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Effect of seed burial in different soils on the germination of three specially protected cactus species.

Favorable conditions for recruitment in arid systems are rare because of prevailing harsh conditions (Flores and Jurado, 2003; Zhang et al., 2011). Seedling establishment of many species appears to be more frequent under canopies of adult plants of other species that provide a less stressful microenvironment (Ellner and Shmida, 1981). This association of emergent seedlings and adult plants has been called "nurse plant syndrome" (Niering et al., 1963) or "nurse-protege" interaction (Cody, 1993; Flores and Jurado, 2003).

The causes of nurse-seedling relationships can vary between species and environments, and it is possible that multiple causes account for this association (Flores and Jurado, 2003). For example, a larger number of seeds can be recruited under shrubs compared with bare soil (seed trapping); more water is available under established shrubs than on bare soil (moisture safe site); more nutrients are available in the soil under established shrubs than under surrounding soil (nutrient safe site); greater protection of protege species from grazing and trampling is available under shrubs (safe site from herbivores), or greater physical support for protege species is available, at least in the early stages of their life cycle (physical support safe site).

Nutrient levels in the soil could be higher under the canopies of established shrubs than in surrounding soil as a result of nutrient concentration from vertical and horizontal root uptake, accumulation of litter, increased bird and insect droppings, and, in some cases, nitrogen fixation (Flores and Jurado, 2003). These higher nutrient levels in the soil could promote higher seed germination (Godinez-Alvarez and Valiente-Banuet, 1998; Baskin and Baskin, 2001).

Many cactus species grow under nurse plants (Flores and Jurado, 2003). Soil characteristics have been found to affect seed germination of several cacti, like Carnegiea gigantea and Stenocereus thurberi (McDonough, 1964), Ferocactus histrix (Del Castillo, 1986), Mammillaria heyderi (Trejo-Hernandez and Garza-Castillo, 1993), Turbinicarpus polaskii, T. schwarzii, and Echinocereus morricallii (Jolly and Lockert, 1996). The soil under mesquite plants has been found to have more organic matter and nutrients than soil from open areas (Muro-Perez et al., 2012); however, there are no studies evaluating whether the soil under nurse plants, likely to have more nutrients, results in higher seed germination than soil from open spaces. Nutrients in the soil are important for germination of some species (i.e., biological soil crusts) that have higher nutrients than soils without them, and have a positive effect on the seed germination of the cactus Myrtillocactus geometrizans (Rivera-Aguilar et al., 2005).

Another factor influencing germination and seedling emergence is the depth of seed burial in the soil (Fuchs et al., 2000; Traba et al., 2004; Flores-Cano et al., 2012). Seed burial may be promoted by abiotic-driven soil disturbances, such as those caused by water and wind, as well as by biotic factors, including the foraging behavior of seed dispersers and earthworm activity (Vander-Wall 1990, 1993; Chambers and MacMahon, 1994; Renard et al., 2010). Seed burial helps seeds escape from postdispersal predation and prevents death of the embryo by desiccation or exposure to extreme temperatures during an unfavorable season (Borchert et al., 1989; Vander-Wall, 1990; Seiwa et al., 2002; Cheng et al., 2007). Burial may occur by seeds falling in the litter or in soil cracks, and is important for germination, because it may provide benefits such as reduction of air exposure, maintenance of high humidity levels, and protection against extreme temperatures and foraging granivores (Everitt, 1983; Seiwa et al., 2002; Li et al., 2012). However, buried seeds are in the dark, which has been shown to inhibit seed germination for some cactus species (Benitez-Rodriguez et al., 2004; Flores et al., 2006, 2011).

We evaluated germination percentage on nutrient-rich soil under nurse plants and poor soil from open spaces, and the effect of seed burial (buried and unburied seeds) on seed germination of three cactus species: Coryphantha durangensis, Peniocereus greggii, and E. longisetus, that grow under nurse plants (Muro-Perez et al., 2012). The three studied species are under special protection status (Hunt, 1992; SEMARNAT, 2010).

Materials and Methods--Study Area and Studied Species--Coryphantha durangnesis, P. greggii, and E. longisetus are distributed in a canyon in Carton de Fernandez State Park (25[degrees]27'N, 103[degrees]46'W) within the Chihuahuan Desert in Mexico at an elevation of 1,200 m above sea level. Temperature ranges from 1.6[degrees]C (in January) to 37.4[degrees]C (in June), with an annual rainfall of 200-350 mm. The main plant communities are thornscrub dominated by either small-leaved, rosette, or hemisucculent and succulent plants (Muro-Perez et al., 2012). Coryphantha durangensis grows 10-15 cm high and 4-6 cm wide as isolated individuals or in small clumps (Bravo-Hollis, 1978; Bravo-Hollis and Sanchez-Mejorada, 1989). Echinocereus longisetus is cylindrical, 15-30 cm high and 5-7 cm wide (Bravo-Hollis and Sanchez-Mejorada, 1989). Peniocereus greggii has an erect curved stem 20-60 cm high and 3 cm in diameter (Bravo-Hollis and Sanchez-Mejorada, 1989).

Area of Species Distribution--Coryphantha durangensis grows in Coahuila and Durango, Mexico; P greggii is distributed in Chihuahua, Coahuila, Durango, Nuevo Leon, Sonora, and Zacatecas, Mexico (Guzman et al., 2003) as well as in Texas, New Mexico, and Arizona, USA (Sanchez-Salas et al., 2009). Echinocereus longisetus is found in Coahuila and Nuevo Leon (Guzman et al., 2003). Seeds from these species were collected in the Cauon de Fernandez, an area with high cactus richness in the southern Chihuahuan Desert (Valencia-Castro, 2005).

