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Serotiny and seed germination in three threatened species of Mammillaria (Cactaceae)
ARTICLE IN PRESS Basic and Applied Ecology 7 (2006) 533—544
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Serotiny and seed germination in three threatened species of Mammillaria (Cactaceae) Ce ´sar Rodrı´guez-Ortegaa, Miguel Francob,, Maria C. Mandujanoa a
Laboratorio de Dina´mica de Poblaciones y Evolucio ´n de Historias de Vida, Departamento de Ecologı´a de la Biodiversidad, Instituto de Ecologı´a, Universidad Nacional Auto ´noma de Me ´xico, Apartado Postal 70-275, 04510 Me´xico, D.F. Me ´xico b Terrestrial Ecology Research Group, School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth, Devon, PL4 8AA, UK Received 21 November 2004; accepted 23 November 2005
KEYWORDS Habitat harshness; Photoblastism; Tehuacan-Cuicatlan; Unpredictable environment; Variable environment
Summary Individuals of some species of Mammillaria (Cactaceae) store some seeds on the plant over periods exceeding 1 year (serotiny). We examined the phenomenon of serotiny and germination behaviour of three rare and endangered Mammillaria species that occur in central Mexico. The species with the highest seed retention was Mammillaria solisioides, whose individuals kept on average 24% of their total seed crop throughout their observable lifetime. Individuals of Mammillaria napina and Mammillaria hernandezii did not differ in their degree of seed retention (about 5%). In M. solisioides and M. hernandezii, seed germination declined significantly with seed age, whereas in M. napina germination increased slightly. In all three species, over 70% of retained seeds were still alive after 8 years. Increasing fractions of dormant seeds were observed with seed age in M. solisioides and M. hernandezii, whereas in M. napina this fraction followed the opposite trend. All three species showed strict light dependence for germination. Serotiny was positively correlated with the harshness of the environment when species and populations were assumed independent. However, these correlations were not significant at the 5% level when the degree of relatedness of species and populations was taken into account using phylogenetically independent constrasts. We hypothesise that serotiny in these species represents a mechanism by which they can cope with a harsh, unpredictable environment. To our knowledge, this is the first assessment of serotiny in cacti. ¨ kologie. Published by Elsevier GmbH. All rights reserved. & 2006 Gesellschaft fu ¨r O
Corresponding author. Tel.: +44 1752 232796; fax: +44 1752 232970.
E-mail address: [email protected] (M. Franco). ¨ kologie. Published by Elsevier GmbH. All rights reserved. 1439-1791/$ - see front matter & 2006 Gesellschaft fu ¨r O doi:10.1016/j.baae.2006.04.001
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Zusammenfassung Individuen einiger Arten der Mammilaria (Cactaceae) speichern einige Samen u ¨ber einen Zeitraum von mehr als einem Jahr auf der Pflanze (serotiny). Wir untersuchten das Pha ¨nomen serotiny und das Keimverhalten von drei seltenen und gefa ¨hrdeten ’’ Mammilaria Arten, die in Zentralmexiko vorkommen. Die Art, die am meisten Samen zuru ¨ckbeha ¨lt, war Mammillaria solisioides, die bis zu 24% der gesamten Samenproduktion u ¨ber die beobachtbare Lebenszeit zuru ¨ckbehielt. Die Individuen von Mammillaria napina und Mammillaria hernandezii unterschieden sich nicht im Grad der Samenzuru ¨ckbehaltung (circa 5%): Bei M. solisioides und M. hernandezii nahm die Samenkeimung signifikant mit dem Samenalter ab, wa ¨hrend bei M. napina die Keimung geringfu ¨gig zunahm. Bei allen drei Arten waren mehr als 70% der Samen nach acht Jahren immer noch lebendig. Es wurden zunehmende Anteile von ruhenden Samen mit zunehmenden Samenalter bei M. solisioides und M. hernandezii beobachtet, wa ¨hrend bei M. napina dieser Anteil dem gegenla ¨ufigen Trend folgte. Alle drei Arten zeigten eine strikte Lichtabha ¨ngigkeit fu ¨r die Keimung. Die serotiny’’ war positiv mit der Ha ¨rte der Umwelt korreliert, wenn Arten und ’’ Populationen unabha ¨ngig voneinander betrachtet wurden. Diese Korrelationen waren jedoch auf dem 5% Level nicht signifikant, wenn der Verwandtschaftsgrad der Arten und Populationen mit beru ¨cksichtigt wurde, indem phylogenetisch unabha ¨ngige Kontraste benutzt wurden. Wir stellen die Hypothese auf, dass serotiny’’ bei diesen Arten einen Mechanismus darstellt, durch den sie mit einem ’’ harten, unvorhersagbaren Lebensraum zurechtkommen ko ¨nnen. Nach unserem Wissen ist dies die erste Einscha ¨tzung von serotiny’’ bei Kakteen. ’’ ¨ kologie. Published & 2006 Gesellschaft fu ¨r O by Elsevier GmbH. All rights reserved. ’’
Introduction Serotiny, the accumulation and persistence of consecutive seed crops by a plant for more than 1 year, is an important mechanism that allows plants to persist in harsh and unpredictable environments (Lamont, 1991; Enright, Marsula, Lamont, & Wissel, 1998a; Lamont & Enright, 2000). These seed banks constitute the next generation for populations of several plant species in a variety of habitats, including sclerophyll scrublands of Australia and South Africa (Cowling & Lamont, 1985; Enright & Lamont, 1989; Enright et al., 1998a), the arid deserts of Namibia and India (Gu ¨nster, 1992, 1994; Narita, 1998) and coniferous forests of North America and Europe (Perry & Lotan, 1979; McMaster & Zedler, 1981; Gauthier, Bergeron, & Simon 1996). The phenomenon has been described for at least eight plant families, including Pinaceae (McMaster & Zedler, 1981; Gauthier et al., 1996; Habrouk, Retama, & Espelta, 1999), Cupressaceae (Vogl, Armstrong, White, & Cole, 1977, cited in Lamont, 1991), Myrtaceae (Lamont, le Maitre, Cowling, & Enright, 1991), Proteaceae (Cowling & Lamont, 1985; Enright, Lamont, & Marsula, 1996; Enright et al., 1998a; Enright, Marsula, Lamont, & Wissel, 1998b; Brown & Whelan, 1999), Acanthaceae (Gu ¨nster, 1994; Narita, 1998) and Asteraceae (Gu ¨nster, 1992). Lamont (1991) estimates that 1200 species in 40 genera of woody plants are serotinous.
