Review

Ecophysiological constraints on the production of shaded

and unshaded coffee: a review
Fabio M. DaMatta
*
Departamento de Biologia Vegetal, Universidade Federal de Vicosa, 36571-000 Vicosa, MG, Brazil
Received 21 May 2003; received in revised form 27 August 2003; accepted 2 September 2003
This review is dedicated to Dr. M. Antonieta Nunes (IICT, Portugal) on the occasion of her retirement
Abstract
The ecophysiological constraints on the production of the arabica and robusta coffee under shading or full sunlight are
reviewed. These two species, which account for almost all the worlds production, were originally considered shade-obligatory,
although unshaded plantations may out-yield shaded ones. As a rule, the benets of shading increase as the environment
becomes less favorable for coffee cultivation. Biennial production and branch die-back, which are strongly decreased under
shading, are discussed. The relationships between gas exchange performance and key environmental factors are emphasized.
Ecophysiological aspects of high density plantings are also examined.
# 2003 Elsevier B.V. All rights reserved.
Keywords: Coffea; Environmental factors; Gas exchange; High density planting; Photosynthesis; Shading
1. Introduction
Coffee is the most important commodity in the
international agricultural trade, representing a signi-
cant source of income to several Latin American,
African and Asian countries. In 2000/2001, coffee was
planted on some 11 million ha, yielding 115 million
bags (60 kg) of green coffee beans, of which Coffea
arabica L. (arabica coffee) accounted for 63%, and
C. canephora Pierre (robusta coffee) the remainder
of the coffee produced. This paper reviews the produc-
tion of shaded and unshaded coffee of these two
species.
Coffee is native to tropical Africa where it is
believed to have evolved as an understorey tree.
Early plantations were shaded by planting overstorey
trees to simulate the natural habitat. In many situa-
tions, however, coffee grows well without shade and
even out-yields shaded coffee (Fournier, 1988; Beer
et al., 1998). Shading was therefore abandoned as a
regular cultural practice in several regions. In Brazil,
the worlds largest coffee producer, the practice was
almost completely abandoned in 1950s (Malavolta,
2000).
The question of whether the coffee tree benets or
not from shelter trees has been disputed for more than
a century (Lock, 1888; Mayne, 1966; Gopal et al.,
1970; Fournier, 1988; Muschler, 1997; Beer et al.,
1998; DaMatta and Rena, 2002). Yield potential,
competition for water and nutrients, and pest/disease
incidence are central issues in this controversy (Beer
et al., 1998). Unshaded plantations generally require
high levels of external inputs to maximize crop yield
Field Crops Research 86 (2004) 99114
*
Fax: 55-31-3899-2580.
E-mail address: fdamatta@ufv.br (F.M. DaMatta).
0378-4290/$ see front matter # 2003 Elsevier B.V. All rights reserved.
doi:10.1016/j.fcr.2003.09.001
limitaciones
sin sombreamiento mismo rendimiento
rendimiento
resto
sotobosque
estrato superior
and are often associated with soil degradation and
environmental pollution. Small holder producers of
unshaded coffee face serious economic risks related
to high variable costs and unstable market prices.
On the other hand, shaded plantations conserve natural
resources, require less inputs and provide a more
stable income due to cash income supplement pro-
vided by fruits or timber from the shelter trees. These
characteristics of shaded coffee have stimulated
renewed interest in the use of shade trees, particularly
in areas where they had previously been eliminated
(Beer et al., 1998).
Previous reviews on the ecophysiology of the coffee
tree (e.g. Maestri and Barros, 1977; Cannell, 1985;
Rena et al., 1994; Barros et al., 1995, 1999) did not
examine various aspects related to shade and produc-
tion. Knowledge about this issue is useful for estab-
lishing the best management practices as well as for
designing coffee production systems. This review
focuses on ecophysiological aspects of both shaded
and unshaded coffee production, but does not discuss
shade management (Beer, 1987; Beer et al., 1998).
The review is organized into sections dealing with (i)
climatic factors and requirements, (ii) shading and
yield, (iii) branch die-back, (iv) effects of climatic
factors (radiant energy, temperature, wind and relative
humidity) on gas exchange and production, and (v)
high density plantings.
2. Climatic factors and requirements
Before examining, the shade effects on the ecophy-
siologyof the coffee tree, it would be helpful to describe
the basic climatic characteristics of the regions where
coffee is believed to be indigenous, in order to ensure a
better understanding of its response to environmental
constraints.
Arabica coffee is native to Ethiopian tropical forests
at altitudes of 16002800 m. In this region, air tem-
perature shows little seasonal uctuations, averaging
annually at about 20 8C. Rainfall is well distributed,
varying from 1600 to more than 2000 mm, with a dry
season lasting 34 months coinciding with the coolest
months. In this environment, arabica coffee became
established as an understorey shrub (Sylvain, 1955).
Robusta coffee, in turn, is native to the lowland forests
of the Congo river basin which extend up to Lake
Victoria in Uganda. The altitude of this vast region
varies from sea level up to 1200 m in Uganda. This
species developed as a midstorey tree in dense, equa-
torial rainforest. In that region, the average temperature
is between24and26 8C, without wide oscillations, with
abundant rainfall superior to 2000 mm distributed over
a 910-month period, and with air humidity at a near
constant level approaching saturation (Coste, 1992).
The optimum mean annual temperature range for
arabica coffee is 1821 8C (Ale`gre, 1959). Above
23 8C, development and ripening of fruits are acceler-
ated, often leading to loss of quality (Camargo, 1985).
Continuous exposure to temperatures as high as 30 8C
results not only in depressed growth but also in
abnormalities such as yellowing of leaves and growth
of tumors at the base of the stem (Franco, 1958).