Seed Collection--Fruits from the three cactus species were collected in April 2009 at Canon de Fernandez State Park from at least 10 mother plants. Fruits were placed in paper bags and set to dry at room temperature for a month to prevent any moisture development that might prompt germination or decomposition (Moreno et al., 1992).

Experimental Design--Germination was recorded daily for 1 month as the emergence of the radicle or any part of the embryo, as recommended for arid-zone plants (Baskin and Baskin, 2001). The experimental design was complete random factorial 3 x 4 x 5. There were 20 seeds per plot and five plots per line, with a total of 100 seeds per treatment. There were four treatments: 1) seeds placed on mesquite soil, 2) seeds placed on poor soil, 3) seeds buried at 0.5 cm under mesquite soil, and 4) seeds buried 0.5 cm under poor soil.

Statistical Analyses--Treatment and species were used as factors for the analysis of variance. Percentage germination data were arcsine transformed before analysis to comply with analysis of variance requirements.

Results and Discussion--Previous studies have shown that nutrient levels in the soil are higher under the canopies of established shrubs than in the surrounding soil (Flores and Jurado, 2003; Muro-Perez et al., 2012). We hypothesized that higher nutrient levels in the soil could promote higher seed germination (GodinezAlvarez and Valiente-Banuet, 1998; Baskin and Baskin, 2001). Echinocereus longisetus had very low germination (4% [+ or -] 1.2%) across substrates, and there were no significant differences among treatments (F = 2.66; P = 0.08). Coryphanta durangensis (Fig. 1) had higher germination on mesquite soil (96% [+ or -] 0.024%) than on poor soil (56% [+ or -] 0.605%; F = 21.09, P < 0.0001). A similar result was found for P greggii seeds (Fig. 2), which had higher germination on mesquite soil (85% [+ or -] 0.076%) than on poor soil (69% [+ or -] 0.55%; F = 7.67, P < 0.0001). The results for these two species are in agreement with the proposed hypothesis, in that more seeds of C. durangensis and P greggii germinated on mesquite soil than on poor soil. For these species, germination on poor soil was also high; suggesting that seed distribution and seedling establishment may differ under both conditions for other reasons besides soil quality, such as hydraulic uplift or protection from trampling (Flores and Jurado, 2003). These results should be considered in conservation programs for these protected species.

We also hypothesized that cactus seeds would not germinate when buried, because they would be in total darkness and require light to germinate (Flores et al., 2006, 2011). Accordingly, we found very low germination for buried seeds of C. durangensis (Fig. 1) and P. greggii (Fig. 2). Coryphantha durangensis buried seeds had lower germination (2% for seeds buried in mesquite soil and no germination for seeds buried in poor soil) than seeds on the soil surface (F = 21.09, P < 0.0001). Germination of P greggii buried seeds had lower germination (F = 7.67, P < 0.0001) than seeds on the soil surface (6% [+ or -] 0.604% under mesquite soil and 8% [+ or -] 0.152% under poor soil). Most cactus seeds need light to germinate (Flores et al., 2011); hence it is possible that ungerminated buried seeds in our study were dormant, because burial is an essential prelude to dormancy in several species (Thompson et al., 1993; Grime, 2001). Burial may also provide safe sites from harsh conditions for seeds until germination occurs, although other processes such as seed predation and fungal attack could also be operating (Borchert et al., 1989; Vander-Wall, 1993; Seiwa et al., 2002).

Seeds of E. longisetus appear to exhibit seed dormancy even under light conditions. In arid and semiarid environments, seed germination and seedling establishment are infrequent because of extreme temperatures and low water availability (Flores and Jurado, 2003; Flores et al., 2004). Thus, a common plant strategy in these environments is seed dormancy, which is found in several plant families (Baskin and Baskin, 2001; Jurado and Moles, 2003; including Cactaceae (Rojas-Arechiga and Vazquez-Yanes, 2000; Flores et al., 2005, 2006, 2008, 2011).

Conclusions--Echinocereus longisetus had very low germination across substrates. Seeds of C. durangensis and P. greggii had higher germination on soil from under nurse mesquites than on poor soil. Buried seeds of both species had lower germination than seeds on the soil surface.

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Submitted 8 November 2012.

Acceptance recommended by Associate Editor, Mara L. Alexander, 22 October 2013.

Gisela Muro-Perez, Enrique Jurado, * Joel Flores, and Jaime Sanchez-Salas

Facultad de Ciencias Forestales, Universidad Autonoma de Nuevo Leon, A.P. 41. Carretera Nacional km. 145, Linares, N.L. 67700, Moxico (GM, EJ, JS)

Instituto Potosino de Investigacion Cientifica y Tecnologica, A.C., Division de Ciencias Ambientales.

Camino a la Presa San Jose No. 2055, Lomas 4a Seccion, San Luis Potoso, 78216, S.L.P., Moxico (JF) Facultad de Ciencias Biologicas-UJED, Av. Universidad s/n, Fracc. Filadelfia, Gomez Palacio 35010, Dgo., Moxico (JS)

* Correspondent: enrique_jurado@hotmail.com
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Author:Muro-Perez, Gisela; Jurado, Enrique; Flores, Joel; Sanchez-Salas, Jaime
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1USA
Date:Sep 1, 2014
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