ARTICLE IN PRESS

Journal of
Arid
Environments
Journal of Arid Environments 60 (2005) 437–455
www.elsevier.com/locate/jnlabr/yjare

Successional trends in Sonoran Desert abandoned

agricultural fields in northern Mexico
A.E. Castellanosa,b,, M.J. Martinezc, J.M. Llanoa,
W.L. Halvorsonb,d, M. Espiricuetaa, I. Espejele
a
DICTUS, Apdo. Postal #54, Universidad de Sonora, Hermosillo, Sonora 83000, Mexico
b
School of Natural Resources, University of Arizona, Tucson, AZ 85721, USA
c
Reserva de la Biosfera del Pinacate, San Luis Rı´o Colorado, Sonora, Mexico
d
US Geological Survey, Southwest Biological Science Center, University of Arizona, Tucson,
AZ 85721, USA
e
Facultad de Ciencias, Universidad Autónoma de Baja California, Km. 105 Carr. Ensenada-Tijuana,
Ensenada, B. C., Mexico
Received 24 January 2003; received in revised form 15 April 2004; accepted 15 June 2004
Available online 15 September 2004

Abstract

Excessive ground-water use and saline intrusion to the aquifer led, in less than three
decades, to an increase in abandoned agricultural fields at La Costa de Hermosillo, within the
Sonoran Desert. Using a chronosequence from years since abandonment, patterns of field
succession were developed. Contrary to most desert literature, species replacement was found,
both in fields with and without saline intrusion. Seasonal photosynthetic capacity as well as
water and nitrogen use efficiencies were different in dominant early and late successional plant
species. These ecological findings provided a framework for a general explanation of species
dominance and replacement within abandoned agricultural fields in the Sonoran Desert.
r 2004 Elsevier Ltd. All rights reserved.

Keywords: Desert succession; Abandoned fields; Water use efficiency; Nitrogen use efficiency;
Photosynthesis; Sonoran Desert; Salinized fields

Corresponding author. Apdo. Postal No. 54., Hermosillo, Sonora 83000, Mexico. Fax: +52-662-259-
2197.
E-mail address: [email protected] (A.E. Castellanos).

0140-1963/$ - see front matter r 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jaridenv.2004.06.004
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438 A.E. Castellanos et al. / Journal of Arid Environments 60 (2005) 437–455

1. Introduction

Land degradation due to human practices has been identified as a worldwide

problem (Beaumont, 1989) that has ecological and socio-economic implications on
the sustainability of ecosystems (Mouat and Hutchinson, 1995; Arnalds and Archer,
2000). Abandoned agricultural fields resulting from either economic or ecological
causes such as depletion of available soil, nutrients, or water are becoming a major
component of desert landscapes. Agricultural use of marginal lands is usually only a
short-term benefit, yet is a widespread practice globally. Abandonment of such lands
is expected to increase land degradation and desertification problems over the next
few decades. In the arid regions of North America, agriculture was greatly expanded
during the 1950s, with the help of large water and nitrogen inputs. Unsustainable
agricultural practices were developed with cultivars requiring large amounts of
limited resources to achieve increased productivity and short-term gain (Garcı́a,
1987; Moreno, 1994). Ultimately such practices caused and continue to cause an
increase in the number of abandoned agricultural fields (Halvorson et al., 2003).
Disturbed desert habitats are not well characterized or studied because there has
been no ‘‘ecological services’’ assigned to desert vegetation and no social or
ecological benefits have been determined by non-indigenous societies. Although
agricultural productivity in desert agricultural lands has provided an important
income to individuals and society, and has been a matter of regional pride, once
abandoned, these lands represent no economic or societal value and their
rehabilitation is generally not pursued. Only when economic or conservation
perspectives have overcome the ‘‘wasteland’’ perceptions have restoration efforts
been developed (Bainbridge and Virginia, 1990; Jackson et al., 1991).
It is important to study secondary succession on abandoned agricultural fields
because of the increasingly large area they occupy and the large extent of
transformation that takes place from the natural environment in which they are
placed. In order to effectively manage these areas in the future, it is imperative that
we better understand the causes underlying such ecological changes (Bazzaz, 1979;
Tilman, 1987, 1988; Bazzaz, 1996). Given the extremely high rates of land conversion
in most ecosystems (Beaumont, 1989), ecological succession is now a key component
for restoration and ecological management (Glenn-Lewis et al., 1992; Landsberg and
Gower, 1997). In defining restoration and ecological management as the manage-
ment of succession (Luken, 1990) gives us a sense of the centrality of this ecological
process at local, regional and global scales.
Structure, function and species diversity of plant communities established during
ecological succession, are determined by life history characteristics, resource
availability and differences in the ecological niche of different dominant species
(Connell and Slatyer, 1977; Grubb, 1977; Grime, 1979, Noy-Meir and van der
Maarel, 1987; Pickett et al., 1987; Tilman, 1988). Disturbance was incorporated as
an important component in generalized models for secondary ecological succession
by Connell and Slatyer (1977). Their three models are: facilitation, inhibition and
tolerance, of these only the inhibition model has been proposed for desert plant
communities. In desert habitats, facilitation or relay floristics has not been found
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A.E. Castellanos et al. / Journal of Arid Environments 60 (2005) 437–455 439