In some species, this phenomenon is thought to be an adaptation to successfully recruit seedlings in fire-prone environments (Givnish, 1981; Muir & Lotan, 1985; Enright et al., 1996; Habrouk et al., 1999). Obligate pyriscent species (sensu Lamont, 1991) disperse their seeds after fire, when conditions for germination and recruitment improve. This is because the intensity of competition for light, moisture and nutrients decreases after fire has killed a substantial amount of dominant, vigorous plants. Indeed, interfire established individuals must compete with neighbours, which decreases their probability to survive, grow and accumulate seeds ready to germinate when the next fire occurs (McMaster & Zedler, 1981; Cowling & Lamont, 1987). Although fire has been considered the main trigger for seed dispersal in serotinous species, other mechanisms such as branch death, whole plant death, solar radiation and variation in moisture may promote seed release in many species (Cowling & Lamont, 1985; Enright & Lamont, 1989; Lamont, 1991). In desert plants, for example, rainfall could be the principal factor promoting the release of seeds (Gu ¨nster, 1992, 1994). It has been suggested that serotiny in desert plants could be promoted by spatial and temporal variation in water availability (Evenari, Shanan, & Tadmor, 1982). This kind of persistent seed bank (sensu Thompson & Grime, 1979, but see also Baskin & Baskin,
ARTICLE IN PRESS Seed germination in serotinous cacti 1998, p. 133) has been associated with habitats where the environmental or disturbance regimes are unpredictable and seedling recruitment is low or variable (Parker, Simpson, & Leck, 1989). Unpredictable environments can promote the evolution of life history traits that reduce temporal variance in fitness, such as delayed dispersal and germination, which reduces mean fitness (Venable & Lawlor, 1980; Venable, 1985; Stearns, 1992; Philippi, 1993a; Hopper, 1999). Both theoretical and empirical studies suggest that populations subject to environmental variability can diversify their germination behaviour, spreading germination through time by means of innate dormancy (Cohen, 1966; Venable & Lawlor, 1980; Venable, 1985; Pake & Venable, 1996; Mandujano, Golubov, & Montan ˜a, 1997). Clearly, serotinous plants must produce longlived seeds that survive until favourable conditions occur. Seed longevity changes across plant families and species: for example, 13-year-old seeds of Pinus torreyana showed a 20% germination rate (McMaster & Zedler, 1981), while in 25-year-old seeds of Pinus banksiana germination rate was 50% (Cayford & McRae, 1982 in Lamont, 1991). In the case of serotinous Proteaceae, 10-year-old seeds of Banksia baxteri retained 100% germination ability (King unpublished, cited in Lamont et al., 1991), while in B. tricuspis germination rates decreased to 18% in seeds 15 years of age (Lamont & van Leeuwen, 1988). In this paper, we report on the germination characteristics of three cactus species that exhibit the phenomenon of serotiny and discuss the possible importance of this phenomenon to the species studied. The phenomenon of seed retention occurs in several species of Mammillaria. We have found that ten out of 184 species mature their fruits while these sink into the stems over time. These species belong to the series Longiflorae and Lasiacanthae (sensu Hunt, 1987) (Rodrı´guez-Ortega & Franco, 2001) and are exclusively distributed in arid and semi-arid deserts of Mexico. While the internal development of the fruits in this genus has been known for some time (e.g. it has been mentioned by Bravo-Hollis & Sa ´nchez-Mejorada, 1991) and has also been reported recently for Mammillaria crucigera (Contreras & Valverde, 2002), this is the first time that the ecological significance of serotiny is explored in cacti. We were specifically interested in three questions: (i) are seed retention time (or ‘seed age’) and seed survival (viability) correlated in these species, (ii) how do the germination characteristics of their seeds change with seed age, and (iii) is climatic uncertainty in natural populations correlated with different levels of serotiny?
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Materials and methods Study site and species Plant material was collected from wild populations of the three species at the TehuacanCuicatlan Valley Biosphere Reserve (Fig. 1), located between the states of Puebla and Oaxaca in Mexico, 200 km south-east of Mexico City (171480 to 181580 N and 971030 to 971430 W). The vegetation in the reserve includes areas dominated by columnar cacti, shrublands and grasslands with different floristic composition (Jaramillo-Luque & Gonza ´lez-Medrano, 1983). Mean annual precipitation is 380 mm concentrated during the summer season with a mean annual temperature of 21.2 1C (Garcı´a, 1973; Jaramillo-Luque & Gonza ´lez-Medrano, 1983). Mammillaria solisioides Backeberg, Mammillaria napina Purpus and Mammillaria hernandezii Glass
Figure 1. Location of the Tehuacan-Cuicatlan Valley Biosphere Reserve in Mexico and detailed map showing the study sites (adapted from Jaramillo-Luque & Gonzalez-Medrano, 1983). Diamonds correspond to populations of M. solisioides (La Virgen, 1, and Petlalcingo, 2), square to the M. napina population (Azumbilla, 3) and triangles to the M. hernandezii populations (Loma de la Estrella, 4, and La Pedrera, 5).
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Degree of serotiny among species, populations and years
Figure 2. Diagrammatic representation of a longitudinal section of the stem of a serotinous Mammillaria cactus. Fruits from individual (annual) reproductive events are distributed in a ring at the same height in the plant. Shoots (tubercles or mammillae) produced during the growing season occur between two consecutive reproductive events. In two of the species (M. hernandezii and M. solisioides) the underground stem (i.e., excluding roots) becomes compressed as it ages and dries out, and rarely exceeds 4 cm. In M. napina, however, the underground stem may exceed 10 cm.
et Foster are three small species of globose cacti (plant diameter o6 cm in all species) endemic to the Tehuacan-Cuicatlan Valley Biosphere Reserve. These species are listed in the IUCN Red List as rare (M. hernandezii) and vulnerable (M. solisioides and M. napina) (Oldfield, 1997) and are protected by Mexican law. They occur in only a few isolated localities. These species grow in open spaces and barely rise above the ground. They produce their first flowers when still small (o2 cm in diameter). After pollination, fruits mature partially sunken into the stem. After abundant rain, the plant swells and recently produced fruits become partially exposed among the spines, thus increasing the chance of seed dispersal (C. Rodrı´guez-Ortega, unpublished). If no dispersal occurs, intact dry fruits or naked seeds (resulting from decay of the pericarp) remain embedded within the tubercles. As the plant grows, the newly developed tubercles displace older ones, forcing them to move lower down the stem. After a few reproductive seasons, and as the stem dries out and shrinks, intact fruits and/or naked seeds embedded within the plant are buried below ground (Fig. 2). These embedded seeds are released when the plant dies and rots away or when herbivores, such as hares and rodents, feed on whole plants (C. Rodrı´guez-Ortega, personal observations).
