Plant Biology ISSN 1435-8603

RESEARCH PAPER

Germination, survival and growth of three vascular plants on

biological soil crusts from a Mexican tropical desert
H. Godnez-Alvarez, C. Morn & V. Rivera-Aguilar
UBIPRO, FES Iztacala, UNAM., Los Reyes Iztacala, Tlalnepantla, Edo. de Mexico, Mexico

Keywords
Agave marmorata; cyanobacteria; mosses;
Neobuxbaumia tetetzo; Prosopis laevigata;
Tehuacan-Cuicatlan Valley.
Correspondence
H. Godnez-Alvarez, UBIPRO, FES Iztacala,
UNAM. Av. de los Barrios 1, Los Reyes
Iztacala, Tlalnepantla 54090, Ap. Postal 314,
Edo. de Mexico, Mexico.
E-mail: hgodinez@campus.iztacala.unam.mx
Editor
M. Riederer
Received: 21 February 2011; Accepted: 11
June 2011
doi:10.1111/j.1438-8677.2011.00495.x

ABSTRACT
Information about the effects of biological soil crusts (BSC) on germination, seedling survival and growth of vascular plants is controversial because they can have
positive, neutral or negative effects. This controversy may be because most studies
conducted until now have just analysed one or two recruitment stages independently. To understand the BSC effects on vascular plants, it is necessary to consider
each stage of the recruitment process and synthesise all this information. The goal
of this study was twofold. First, we analyse germination, seedling survival and
growth of three vascular plants (Agave marmorata, Prosopis laevigata and Neobuxbaumia tetetzo) on BSC (cyanobacteria and mixed crust) from a tropical desert
region of south-central Mexico. Second, we synthesise the information to determine
the total effect of BSC on plant species performance. We conducted experiments
under controlled conditions to evaluate the proportion of germinated seeds, proportion of surviving seedlings and seedling dry weight in BSC and bare soil. Results
showed that BSC have different effects on germination, seedling survival and
growth of plant species. Plant species performance was qualitatively higher on BSC
than bare soil. The highest performance of A. marmorata and P. laevigata was
observed on cyanobacteria and mixed crusts, respectively. The highest performance

INTRODUCTION
Germination, seedling survival and growth are main stages in
the population recruitment process of vascular plants (Harper
1977). The success of each of these stages depends on biotic
(e.g. abundance of seed predators, herbivores and competitors) and abiotic (e.g. light, water and nutrient availability)
factors existing in the microhabitats where seeds were dispersed (Schupp 1995, 2007; Schupp & Fuentes 1995). These
microhabitats, however, may differ in their suitability for seed
germination, seedling survival and growth (Schupp 2007).
For example, the most suitable microhabitats for germination
may be unsuitable for seedling survival or seedling growth.
The study of microhabitat effects on each recruitment stage
is essential to understand population recruitment patterns
and plant species performance.
Biological soil crusts (BSC) are assemblages of cyanobacteria, green algae, fungi, mosses and lichens growing over the
soil surface that affect seed germination, seedling survival and
seedling growth (Belnap & Lange 2003). Information about
the effect of BSC on these recruitment stages is controversial
because they can have positive, neutral or negative effects,
depending on the stage, plant species and crust type (St. Clair
et al. 1984; Zaady et al. 1997; Evans & Johansen 1999; Belnap
& Lange 2003; Escudero et al. 2007). This controversy may
be due to the fact that most of the studies conducted until
now have just analysed one or two recruitment stages independently (St. Clair et al. 1984; Zaady et al. 1997; Pendleton
et al. 2003; Hawkes 2004; Li et al. 2005; Rivera-Aguilar et al.
2005; Escudero et al. 2007; Su et al. 2007, 2009; Beysch-