(Connell and Slatyer, 1977; Goldberg and Turner, 1986), however, secondary
succession in these habitats has yet to be studied extensively. There is the generalized
perception that vegetation changes within desert habitats take an extraordinarily
long time with no species replacement during secondary succession (Shreve, 1929;
Shreve and Hinckley, 1937; Goldberg and Turner, 1986). Long-term studies in the
Sonoran Desert have found changes in population structure for certain species but
no changes of dominant species composition (Shreve, 1929; Shreve and Hinckley,
1937; Goldberg and Turner, 1986), even after more than 60 years (Turner, 1990;
Bowers and Turner, 2001, 2002). This was found to be true also during cyclic
succession in the Chihuahuan Desert (Yeaton, 1978). In most studies, adaptation to
the stressful physical conditions of the habitat is emphasized over biotic interactions,
although facilitation and nurse–plant relationships are known to have an important
role in desert habitats (Turner et al., 1966; Valiente-Banuet and Ezcurra, 1991; Suzán
et al., 1997, Carrillo-Garcia et al., 1999, 2000). Some of the ecophysiological
implications of these biotic interactions may be in response to heterogeneity in
resource availability (Garcia-Moya and McKell, 1970; Schlesinger et al., 1990) which
may promote facilitation rather than competition, among different species and
growth forms (Pugnaire et al., 1996; Suzán et al., 1997; Tielbörger and Kadmon,
2000).
Individual ecophysiological response during successional stages is also a gap in
studies in desert habitats. Bazzaz (1979, 1996) described the importance of species
ecophysiological characteristics during secondary succession in a number of
ecosystems and concluded that fast-growing, high photosynthetic capacity, sun-
tolerant species are associated with early stages, while slow growing, low
photosynthetic capacity and shade-tolerant species are more generally found in late
successional stages. Tilman (1987, 1988) suggested that species replacement during
secondary succession is determined by resource availability, in particular light and
soil nitrogen. How species function in relation to the most limiting resource available
may determine the sequence of ecological succession. Since light is not limiting in
deserts, we may not expect these models to explain many of the trends and
ecophysiological characteristics of species during secondary succession in desert
habitats. Water has been suggested as the major limiting resources for plants in
desert habitats, although more recently, the importance of nitrogen has been
identified (Mooney et al., 1981; Whitford and Gutierrez, 1989; Gebauer and
Ehleringer, 2000).
Water use efficiency is a physiological measure of plant adaptation to arid and
stressful habitats. Higher plant water use efficiency allows plants to conserve water
while still able to assimilate carbon through photosynthesis. This water-conserving
trait has been found to be a characteristic of late but not of early successional species
in most ecosystems (Grime, 1979; Bazzaz, 1996). Similar to water, early successional
species are thought to thrive in habitats where nitrogen availability is higher, i.e.,
recently abandoned fields (Bazzaz, 1979). Nitrogen is then found to be decreasing
through mid stages of succession and finally becoming a low availability and
therefore a limiting resource at the latest stages (Tilman, 1988). However, no
adaptive plant strategies have been studied for nitrogen in desert habitats.
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In this paper our objective is to answer two main questions: Is there plant species
substitution during succession on abandoned desert agricultural fields? How do
individual traits and ecophysiological characteristics of dominant species differ
between early and late successional species? In order to answer those questions, we
characterized secondary successional stages within abandoned agricultural fields in
desert habitats, using a chronosequence of up to 30 years since abandonment, and
comparing two causes of abandonment. We also characterized some ecophysiolo-
gical responses, in particular the potential use efficiencies of water and nitrogen of
important early and late successional species.

2. Materials and methods

La Costa de Hermosillo is located in the western portion of the Central Region of

Sonora, Mexico, between 28
300 and 29
Lat. N and 111
and 112
Long. W. The
area covers close to 833 km2 and has been one of the most important irrigated
agriculture districts in Mexico. It is located within the plains subdivision of the
Sonoran Desert (Shreve and Wiggins, 1964). La Costa has a mean annual
temperature of 22
C and mean monthly maxima of 30
C in July and August,
with daily temperatures of up to 47
C during summer months. Winter mean
monthly temperatures are 12
C (January and February), with no freezing. Annual
rainfall varies from 100 to 225 mm with two distinctive rainy periods, summer
(80–90%) and winter (up to 20%). The driest months are from the end of March to
mid-June. The soils are extensive alluvial deposits with a mixed structure of clay, silt
and sand (45%, 35%, 20%, respectively).

2.1. Site conditions

Because of saline intrusion into the Costa de Hermosillo aquifer, a risk zone was
determined by the federal government (CNA, 1992) and by decree all working deep
wells were shut down and canceled to avoid further salinization of agricultural fields.
All abandoned agricultural fields within this zone had already been irrigated with
salty water. We called these fields, ‘‘saline’’ fields (Fig. 1). Some agricultural fields
outside this zone, never irrigated with salty water, had been abandoned because of
economic or other reasons. We called them ‘‘non-saline’’ fields. We sampled 30
abandoned fields, ten under non-saline and 20 in saline conditions. Most abandoned
fields ranged between 500 to 2000 ha in size.