A total of 46 reproductive individuals from two populations of M. solisioides and 43 reproductive individuals from two populations of M. hernandezii were collected in December 1999. These populations are La Virgen (Oaxaca state) and Petlalcingo (Puebla state) for M. solisioides, and Loma de la Estrella and La Pedrera (both in Oaxaca) for M. hernandezii. For M. napina, 42 reproductive individuals were collected from one population in Azumbilla (Puebla) in May 2000. Sample sizes were constrained by the collecting permit issued by the Mexican authorities, which amounted to 50 for each species, and the reproductive history of the individuals collected; for example, a few individuals reproduced for the first time in the year of collection, which was only revealed after digging them out. In the laboratory, each plant was examined for the number of fruits (empty or with seeds), their condition (intact or fragmented) and their number of seeds. The age of fruits/seeds could be determined accurately because flowers are produced in a ring below the apical zone of the plant and are always separated from the fruits of the previous reproductive season by the shoots (tubercles or ‘mammillae’) produced during the growing season. Although some plants do not produce fruits each year, their fairly constant rate of growth allows estimation of the number of years between reproductive events. Thus, once the most recent reproductive event was identified, seed age could be accurately determined. Seeds were stored in the laboratory at room temperature for 6 months, after which germination tests were conducted.
Dynamics of mature fruits during their first year after production We studied the dynamics of newly produced fruits by calculating their annual probability of (i) remaining intact with all their seeds, (ii) fragmenting and releasing all their seeds, or (iii) fragmenting and retaining one or more seeds. The fruits employed in this analysis were those produced in the previous fruiting season, i.e., 1998 for M. solisioides and M. hernandezii, and 1999 for M. napina.
Germination, viability and photoblastism In order to investigate how germination and viability of seeds change with age, we conducted germination and viability tests employing the seeds collected from the 131 individuals described above.
ARTICLE IN PRESS Seed germination in serotinous cacti Because some ages were represented by few seeds, six seed ages for M. solisioides (2–7 years old), seven for M. hernandezii (2–8 years old) and eight for M. napina (1–8 years old) were tested. Also, because the numbers of seeds obtained for different ages were unequal, particularly for older ages, it was not possible to design an experiment with replicated treatments (seed ages). Instead, we employed a randomised design. A total of 60 randomly selected seeds were sown for those seed ages with a large sample size, whereas for seed ages with smaller sample size all seeds were used. Seeds were randomly sown in Petri dishes containing seeds of individual species. The age and position of each seed in the experiment was recorded. A maximum of 70 seeds was sown per Petri dish in 1% agar. To prevent fungal attack, seeds were disinfected in 5% sodium hypochlorite solution for 5 min and washed in distilled water. Dishes were incubated in a germination chamber at 25 1C with a 12 h day1 photoperiod. Germination (radicle appearance) was recorded daily for 31 d. At the end of the experiment, ungerminated seeds were examined to verify whether they were alive by dissecting them under a stereomicroscope. In dead seeds, endosperm and embryo dry out and only the testa remains, whereas in live seeds the endosperm and embryo completely fill the seed. Embryos were too small and the testa too hard to allow exposure of the embryo without damaging it. This prevented the use of a tetrazolium-chloride test. The possible photoblastic response of seeds was tested employing two levels of light, full light and darkness, on recently produced seeds. Four replicates of 25 seeds per treatment (each combination of species by light) were sown in 1% agar in Petri dishes. The darkness treatment was provided by wrapping the Petri dishes in two layers of aluminium foil. M. solisioides and M. hernandezii seeds used in this experiment were collected in 2001 in the same wild populations mentioned above. Seeds of M. napina could not be collected in 2001 because we missed fruit production in this species that year. Instead, we used seeds produced in 2000. Seeds in this experiment were disinfected in 5% sodium hypochlorite solution for 5 min and washed in distilled water. Dishes were incubated in a germination chamber at constant temperature (25 1C) with a 12 h day1 photoperiod. Germination was recorded after 30 d.
Serotiny and environment In order to investigate whether climatic variability was related to serotiny in these species,
537 meteorological information for the studied populations was obtained from the Mexican Meteorological Service (National Water Commission, Mexico). Monthly temperature, rainfall and evaporation data were obtained from four stations. These stations were the closest to the five populations studied. The stations (plus the number of years for which records existed) and the species and populations to which climatic records were associated (plus the approximate distance between stations and populations) were: (i) Tepelmeme, Oaxaca state (14 years): M. hernandezii, at La Estrella (10 km) and La Pedrera (6.7 km); (ii) Huajuapan de Leo ´n, Oaxaca (24 years): M. solisioides at La Virgen (2 km); (iii) Acatla ´n de Osorio, Puebla (10 years): M. solisioides at Petlalcingo (18 km); (iv) Chapulco, Puebla (22 years): M. napina at Azumbilla (7.5 km). Missing data were substituted by averages for the corresponding months calculated from the remaining years. Seven percent of monthly records in all three variables were missing in stations associated with M. solisioides, 13% in those for M. napina and 2% in those for M. hernandezii.
