germination, survival and growth of three vascular plants on biological soil crusts

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R E S E A R C H P A P E R

Germination, survival and growth of three vascular plants onbiological soil crusts from a Mexican tropical desertH. Godnez-Alvarez, C. Morn & V. Rivera-Aguilar

UBIPRO, FES Iztacala, UNAM., Los Reyes Iztacala, Tlalnepantla, Edo. de Mexico, Mexico

INTRODUCTION

Germination, seedling survival and growth are main stages inthe population recruitment process of vascular plants (Harper1977). The success of each of these stages depends on biotic(e.g. abundance of seed predators, herbivores and competi-tors) and abiotic (e.g. light, water and nutrient availability)factors existing in the microhabitats where seeds were dis-persed (Schupp 1995, 2007; Schupp & Fuentes 1995). Thesemicrohabitats, however, may differ in their suitability for seedgermination, seedling survival and growth (Schupp 2007).For example, the most suitable microhabitats for germinationmay be unsuitable for seedling survival or seedling growth.The study of microhabitat effects on each recruitment stageis essential to understand population recruitment patternsand plant species performance.

Biological soil crusts (BSC) are assemblages of cyanobacte-ria, green algae, fungi, mosses and lichens growing over thesoil surface that affect seed germination, seedling survival andseedling growth (Belnap & Lange 2003). Information aboutthe effect of BSC on these recruitment stages is controversialbecause they can have positive, neutral or negative effects,depending on the stage, plant species and crust type (St. Clairet al. 1984; Zaadyet al. 1997; Evans & Johansen 1999; Belnap& Lange 2003; Escudero et al. 2007). This controversy maybe due to the fact that most of the studies conducted untilnow have just analysed one or two recruitment stages inde-pendently (St. Clair et al. 1984; Zaady et al. 1997; Pendletonet 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 crustsmay provide microhabitats suitable for seed germination, butunsuitable for seedling survival or seedling growth. To under-stand the BSC effects on vascular plants, it is necessary toconsider each stage of the recruitment process and synthesiseall this information. The latter is particularly importantbecause the total effect of BSC is the net outcome of thepositive and negative effects.

The goal of this study is twofold. First, we analyse germi-nation, survival and growth of three vascular plants Agavemarmorata(Agavaceae), Prosopis laevigata (Mimosaceae) and

Neobuxbaumia tetetzo (Cactaceae) on two types of BSCfrom the Zapotitlan Valley, a tropical desert region of south-central Mexico. Second, we synthesise the information todetermine the total effect of BSC on plant species perfor-mance. 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 localinhabitants and several animal species (Godnez-Alvarez et al.1999; Casas et al. 2001; Ornelas et al. 2002; Sanchez de laVega & Godnez-Alvarez 2010). These species frequently growin areas where BSC are common (Godinez-Alvarez H., per-sonal observation) hence it is necessary to understand howBSC affect their recruitment processes. Biological soil crustsare widely distributed in the Zapotitlan Valley, where theyoccur in a great variety of environments (Rivera-Aguilar et al.2006, 2009). Their species composition differs from thatreported for BSC in other North American desert regions(Rivera-Aguilar et al. 2006). Previous studies show that BSCincrease both germination and seedling growth of two vascu-

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: [email protected]

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, seed-ling survival and growth of vascular plants is controversial because they can havepositive, neutral or negative effects. This controversy may be because most studiesconducted until now have just analysed one or two recruitment stages indepen-dently. To understand the BSC effects on vascular plants, it is necessary to considereach stage of the recruitment process and synthesise all this information. The goalof this study was twofold. First, we analyse germination, seedling survival andgrowth of three vascular plants (Agave marmorata, Prosopis laevigata and Neobux-

baumia tetetzo) on BSC (cyanobacteria and mixed crust) from a tropical desertregion of south-central Mexico. Second, we synthesise the information to determinethe total effect of BSC on plant species performance. We conducted experimentsunder controlled conditions to evaluate the proportion of germinated seeds, propor-tion of surviving seedlings and seedling dry weight in BSC and bare soil. Resultsshowed that BSC have different effects on germination, seedling survival andgrowth of plant species. Plant species performance was qualitatively higher on BSCthan bare soil. The highest performance of A. marmorata and P. laevigata wasobserved on cyanobacteria and mixed crusts, respectively. The highest performance