2.2. Vegetation sampling and floristics

Vegetation was sampled using the plotless point-centered quarter method. At each
abandoned field, the number of points was determined by plotting the running mean
of three points for the cumulative number of species (Mueller-Dumbois and
Ellenberg, 1974). For each quadrant, absolute and relative values of mean density,
dominance and frequency were obtained from formulas provided in Mueller-
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A.E. Castellanos et al. / Journal of Arid Environments 60 (2005) 437–455 441

Fig. 1. Localization of La Costa de Hermosillo agricultural district within Hermosillo county (solid
surrounding line) in Sonora, Mexico. Isoline (dashed) delimiting ground-water salt intrusion is shown.
Abandoned agricultural study sites were located. Closed circles are non-saline, and open circles are saline
study sites.

Dumbois and Ellenberg (1974). The same methodology was used to sample nearby
natural vegetation patches when available. Plant species were identified following
Shreve and Wiggins (1964).

2.3. Physiological measurements

Net photosynthesis was measured using a Portable Photosynthesis System

(LICOR, 6200) for Atriplex polycarpa, Baccharis sarathroides, Encelia farinosa and
Prosopis glandulosa in non-saline abandoned agricultural fields. Atriplex canescens,
Baccharis sarathroides, Encelia farinosa, Larrea tridentata and Cercidium micro-
phyllum were measured in saline-abandoned fields. Daily courses of net photosynth-
esis, stomatal conductance and transpiration were measured from February to
November, except in April and October. Six leaves each of three individuals were
measured at each date for both Atriplex species and B. sarathroides. For all other
species at least two leaves were measured. Leaves were measured for area in the lab
with a leaf area meter (LICOR, 3100), oven-dried for 48 h at 70
C; and weighed.
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442 A.E. Castellanos et al. / Journal of Arid Environments 60 (2005) 437–455

Leaf nitrogen was determined by means of a total Kjeldahl rapid flow analyzer
(RFA300, Alpkem), using the phenol method (EPA-600/4-79-020, Nitrogen
Ammonia, Method 350.1. Colorimetric Automated Phenate) modified for the
auto-analyzer (EPA, 1984). Dried leaves were ground using a mill with mesh 40. Up
to 150 mg of sample per leaf were digested at 160
C for an hour in a solution of
sulfuric acid with potassium sulfite and oxide of mercury and at 290
C for 3
additional hours. Leaf nitrogen was calculated on a per mass and a per area basis.
Photosynthetic nitrogen use efficiency (PNUE) was calculated from the highest net
photosynthetic rate determined during the morning and expressed on a per area
nitrogen basis for the same measured leaf.

2.4. Environmental change history at La Costa

Environmental changes in La Costa de Hermosillo, including details of ground-

water pumping, are discussed elsewhere (Halvorson et al., 2003) and only a brief
overview is described here. In Mexico, about 51% of its territory is classified as arid
or semi-arid (Rzedowski, 1978). Within these regions, many large irrigated
agriculture projects have been developed with still more planned for the future. In
some of these areas, a combination of high cost of water and nitrogen fertilizers, as
well as a decreasing market value of crops, have led to the stoppage of agriculture on
these lands; this is the case in large parts of La Laguna region in northeastern
Mexico (Garcı́a, 1987), and Northwestern Mexico, in Caborca and La Costa de
Hermosillo in Sonora (Moreno, 1994; Halvorson et al., 2003), and Mexicali and San
Quintı́n Valleys in Baja California.
Irrigated agriculture at La Costa de Hermosillo (LCH) was initiated in 1945 when
river-bed agriculture was expanded through the use of well irrigation (Valenzuela,
1982). About 45% of agricultural fields at La Costa were larger than 20 ha and about
an equal proportion were larger than 50 ha. Starting in the 1950s water extraction
and hectares incorporated into cultivation increased at a fast rate into the 1970s
(rising to 800 Mm3 yr1 of water used to irrigate over 132,000 ha) when aquifer
abatement and salinization of ground-water were recognized as serious problems. By
1990, the cultivated area had decreased to what it was during the 1950s (Halvorson
et al., 2003), decreasing by half from the maximum during the 1970s. Most
abandoned fields were between 1000 and 5500 ha in size.

3. Results

Saline-abandoned agricultural fields, those already irrigated with salty water, had
an average electrical conductivity of 2:7  0:9 mmhos cm1 : Fields outside this zone,
either not previously irrigated with salty water or abandoned because of economic
reasons, had an average electrical conductivity of 0:69  0:18 mmhos cm1 (Table 1).
Percent organic matter in soils of saline fields ð0:79  0:09Þ was slightly higher,
although not statistically different from soils of non-saline fields (data not shown).
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A.E. Castellanos et al. / Journal of Arid Environments 60 (2005) 437–455 443

Table 1
Soil characteristics for saline and non-saline field conditions. Saline fields refer to those where cultivars had
been irrigated with water from saline-intruded wells

Conductivity Sand Clay Nitrogen Carbon Potassium Phosphorous

ðmmhos cm1 Þ % % % % % %
Mean  s.e. Mean  s.e. Mean  s.e. Mean  s.e. Mean  s.e. Mean  s.e. Mean  s.e.