Data analyses Degree of serotiny among species, populations and years: The retained seed fraction per plant per observable reproductive lifespan (R, also referred to as the degree of serotiny or seed retention) was calculated as R¼
Sretained , Stotal
where Sretained is the observed number of retained seeds in all the fruits embedded in a plant and Stotal is the expected original number of seeds in those fruits. The latter is the product of the observed number of fruits on the plant (Ftotal) and the average number of seeds per fruit found in the 1999 fruit crop (S1999): Stotal ¼ S1999 F total . Average seed number per fruit in 1999 was obtained from the same populations where the plants/fruits were collected. The use of the average number of seeds per fruit in 1999 was appropriate because only in 1 year (2000) did individuals in one population each of M. solisioides and M. hernandezii exhibited a significantly lower number of seeds per fruit (23% and 36% lower than in 1999, respectively). This difference was tested with a generalised linear model adjusted for overdispersion (see below). Thus, for M. solisioides: F 2;169 ¼ 7:4, Po0:01; for M. hernandezii: F 2;70 ¼ 3:7, Po0:05. The fraction of seeds retained
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per plant per year (Pyear) was calculated as P year ¼
Sretained year , Stotal year
where Sretained year is the number of seeds in a particular year and Stotal year is the estimated number of seeds produced by this plant in the same year. That is, Stotal year is the product of the observed number of retained fruits in a particular year and the average number of seeds per fruit found in the 1999 fruit crop (S1999). To test for differences in degree of serotiny among species, populations and years, we used a generalised linear model (GLM) assuming a proportional response variable (fraction of retained seeds) with a logit link function (Crawley, 1993). In all cases, it was necessary to adjust the w2 statistic to account for overdispersion employing a corrected F test (Crawley, 1993). Germination, viability and photoblastism: We tested for differences in germination and viability among seeds of different ages in all three species. For each dependent variable, we used a GLM with a binary response (germination vs. no germination and live vs. dead seeds, respectively) with a logit link function (Crawley, 1993). In the case of viability, seeds were considered alive when they germinated in germination experiments or when deemed viable (i.e., full) after dissection. In the case of M. napina, it was necessary to adjust the w2 statistic to account for overdispersion in the germination data analysis (Crawley, 1993). Differences in germination between light and dark treatments were also tested using a GLM with a proportional response variable (fraction of germinated seeds) and a logit link function (Crawley, 1993). Serotiny and environment: The degree of serotiny of the five populations was correlated with indirect measures of potential productivity (or its inverse, the harshness of the environment) and measures of environmental variability. A population-level degree of serotiny (Rpopulation) was calculated as the average of the individual R values in each population. Using monthly data, we calculated the mean annual temperature and total annual rainfall and evaporation for the years for which information was available at each station. Annual water deficit was estimated as the difference between mean annual rainfall and mean annual evaporation. The coefficients of variation (CV) of mean annual temperature, total annual rainfall and mean annual evaporation were employed as indices of climatic variability and, therefore, environmental unpredictability.
Two types of analyses were performed. First, assuming taxonomic independence of species and populations, these were treated as independent points (TIPs analyses sensu Silvertown & Dodd, 1996). Because there was only one meteorological station (Tepelmeme) for the two populations of M. hernandezii, its Rpopulation value was calculated as the average of the two populations. This reduced sample size to four populations or points. Second, the phylogenetic differentiation among species and populations was incorporated in an analysis of phylogenetically independent contrasts (PICs sensu Silvertown & Dodd, 1996). The classification employed was that of Hunt (1987) where M. napina and M. hernandezii belong to the series Longiflorae and M. solisioides belongs to the series Lasiacanthae. Populations of the same species were also treated as bifurcating. This produced a 4-tip, completely resolved tree with three contrasts. PIC analyses were conducted with the programme CAIC (Purvis & Rambaut, 1995) with all variables log transformed and assuming constant branch lengths. As is standard with this method, the resulting contrasts were regressed through the origin and the significance of each relationship was tested.
Results Degree of serotiny among species, populations and years There were significant differences in degree of serotiny (R values) among the three Mammillaria species (GLM adjusted for overdispersion: F 2;112 ¼ 29:1, Po0:001). M. solisioides was the most serotinous species, storing on average 24.1% (S.E. ¼ 0.9, n ¼ 32) of its reproductive output. This was between four and five times the percentage of seeds stored by either M. napina or M. hernandezii. The difference between M. napina (6.5%, S.E. ¼ 1.5, n ¼ 40) and M. hernandezii (4.5%, S.E. ¼ 4.0, n ¼ 43) was not significant at the 5% level (GLM F 1;81 ¼ 3, P ¼ 0:09). In addition, important intraspecific variation in R values was observed among species. While many plants of M. solisioides successively released all their seeds, others plants retained up to 80% of the total produced. In M. napina and M. hernandezii this percentage ranged from 0% to 39% and from 0% to 25%, respectively. Interpopulation differences in seed retention were not statistically significant in M. solisioides (GLM F 1;30 ¼ 0:7, P ¼ 0:42) and M. hernandezii (GLM F 1;41 ¼ 0:6, P ¼ 0:46)–for M. napina we only had information from one
ARTICLE IN PRESS Seed germination in serotinous cacti
539 Table 1. Results of generalised linear models of seed germination and seed viability versus seed age in three Mammillaria species Source of variation Seed M. M. M. Seed M. M. M.
Figure 3. Fraction of seeds retained (Pyear averages, 7S.E.) by three Mammillaria species in eight consecutive years. Data were collected in 2000 before M. solisioides and M. hernandezii reproduced. In 1994 M. solisioides had too few fruits/seeds to allow calculation of these figures. The same was true for M. solisioides and M. hernandezii in 1993.
population. No significant differences were found in seed retention (Pyear) among 11 years examined in M. napina (GLM F 10;129 ¼ 0:8, P ¼ 0:65) and 7 years in M. hernandezii (GLM F 6;160 ¼ 1:2, P ¼ 0:31) (Fig. 3). However, significant differences were found among 7 years in M. solisioides (GLM F 6;85 ¼ 2:3, P ¼ 0:04; Fig. 3).
Dynamics of mature fruits during their first year after production The probability of remaining closed for 1 year after production was low for fruits of all species (M. solisioides ¼ 0.06, M. napina ¼ 0, M. hernandezii ¼ 0.02). However, the probability of seed retention (Xone seed) considering both closed and open fruits was X0.24 in all three species (0.64, 0.25 and 0.24, respectively), hence, the highest proportion of fruits loosing all their seeds within 1 year of production was found in M. napina and M. hernandezii (0.75 and 0.74, respectively), whereas in M. solisioides this was 0.3.
Germination, viability and photoblastism There was a statistically significant correlation between seed germination and seed age in all three species and between seed viability and seed age in two of the three species (Table 1). In M. solisioides, germination of 7-year-old seeds was one-fourth that of 2-year-old seeds (0.1 vs. 0.4; Fig. 4A). The fraction of live seeds was not significantly affected
germination solisioides napina hernandezii viability solisioides napina hernandezii
df
w2 or F
P
5 7, 325 6
19.1 3.0 58.0
0.002 0.004 o0.001
5 7 6
6.3 62.2 14.7
NS o0.001 0.02
Due to overdispersion of the germination data in M. napina, a corrected F test was necessary to assess the significance of the models (Crawley 1993). NS ¼ non-significant differences.
by seed age and over 70% of seeds were still alive after 8 years (Fig. 4B). M. hernandezii germination and seed viability were negatively correlated with seed age. Its germination decreased from 0.9 in 2-year-old seeds to 0.38 in 8-year-old seeds, while its seed viability decreased from 0.96 in 2-year-old seeds to 0.8 in 8-year-old seeds. In the case of M. napina, the fitted model indicated that germination actually increased with seed age, from 0.55 in 1-year-old seeds to 0.68 in 8-year-old ones. This was affected by a small decline in the fraction of viable seeds, from 0.82 in 1-year-old seeds to 0.71 in 8-year-old ones (Fig. 4B). The dormant seed fraction (calculated from the fitted models as the difference between surviving seed fraction and germinated seed fraction) for both M. solisioides and M. hernandezii increased with seed age, while that of M. napina decreased (Fig. 4C). Seeds did not germinate in the dark (all species). Germination rates under light were 87% (S.D. ¼ 9.5%) for M. hernandezii, 24% (S.D. ¼ 15%) for M. napina and 23% (S.D. ¼ 13.2%) for M. solisioides. Thus, seeds of all three species are positively photoblastic.