Relatively high temperature during blossoming, espe-
cially if associated to a prolonged dry season, may
cause abortion of owers (Camargo, 1985). In regions
with mean annual temperature below 18 8C, growth is
largely depressed. Occurrence of frosts, even if spora-
dic, may limit strongly the success of the crop, as
occurs in some Brazilian regions producing arabica
coffee. In addition, slow development of fruits results
in late ripening which, in several cases, may overlap or
even surpass the next blossoming (Camargo, 1985).
For robusta coffee, the optimum annual mean tem-
perature ranges from 22 to 26 8C (Matiello, 1998), or
according to Willson (1999), from 24 to 30 8C. High
temperatures are harmful, especially if the air is dry
(Coste, 1992). Robusta is much less adaptable to lower
temperatures than arabica. Both leaves and fruits
neither withstand temperatures below 56 8C nor long
periods at 15 8C (Willson, 1999).
The optimum annual rainfall range is 1200
1800 mm for arabica coffee (Ale`gre, 1959). A similar
range seems to be required for robusta, although it
adapts better than arabica to intensive rainfall exceed-
ing 2000 mm (Coste, 1992). For both species, a short
dry spell, lasting 24 months, corresponding to the
quiescent growth phase, is important to trigger ower-
ing (Haarer, 1958). Abundant rainfall throughout the
year is often responsible for scattered harvest and low
yields. Lack of a dry period can also limit coffee
cultivation in lowland tropical regions (Maestri and
Barros, 1977).
Air humidity has a signicant impact on the vegeta-
tion of the coffee tree. Robusta thrives well under high
100 F.M. DaMatta / Field Crops Research 86 (2004) 99114
abrigo
renovado
tratar
indigena
arbusto
superar
no soportan
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dispersin
prospera
air humidity approaching saturation. It also does well
in less humid sites provided dry season is short. By
contrast, arabica coffee requires a less humid atmo-
sphere, comparable to that of the Ethiopian highlands
(Haarer, 1958; Coste, 1992).
Wind can also have profound effects on coffee. Hot
winds increase evapotranspiration and therefore rain-
fall (or irrigation) requirements to the trees increase.
Strong winds may severely damage leaves and buds in
addition to exacerbating shedding of developing ow-
ers and fruits (Camargo, 1985; Matiello et al., 2002).
Where strong wind is frequent, wind-breaks need to be
provided.
3. Shading and yield
Coffee yields may decrease with increasing shading
because of (i) lower whole-tree carbon assimilation
under excessive shading, (ii) greater stimulus to vege-
tative rather than ower buds (Cannell, 1976), and
(iii) fewer nodes formed per branch and ower buds
at existing nodes (Montoya et al., 1961; Castillo and
Lopez, 1966). If the number of nodes is the key
component of coffee production (Cannell, 1976), yields
should then decline with increased shading.
Shaded coffee tends to ower and produce a good
crop each year, whereas under unshaded plantation
conditions, the crop tends to alternate between years
with heavy owering and light owering leading to a
biennial production trend. As discussed teleologically
by Cannell (1985), coffee produces very fewowers in
its shaded native habitat, and thus failed to evolve
satisfactory mechanisms, common in many fruit trees,
to maintain its fruiting burden in balance with carbo-
hydrate and mineral resources when grown under full
exposure. Hence, the coffee tree becomes committed
to lling all the beans that are formed after the fruit
expansion stage. According to this point of view, the
causes of overbearing are associated with profuse
ower initiation without shading and very sparse
compensatory fruit shedding, resulting in a large sink
capacity in the seed endosperms (Cannell, 1985).
Overbearing exhausts the trees reserves and limits
both the production and retention of leaves, leading to
poor crop the next year. This allows an excessive
foliage to form which, in turn, permits a profuse
owering and hence a heavy crop. As a consequence,
unshaded coffee plantations produce irregularly and,
even under good cropping conditions, production is
often irregular and follows a biennial pattern. The use
of shelter trees reduce overbearing and buffer biennial
uctuations of crop yields. This should reduce exhaus-
tion of the coffee tree, and allow it to satisfactorily
produce for longer. On economic grounds, higher
yields per harvest in unshaded plantations might be
compensated for, within given limits, by the larger
number of more regular crop harvests in shaded
plantations.
The most important factors for deciding on the use
of shelter trees in coffee plantations can be allotted
into three groups: (i) production objective(s), (ii)
environmental factors, and (iii) level and quality of
inputs available to improve the environment for the
coffee tree (Muschler, 1997). If, in addition to crop
yield per se, stability of production and conservation
of natural resources are important goals, then the
shade system will be favored. Similarly farmers will
favor shade systems if they are interested in the
production of organic coffee and/or extra products
from the shelter trees. On sub-optimal sites with poor
soils, water decit, microclimatic stress and high
wind-speed conditions, farmers will also favor the
use of shade. Conversely under optimal conditions,
farmers will choose unshaded plantations as the most
feasible option. In addition, unshaded plantations
should be recommended if agrochemical inputs,
mechanization, irrigation and modern, high-yielding
varieties are available (Muschler, 1997; Beer et al.,
1998). The concomitant analysis of these factors
should therefore drive the farmers decision.
From eld observations, Muschler (1997) devel-
oped an empirical model for arabica coffee in Costa
Rica in which he reconciles apparently contradictory
responses to shade by putting them in the context of
the particular local environmental conditions. In this
model, coffee production is evaluated as a function of
site altitudes. In soils without major limitations to
rooting depth, nutrients or moisture, maximum coffee
production would occur under unshaded conditions
in the ideal range of elevations. Outside this range, the
production of open plantations would decrease
strongly in response to high temperature stress at
low elevations, and to low temperature and possibly
wind damage at higher elevations. Under these sub-
optimal conditions, the use of shade trees to buffer
F.M. DaMatta / Field Crops Research 86 (2004) 99114 101
cerca de
aumentar muda
microclimatic extremes should improve production
over that of open plantations as long as tree crop
competition for nutrients or water is not excessive.
By contrast, shading of coffee within the ideal range of
elevations would depress yield relative to unshaded
plantations. On soils with nutrient or moisture limita-
tions, the potential yield advantage of unshaded versus
shaded plantations would be reduced at all elevations.