lag et al. 2008; Langhans et al. 2009). Biological soil crusts

may provide microhabitats suitable for seed germination, but
unsuitable for seedling survival or seedling growth. To understand the BSC effects on vascular plants, it is necessary to
consider each stage of the recruitment process and synthesise
all this information. The latter is particularly important
because the total effect of BSC is the net outcome of the
positive and negative effects.
The goal of this study is twofold. First, we analyse germination, survival and growth of three vascular plants Agave
marmorata (Agavaceae), Prosopis laevigata (Mimosaceae) and
Neobuxbaumia tetetzo (Cactaceae) on two types of BSC
from the Zapotitlan Valley, a tropical desert region of southcentral Mexico. Second, we synthesise the information to
determine the total effect of BSC on plant species performance. The species A. marmorata, P. laevigata and N. tetetzo
are dominant plants in the Zapotitlan Valley (Osorio et al.
1996), where they provide essential resources for the local
inhabitants and several animal species (Godnez-Alvarez et al.
1999; Casas et al. 2001; Ornelas et al. 2002; Sanchez de la
Vega & Godnez-Alvarez 2010). These species frequently grow
in areas where BSC are common (Godinez-Alvarez H., personal observation) hence it is necessary to understand how
BSC affect their recruitment processes. Biological soil crusts
are widely distributed in the Zapotitlan Valley, where they
occur in a great variety of environments (Rivera-Aguilar et al.
2006, 2009). Their species composition differs from that
reported for BSC in other North American desert regions
(Rivera-Aguilar et al. 2006). Previous studies show that BSC
increase both germination and seedling growth of two vascu-

Plant Biology 14 (2012) 157162 2011 German Botanical Society and The Royal Botanical Society of the Netherlands

157

Godnez-Alvarez, Morn & Rivera-Aguilar

Vascular plants and biological soil crusts

lar plants, Mimosa luisana and Myrtillocatus geometrizans (Rivera-Aguilar et al. 2005). To fulfil our goal, we conducted
experiments under controlled conditions to evaluate the proportion of germinated seeds, proportion of surviving seedlings and seedling dry weight in BSC and bare soil. Although
the information on BSC effects on vascular plants is controversial, we expect higher germination, seedling survival and
growth on crusts than bare soil. Similarly, we expect higher
plant species performance on crusts than bare soil.
MATERIALS AND METHODS
Biological soil crusts, bare soil and seed collection

Biological soil crusts, bare soil and seeds were collected in

mesquite shrublands located on fluvial terraces of the Salado
River, Zapotitlan Salinas, Puebla, Mexico (181908
181945 N, 972700972740 W, 14301600 m a. s. l.).
We collected two types of naturally occurring BSC from bare
spaces in summer 2006. The cyanobacteria crust is dominated
by Microcoleus, Scytonema and Chroococcidiopsis species,
which constitute 2550% of the crust surface. Mixed crusts
contained 2550% cyanobacteria and moss (mainly Bryum
and Pseudocrossidium species). Both crust types contained
<25% lichens (mainly Placidium and Collema species). For
each crust type, 12 samples (12 12 2 cm) were collected,
placed in plastic containers and transported to the laboratory.
Samples were watered to soil saturation and maintained at
room temperature. We collected bare soil at the same sites
where BSC were collected. Bare soil was visually defined as
soil not covered by BSC. Thirty-six soil samples
(10 10 5 cm) were collected and mixed to obtain a composite sample. Soil from this sample was placed in plastic
containers and transported to the laboratory.
Seeds were obtained from mature fruits collected in at least
20 individuals of each plant species. Seeds were manually
extracted, washed with tap water to remove fruit pulp, and
dried at room temperature. Subsequently, seeds were placed
in paper bags and stored at room temperature until experiments were conducted.
Germination

The effect of BSC on seed germination was evaluated with a

randomised experimental design in which the single factor
was type of crust and the experimental treatments were: (i)
cyanobacteria crust; (ii) mixed crust; and (iii) bare soil. The
experimental unit was a plastic container filled with soil or
soil covered with cyanobacteria crust or mixed crust. Container size varied depending on plant species. Containers for
A. marmorata and N. tetetzo were 13 12 5 cm. Containers for P. laevigata were 13 18 cm. Four replicates were
conducted for each treatment, for a total of 12 units per
plant species. Depending on seed size, 1025 seeds were
evenly distributed on bare soil or crust surface. Containers
received 100 ml water and were kept at room temperature
(max. temp. 29 3 C, min. temp. 12 2.5 C). Germination (i.e. radicle emergence) was recorded for 810 days
because no further germination was recorded after this time.
Containers were watered with 50 ml water every 3 days to
maintain moisture conditions relatively constant. The pro158

portion of germinated seeds and the number of days to 50%

of total germination (T50) were calculated for each species.
Seedling survival and growth

