample and standard atmospheric N2, respectively.
The proportion of the litter N derived from the atmosphere 
by symbiotic fixation (%Ndfa) was estimated by the equation 
described by Shearer and Kohl (1986):
15 15
15
Nreference Nlegume
%Ndfa =100×
Nreference B
d d
d
-
-
where δ15Nreference is the 15N signal of a non-N fixing species, 
taken as a reference species; δ15Nfixing is the 15N abundance 
in the litter of the two legume fixing species (gliricidia and 
sabiá) and B (also known as B value) is the δ15N of the fixing 
plant in the absence of N. The B value for gliricidia was consid-
ered as –1.45 (Boddey et al., 2000) and that for sabiá as –1.23 
(Reis et al., 2010). Jurubeba (Solanum paniculatum L.), mango 
(Mangifera indica L.) and cashew tree (Anacardium occidentale 
L.) were taken as reference species and senescent leaves from 
several specimens surrounding the experimental were collected, 
dried, and analyzed for δ15N, as described. The average value of 
the three species was used in Eq. [2].
We analyzed dependent variable data as repeated measures 
using PROC MIXED with SAS (SAS Institute, 1996). Fixed 
effects included species, months, and years. Blocks and their 
interactions with fixed effects were considered random effects. 
Monthly (28 d periods) evaluation was considered the repeated 
measure. Means were compared using LSMEANS adjusted for 
Tukey’s test at 5% probability for species, months, and years. 
Differences were considered significant at P ≤ 0.05.
results and discussion
The two legume species had similar litter deposition patterns 
throughout the two consecutive 12 28-d cycles, the patterns of 
the first cycle being slightly different from those of the second 
cycle (Fig. 3). In both cycles, the lowest deposition occurred 
in the rainy season and the greatest in the beginning of the 
dry season. The first cycle, which included most of the drier 
2012 yr (Fig. 1), had a shorter period of high litterfall, with two 
peaks, contrasting with the longer high litterfall period with 
a single peak of the rainier 2013 yr. In spite of this difference, 
the total amounts of litterfall in the two cycles were similar 
for both gliricidia (5096 and 5312 kg ha–1) and sabiá (5486 
and 5305 kg ha–1) in the two 336-d cycles, the sum of the two 
cycles being slightly, but significantly (P < 0.001), greater for 
sabiá. This indicates that rainfall affected litter deposition 
but even in the drier year, water availability must have been 
Fig.	2.	Plot	layout	demonstrating	double	rows	(dashed	lines)	and	
plant	spacing;	figure	not	drawn	to	the	scale.
Fig.	3.	Litterfall	along	two	336-d	cycles	in	a	silvopasture	system	at	Itambé	municipality,	Pernambuco	state,	Brazil.	Total	gliricidia	
10,415	kg	ha–1	and	sabiá	10,791	kg	ha–1	of	ash-free	biomass.
Agronomy	 Journa l 	 • 	 Volume	108,	 Issue	6	 • 	 2016	 2481
Fig.	4.	Gliricidia	and	sabiá	litter	N	(A)	concentration	and	(B)	deposition	in	a	silvopasture	system	at	Itambé	municipality,	Pernambuco	state,	Brazil.
Fig.	5.	(A)	Proportion	of	the	total	N	in	the	litter	biomass	and	(B)	amount	of	N	deposited	by	the	litter	derived	from	symbiotic	fixation	by	
gliricidia	and	sabiá	trees	growing	in	a	silvopastoral	system	at	Itambé	municipality,	Pernambuco	state,	Brazil.
2482	 Agronomy	 Journa l 	 • 	 Volume	108,	 Issue	6	 • 	 2016
sufficient to allow for high biomass productivity. The total 
amounts of produced litter are lower than those reported in 
tropical forests and other highly productive ecosystems, which 
can reach the range of 10 to 17 t ha–1 (Leόn and Osorio, 2014). 
The amounts of litter observed in the current study, however, 
can be considered similar taking into account the size and 
number of the legume trees in the silvopastoral system. These 
amounts corresponded to about 10% of the total aboveground 
biomass of the legume trees in the area (Apolinário et al., 
2015). Besides this contribution to the cycling of C in the sys-
tem, an unknown underground biomass must turn over every 
year, including exudates, root death, and decomposition (Pinho 
et al., 2012). Root biomass in tropical humid vegetation usu-
ally ranges from 10 to 20% of the total aboveground biomass 
(Mokany et al., 2006).
The N concentrations in the ash-free biomass of the gliri-
cidia litter was slightly greater than those of sabiá along most 
of the two measurement cycles, with little monthly variation, 
except for the peaks in March 2013, the month with the low-
est litterfall amounts (Fig. 4A). Greater litter N observed in 
March 2013 might be due to water deficit leading to abscis-
sion of immature leaves as litter. In April 2013 the rainfall 
season started and litter N returned to its average pattern. 