Serotiny and environment The TIPs relationships between environmental variables and degree of serotiny in the studied populations are shown in Fig. 5. Serotiny (Rpopulation) showed a positive trend with mean annual temperature (Fig. 5A) and this relationship was significant in the TIPs analysis (r TIP ¼ 0:96; the critical value for all TIP correlations shown in Fig. 5 is r TIP½0:05 ¼ 0:95), but not in PICs (r PIC ¼ 0:91; PICs critical value is r PIC½0:05 ¼ 0:997). The highest mean annual temperatures were recorded in
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C. Rodrı´guez-Ortega et al. solisioides (Fig. 5C; r TIP ¼ 0:98, rPIC ¼ 0:88), while annual water deficit was higher in M. solisioides (about 1580 mm) than in populations of M. napina (1200 mm) and M. hernandezii (1170 mm) (Fig. 5D; r TIP ¼ 0:97, r PIC ¼ 0:89). M. hernandezii populations were subjected to the highest variability in temperature between years, followed by M. napina and M. solisioides populations (Fig. 5E; r TIP ¼ 0:88, r PIC ¼ 0:74). M. napina had the highest among-year variability in annual rainfall, followed by M. hernandezii and M. solisioides populations (Fig. 5F; r TIP ¼ 0:90, rPIC ¼ 0:94).
Discussion The phenomenon of serotiny in cacti
Figure 4. Fitted regression models of the fraction of (A) germinated seeds, and (B) viable seeds versus seed age in three Mammillaria species. The fraction of dormant seeds (C) is the difference between the curves fitted in (B) and (A).
M. solisioides populations (about 7 and 9 1C above those found for M. napina and M. hernandezii populations, respectively). Annual rainfall was highest for M. solisioides populations (about 280 and 140 mm more than for M. napina and M. hernandezii populations, respectively), but this relationship was not significant for either TIPs or PICs (Fig. 5B; rTIP ¼ 0:82, r PIC ¼ 0:56). Mean annual evaporation was lower in populations of M. napina and M. hernandezii than in populations of M.
As far as we are aware, this is the first study to describe the ecological features and seed germination responses of serotinous cacti. In Cactaceae, this phenomenon has only been found in ten species of Mammillaria (Rodrı´guez-Ortega & Franco, 2001). Other species of cacti can retain a few seeds on external structures such a spines and apical wool. However, it is not known whether they retain significant amounts of seeds for long periods of time and, more importantly, whether this retention is a regular and significant feature of their life history, as seems to be the case in the Mammillaria species. Some differences between the cacti studied here and other serotinous species exist. First, the release of seeds X2 years old in Mammillaria seems to be triggered by death of whole plants (necriscence, sensu Lamont, 1991) instead of fire (pyriscence) or moisture (hygriscence), which have been described as the most common mechanisms in serotinous species. Second, at first sight our results suggest that these Mammillaria species are only weakly serotinous. Mean annual seed accumulation per plant in the most serotinous species (M. solisioides) did not exceed 35% of seed production in all study years, while in the other two species the respective values were close to 15%. These values are low when compared with those of, for example, pyriscent species such as Banksia (Proteaceae) or Pinus (Pinaceae) whose retention fractions per reproductive season range between 60% and 100% (McMaster & Zedler, 1981; Cowling & Lamont, 1985). Although Banksia and Pinus plants store a higher proportion of their seed crop than do mammillarian cacti, subsequent spontaneous follicle rupture, granivory and seed decay can substantially reduce the number of viable seeds. In
ARTICLE IN PRESS Seed germination in serotinous cacti
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Figure 5. Relationships between degree of serotiny (Rpopulation) and both mean annual climatic variables (A, temperature; B, rainfall; C, evaporation; D, water deficit) and their variability among years (E, CV of temperature; F, CV of rainfall) in populations of three Mammillaria species. Diamonds correspond to populations of M. solisioides (Petlalcingo being the most serotinous of them), squares to the M. napina population (Azumbilla) and triangles to the average of the M. hernandezii populations.
Banksia hookeriana for example, 50% of seed accumulation may be lost after 10 years (Enright et al., 1996), whereas in P. torreyana only about 5% of total seeds remain in the mother plants after 15 years (McMaster & Zedler, 1981). In contrast, Mammillaria’s sunken fruits prevent seed dispersal and seeds are protected against seed predators because fruits are relatively quickly buried underground. Our field observations suggest that a very small fraction of seeds is damaged after they have been buried in the underground stem. Thus, the most important factor affecting survival of buried seeds in Mammillaria species is seed decay. In consequence, the proportion of the lifetime seed crop retained by Mammillaria species may not be all that different from that of other serotinous species. We are currently evaluating the contribution that this phenomenon may make to population growth rate, as opposed to that of recruitment from current seed production.
Interspecific variation in degree of serotiny Variation in the degree of serotiny was found among the three Mammillaria species. In general, individuals of M. solisioides retain more seeds in each reproductive season and over their lifespan than M. napina and M. hernandezii. Variation in the degree of seed retention has also been shown, for example, in Banksia species (Enright et al., 1998a, b; Lamont & Enright, 2000). In the case of desert species, the evolution of serotiny might be promoted by spatial and temporal variation in water availability (Ellner & Shmida, 1981), constraining seedling recruitment to years when particular favourable conditions occur. It has been suggested that, in order to spread the risk of reproductive failure, delayed germination of desert ephemeral species is an adaptive trait in this environment (Cohen, 1966; Venable & Lawlor, 1980; Venable & Brown, 1988). Spreading the
ARTICLE IN PRESS 542 germination of seeds over time allows exploration of varying environmental conditions from year to year. Death of a small fraction of the seed crop would be compensated by future success of dormant seeds. The result is a bet-hedging strategy in which phenotypes with delayed germination would be favoured over phenotypes with rapid germination (Philippi & Seger, 1989). Although a similar argument has been raised for the presence of dormant seeds in perennial desert plants (e.g. Mandujano et al., 1997; Bowers, 2000; RojasAre´chiga & Va ´zquez-Yanes, 2000), the correlated evolution of traits in the established (vegetative plant) and regenerative (e.g., seed) phases of the life cycle produces a more complex scenario for selection of seed dormancy (Rees, 1994). Thus, although our results suggest a positive correlation between serotiny and harshness of the environment (some of the TIPs analyses in Fig. 5), our small species sample did not provide significant trends employing phylogenetically independent contrasts. Thus, our results (which are based on only four populations/three species) must await confirmation from more detailed demographic analyses.