Non- 0.696 0.186 38.5 8.15 21.48 5.21 0.072 0.014 0.568 0.152 0.44 0.04 0.768 0.038
saline
Saline 2.738 0.901 34.2 13.83 20.36 8.59 0.067 0.027 0.583 0.275 0.47 0.06 0.757 0.089

3.1. Species establishment

Plant density decreases with time since abandonment in both saline and non-saline
sites, as a consequence of changes in the growth form of dominant species, from
herbaceous annuals to shrubs and trees in the oldest fields. Plant density of saline
fields was higher and cover was lower compared to that of non-saline fields, however,
natural stands of vegetation had higher density and cover than any abandoned fields
(data not shown).
By recording the most common species, a floristic relay process was found in our
sites. Changes in species composition in non-saline fields were recognized at four
main periods (Fig. 2). Within the first 2 years, a number of native and non-native
herbaceous species were found. From year 2 to 10, the number of shrub and tree
species increased, some of which are normally found in mature communities. Early
within this period, B. sarathroides invades and can form a monospecific cover that
self-thins with time, allowing other species to become established. After year 4, tree
species like P. glandulosa, C. floridum and C. microphyllum, found as dominant
components in natural non-farmed plant communities, become established. During
years 10–18, L. tridentata, A. canescens and E. farinosa, tend to become established.
These shrub species are found as important components within natural undisturbed
plant communities. During this period, most annual species are native.
No fields with less than 2 years of abandonment were found under saline
conditions, nevertheless there is circumstantial evidence that a number of herbaceous
species are present during those initial stages, although with lower abundance
compared to non-saline fields. After year 2, highly invasive species such as B.
sarathroides and S. kali, become the dominant species in these landscapes (Fig. 2).
Species that are also found in undisturbed natural plant communities such as E.
farinosa, P. glandulosa, A. polycarpa and L. tridentata, will become established after
the fourth year.
After 18 years, shrubs and trees become the dominant species, while annuals and
herbaceous perennials diminish in their importance (Fig. 2). At this stage, the species
assemblage begins to mimic natural communities. At each site, characteristic species
show after all dominant species have become established, species like Croton
wigginsii on non-saline fields, and Opuntia fulgida on saline fields.
 444
Non-saline Saline
Growth Growth

A.E. Castellanos et al. / Journal of Arid Environments 60 (2005) 437–455

Plant Species form Years since abandonment Plant Species form Years since abandonment
0É.2 >2É..4 >4É.10 >10É18 >18ÉÉ 0É.2 >2É..4 >4É.10 >10É18 >18ÉÉ
Amaranthus fimbriatus H Sphaeralcea ambigua HP
Argemone intermedia H Sesbania exaltata SH
Boerhavia coccinea H Euphorbia polycarpa HP
Convolvulus arvensis HP Ambrosia confertiflora H
Helianthus annus HP Salsola kali H
Salsola kali H Baccharis sarathroides SH

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Taraxacum officinale H Physalis acutifolia H
Tidestromia lanuginosa H Pectis papposa H
Ambrosia confertiflora H Convolvulus arvensis HP
Acacia constricta SH Atriplex semibaccata SH
Baccharis sarathroides SH Encelia farinosa SH
Cercidium microphyllum T Sphaeralcea coulteri H
Prosopis glandulosa T Palafoxia linearis HP
Cercidium floridum T Euphorbia albomarginata H
Abutilon reventum H Ditaxis neomexicana H
Chenopodium leptophyllum H Amaranthus spinousus H
Cryptantha grayi H Acacia constricta SH
Haplopappus sonorensis H Prosopis glandulosa T
Nicotiana trigonophylla HP Portulaca oleracea H
Ricinus communis HP Atriplex polycarpa SH
Sphaeralcea coulteri H Larrea tridentata SH
Atriplex canescens SH Opuntia fulgida SH
Encelia farinosa SH
Larrea tridentata SH
Croton wigginsii SH

Fig. 2. Chronosequence of species successional changes in non-saline and saline-abandoned agricultural fields. Species growth form are H = herbaceous; HP =
herbaceous perennials; SH = shrubs and T = trees. Filled circles represent species found as components of natural communities.
 ARTICLE IN PRESS
A.E. Castellanos et al. / Journal of Arid Environments 60 (2005) 437–455 445

Comparing both sequences, a distinct pattern arises in which herbs are

predominant immediately after abandonment, aggressive colonizers come after the
second year to self-thin and give way to late dominant species that become
established after 4 years and then slowly take over. Site-characteristic species become
established after other dominant species have already done so. The outcome is that
natural community species richness is re-established after 10 to 18 years. As to when
structure and function will become similar to pristine conditions, that will be the
subject of continuing studies for years to come.