The peak observed in March 2013 did not repeat in 2014. A 
possible explanation is the greater rainfall occurred during 
the 2013–2014 season. The overall average for gliricidia litter 
N was 21.5 g kg–1 while that of sabiá was 18.8 g kg–1. These 
concentrations are below those of the average live plant parts, 
except thicker branches (Apolinário et al., 2015), as a result 
of the internal translocation before the senescence of leaves 
and branches (Pirhofer-Walzl et al., 2012). The small monthly 
variation of litter N concentration means that the patterns of 
N deposition followed primarily those of the litterfall biomass 
(Fig. 4B). The N amounts cycled through the litter were greater 
for gliricidia in both periods (105.3 and 108.7 kg ha–1) than 
for sabiá (87.3 and 98.3 kg ha–1). On average, gliricidia had 
lower C/N ratio (20:1) than sabiá (24:1), indicating a likely 
faster decomposition rate and nutrient release (Apolinário et 
al., 2015). However, both ratios were below 30:1, a threshold 
below which mineralization tends to prevail over immobiliza-
tion (Heal et al., 1997), depending on other litter character-
istics and environmental factors (Caldeira et al., 2013). In a 
long-term experiment (11 yr) in Africa, addition of gliricidia 
prunings increased maize (Zea mays L.) yield and soil chemi-
cal properties (Makumba et al., 2006), reflecting the quality of 
gliricidia residue.
The proportions of the N in the litter that were derived from 
the atmosphere (%Ndfa) by the symbiotic fixation were similar 
in both species and varied little along the two cycles (Fig. 5A), 
averaging 55% for both species. As expected, this proportion 
is very close to those fixed by the plants in the live material 
(58% for gliricidia and 54% for sabiá; Apolinário et al., 2015), 
since N must have been fixed continuously along the period 
and easily translocated, becoming well distributed within the 
plants (Pirhofer-Walzl et al., 2012). Multiplying the %Ndfa 
by the amount of N in the litterfall, the N deposited via lit-
terfall originated from biological N2–fixation correspond to 74 
and 56 kg N ha–1 cycled by the litter of gliricidia and 46 and 
54 kg N ha–1 by sabiá, along the two 12 28-d periods, respec-
tively (Fig. 5B). Reports of proportions of fixed N in litter are 
Fig.	6.	Gliricidia	and	sabiá	litter	lignin	concentration	in	a	silvopastoral	system	at	Itambé	municipality,	Pernambuco	state,	Brazil.
Fig.	7.	Gliricidia	and	sabiá	litter	lignin/N	ratio	in	a	silvopastoral	system	at	Itambé	municipality,	Pernambucostate,	Brazil.
Agronomy	 Journa l 	 • 	 Volume	108,	 Issue	6	 • 	 2016	 2483
not common in the literature and very scarce in relation to 
tree legumes in silvopastoral systems (Bouillet et al., 2008) but 
more information is available regarding proportions of fixed 
N in live plants (Freitas et al., 2010). Values around 50% and 
even greater are commonly found (Xavier et al., 2014), repre-
senting amounts that can reach up to a few hundred kilograms 
(Paulino et al., 2009), however, values <100 kg N ha–1 yr–1 are 
more typical. This is certainly an important contribution to a 
silvopastoral system, adding N that can increase grass produc-
tion in the system and, eventually increase cattle production or 
reduce the need of concentrate feeding (Paciullo et al., 2011). 
Livestock browse gliricidia more extensively than they do on 
sabia, and that might be a decision factor on what tree to estab-
lish. If the main goal is the lumber production, sabia should 
be preferred. If improved livestock nutrition is key, gliricidia 
should be preferred.
Lignin concentration, one of the key factors influencing 
litter decomposition, was similar in both species, averaging 
238 and 214 g kg–1 in the two 336-d cycles for gliricidia and 
233 and 246 g kg–1 for sabiá (Fig. 6). Due to the greater N 
concentration of gliricidia, its lignin/N ratio was slightly lower 
(Fig. 7). Lignin/N ratio is negatively correlated with biomass 
loss (Thomas and Asakawa, 1993) and it is an important 
indicator of long-term decay (Magid et al., 1997). Lignin/N 
fluctuated based on lignin and N concentration, with N con-
centration varying more along the season, reducing lignin/N. 
In general, lignin concentrations were greater than those found 
in grasses (Liu et al., 2011), but legume lignin is concentrated 
primarily in xylem tissue, which may facilitate N mineral-
ization, whereas in grasses, lignin is found more in vascular 
bundles, sclerenchyma, and parenchyma, thereby making it 
recalcitrant to breakdown (Kerbauy, 2008).
conclusions
Sabiá produced slightly greater (P < 0.0001) litterfall 
amounts in the two cycles (10,791 kg ha–1) than gliricidia 
(10,415 kg ha–1), but with lower litter N concentration (18.8 
and 21.5 g kg–1, respectively). Thus, the N amounts cycled 
through the litter were greater for gliricidia in both cycles (105 
and 109 kg N ha–1) than for sabiá (87 and 98 kg N ha–1). The 
proportion of litter N that was derived from the atmosphere by 
symbiotic fixation were similar in both species (55%) and var-
ied little along the two cycles. Lignin concentration was similar 
in both species, averaging 238 and 214 g kg–1 in the two cycles 
for gliricidia and 233 and 246 g kg–1 for sabiá. Greater litter N 
concentration, lower litter C/N ratio, and lower lignin concen-
tration indicate that gliricidia litter may have a faster cycling 
than sabiá litter, besides adding more symbiotic N to the 
system. Sabiá could be a more promising species for soil cover 
and protection due to its high C/N ratio. The results from this 
study reflect the importance of litter deposition as a pathway of 
N return in tropical silvopasture systems.
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