Intraspecific variation in degree of serotiny Important intraspecific variation in the degree of seed retention was found in all three Mammillaria species. Similar variation has been found in other serotinous species, including pines (Muir & Lotan, 1985; Gauthier et al., 1996). These authors have pointed out that spatial and temporal variability in environmental conditions, such as intensity, frequency and spatial distribution of disturbance, could promote phenotypic variation in the degree of serotiny (McMaster & Zedler, 1981; Cowling & Lamont, 1985; Lamont et al., 1991; see also Mathias & Kisdi, 2002). Although germination fractions seem to be low after 8 years in two species (M. solisioides and M. napina), their viability points to long-lived seeds. Seventy-per cent of retained seeds in all three Mammillaria species were still alive after 8 years. Indeed, longlived seeds may not be uncommon in the Cactaceae (Mandujano et al., 1997; Rojas-Are ´chiga & Va ´zquezYanes, 2000).
Dormant seed fractions and photoblastism One interesting result concerning serotiny in Mammillaria seeds refers to the size of the dormant fraction as seeds age. These fractions increased in M. solisioides and M. hernandezii, but decreased in M. napina (Fig. 5C). Dormant seeds have been
C. Rodrı´guez-Ortega et al. reported in several species of desert ephemerals, for which germination could be prolonged over a period of 2 years, even when conditions for germination were favourable each year (Philippi, 1993a). Both theoretical and empirical work suggest that (monocarpic) populations subject to high environmental variability produce higher fractions of dormant seeds than populations inhabiting places with more stable or favourable environmental conditions (Cohen, 1966; Venable & Lawlor, 1980; Venable & Brown, 1988; Philippi, 1993b; Pake & Venable, 1996). Of interest here is that larger dormant fractions were found in M. solisioides (the most serotinous species), whose seeds also exhibited the highest survival fraction after 8 years. In contrast, species with lower seed retention had smaller dormant fractions. Positive photoblastism has been suggested to be an important mechanism to build persistent seed banks in many species (Pons, 1992). For example, seeds of Ferocactus wislizeni, which develops persistent soil seed banks in the Sonoran Desert, did not germinate when incubated in the dark (Bowers, 2000). The same occurred in the three Mammillaria species studied here. The ecological significance of photoblastic seeds in species with persistent seed banks seems clear. In the case of serotinous Mammillaria, the germination of seeds buried in the soil would lead to the death of the seedlings if they were not able to reach the ground surface. Because growth rates in the Cactaceae are low, particularly in the early stages of the life cycle (Nobel, 1988), growth alone would limit the recruitment success of buried seeds. Seeds would therefore only be exposed after being dispersed by herbivores (endozoochory) or after disintegration of the plant after death.
Conclusions The correlative evidence of retention, germination, viability and dormancy of seeds in these three species of Mammillaria suggests that serotiny is not a fortuitous attribute, but one that may confer some advantage under the harsh environments where they live. Although these attributes would seem to allow the plants to spread the risk of reproductive failure in both time and space, adequate quantification of their ecological and evolutionary significance is necessary before we can reject alternative hypotheses. All three species are rare and endangered and it is possible that their rarity is due to their inability to recruit successful offspring more often than they do. Presently, we
ARTICLE IN PRESS Seed germination in serotinous cacti are therefore conducting a detailed demographic study to assess the consequences of serotiny under different environmental scenarios. Coupling the information on seedling recruitment with an analysis of prevailing environmental conditions will allow us to appraise the demographic and evolutionary consequences of seed retention in these plants.
Acknowledgements The authors thank Teresa Valverde, Arturo Flores-Martı´nez and Jordan Golubov for guidance and support throughout the course of this study and useful criticism of earlier versions of the manuscript. We particularly thank Rube´n Pe ´rez-Ishiwara for his help with fieldwork and overall technical assistance. We also thank the anonymous reviewers and the editorial team of BAE whose suggestions greatly improved the quality of the presentation. This work was financed by grants IN205500 of DGAPA-UNAM to M.C.M. and M.F. and W031 of CONABIO to M.C.M. C.E.R.O. thanks CONACyT and DGEP-UNAM for a Ph.D. scholarship, and the Posgrado en Ciencias Biolo ´gicas (UNAM) for financial support to complete this work at the University of Plymouth. Permit to collect specimens (DOO 024152) was granted by the Ministry of the Environment, Natural Resources and Fisheries (SEMARNAP), Mexico.
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C. Rodrı´guez-Ortega et al. Philippi, T. (1993b). Bet-hedging germination of desert annuals: variation among populations and maternal effects in Lepidium lasiocarpum. The American Naturalist, 142, 488–507. Philippi, T., & Seger, J. (1989). Hedging one’s evolutionary bets, revisited. Trends in Ecology and Evolution, 4, 41–44. Pons, T. L. (1992). Seed responses to light. In M. Fenner (Ed.), Seeds: The ecology of regeneration in plant communities. England: Commonwealth Agricultural Bureau. Purvis, A., & Rambaut, A. (1995). Comparative analysis by independent contrasts (CAIC): An Apple Macintosh application for analysing comparative data. Computer Applications in the Biosciences, 11, 247–251. Rees, M. (1994). Delayed germination of seeds: A look at the effects of adult longevity, the timing of reproduction, and population age/stage structure. The American Naturalist, 144, 43–64. Rodrı´guez-Ortega, C., & Franco, M. (2001). La retencio ´n de semillas en el ge ´nero Mammillaria (Cactaceae). Cacta´ceas y Suculentas Mexicanas, 46, 63–67. Rojas-Are´chiga, M., & Va ´zquez-Yanes, C. (2000). Cactus seed germination: A review. Journal of Arid Environments, 44, 85–104. Silvertown, J., & Dodd, M. (1996). Comparing plants and connecting traits. Philosophical Transactions of the Royal Society of London B, 351, 1233–1239. Stearns, S. C. (1992). The Evolution of Life Histories. USA: Oxford University Press. Thompson, K., & Grime, J. P. (1979). Seasonal variation in the seed banks of herbaceous species in ten contrasting habitats. Journal of Ecology, 67, 893–921. Venable, D. L. (1985). The evolutionary ecology of seed heteromorphism. The American Naturalist, 126, 577–595. Venable, D. L., & Brown, J. S. (1988). The selective interaction of dispersal, dormancy, and seed size as adaptations for reducing risk in variable environments. The American Naturalist, 131, 360–384. Venable, D. L., & Lawlor, L. (1980). Delayed germination and dispersal in desert annuals: Escape in space and time. Oecologia, 46, 272–282.