Plant Biology ISSN 1435-8603

Plant Biology 14 (2012) 157162 2011 German Botanical Society and The Royal Botanical Society of the Netherlands 157


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lar plants, Mimosa luisana andMyrtillocatus geometrizans (Ri-vera-Aguilar et al. 2005). To fulfil our goal, we conductedexperiments under controlled conditions to evaluate the pro-portion of germinated seeds, proportion of surviving seed-lings and seedling dry weight in BSC and bare soil. Althoughthe information on BSC effects on vascular plants is contro-

versial, we expect higher germination, seedling survival andgrowth on crusts than bare soil. Similarly, we expect higherplant 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 inmesquite shrublands located on fluvial terraces of the SaladoRiver, Zapotitlan Salinas, Puebla, Mexico (181908181945 N, 972700972740 W, 14301600 m a. s. l.).We collected two types of naturally occurring BSC from barespaces in summer 2006. The cyanobacteria crust is dominated

by Microcoleus, Scytonema and Chroococcidiopsis species,which constitute 2550% of the crust surface. Mixed crustscontained 2550% cyanobacteria and moss (mainly Bryumand Pseudocrossidium species). Both crust types contained


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A. marmorata on cyanobacteria crust and bare soil germi-nated in 4.8 0.3 and 5.5 0.3 days, respectively. Thesedifferences were not statistically significant (t = 1.73, df = 6,P = 0.13). Germination on mixed crust was


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laevigata performance on cyanobacteria crust was half thaton bare soil, while performance on mixed crust was 2.3-timeshigher. Neobuxbaumia tetetzo performance on cyanobacteria(2.6-times) and mixed crust (2.4-times) was relatively similarand higher than on bare soil.

DISCUSSION

Results show that cyanobacteria and mixed crust have differ-ent effects on germination, seedling survival and growth ofthe three vascular plant species evaluated in this study. These

effects in turn determined variation in plant species perfor-mance depending on crust type.

The species A. marmorata showed higher performance onBSC than on bare soil. This performance was particularlyhigh (10-fold higher) on cyanobacteria crust because it signif-icantly increased all recruitment stages: germination, seedlingsurvival and growth. The positive effect of cyanobacteriacrust on germination and seedling survival might be relatedto the fact that this crust provides better conditions of soilwater availability in comparison to bare soil (Maya et al.2002; George et al. 2003; Su et al. 2007, 2009). Other studieshave reported that cyanobacteria crust positively affectsgermination of several annual and perennial plants (St. Clairet al. 1984; Hawkes 2004; Li et al. 2005; Rivera-Aguilar et al.

2005; Langhans et al. 2009; Su et al. 2009). The positive effectof cyanobacteria crust on A. marmorata seedling growthmight 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 inmixed 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 BSCincrease the concentration of soil nitrogen, having a positiveeffect on the establishment and growth of vascular plants(Pendletonet al. 2003).

In contrast, the performance of A. marmorata on mixedcrust was only twice that on bare soil. Mixed crust decreasedgermination, but increased seedling survival and growth. Thenegative effects on germination might be related to speciescomposition of the crust, which was dominated by the mossBryum argenteum. Serpeet al.(2006) reported that BSC domi-

Agave marmorata

Cyanobacteria crust Mixed crust Bare soil

Germination

Survival

Performance

0.72 0.30 0.53

0.94 0.92 0.57

10.67 2.21 1.10

Prosopis laevigata


Germination

Survival

Performance

0.28 0.25 0.28

0.27 0.42 0.42

0.02 0.09 0.04

Neobuxbaumia tetetzo


Germination

Survival

Performance

0.72 0.79 0.63

0.96 1.00 0.93

10.39 9.65 4.00

Growth 15.76 8.01 3.63

Growth 0.27 0.88 0.35

Growth 15.04 12.22 6.83

Fig. 4. Plant species performance on two crust types and bare soil. Per-

formance 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.