Biological soil crust effect on seedling survival and growth

was analysed using the same experimental design as that for
germination. Seedlings that emerged in each treatment were
considered as experimental units. They were maintained at
laboratory conditions for 80 days and given 50 ml water
every 4 days, to maintain moisture conditions relatively constant. The experiment lasted only 80 days to avoid competition among seedlings. Any new seedling that emerged during
this time was discarded to avoid affecting monitoring of
seedling survival and growth. We recorded the number of
surviving seedlings in each treatment at the end of the experiment and calculated the proportion of surviving seedlings.
Seedlings (including their roots) were harvested and oven
dried at 70 C for 3 days to measure dry weight.
Plant species performance on BSC and bare soil

Performance of each plant species was calculated as the product of the proportion of germinated seeds, proportion of surviving seedlings and seedling dry weight on the two crust
types and bare soil. All factors were considered equally
important, hence we did not conduct any weighting.
Statistical analysis

The proportion of germinated seeds, T50, proportion of surviving seedlings and seedling dry weight of each plant species
were analysed with one-way anova to determine whether
there were significant differences among treatments. The proportion of germinated seeds and proportion of surviving
seedlings were normalised using angular transformation. Differences among treatments were detected with Tukeys HSD
test. All analyses were conducted with spss, version 9.0 (SPSS
1998).
Data for dry weight of P. laevigata seedlings were not normally distributed, hence they were analysed with a randomisation test for a one-way anova. This test was conducted
with EcoSim, version 7.0 (Gotelli & Entsminger 2001).
RESULTS
Germination

Biological soil crusts significantly increased the germination

of A. marmorata (F = 10.17, df = 2, 9, P = 0.005), but they
did not have any effect on the germination of P. laevigata
(F = 0.16, df = 2, 9, P = 0.85) and N. tetetzo (F = 1.04,
df = 2, 8, P = 0.4). Germination of A. marmorata was significantly higher on cyanobacteria crust (72.5%) than mixed
crust (30%). Germination on bare soil (52.5%) had intermediate values that did not differ significantly from these treatments (Fig. 1a). Germination of P. laevigata (2527.5%) and
N. tetetzo (62.579.2%) was relatively similar in all treatments
(Fig. 1b and c).
The number of days to 50% of the total germination (T50)
was only analysed for A. marmorata and N. tetetzo. Seeds of

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Godnez-Alvarez, Morn & Rivera-Aguilar

100

Vascular plants and biological soil crusts

(a)

1.0 (a)

80

60

0.8

ab

0.6

40
b

20

0.4
0.2

0
2

(b)

40
30
20
10
0
0

0
Seedling survival (proportion)

Germination (%)

0.7 (b)
0.6
0.5
0.4
0.3
0.2
0.1
0
1.0 (c)

(c)

100

0.8
80

0.6
60

0.4
40

0.2
20
0
0

4
6
Time (days)

10

Fig. 1. Germination (mean 1 SE) of Agave marmorata (a), Prosopis laevigata (b) and Neobuxbaumia tetetzo (c) on cyanobacteria crust (diamonds), mixed crust (squares) and bare soil (triangles). For each species,
letters indicate significant differences among treatments (P < 0.05).