3.2. Comparative species functioning

We compared seasonal and diurnal ecophysiological characteristics of B.

sarathroides (an early-succession species), with dominant late-succession species A.
canescens (non-saline) and A. polycarpa (saline). Some comparisons included to a
lesser extent, other late-succession dominant species such as P. glandulosa, L.
tridentata, E. farinosa and C. microphyllum.
In non-saline fields, leaf water potential was 1 to 1:5 MPa significantly lower
for A. canescens during August and November compared to B. sarathroides.
Similar patterns were found in saline fields but with lower water potentials in A.
polycarpa ð5 MPaÞ and up to 2:5 MPa difference with B. sarathroides during
August (Fig. 3).
When comparing leaf photosynthetic capacity for three different periods during
the year, spring, summer and autumn, maximum rates were present in the sub-shrub
E. farinosa ð28:1 mmol CO2 m2 s1 Þ during the summer. During most periods, lower

Non-saline Saline
0

B. sarathroides B. sarathroides
-1
WATER POTENTIAL (MPa)

-2

-3

-4
A. canescens

-5 A. polycarpa

-6
8 10 12 14 16 18 20 8 10 12 14 16 18 20
HOUR HOUR

Fig. 3. Water potential in species from saline and non-saline-abandoned agricultural fields. Symbols
represent daily courses in different months for Atriplex species (diamonds) and B. saratrhoides (circles).
Open symbols represent data collected in July, symbols with crosses represent data collected in November,
and closed symbols and lines represent data collected in August.
 446
Table 2
Photosynthetic capacity and gas exchange characteristics for early and late successional species at La Costa de Hermosillo, Sonora

Plant species Non-saline fields Saline fields

Net photosynthesis PNUE Leaf N WUE Net photosynthesis PNUE Leaf N WUE

A.E. Castellanos et al. / Journal of Arid Environments 60 (2005) 437–455

ðmmol CO2 m2 s1 Þ ðmmol CO2 mol N1 s1 Þ ðmol N m2 Þ ðmmol CO2 mmol H2 O1 Þ ðmmol CO2 m2 s1 Þ ðmmol CO2 mol N1 s1 Þ ðmol Nm2 Þ ðmmol CO2 mmol H2 O1 Þ

Mar 7.12 (0.85) 17.88 (1.85) 0.40 (0.04) n.d.

Atriplex Jul 16.21 25.95 0.62 3.74
polycarpa Sep 18.88 53.08 0.36 3.17
Nov

Mar 17.74 (3.96) 42.98 (10.29) 0.42 (0.03) 3.18 (0.02) 6.85 (0.65) 23.90 (1.99) 0.29 (0.03) 0.91 (1.68)
Atriplex Jul 12.13 (2.38) 59.35 (7.30) 0.21 (0.06) 0.42 (0.10) 10.49 (2.87) 34.84 (7.50) 0.29 (0.04) 2.09 (0.43)

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canescens Sep 10.78 (1.77) 43.71 (10.88) 0.27 (0.03) 0.96 (0.17) 7.76 (0.99) 37.52 (4.28) 0.21 (0.01) 0.74 (0.23)
Nov 6.06 (2.08) 22.99 (11.93) 0.30 (0.06) 3.29 (1.25) 4.15 36.61 0.11 0.41

Mar 10.60 (2.53) 31.28 (3.38) 0.33 (0.04) 1.23 (0.20)

Baccharis Jul 7.37 (1.10) 30.00 (2.80) 0.25 (0.04) 1.69 (0.37)
sarathroides Sep 8.50 (4.75) 27.86 (16.48) 0.31 (0.01) 1.19 (0.29)
Nov 6.25 (2.01) 22.78 (5.33) 0.29 (0.15) 2.18 (1.87)

Mar 12.23 39.88 0.31 1.83

Cercidium Jul 12.53 (2.78) 26.10 (5.43) 0.48 (0.01) 0.53 (0.33)
microphyllum Sep 11.43 65.70 0.17 1.13
Nov

Mar
Encelia Jul 22.50 (1.02) 75.09 (5.75) 0.30 (0.01) 3.40 (0.85) 28.13 (0.98) n.d. n.d. 3.97 (0.55)
farinosa Sep 21.10 (3.37) 97.81 (8.67) 0.22 (0.02) 0.93 (0.01) 17.65 (2.59) n.d. n.d. 0.84 (0.05)
Nov 15.45 (1.76) 58.43 (0.64) 0.27 (0.03) 1.36 (0.25)

Mar
Larrea Jul 7.65 (0.58) 25.17 (1.58) 0.30 (0.01) 2.46 (0.31)
tridentata Sep 7.75 (1.45) n.d. n.d. 0.87 (0.58)
Nov 8.37 (1.28) 38.55 (6.64) 0.22 (0.01) 2.39 (0.45)

Mar 9.91 22.77 0.44 n.d.