D

ryweight(mg)

Dryweight(g)

0

3

6

9

12

15

18 a

b

c

0

0.3

0.6

0.9

1.2

a

b

a

Dryweight(mg)

Treatment

0

3

6

9

12

15

18


b

a

a

(a)

(c)

(b)

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 treat-

ments (P < 0.05).

Vascular plants and biological soil crusts Godnez-Alvarez, Morn & Rivera-Aguilar

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


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nated by this moss species decreased seed water status, thusreducing germination. The positive effects of mixed crust onseedling survival and growth were probably related to bettersoil nutrient conditions (St. Clair et al. 1984; Li et al. 2005;Langhanset al.2009). These positive effects, however, were notas high as those of the cyanobacteria crust.

The species P. laevigata and N. tetetzo showed higher per-formance on BSC (ca. twice as high) than on bare soil, exceptfor P. laevigata on cyanobacteria crust, which showed lowerperformance (0.5-times lower). The higher performance wasdue to mixed crust leading to an increase in seedling dryweight of P. laevigata, while cyanobacteria and mixed crustincreased dry weight of N. tetetzo seedlings. It has been sug-gested that BSC have higher levels of organic matter, electro-lytic conductivity, N, Ca, Mg, Na and Cu, thus having apositive effect on the establishment and growth of vascularplants (Harper & Belnap 2001; Pendleton et al. 2003; Li et al.2005; Beyschlag et al. 2008; Langhans et al. 2009). This infor-mation, along with the preliminary data on soil nitrogen con-tent ofA. marmorata, suggest that positive effects of BSC on

seedling growth might be related to an increase in soil nutri-ent content. However, we did not analyse soil samples fromP. laevigata or N. tetetzo, hence we were unable to corrobo-rate this suggestion. The lower P. laevigata performance oncyanobacteria crust might be related to lower seedling sur-vival. This negative effect however could not be detected dueto the high data variance. Very few studies have analysedBSC effects on seedling survival, finding positive as well asnegative effects (St. Clair et al. 1984; Li et al. 2005; Langhanset al. 2009). Further studies should consider these issues to

determine mechanisms responsible for the survival andgrowth responses observed in these plant species.

In summary, the results show that BSC have differenteffects on the recruitment stages analysed in this study. Bio-logical soil crusts had positive, neutral or negative effects onseed germination. They had positive or neutral effects on

seedling survival and growth. Despite these differences, plantspecies performance tended to be higher in BSC than on baresoil. As far as we know, this is the first study that has syn-thesised all this information to evaluate the total effect ofBSC on vascular plants. This synthesis is essential because thetotal effect of BSC depends on the balance between negativeand positive effects on each recruitment stage. Only throughthis kind of synthesis will it be possible to understand theBSC effects on population recruitment patterns and plantspecies performance. Lastly, it is important to consider thatplant species performance in this study was evaluated foronly 80 days; hence it is necessary to conduct future evalua-tions for longer periods of time. Further, it is necessary toconduct field studies to confirm our results.

ACKNOWLEDGEMENTS

This study was supported by Programa de Apoyo a los Profe-sores de Carrera para la Formacion de Grupos de Investiga-cion (PAPCA No. 77), Periodo 20072008, Facultad deEstudios Superiores Iztacala, Universidad Nacional Autonomade Mexico. Thanks to David Eldridge and two anonymousreviewers for helpful comments on a previous version of thismanuscript.

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germination, survival and growth of three vascular plants on biological soil crusts

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