A. marmorata on cyanobacteria crust and bare soil germinated in 4.8 0.3 and 5.5 0.3 days, respectively. These
differences were not statistically significant (t = 1.73, df = 6,
P = 0.13). Germination on mixed crust was <50%. Seeds of
N. tetetzo on mixed crust tended to germinate faster
(1.8 0.3 days) than on cyanobacteria crust (3.5 1.2 days)
and bare soil (3.8 1.1 days). However, these differences
were not statistically significant (F = 0.91, df = 2, 8,
P = 0.44). T50 for P. laevigata could not be analysed because
germination was <50% in all treatments.
Seedling survival and growth

Biological soil crusts significantly increased seedling survival

of A. marmorata (F = 5.83, df = 2, 9, P = 0.02), but they did
not have any effect on survival of P. laevigata (F = 0.56,
df = 2, 6, P = 0.6) and N. tetetzo (F = 0.82, df = 1, 6,
P = 0.4). Survival of A. marmorata on cyanobacteria (0.94
0.06) and mixed (0.92 0.08) crust was similar and significantly higher than on bare soil (0.57 0.13; Fig. 2a). Survival
of P. laevigata did not differ among treatments because data
showed high variance (Fig. 2b). Survival of N. tetetzo was
relatively similar in all treatments hence there were no significant differences (Fig. 2c).

0
Cyanobacteria crust

Mixed crust
Treatment

Bare soil

Fig. 2. Seedling survival (mean 1 SE) of Agave marmorata (a), Prosopis

laevigata (b) and Neobuxbaumia tetetzo (c) on two crust types and bare
soil. For each species, letters indicate significant differences among treatments (P < 0.05).

Biological soil crusts significantly increased seedling growth

of all plant species (A. marmorata: F = 44.35, df = 2, 50,
P < 0.00001; P. laevigata: observed F-ratio = 22.85, P =
0.002; N. tetetzo: F = 21.52, df = 2, 147, P < 0.00001). Seedlings of A. marmorata on cyanobacteria crust (15.8 0.9 mg)
had the highest dry weight, followed by seedlings on mixed
crust (8.0 0.8 mg) and bare soil (3.6 0.5 mg). All differences were statistically significant (Fig. 3a). Seedlings of
P. laevigata on mixed crust (0.9 0.1 g) had higher dry
weight than seedlings on cyanobacteria crust (0.27 0.005 g)
and bare soil (0.35 0.03 g). Differences between the last
two treatments were not statistically significant (Fig. 3b).
Seedlings of N. tetetzo on cyanobacteria (15.04 1.05 mg)
and mixed crust (12.2 0.6 mg) had similar dry weight,
which significantly differed from bare soil (6.8 0.5 mg;
Fig. 3c).
Plant species performance on BSC and bare soil

Plant species performance varied depending on crust type

(Fig. 4). Agave marmorata performance on both crust types
was higher than on bare soil. However, performance on
cyanobacteria crust was almost 10-fold higher, while
performance on mixed crust was only twice as high. Prosopis

Plant Biology 14 (2012) 157162 2011 German Botanical Society and The Royal Botanical Society of the Netherlands

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Godnez-Alvarez, Morn & Rivera-Aguilar

Vascular plants and biological soil crusts

18 (a)

Agave marmorata

Dry weight (mg)

15
12
9

Mixed crust

Bare soil

Germination

0.72

0.30

0.53

Survival

0.94

0.92

0.57

Growth

15.76

8.01

3.63

Performance

10.67

2.21

1.10

6
3
0
1.2 (b)

Dry weight (g)

Cyanobacteria crust

0.9
0.6

Prosopis laevigata

Cyanobacteria crust

Mixed crust

Bare soil

Germination

0.28

0.25

0.28

Survival

0.27

0.42

0.42

Growth

0.27

0.88

0.35

Performance

0.02

0.09

0.04

0.3
0

Dry weight (mg)

18 (c)

15

12
b

9
6

Neobuxbaumia tetetzo

3
0
Cyanobacteria crust

Mixed crust
Treatment

Fig. 3. Seedling growth (mean 1 SE) of Agave marmorata (a), Prosopis

laevigata (b) and Neobuxbaumia tetetzo (c) on two crust types and bare
soil. For each species, letters indicate significant differences among treatments (P < 0.05).