Prosopis Jul
glandulosa Sep 11.51 (0.23) 41.31 (1.26) 0.28 (0.01) 0.52
Nov 6.70 (2.50) 24.65 (5.80) 0.27 (0.04) 0.87 (0.20)

Unique values do not show  s.e. Blank spaces indicate either the species is not present or values not measured at specific dates.
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A.E. Castellanos et al. / Journal of Arid Environments 60 (2005) 437–455 447

photosynthetic rates were consistently found in B. sarathroides and L. tridentata

(Table 2). B. sarathroides had higher rates early in the season and a downward trend
through November in both non- and saline fields.
Maximum net photosynthetic rates in late successional Atriplex species showed
decreasing rates from March to November for A. canescens, the dominant species in
non-saline fields, but increasing rates for A. polycarpa in saline fields. In both species,
peak photosynthesis occurred for only a short period near mid-morning, afternoon
rates remained low after a mid-day depression.
Positive relationships between leaf photosynthetic capacity and leaf nitrogen had a
large dispersion associated with it, although some differences among species are
shown. Atriplex species had higher net photosynthetic capacity per unit leaf area
nitrogen, photosynthetic nitrogen use efficiency, as well as higher overall leaf
nitrogen concentration, compared to B.sarathroides in non-saline fields (Fig. 4).
Within desert habitats, water and nitrogen are the two most important and
selective resources for plants. A relationship between photosynthetic nitrogen
(PNUE) and water use efficiencies (WUE), allowed us to predict how net
photosynthetic capacity is optimized per unit of water and nitrogen in leaves, and
as a consequence to obtain the relationship of leaf nitrogen per unit of water
transpired. We obtained these relationships from the mean maximum photosynthetic
capacity per unit resource utilized (water or nitrogen per unit area) at each month, so
points will represent resource use efficiencies for each species at different times of the
year.
When related, water and nitrogen resource use efficiencies differed between early
and late successional species. In both saline and non-saline fields, Baccharis
sarathroides, the early successional dominant shrub, had an exponential increasing
NET PHOTOSYNTHESIS (µmol CO2 m-2 s-1)

Non-saline Saline

20 A. polycarpa
A. canescens

15
Ps. mean

10

B. sarathroides
0
0 0.1 0.2 0.3 0.4 0 0.1 0.2 0.3 0.4 0.5

LEAF NITROGEN (mol N m-2 )

Fig. 4. Maximum diurnal photosynthetic rate to leaf nitrogen content for early and late successional
species under non-saline and saline field conditions. Trends are shown for Atriplex species (diamond) and
B. sarathroides (circles). Error line is the highest found for each species.
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448 A.E. Castellanos et al. / Journal of Arid Environments 60 (2005) 437–455

Non-saline Saline
5
B. sarathroides A. polycarpa
WATER USE EFFICIENCY

4 A. canescens

L. divaricata
B. sarathroides
2 E. farinosa

1
P. glandulosa
C. microphyllum
0
0 25 50 75 0 10 20 30 40 50 60

PHOTOSYNTHETIC NITROGEN USE EFFICIENCY

Fig. 5. Water and photosynthetic nitrogen use efficiencies for early and late successional species under
non-saline and saline-abandoned field conditions. Early species represented by B. sarathroides (open
circles) and E. farinosa (triangles); Late successional by Atriplex species (diamonds), C. microphyllum and
P. glandulosa (crossed squares), and L. divaricata (inverted triangles). For each species, points represent
the mean of gas exchange measurements made on three to six leaves at different times of the year.

trend where a small increase in PNUE resulted in a large increase in WUE (Fig. 5).
Similar relationships were found for Encelia farinosa and Larrea tridentata under
non-saline field conditions. A different pattern was found for late successional
dominant shrubs and trees. In non- and saline-abandoned fields, increasing PNUE
was related to decreasing WUE in shrub, A. canescens and A. polycarpa, and tree
species, C. microphyllum and P. glandulosa. A higher intercept in the WUE axis was
found for Atriplex compared to tree species (Fig. 5).

4. Discussion

Grazing, wood extraction and agriculture are three major ways in which plant
cover has been used in desert habitats. Selective use of species during grazing and
wood harvesting, when moderate pressure is exerted on plant communities, can
trigger processes associated with niche regeneration and gap replacement responsible
for the maintenance of species composition, structure and diversity within plant
communities (Grubb, 1977; Pickett et al., 1987). Large-scale agriculture, as practiced
in La Costa de Hermosillo, involves major disturbance to the soil, community
structure and native species such that successional processes at different scales are
required to restore natural conditions (Bazzaz, 1979, 1996). At this scale, interactions
from different species lead to recognizable patterns of replacement in which pioneer
species either facilitate, inhibit or tolerate colonization by other species (Connell and
Slatyer, 1977; Peet and Christiensen, 1980). Within desert habitats, there is an
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extremely poor literature in which these models of successional processes have been
tested, in particular following agriculture abandonment (Bazzaz, 1996).