Muschlers (1997) model seems to t Brazilian
regions where arabica coffee is cultivated. In Brazil,
however, coffee production is largely determined as a
function of latitude rather than altitude. In optimal or
near-optimal regions located between 20 and 248S,
characterized by a subtropical climate with a dened
dry season coinciding with cool months, shading
provides little, if any, benet to the crop. In some
cases, it may be even detrimental (Camargo, 1990).
However, shade can greatly reduce frost damage, a
major and unpredictable cause of yield loss at higher
latitudes in Brazil (Caramori et al., 1996; Baggio
et al., 1997). By contrast, in regions at lower latitudes
(8158S), characterized by warmer temperatures and
prolonged, unpredictable droughts, shading is pro-
mising. In Brejao, northeastern Brazil, the yield over
six harvests increased remarkably in unirrigated ara-
bica coffee shaded by cashew trees (Anacardium
occidentale), as compared to unshaded coffee (about
170% increase under 50 or 75% ground cover, and
about 100% increase under 25 or 100% ground cover;
different ground cover percentages were obtained by
thinning the shelter trees) (Matiello et al., 1989).
Similar results have been found in arabica coffee
shaded by Grevillea robusta in other sites from north-
eastern Brazil (e.g. Matiello and Fernandes, 1989;
Dantas et al., 1990). For robusta coffee, there also
seems to be a positive association between shade
extent and maximization of crop yield as the environ-
mental conditions become less adequate for cultiva-
tion, as found in Ghana by Amoah et al. (1997).
Camargo (1990) pointed out, from both experimental
and eld observations in Brazil, that ground cover by
shelter trees should not exceed 2030%, although it
may reach 50% in drier and hotter regions. Hence, it
may be proposed that, as a general rule, the more the
sub-optimal for coffee production the site is, the
greater would be the shading benets for the coffee
plantation (Fournier, 1988; Camargo, 1990; Matiello
et al., 2002).
In most cases, shade trees, particularly those with
deep rooting, seem not to adversely affect the water
balance of the coffee crop. In Mexico, Jimenez and
Golberg (1982) estimated the annual evapotranspira-
tion of an open plantation of arabica coffee to be
1327 mm compared with 703 mm for the crop shaded
by Inga leptoloba and 1052 mm for a system with a
mixture of shade trees. As compared with unshaded
schemes, adequate shade management may even
improve the water status of the soil after prolonged
droughts, as found in India by Gopal et al. (1970) and in
Brazil by Miguel et al. (1995), or the water status of the
crop, as found in northeastern Brazil by Matsumoto
et al. (2000). Therefore, provided that the agrosystemis
correctly managed (proper choice of shelter tree spe-
cies, judicious evaluation of planting density, soil type,
water and thermal regimens), the use of shelter trees
appears to be feasible, as it would reduce wind speeds
and temperature, and would increase relative humidity
(RH) (Barradas and Fanjul, 1986; Caramori et al.,
1995). Hence, water loss from excessive evapotran-
spiration is expected to be decreased and, as a result,
water-use efciency should increase. Particularly in
regions experiencing prolonged droughts and/or high
evaporative demand, a higher water-use efciency
should be translated into obvious advantages to the
production of coffee plantations.
Overall, comparisons amongst different experi-
ments dealing with effects of shading on coffee pro-
duction are difcult since almost always investigators
have omitted important data such as intensity and
quality of irradiance at the crop level, daily and
seasonal uctuations of temperature and RH, nutri-
tion, crown architecture, proper shade management
and design, from among other conditions. Further-
more, it should be emphasized that in many compara-
tive studies in which production of shaded plantations
exceeds that of open ones, such a higher yield refers to
the rst harvests; in the longer term, this may not be
true due to severe competition between the coffee
plant and the shelter tree (e.g. Matiello and Almeida,
1991). In any case, the relative yield advantage of open
plantations over shaded plantations may be limited:
(i) to optimal or near-optimal soil and climatic con-
ditions, (ii) to one or two decades of production, after
which environmental degradation, particularly via soil
erosion and pesticide residues, may seriously reduce
productivity and/or environmental quality, and (iii) to
102 F.M. DaMatta / Field Crops Research 86 (2004) 99114
frequently replanted and pruned plantations since
unshaded coffee bushes have a shorter life expectance
than shaded bushes (Beer et al., 1998, and references
therein).
4. Branch die-back
Die-back or descending branch death refers to the
death of twigs, starting from the apex and progressing
downwards. It has been registered in practically all
coffee growing countries, resulting in severe loss of
both yield and quality of coffee (Clowes, 1973). The
syndrome does not usually arise under natural condi-
tions where coffee thrives under shade and when fruit
production is barely sufcient to ensure the survival of
the species (Ananth et al., 1960). Die-back does not
constitute a problem in the juvenile phase, but has to
be considered as the trees enter the reproductive phase
with heavy crops (Clowes, 1973). Under these circum-
stances, leaves are turned yellow prematurely and fall,
leading to extensive defoliation of the trees. The
affected branches dry out and are ultimately shed.
Furthermore, branch die-back appears to be preceded
by death of a large proportion of absorbing roots (Rena
and DaMatta, 2002). Taken together, these effects may
accentuate the biennial production cycle (and vice
versa), as it takes two more years for the trees to
recover (Barros et al., 1999).
Research indicates that die-back is primarily a
physiological, rather than a pathological, phenomenon
(Ramaiah and Raman, 1967; Barros et al., 1999). Its
occurrence has been associated with environmental
stresses such as soil and atmospheric water decits,
high temperatures, high insolation or to the combined
effects of these stresses (Barros et al., 1999, and
references therein). As shading can attenuate such
adverse environmental effects, a lower incidence of
die-back in sheltered plantations is to be expected
(Ramaiah and Raman, 1967; Gopal and Ramaiah,
1968). The phenomenon seems to be associated with
nutrient starvation of K (Malavolta et al., 1958;
Clowes, 1973) or N (Malavolta et al., 1958; Montoya
and Umana, 1961). Montoya and Umana in Costa Rica
found a 44% reduction in die-back occurrence with an
application of 100 g N per plant per year, and 66%
reduction with an application of 200 g in relation to
trees to which no N was applied.