laevigata performance on cyanobacteria crust was half that

on bare soil, while performance on mixed crust was 2.3-times
higher. Neobuxbaumia tetetzo performance on cyanobacteria
(2.6-times) and mixed crust (2.4-times) was relatively similar
and higher than on bare soil.
DISCUSSION
Results show that cyanobacteria and mixed crust have different effects on germination, seedling survival and growth of
the three vascular plant species evaluated in this study. These
effects in turn determined variation in plant species performance depending on crust type.
The species A. marmorata showed higher performance on
BSC than on bare soil. This performance was particularly
high (10-fold higher) on cyanobacteria crust because it significantly increased all recruitment stages: germination, seedling
survival and growth. The positive effect of cyanobacteria
crust on germination and seedling survival might be related
to the fact that this crust provides better conditions of soil
water availability in comparison to bare soil (Maya et al.
2002; George et al. 2003; Su et al. 2007, 2009). Other studies
have reported that cyanobacteria crust positively affects
germination of several annual and perennial plants (St. Clair
et al. 1984; Hawkes 2004; Li et al. 2005; Rivera-Aguilar et al.
160

Cyanobacteria crust

Mixed crust

Bare soil

Germination

0.72

0.79

0.63

Survival

0.96

1.00

0.93

Growth

15.04

12.22

6.83

Performance

10.39

9.65

4.00

Bare soil

Fig. 4. Plant species performance on two crust types and bare soil. Performance was calculated as the product of proportion of germinated
seeds, proportion of surviving seedlings and seedling dry weight in each
treatment. Boxes with bold lines indicate the highest significant values in
each row.

2005; Langhans et al. 2009; Su et al. 2009). The positive effect

of cyanobacteria crust on A. marmorata seedling growth
might be the result of changes in soil nutrient content,
particularly nitrogen. Preliminary analyses of soil samples
taken from this crust showed that nitrate (0.13 0.002%)
and ammonium (0.29 0.01%) content were higher than in
mixed crust (nitrate: 0.07 0.008%; ammonium: 0.23
0.007%) and bare soil (nitrate: 0.02 0.007%; ammonium:
0.16 0.008%). These results support the notion that BSC
increase the concentration of soil nitrogen, having a positive
effect on the establishment and growth of vascular plants
(Pendleton et al. 2003).
In contrast, the performance of A. marmorata on mixed
crust was only twice that on bare soil. Mixed crust decreased
germination, but increased seedling survival and growth. The
negative effects on germination might be related to species
composition of the crust, which was dominated by the moss
Bryum argenteum. Serpe et al. (2006) reported that BSC domi-

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Godnez-Alvarez, Morn & Rivera-Aguilar

Vascular plants and biological soil crusts

nated by this moss species decreased seed water status, thus

reducing germination. The positive effects of mixed crust on
seedling survival and growth were probably related to better
soil nutrient conditions (St. Clair et al. 1984; Li et al. 2005;
Langhans et al. 2009). These positive effects, however, were not
as high as those of the cyanobacteria crust.
The species P. laevigata and N. tetetzo showed higher performance on BSC (ca. twice as high) than on bare soil, except
for P. laevigata on cyanobacteria crust, which showed lower
performance (0.5-times lower). The higher performance was
due to mixed crust leading to an increase in seedling dry
weight of P. laevigata, while cyanobacteria and mixed crust
increased dry weight of N. tetetzo seedlings. It has been suggested that BSC have higher levels of organic matter, electrolytic conductivity, N, Ca, Mg, Na and Cu, thus having a
positive effect on the establishment and growth of vascular
plants (Harper & Belnap 2001; Pendleton et al. 2003; Li et al.
2005; Beyschlag et al. 2008; Langhans et al. 2009). This information, along with the preliminary data on soil nitrogen content of A. marmorata, suggest that positive effects of BSC on
seedling growth might be related to an increase in soil nutrient content. However, we did not analyse soil samples from
P. laevigata or N. tetetzo, hence we were unable to corroborate this suggestion. The lower P. laevigata performance on
cyanobacteria crust might be related to lower seedling survival. This negative effect however could not be detected due
to the high data variance. Very few studies have analysed
BSC effects on seedling survival, finding positive as well as
negative effects (St. Clair et al. 1984; Li et al. 2005; Langhans
et al. 2009). Further studies should consider these issues to
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Plant Biology 14 (2012) 157162 2011 German Botanical Society and The Royal Botanical Society of the Netherlands