4.1. Changes in species composition during succession

Our study shows, that there is a species replacement pattern following agriculture
abandonment in La Costa de Hermosillo desert region. Previously, plant species
successional changes were thought not to be present in desert habitats, since changes in
species composition or replacement had not been observed (Shreve, 1929; Connell and
Slatyer, 1977). Most previous successional studies in warm desert environments, however,
have been performed by following changes in permanent plots from non-disturbed
habitats (Shreve and Hinckley, 1937; Goldberg and Turner, 1986; Turner, 1990).
Differences in our results with those where no species replacement were found
during succession in deserts, may point to important differences in habitat
conditions following large disturbances in space and time, where some limiting
resources may be freed and available for opportunistic species. Large disturbances
are a common characteristic of our study with those where changes in vegetation
structure and species composition have been found, such as in ghost towns in cold
desert habitats (Webb and Wilshire, 1980), or abandoned agricultural fields
(Karpiscak, 1980; Jackson et al., 1991). At la Costa abandoned fields, seed source
availability as well as wood cutting or grazing do not seem to be issues that could
influence regulating trends in plant succession.
In our study we found that species replacement and establishment of late
successional species was relatively fast (after 4–10 years), at which time, most pioneer
species were not present. Other studies using chronosequences of abandoned
agricultural fields within the Northern edge of the Sonoran Desert, found very
similar patterns of relatively fast species replacement (Karpiscak, 1980). Similarity of
the patterns found between the two field conditions studied (Fig. 2) and a similar
study in Arizona (Karpiscak, 1980), suggests a definite pattern within the Sonoran
Desert. Although a chronosequence approach has been shown to be able to detect
major trends in replacement processes (Foster and Tilman, 2000), this was somewhat
surprising since we were expecting larger variability in the successional processes due
to the environmental heterogeneity expected within desert habitats.
Soil salinity differences lead to changes in species characteristics of pioneer and
late successional plant species. Our study showed that different species, both native
and exotic, were present in non- and saline fields within the similar climatological
conditions of La Costa de Hermosillo region. Both non- and saline fields had some
pioneer and late dominant species in common, but also a number of species that were
not shared. This resulted in different plant community structures for non- and saline
fields (Fig. 2).

4.2. Ecophysiological differences

Changes in species composition may reflect selective pressures in the physiological

characteristics of species, due to resource limitation or availability during establishment
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and growth. Plant ecophysiological processes are known to be important within

tropical and temperate forest succession, where light resource availability has been
proposed as the main adaptive factor in the differentiation of incoming species (Bazzaz,
1996), although Bazzaz (1979) recognized that this may not be applicable to desert
ecosystems. Light is generally not a limiting resource in most desert habitats, except for
species which require ‘‘nurse’’ plants (Valiente-Banuet and Ezcurra, 1991; Suzán et al.,
1997) and vines within tree canopies (Castellanos et al., 1999) for which too much light
and heat is a problem. Because of this, other resources such as water (Noy-Meir, 1973;
Schulze, 1982; Whitford and Gutierrez, 1989) and nitrogen (Whitford and Gutierrez,
1989; Hooper and Johnson, 1999; Gebauer and Ehleringer, 2000) may be of outmost
importance within deserts and during secondary succession (Tilman, 1988).
Our study found similar general trends in photosynthetic capacity during
secondary succession as a previous review (see Table 2 in Bazzaz, 1979), but no
other study was found for desert systems where photosynthetic responses were
compared among species during plant succession. E. farinosa a perennial sub-shrub,
had larger photosynthetic capacity than B. sarathroides, Atriplex spp, and L.
tridentata (shrubs), and trees like C. microphyllum and P. glandulosa (Table 2).
However, L. tridentata and to a lesser extent B. sarathroides showed lower
photosynthetic capacity than either tree species.
Some differences were not expected. An early successional species in both non-
and saline fields, B. sarathroides, had higher (less negative) leaf water potentials
during most of the growing and fall seasons, than Atriplex species. Since they were
measured at the same site, early successional Baccharis either may have better uptake
mechanisms, conserving strategies (lower conductance) or may be utilizing different
sources of soil moisture. Better water relations may come with a cost, since lower
photosynthetic rates and stomatal conductances (not shown), that may be related to
the maintenance of higher leaf water potentials in Baccharis, may result in lower
carbon assimilation and competitive ability in the long run (Schulze et al., 1986).
Other less well-known ecological interactions may also play an important role in
the replacement of B. sarathroides. The species was an early successional species
in both non- and saline fields conditions, and could be found during a long period in
the chronosequence, with diminishing densities through time. It has been found, that
abandoned fields, have initially large amounts of soil nitrogen, as a result of previous
farming practices (Bazzaz, 1979; Tilman, 1988), although in some cases it has been
found to parallel changes in biomass, diminishing during early stages and increasing
during late succession. Nitrogen availability in arid and semi-arid plant communities
plays an important role in the dynamics of successional processes (McLendon and
Redente, 1992). Our data show lower photosynthetic capacity per leaf area nitrogen
in Baccharis compared with the late successional species of Atriplex (Fig. 4),
however, nonlimiting initial conditions and faster growth rates in the species (pers.
obs.), allowed initial successful establishment of the former species. Differences in
the response of these species may reflect contrasting photosynthetic pathways, with
higher rates of photosynthesis per unit nitrogen in Atriplex ðC4 Þ than Baccharis ðC3 Þ:
Differences in the slope of the leaf photosynthesis-nitrogen relationship has been
documented mostly for species with different photosynthetic pathway (Sage and
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Pearcy, 1987; Evans, 1989), as a consequence of the lower amount of the enzyme
Ribulose-bisphosphate carboxylase (RUBISCO) and concentrating activity of
phosphoenol pyruvate carboxylase (PEP) during photosynthesis of C4 species.