When the trees are cultivated without shade, the
number of potential fruiting points is greatly increased
without a commensurate increase in leaf area (Can-
nell, 1985; Maestri et al., 2001). One fruit requires
about 2000 mm
2
leaf area to develop (Cannell, 1976).
As the fruit to leaf ratio increases, the current photo-
synthesis is not sufcient to support the normal devel-
opment of fruits and mobilization of the trees reserves
leads to exhaustion. However, as opposed to early
works (Nutman, 1933; Cooil, 1960; Wormer and
Egabole, 1965; Patel, 1970) which linked die-back
to strong decreases in starch content in the roottrunk
system, Carvalho et al. (1993) in Brazil found that
branches from bearing trees die-back regardless of
their starch content. They also showed that unshel-
tered coffee trees can sustain an overbearing load
without simultaneously showing any sign of die-back
as long as adequate photosynthetically active leaf area
is maintained in the tree.
5. Radiant energy
5.1. Gas exchange
Cannell (1985) pointed out that the maximal photo-
synthetic rates of sun leaves of coffee are low, around
7 mmol CO
2
m
2
s
1
, but higher for shade leaves, up
to 14 mmol CO
2
m
2
s
1
. This later value refers to the
work of Kumar and Tieszen (1980), who obtained a
maximal rate about 1.4 g CO
2
m
2
h
1
that, in fact,
equals 8.8 mmol m
2
s
1
rather than the quoted value
of 14 mmol m
2
s
1
. There is considerable informa-
tion that contradicts the observations of Cannell
(1985). In as much as stomatal aperture is not limiting,
the rate of net CO
2
assimilation (A) of coffee trees
appears to be higher under full sun than under shade.
In Hawaii, Gutierrez and Meinzer (1994) observed in
arabica coffee a higher A in sun leaves from the upper
canopy than in shade leaves from the middle canopy.
In contrast to A, stomatal conductance to water vapor
(g
s
) was lower in sun than in shade leaves. This pattern
was manifested by lower carbon isotope discrimina-
tion (an integrated, long-term indicator of gas
exchange performance; Farquhar et al., 1989) in sun
leaves. As a whole, these results indicate that A of
shade leaves was limited by the low light availability,
rather than by g
s
. Yamaguchi and Friend (1979),
F.M. DaMatta / Field Crops Research 86 (2004) 99114 103
Friend (1984) and Fahl et al. (1994) also observed
higher A in sun-grown than in shade-grown arabica
coffee plants. By contrast, Carelli et al. (1999) did not
nd differences in A and g
s
from plants of arabica and
robusta coffee grown either under full sunlight or
under 50% articial shade, although A and g
s
strongly
decreased in both species when grown under 80%
shade. Furthermore, the net assimilation rate (rate of
increase in dry mass of the plant per unit leaf area per
unit time) is also frequently greater in plants under full
sun than under shade (Maestri and Barros, 1977, and
references therein). In a few cases in which such a
rate initially is greater under shade, the opposite trend
may be found later as the canopy develops and the
self-shading increases (e.g. Huxley, 1967), suggesting
an irradiance limitation.
In most work showing higher A under shade than
under full sun, a lower g
s
for exposed leaves may at
least partially explain that pattern (e.g. Kumar and
Tieszen, 1980; Kanechi et al., 1995; Freitas, 2000;
Carelli et al., 2001; Paiva et al., 2001). Kumar and
Tieszen (1980), for example, pointed out that shade-
grown plants photosynthesized at nearly twice the rate
of those grown in the sun, with corresponding changes
in leaf conductance. Since stomatal aperture is greater
under shade or on cloudy/rainy days (Nutman, 1937b;
Franco, 1938; Maestri and Vieira, 1958; Butler, 1977;
Fanjul et al., 1985), it may be suggested that under full
sun photosynthesis would be largely restricted by low
g
s
. However, it is unlikely that high irradiance per se
leads to stomatal closure, as originally pointed out by
Nutman (1937b).
For single coffee leaves, the saturating irradiance
(I
s
) is relatively low, ranging from about 300 to 600
700 mmol photons m
2
s
1
, with shade leaves showing
the lowest values (Kumar and Tieszen, 1980; Fahl et al.,
1994). Values for I
s
smaller than 300 mmol photons
m
2
s
1
(e.g. Rhizopoulou and Nunes, 1981; Friend,
1984; Nunes, 1988) are probably due to growth of the
plants at extremely low levels of irradiance. In any
case, values for I
s
have been estimated under experi-
mental conditions, in which incident light beams are
normally perpendicular to the leaf, as occurs in
Parkinson leaf chambers of infrared gas analyzers.
Under natural conditions, individual leaves intercept
light at different angles of incidence during the course
of the day, thus the leaves are only exposed to full
irradiance for very short periods. In addition, because
many leaves are partly to deeply shaded within the
coffee canopy, with leaves in the interior of the crown
of adult coffee trees receiving as little as 10% of full
solar radiation (Franco, 1951; Huxley, 1967), or even
less (Jaramillo and Santos, 1980), it may be proposed
that canopy photosynthesis would be saturated at
irradiances considerably higher than 600
700 mmol photons m
2
s
1
. Thus, by considering the
canopy as a whole, the values of I
s
should be much
higher than for individual leaves. An increase in A for
the full canopy under full sunlight is thus to be
expected, as the inner leaves would contribute more
appreciably to carbon assimilation, as they receive a
greater photon ux and the majority of leaves in the
outer levels of the canopy would not be fully exposed
to perpendicular light.