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Serotiny and seed germination in three threatened species of Mammillaria (Cactaceae) Ce ´sar Rodrı´guez-Ortegaa, Miguel Francob,, Maria C. Mandujanoa a
Laboratorio de Dina´mica de Poblaciones y Evolucio ´n de Historias de Vida, Departamento de Ecologı´a de la Biodiversidad, Instituto de Ecologı´a, Universidad Nacional Auto ´noma de Me ´xico, Apartado Postal 70-275, 04510 Me´xico, D.F. Me ´xico b Terrestrial Ecology Research Group, School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth, Devon, PL4 8AA, UK Received 21 November 2004; accepted 23 November 2005
KEYWORDS Habitat harshness; Photoblastism; Tehuacan-Cuicatlan; Unpredictable environment; Variable environment
Summary Individuals of some species of Mammillaria (Cactaceae) store some seeds on the plant over periods exceeding 1 year (serotiny). We examined the phenomenon of serotiny and germination behaviour of three rare and endangered Mammillaria species that occur in central Mexico. The species with the highest seed retention was Mammillaria solisioides, whose individuals kept on average 24% of their total seed crop throughout their observable lifetime. Individuals of Mammillaria napina and Mammillaria hernandezii did not differ in their degree of seed retention (about 5%). In M. solisioides and M. hernandezii, seed germination declined significantly with seed age, whereas in M. napina germination increased slightly. In all three species, over 70% of retained seeds were still alive after 8 years. Increasing fractions of dormant seeds were observed with seed age in M. solisioides and M. hernandezii, whereas in M. napina this fraction followed the opposite trend. All three species showed strict light dependence for germination. Serotiny was positively correlated with the harshness of the environment when species and populations were assumed independent. However, these correlations were not significant at the 5% level when the degree of relatedness of species and populations was taken into account using phylogenetically independent constrasts. We hypothesise that serotiny in these species represents a mechanism by which they can cope with a harsh, unpredictable environment. To our knowledge, this is the first assessment of serotiny in cacti. ¨ kologie. Published by Elsevier GmbH. All rights reserved. & 2006 Gesellschaft fu ¨r O
Corresponding author. Tel.: +44 1752 232796; fax: +44 1752 232970.
E-mail address: [email protected] (M. Franco). ¨ kologie. Published by Elsevier GmbH. All rights reserved. 1439-1791/$ - see front matter & 2006 Gesellschaft fu ¨r O doi:10.1016/j.baae.2006.04.001
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Zusammenfassung Individuen einiger Arten der Mammilaria (Cactaceae) speichern einige Samen u ¨ber einen Zeitraum von mehr als einem Jahr auf der Pflanze (serotiny). Wir untersuchten das Pha ¨nomen serotiny und das Keimverhalten von drei seltenen und gefa ¨hrdeten ’’ Mammilaria Arten, die in Zentralmexiko vorkommen. Die Art, die am meisten Samen zuru ¨ckbeha ¨lt, war Mammillaria solisioides, die bis zu 24% der gesamten Samenproduktion u ¨ber die beobachtbare Lebenszeit zuru ¨ckbehielt. Die Individuen von Mammillaria napina und Mammillaria hernandezii unterschieden sich nicht im Grad der Samenzuru ¨ckbehaltung (circa 5%): Bei M. solisioides und M. hernandezii nahm die Samenkeimung signifikant mit dem Samenalter ab, wa ¨hrend bei M. napina die Keimung geringfu ¨gig zunahm. Bei allen drei Arten waren mehr als 70% der Samen nach acht Jahren immer noch lebendig. Es wurden zunehmende Anteile von ruhenden Samen mit zunehmenden Samenalter bei M. solisioides und M. hernandezii beobachtet, wa ¨hrend bei M. napina dieser Anteil dem gegenla ¨ufigen Trend folgte. Alle drei Arten zeigten eine strikte Lichtabha ¨ngigkeit fu ¨r die Keimung. Die serotiny’’ war positiv mit der Ha ¨rte der Umwelt korreliert, wenn Arten und ’’ Populationen unabha ¨ngig voneinander betrachtet wurden. Diese Korrelationen waren jedoch auf dem 5% Level nicht signifikant, wenn der Verwandtschaftsgrad der Arten und Populationen mit beru ¨cksichtigt wurde, indem phylogenetisch unabha ¨ngige Kontraste benutzt wurden. Wir stellen die Hypothese auf, dass serotiny’’ bei diesen Arten einen Mechanismus darstellt, durch den sie mit einem ’’ harten, unvorhersagbaren Lebensraum zurechtkommen ko ¨nnen. Nach unserem Wissen ist dies die erste Einscha ¨tzung von serotiny’’ bei Kakteen. ’’ ¨ kologie. Published & 2006 Gesellschaft fu ¨r O by Elsevier GmbH. All rights reserved. ’’
Introduction Serotiny, the accumulation and persistence of consecutive seed crops by a plant for more than 1 year, is an important mechanism that allows plants to persist in harsh and unpredictable environments (Lamont, 1991; Enright, Marsula, Lamont, & Wissel, 1998a; Lamont & Enright, 2000). These seed banks constitute the next generation for populations of several plant species in a variety of habitats, including sclerophyll scrublands of Australia and South Africa (Cowling & Lamont, 1985; Enright & Lamont, 1989; Enright et al., 1998a), the arid deserts of Namibia and India (Gu ¨nster, 1992, 1994; Narita, 1998) and coniferous forests of North America and Europe (Perry & Lotan, 1979; McMaster & Zedler, 1981; Gauthier, Bergeron, & Simon 1996). The phenomenon has been described for at least eight plant families, including Pinaceae (McMaster & Zedler, 1981; Gauthier et al., 1996; Habrouk, Retama, & Espelta, 1999), Cupressaceae (Vogl, Armstrong, White, & Cole, 1977, cited in Lamont, 1991), Myrtaceae (Lamont, le Maitre, Cowling, & Enright, 1991), Proteaceae (Cowling & Lamont, 1985; Enright, Lamont, & Marsula, 1996; Enright et al., 1998a; Enright, Marsula, Lamont, & Wissel, 1998b; Brown & Whelan, 1999), Acanthaceae (Gu ¨nster, 1994; Narita, 1998) and Asteraceae (Gu ¨nster, 1992). Lamont (1991) estimates that 1200 species in 40 genera of woody plants are serotinous.