4.3. Use efficiencies

When daily maximum photosynthetic rates were plotted against leaf nitrogen per
unit area a positive trend was present, although a large variability was associated
with it (Fig. 4). A robust relationship has been found between maximum
photosynthetic rate and leaf nitrogen on a weight basis (Field and Mooney, 1986;
Peterson et al., 1999), but larger variability has been found when expressed on a per
unit leaf area basis (Sobrado and Medina, 1980; Field and Mooney, 1986; Evans,
1989; Peterson et al., 1999). Differences in the intercept of the relationship
photosynthesis—nitrogen have been found between early and late successional
tropical species (Peterson et al., 1999).
Seasonal differences in resource use efficiency for different successional species,
may represent adaptive responses of growth and carbon gain to the two most
limiting resources in arid lands, water and nitrogen. Use efficiencies of these two
most limiting resources in desert habitats followed two different trends when
seasonal data were used. In general, late successional and tree species followed a
linear trend of high water and low nitrogen use efficiency to higher nitrogen and low
water use efficiency, while early successional species followed an exponential
relationship from low nitrogen and water to high nitrogen and water use efficiencies
(Fig. 5). During successional stages, early colonizers may find initial low nitrogen
availability in the soil (Tilman, 1988). However, in abandoned agricultural fields,
initial soil conditions may have higher nutrient availability, particularly in those fields
abandoned not because decreasing productivity potential but saline soil or economic
conditions, as in La Costa de Hermosillo. Those conditions may be advantageous for
early colonizers with maximum water use when nitrogen use is high. This may also be
an important strategy for L. tridentata, the only ‘‘late’’ successional species with a use
efficiency pattern similar to ‘‘early’’ successional species. L.tridentata, a species
considered a late colonizer, is at the same time, a successful invader within the most
dry and hot desert plant communities in North America.
We may expect that as nitrogen becomes more limiting, after agricultural
abandonment, and when water is not ‘‘as’’ limiting (lower water use efficiency), late
successional species and particularly legume trees, will increase their dominance, as
found in our field sites. Bigger changes in nitrogen use efficiencies with small changes
in water use efficiencies in trees compared to shrubs, point to the relative importance
of the two resources within these different functional types.
This study shows that early and late successional species have different
ecophysiological characteristics within desert habitats, and differences in resource
limitations may result from ecophysiological or biophysical adaptive strategies.
Increased water availability may be achieved, by roots tapping deep water (Prosopis)
or by partitioning soil moisture or seasonal changes in their gas exchange activity
(Atriplex). Several mechanisms, biochemical and biophysical, may be responsible for
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the nitrogen use efficiency within a species (Field and Mooney, 1986; Evans, 1989;
Grindlay, 1997; Peterson et al., 1999), and throughout the growing cycle. Allocation
of resources for growth while maximizing photosynthetic nitrogen use efficiency and
water use efficiency has been found in invasive species (McDowell, 2002).
The mechanistic basis of the relationship between photosynthetic water and
nitrogen use efficiencies is not completely understood, however it has been shown to
differ for leaf age, species (Fredeen et al., 1991; Reich et al., 1998; Gerdol et al.,
2000), functional types (Reich et al., 1998), sites (Reich et al., 1998, 1999; Wright et
al., 2001) and successional stages (Abrams and Mostoller, 1995; Ellsworth and
Reich, 1996; Peterson et al., 1999). Increased water use efficiency (WUE) can be
related to either high or low photosynthetic rates due to stomatal limitations,
although WUE has been inversely related to biomass (Pereira, 1995). These studies
found an inverse relationship between water and nitrogen use efficiencies as
proposed here for late successional species. McDowell (2002) on the other hand,
found that the most important predictive factor for invasiveness of Rubus species
was WUE, and her data showed a positive relationship for water and nitrogen use
efficiencies, similar to the trend described for early successional species in our study.
She proposes that high photosynthetic rate is possible even with lower stomatal
conductance at high WUE, due to a larger Ci =Ca CO2 gradient between the leaf
mesophyll and the external surrounding air. Positive relationships for NUE and
WUE between evergreen and deciduous species have also been found for Vaccinium
in stressful subalpine habitats (Gerdol et al., 2000).
Land-use and cover change impacts at regional and global scales are now
widespread. Further studies on the ecophysiological resource-use strategies of early
and late successional species should provide important insights to the general
adaptive traits of such species. This will lead to better understanding of the
mechanistic basis for plant species diversity, replacement and structure within
natural, degraded, and recovering ecosystems.

Acknowledgements

We express our thanks to Alejandro Nava and Fausto Santiago for their help with
Fig. 1. This work was supported by CONACYT (5235-T) and IAI (ISP-I-071) grants
to A. Castellanos, and Universidad de Sonora—University of Arizona competitive
grants to A. Castellanos and W. Halvorson. A. Castellanos thanks SAHRA-
University of Arizona, CONACYT and Universidad de Sonora for support during
the writing of this manuscript. This manuscript benefited from the comments and
suggestions of three anonymous reviewers.

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