One must be cautious when scaling photosynthesis
estimates from the leaf to the canopy level. In ever-
green species like coffee, the current gas exchange
characteristics of a particular leaf may deviate con-
siderably fromthose of the other leaves (Meinzer et al.,
1993). Because shade leaves are usually older than
sun leaves within the coffee canopy, differences in
photosynthetic performance between them cannot be
attributed solely to shading conditions or age as these
two variables may be confounded (DaMatta, 2003).
The potential for adjustments in gas exchange as the
leaf becomes shaded (and aged) is large in coffee,
and such adjustments may occur over relatively long
periods that may span the life of the leaf (Gutierrez
and Meinzer, unpublished results). Thus, short-term
single-leaf gas exchange measurements may not
reveal differences in total carbon assimilation at the
canopy level when differences in leaf age or resource
availability are not considered, even if total leaf area is
taken into account (Meinzer et al., 1992, 1993).
5.2. Acclimation to full sun
Since the reports by Nutman (1937a,b), there
appears to be a general belief that coffee is a typical
shade species. Some shade adaptation attributes, e.g.
relatively low values for compensation irradiance
(Rena et al., 1994) and low chlorophyll a to chlor-
ophyll b ratio (Bergmann et al., 1970; Fahl et al., 1994;
DaMatta and Maestri, 1997; Carelli and Fahl, 2000),
have been associated with that belief. By contrast,
coffee leaves may show enough plasticity to acclimate
104 F.M. DaMatta / Field Crops Research 86 (2004) 99114
themselves to sunny environments; Gindel (1962) in
Israel, where the number of sun hours is much greater
than in traditional coffee growing countries, found
reductions in leaf surfaces, formation of thick cuticle,
development of columnar tissue, change in color of the
leaves from glossy dark green to dull light green, from
amongst other morphological adaptations to the harsh
environment. Furthermore, in Brazil, modern, high-
yielding cultivars have been selected in test-trials
conducted under full sunlight and, in most cases, using
wide spacings. Hence, these cultivars may be better
adapted to high irradiance than cultivars selected
for shade environments. Several attributes may be
associated with acclimation or adaptation to high
irradiance in coffee, such as: increased stomatal den-
sity (Voltan et al., 1992), decreased specic leaf area,
thicker cuticle (Voltan et al., 1992; Fahl et al., 1994)
with more epicuticular wax (Akunda et al., 1979b),
higher I
s
, chloroplasts with fewer grana and less
thylakoid per granum (Fahl et al., 1994), increases
in amount and activity of Rubisco (ribulose-1,5-
bisphosphate carboxylase/oxigenase) (Kanechi et al.,
1996; Ramalho et al., 1999), and relatively fast recov-
ery from photoinhibition (DaMatta and Maestri,
1997). In addition, in single sun leaves of coffee, after
reaching I
s
, there is no depression in photosynthesis up
to 1200 mmol photons m
2
s
1
(Tio, 1962; Kumar and
Tieszen, 1980; Ramalho et al., 2000a). This suggests
that the coffee tree has mechanisms to thermally or
non-photochemically dissipate the excess excitation
energy, which would partially explain why coffee can
respond plastically to changing irradiance. Therefore,
it seems more appropriate to consider the coffee plant
as a shade-tolerant species, rather than as a typical
shade plant, as is frequently reported. Alternatively, it
could be considered as a species with wide plasticity in
response to varying irradiance.
Nitrogen is believed to be a key factor allowing
plants to endure and counteract photoinhibitory
effects. By enhancing A, it may indirectly decrease
the excitation energy pressure on the photosystems
and, therefore, decreases the probability of occurrence
of photodamage in coffee plants at full sun (DaMatta
et al., 2002). Nitrogen might also directly minimize
the potentially deleterious effects of light stress on the
photosynthetic apparatus. In arabica coffee, leaves
developed under low irradiance were able to acclimate
to high irradiance by way of processes which at least
are partially N-dependent. This is particularly evident
when young coffee plants are transferred from the
nursery to the open. After 130 days of exposure to the
harsh full sunlight environment, all plants receiving no
extra N died, whilst 70% of the N-supplied plants
survived in experiments in Portugal (Nunes et al.,
1993). During the acclimation period to high irradi-
ance, only the leaves of the high-N plants showed an
almost complete restoration of A and several chlor-
ophyll a uorescence variables besides an increase in
I
s
(Ramalho et al., 2000a). The acclimation process
involved an increase in non-photochemical quenching
which apparently constituted the rst line of defense
against high irradiance (Ramalho et al., 1997, 2000a).
This would provide the high-N plants with enough
time to trigger later mechanisms to consolidate the
acclimation, e.g. increases in the activity of the anti-
oxidant system and changes in fatty acid composition
of chloroplast membranes, to decrease the suscept-
ibility to photooxidative damage (Ramalho et al.,
1998). In addition, increases in photoprotective pig-
ments (e.g. lutein, neoxanthin) suggest that N can
promote specic mechanisms of acclimation other
than those that might be expected from a preferential
partition of N into photosynthetic electron ow com-
ponents (Ramalho et al., 2000a). Altogether, the above
ndings partially illustrate the strong dependence on
N by open-grown coffee plantations, a fact little
observed in plantations under shade (Carvajal, 1984).
In unstressed coffee trees, photoinhibition, if occur-
ring, would be mainly concentrated in the outer leaves.
Even in such leaves photoinhibition may be consid-
ered as a strategy of acclimation of photosystem II,
providing protection against high irradiances
(Osmond, 1994). For both arabica and robusta coffee,
photoinhibition might not be translated into decreases
in A. Thus photoinhibition per se might not result
in substantial depressions in the yield of the coffee
tree grown in the open, which lends some support
to explain the successful cultivation of commercial
cultivars under full sun (DaMatta and Maestri, 1997).
By contrast, under certain conditions, the defense
mechanisms of the plant may be unable to adequately
dissipate the surplus excitation energy, and then
photodamage may ensue (Nunes et al., 1993; Lima
et al., 2002). Among these conditions are: decient
fertilization, heavy fruit load, water decits, low tem-
peratures, especially low night temperature followed
F.M. DaMatta / Field Crops Research 86 (2004) 99114 105
by sunny days, or any other factor leading to the
exhaustion of the coffee tree. Combined or not, these
factors may lead to a sequence of potentially harmful
events, particularly in coffee plantations receiving
direct solar radiation during the afternoon. As a con-
sequence, chlorotic/necrotic lesions are formed which
result in leaf shedding. Under such circumstances,
the incidence of brown eye (Cercospora coffeicola),
leaf rust (Hemileia vastatrix) and coffee leaf miner
(Leucoptera spp.) usually increases, which also leads
to leaf shedding. This brings about greater light pene-
tration to deeper layers of the tree canopy which may
cause photodamage to the inside leaves, thus ultimately
exacerbating leaf abscission. In several cases, the
branch dies back or grows little and, as a result, there
is loss of yield in the next harvest. In this context, the
use of shelter trees might considerably minimize the
occurrence of photooxidative damage.
6. Temperature
Low temperatures adversely affect coffee photo-
synthesis and yield through both stomatal and non-
stomatal factors (Bauer et al., 1985; DaMatta et al.,
1997b; Quartin et al., 1998; Ramalho et al., 2000b).
However, this review will only focus on the effects of
high temperature.
In regions with relatively high mean annual tem-
peratures, arabica coffee is often raised under shade, as
occurs in Central America (Maestri and Barros, 1977).
This has been traditionally explained because at tem-
peratures above 24 8C, the net photosynthesis would
decrease markedly, approaching zero at 34 8C (Nunes
et al., 1968). This statement, although misleading (see
below), was to some extent supported by other work.
Heath and Orchard (1957) found that the internal CO
2
concentration of coffee leaves increased logarithmi-
cally up to 30 8C and then more rapidly to 35 8C
(higher temperatures were not evaluated), indicating
a thermal limitation on photosynthesis. Similar results
were noted by Wormer (1965) and Bierhuizen et al.
(1969). Cannell (1976) suggested that maximal A
would occur at about 20 8C. Kumar and Tieszen
(1976) found lower A at 35 8C than at 10 8C. Kumar
and Tieszen (1980) observed decreases in A at tem-
peratures above 25 8C, despite g
s
remaining constant
over the temperature range 2535 8C. Extrapolating
the above results to eld conditions in tropical envir-
onments, when leaf temperature easily reaches values
above 30 8C during a great part of the day, leads to the
conclusion that the production of the coffee tree would
be very low at relatively high temperatures. However,
this is certainly not the case, as has been found in
Vicosa (20845
0
S, 650 m a.s.l.), Brazil, where rates of
both photosynthesis and growth are maximal through-
out the warm season (Silva et al., 2000).
In work conducted from 1950 to the 1970s, cited
above, probably other limitations (e.g. uncontrolled
evaporative demand; use of small pots, a condition
potentially limiting for gas exchange; cultivation
under presumably controlled and constant conditions,
which would obstruct the plants acclimation to a
changing environmental factor) coupled with the fact
of not considering the separate effects of temperature
and leaf-to-air vapor pressure decit (D
s
) might be
invoked to explain why temperature, within given
limits, would directly constrain gas exchange in cof-
fee. Gattli et al. (1980), for example, found in arabica
coffee under controlled conditions that the optimal
temperature for A changed after a period of acclima-
tion to the new conditions. If the temperature was
gradually increased from 15 to 35 8C, the optimal
temperature was at 30 8C. If the temperature was
decreased from 35 to 15 8C, it was between 20 and
25 8C. Frischknecht et al. (1982), also working with
arabica coffee, showed that, by changing the tempera-
ture from24 to 33 8C, there was a 40%decrease in A in
the rst day; 6 days later A adjusted to the new
condition and reached the same efciency as it was
at 24 8C, even though the dark respiration increased
by 50%. Hence, by providing a sufciently long
acclimation time, the optimal temperature range for
A may considerably be wider. Recent results obtained
with plants grown in the open seem to reinforce this
suggestion. In adult robusta coffee trees, Awas appar-
ently insensitive to leaf temperatures at 2535 8C
provided g
s
did not decrease appreciably in response
to increasing D
s
(DaMatta et al., 2003). In potted
arabica coffee plants, Carelli et al. (1999) obtained
high values for A (11 mmol m
2
s
1
) under leaf
temperatures of around 34 8C, paralleling high values
for g
s
(250 mmol m
2
s
1
). Similar results were
found in my studies with eld-grown adult trees. Also,
under saturating light and CO
2
, the photosynthetic
capacity of both arabica (Alves et al., 1985; DaMatta
106 F.M. DaMatta / Field Crops Research 86 (2004) 99114
et al., 2001) and robusta (DaMatta et al., 2001) is
maximal at 35 8C or even slightly above. Thus, the
photosynthetic rates in coffee may be maintained at
high values even at temperatures above 30 8C.
7. Wind
Wind stress on coffee results from desiccation
and mechanical damage, especially on young plants
(Carvajal, 1984). Caramori et al. (1986) found
mechanical damage in arabica coffee seedlings when
exposed to articial wind at speeds up to 3.0 m s
1
,
resulting in decreases in both plant height and
leaf area. The authors also observed a depression in
internode length of the orthotropic and plagiotropic
branches, possibly a consequence of impaired water
status due to enhanced transpiration. Moderate winds
associated with a lower leaf area should to a great extent
increase the coupling between the canopy and the
surrounding atmosphere, thus increasing the boundary
layer conductance and ultimately allowing high tran-
spiration rates. Results by Gutierrez et al. (1994) with
eld-grown adult arabica trees suggest that the apparent
stomatal response to wind is mediated by increases in
boundary layer conductance, leading to high D
s
with
increasing wind speed. Apparent responses of coffee to
wind are thus at least partially a reection of stomatal
responses to D
s
which is related to RH (Gutierrez
et al., 1994). That is, since D
s
rises with increasing
wind speed, transpiration would decline as a conse-
quence of stomatal closure in response to increasing
evaporative demand.
8. Relative humidity and evaporative demand
In Hawaii, Gutierrez et al. (1994) found in arabica
coffee grown in the eld that g
s
was typically high in
the morning and declined after midday as irradiance
and D
s
increased. After normalizing for changes in
irradiance, the observed diurnal hysteresis in the
relationship between g
s
and the air saturation decit
was removed, revealing a strong negative relationship
with the air dryness. These ndings lend support to
various reports that indicate that g
s
strongly decreases
as the air becomes drier (Tesha and Kumar, 1978;
Fanjul et al., 1985; Nunes, 1988; Hernandez et al.,
1989; Kanechi et al., 1995; Barros et al., 1997;
Tausend et al., 2000). During the warmer periods of
the day, articial elevation of RH seems to stimulate
the stomata to open, particularly when soil water
availability is not limiting (Tesha and Kumar,
1978). In effect, the stomata of the coffee tree may
respond to changing evaporative demand irrespective
of the leaf water status (Kanechi et al., 1995; Barros
et al., 1997; Tausend et al., 2000).
The direct, rapid response of stomata to changes in
RH has important consequences for the ability of the
plant to support relatively long periods of soil drought
associated with high atmospheric evaporative demand.
Such behavior would be advantageous for the coffee
tree as it would allow maximization of water-use
efciency as soil water availability decreases. On
the other hand, with non-limiting soil water or with
brief periods of water decit, the sensitivity of stomata
to dry air would be disadvantageous. Under these
circumstances, maximization of crop productivity is
of greater value than optimizing water-use efciency
(DaMatta, 2003).
Compared to arabica, in addition to having a sig-
nicantly higher stomatal frequency (Franco, 1939;
Williams, 1972; Voltan et al., 1992; DaMatta et al.,
1997a), robusta coffee also appears to have a lower
stomatal sensitivity to D
s
(DaMatta et al., 1997a; Fahl
et al., 2001), which leads to a less efcient stomatal
control on transpiration. This could be an ecological
adaptation of robusta, reecting its origin from Afri-
can equatorial lowlands, in contrast to the highland
origin of arabica coffee. Teleologically, it may be
argued that robusta evolved in such a way that it
maintained a higher transpiration ensuing from a
higher g
s
, thus allowing evaporative cooling and low-
ering its leaf temperature. This would not be proble-
matic in terms of water conservation provided D
s
is
low and dry periods are not prolonged, as occurs in its
native home. Hence, robusta could support brief per-
iods of water shortage more efciently than arabica
coffee, bearing in mind the low stomata sensitivity of
the former to the early stages of drought stress. This
would guarantee maintenance of transpiration and
photosynthesis, although permitting a rapid exhaus-
tion of soil water. In arabica, the efcient stomatal
closure would restrain photosynthesis while allowing
the maintenance of a favorable water status for longer,
and ultimately improving survival under prolonged
F.M. DaMatta / Field Crops Research 86 (2004) 99114 107
droughts. However, it should be emphasized that these
simplications are somewhat adventurous considering
the wide genetic variability that exists, particularly
within robusta (DaMatta and Rena, 2001). Whatever
the case, the lower stomatal sensitivity of robusta to
evaporative demand should make it more responsive
to irrigation than arabica. Empirical evidence from the
eld corroborates these theoretical considerations.
By considering (i) the high stomatal sensitivity to
RH, and (ii) the maintenance of A even at relatively
high temperatures and irradiances as long as appreci-
able stomatal limitations do not occur, then D
s
per se,
rather than either irradiance or temperature, is the
most important limiting factor for the production of
coffee throughout the main regions where it is tradi-
tionally cultivated, especially in sites where high
evaporative demand and/or prolonged droughts are
common. In these regions, supplementary irrigation
in periods of hot and dry air will be less efcient with
no shelter trees, particularly for arabica coffee (Rena
and Maestri, 2000). These assumptions appear to
explain at least partially why arabica coffee has been
recently introduced in some zones from northeastern
Brazil, where the annual mean temperature may reach
values as high as 25 8C. In these zones, successful
cropping has been associated with irrigation, shading
and/or high density plantings (see below) and, in
particular, with the use of short-stature cultivars with
dense crowns. The use of cultivars with open crowns,
even if irrigation is supplemented, often results in crop
failure (Matiello et al., 2002). Considered together,
these data suggest that maintenance of a lowD
s
should
be crucial for the success of the crop.
9. High density plantings
High density planting, as it seems to mimic coffees
natural environmental position as understorey shrub
(Akunda et al., 1979a,b), may lead, within given
limits, to more favorable conditions for the mainte-
nance of gas exchange, increasing crop yield. Most of
the worlds coffee has been planted at fewer than
2000 trees ha
1
. However, several reports have indi-
cated that coffee may be more suited to high density
plantings (Browning and Fisher, 1976; Kumar, 1978;
Uribe and Salazar, 1981; Awatramani, 1982; Njoroge
and Waithaka, 1992; Njoroge and Kimemia, 1994;
Nacif, 1997). Some evidence suggests an optimal
planting density of about 5000 trees ha
1
for short-
stature cultivars of arabica coffee (Rena and Maestri,
1987; Rena et al., 1998; Maestri et al., 2001); for
robusta coffee, an optimum density should not exceed
4000 trees ha
1
(Matiello, 1998). The productivity of
dense plantings is much greater than that of traditional
plantings, especially because a high degree of ground
cover is achieved at an early stage. The added value
exceeds the additional costs of crop management
(Barros et al., 1995; Bartholo et al., 1998; Maestri
et al., 2001; Matiello et al., 2002). Thus, where
cultural practices using tractors are not possible or
not required, closer spacings have currently been
adopted worldwide.
Because mutual leaf shading, soil temperature and
D
s
are kept low, evapotranspiration is held in check, an
effect further facilitated by the decreased abundance
of weeds in shade conditions (Maestri et al., 2001).
Moreover, in dense plantings, coffee roots develop
deeper so that they take up water from lower soil
horizons (Cassidy and Kumar, 1984). Except under
extreme densities, internal plant water tensions are
unlikely to be increased (Kumar, 1978; Scalco et al.,
2003). This has been further highlighted elsewhere by
Carr (2001). Also, because mutual shading decreases
profuse oral initiation, overbearing and biennial
production and the resulting branch die-back are
reduced. There appears also to be no increase in the
demand for minerals, at least for planting densities up
to 5000 trees ha
1
(Huxley and Cannel, 1970).
Jaramillo and Santos (1980) in Brazil and Cannell
(1985) in Kenya showed that canopies of adult stands
transmit incident light to the soil at proportions as low
as 4%. Even in the middle of the canopy of short-
stature cultivars (5-year-old arabica coffee at density
of 10,000 trees ha
1
), maximal irradiance may reach
about 300 mmol m
2
s
1
only for short periods during
the day. Depending on the spacing between trees in the
lines, irradiance may never exceed 200 mmol m
2
s
1
,
as found by Marur et al. (2001) in Brazil. Furthermore,
an area of leaf of about 2000, 3200 and 7200 mm
2
,
respectively, at the top, middle and bottom of the
canopy tree (7-year-old arabica coffee at density of
2222 trees ha
1
. The trees were grown in the open in a
hedgerow with height restricted to 2 m) was found to
be required to sustain the normal development of
one fruit in Zimbabwe (Clowes and Allison, 1983).
108 F.M. DaMatta / Field Crops Research 86 (2004) 99114
This means that the decreases in photosynthetic rates
with increasing shading level may be compensated for
by a greater leaf area to support each fruit. Similarly,
an area of leaf required by each fruit should increase
with increasing plant density, as the level of shading
rises. Therefore, as opposed to the general belief (e.g.
Kumar, 1978; Rena and Maestri, 1987; Barros et al.,
1995; Rena et al., 1998; Maestri et al., 2001), it is
likely that irradiance constitutes a limitation for
growth and production of coffee trees in a dense
planting scheme. The limitation of light on each tree
under these circumstances would not contradict max-
imization of crop yield per unit land area as decreased
yields per tree might be offset by the increased number
of trees per unit land area. In any case, yields tend to
decrease as the coffee tree ages. Depending on the
extent of planting density, production of the crop is
limited in principle to three to ve harvests, a period
corresponding to the maximum fruiting potential of
young trees (Willson, 1985; Coste, 1992). Beyond that
period, the production level shifts rapidly, as it is
affected by various adverse constraints. These include
extensive leaf loss at the base of the trunk, excessive
sucker production and a trend of the main axis to
become etiolated. After the end of the cycle, the
plantation will require heavy pruning or thinning by
removing a proportion of the trees for a sustained
economic production.
10. Conclusions
To date, much of fundamental research on ecophy-
siology of the coffee tree has been focused at the leaf
level without advancing substantially towards the
canopy level. Also, several of the studies described
here were conducted using potted seedlings, and the
results may not apply to eld trees. In several cases, it
has not been possible to make valid comparisons
between shaded and unshaded coffee agrosystems,
because there are no concrete, scientic denitions
of the level of irradiance required by the coffee tree as
a whole for optimum growth and yield, and because
the conditions in question, such as crown architec-
ture, environment and cropping techniques, are quite
variable. In addition, part of the available informa-
tion obtained in eld conditions is known on the
grounds of empirical experimentation rather than being
scientically based, with predominantly observational
results and no mechanistic and functional links.
The successful use of shelter trees will largely
depend on site conditions and management. Provided
it is not excessive, shade will allow the crop to
endure adverse climatic and edaphic conditions, thus
facilitating carbon assimilation for longer periods,
particularly in regions suffering fromsoil and/or atmo-
spheric droughts. Moreover, under shade, biennial
production and branch die-back are not major pro-
blems, but have to be considered in open plantations.
Properly managed shading for coffee cultivation may
also be associated with marketing advantages such as
sustainability and organically produced coffee. By
contrast, production of unshaded coffee may be main-
tained at a high level using large external inputs
but often at the expense of a sound environment.
Environmental degradation is the price to be paid,
especially by large scale producers, where the use of
shade trees is difcult.
Under shading, even if internal leaves receive
irradiance below I
s
, the fact that exposed leaves are
subjected to more adequate conditions to maximize
photosynthetic rates might partially compensate for
the lower photosynthetic activity of inner leaves.
By contrast, under full sun, the combination of ele-
vated irradiance, temperature and D
s
might result in
decreased photosynthetic rates of peripheral leaves,
chiey as a consequence of stomatal limitations.
However, the more favorable microclimatic conditions
within the canopy might lead to increased photosynth-
esis of inner leaves, which would potentially offset the
lower photosynthetic activity of exposed leaves. None-
theless, light requirements decline under stressful con-
ditions and, therefore, compensatory effects between
the inner and the outer foliage, in terms of photosyn-
thetic production, may be altered, especially in coffee
plantations at full sun under wide spacings. This is
why shading probably results in greater benets to the
coffee tree, particularly in marginal regions where it is
cultivated.
Acknowledgements
I gratefully acknowledge Professors Moacyr
Maestri and Raimundo S. Barros, Dr. Marco Gutierrez
and an anonymous reviewer for their constructive
F.M. DaMatta / Field Crops Research 86 (2004) 99114 109
criticisms and suggestions that improved the original
version of this review. I owe particular thanks to
Dr. Robert Grange who kindly revised the English
text. Thanks are due also to the Brazilian Science
and Technology Council (CNPq) and to the Brazilian
Consortium for Coffee Research and Development for
the fellowships held by the author during the prepara-
tion of this manuscript.
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