In some species, this phenomenon is thought to be an adaptation to successfully recruit seedlings in fire-prone environments (Givnish, 1981; Muir & Lotan, 1985; Enright et al., 1996; Habrouk et al., 1999). Obligate pyriscent species (sensu Lamont, 1991) disperse their seeds after fire, when conditions for germination and recruitment improve. This is because the intensity of competition for light, moisture and nutrients decreases after fire has killed a substantial amount of dominant, vigorous plants. Indeed, interfire established individuals must compete with neighbours, which decreases their probability to survive, grow and accumulate seeds ready to germinate when the next fire occurs (McMaster & Zedler, 1981; Cowling & Lamont, 1987). Although fire has been considered the main trigger for seed dispersal in serotinous species, other mechanisms such as branch death, whole plant death, solar radiation and variation in moisture may promote seed release in many species (Cowling & Lamont, 1985; Enright & Lamont, 1989; Lamont, 1991). In desert plants, for example, rainfall could be the principal factor promoting the release of seeds (Gu ¨nster, 1992, 1994). It has been suggested that serotiny in desert plants could be promoted by spatial and temporal variation in water availability (Evenari, Shanan, & Tadmor, 1982). This kind of persistent seed bank (sensu Thompson & Grime, 1979, but see also Baskin & Baskin,
ARTICLE IN PRESS Seed germination in serotinous cacti 1998, p. 133) has been associated with habitats where the environmental or disturbance regimes are unpredictable and seedling recruitment is low or variable (Parker, Simpson, & Leck, 1989). Unpredictable environments can promote the evolution of life history traits that reduce temporal variance in fitness, such as delayed dispersal and germination, which reduces mean fitness (Venable & Lawlor, 1980; Venable, 1985; Stearns, 1992; Philippi, 1993a; Hopper, 1999). Both theoretical and empirical studies suggest that populations subject to environmental variability can diversify their germination behaviour, spreading germination through time by means of innate dormancy (Cohen, 1966; Venable & Lawlor, 1980; Venable, 1985; Pake & Venable, 1996; Mandujano, Golubov, & Montan ˜a, 1997). Clearly, serotinous plants must produce longlived seeds that survive until favourable conditions occur. Seed longevity changes across plant families and species: for example, 13-year-old seeds of Pinus torreyana showed a 20% germination rate (McMaster & Zedler, 1981), while in 25-year-old seeds of Pinus banksiana germination rate was 50% (Cayford & McRae, 1982 in Lamont, 1991). In the case of serotinous Proteaceae, 10-year-old seeds of Banksia baxteri retained 100% germination ability (King unpublished, cited in Lamont et al., 1991), while in B. tricuspis germination rates decreased to 18% in seeds 15 years of age (Lamont & van Leeuwen, 1988). In this paper, we report on the germination characteristics of three cactus species that exhibit the phenomenon of serotiny and discuss the possible importance of this phenomenon to the species studied. The phenomenon of seed retention occurs in several species of Mammillaria. We have found that ten out of 184 species mature their fruits while these sink into the stems over time. These species belong to the series Longiflorae and Lasiacanthae (sensu Hunt, 1987) (Rodrı´guez-Ortega & Franco, 2001) and are exclusively distributed in arid and semi-arid deserts of Mexico. While the internal development of the fruits in this genus has been known for some time (e.g. it has been mentioned by Bravo-Hollis & Sa ´nchez-Mejorada, 1991) and has also been reported recently for Mammillaria crucigera (Contreras & Valverde, 2002), this is the first time that the ecological significance of serotiny is explored in cacti. We were specifically interested in three questions: (i) are seed retention time (or ‘seed age’) and seed survival (viability) correlated in these species, (ii) how do the germination characteristics of their seeds change with seed age, and (iii) is climatic uncertainty in natural populations correlated with different levels of serotiny?
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Materials and methods Study site and species Plant material was collected from wild populations of the three species at the TehuacanCuicatlan Valley Biosphere Reserve (Fig. 1), located between the states of Puebla and Oaxaca in Mexico, 200 km south-east of Mexico City (171480 to 181580 N and 971030 to 971430 W). The vegetation in the reserve includes areas dominated by columnar cacti, shrublands and grasslands with different floristic composition (Jaramillo-Luque & Gonza ´lez-Medrano, 1983). Mean annual precipitation is 380 mm concentrated during the summer season with a mean annual temperature of 21.2 1C (Garcı´a, 1973; Jaramillo-Luque & Gonza ´lez-Medrano, 1983). Mammillaria solisioides Backeberg, Mammillaria napina Purpus and Mammillaria hernandezii Glass
Figure 1. Location of the Tehuacan-Cuicatlan Valley Biosphere Reserve in Mexico and detailed map showing the study sites (adapted from Jaramillo-Luque & Gonzalez-Medrano, 1983). Diamonds correspond to populations of M. solisioides (La Virgen, 1, and Petlalcingo, 2), square to the M. napina population (Azumbilla, 3) and triangles to the M. hernandezii populations (Loma de la Estrella, 4, and La Pedrera, 5).
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Degree of serotiny among species, populations and years
Figure 2. Diagrammatic representation of a longitudinal section of the stem of a serotinous Mammillaria cactus. Fruits from individual (annual) reproductive events are distributed in a ring at the same height in the plant. Shoots (tubercles or mammillae) produced during the growing season occur between two consecutive reproductive events. In two of the species (M. hernandezii and M. solisioides) the underground stem (i.e., excluding roots) becomes compressed as it ages and dries out, and rarely exceeds 4 cm. In M. napina, however, the underground stem may exceed 10 cm.
et Foster are three small species of globose cacti (plant diameter o6 cm in all species) endemic to the Tehuacan-Cuicatlan Valley Biosphere Reserve. These species are listed in the IUCN Red List as rare (M. hernandezii) and vulnerable (M. solisioides and M. napina) (Oldfield, 1997) and are protected by Mexican law. They occur in only a few isolated localities. These species grow in open spaces and barely rise above the ground. They produce their first flowers when still small (o2 cm in diameter). After pollination, fruits mature partially sunken into the stem. After abundant rain, the plant swells and recently produced fruits become partially exposed among the spines, thus increasing the chance of seed dispersal (C. Rodrı´guez-Ortega, unpublished). If no dispersal occurs, intact dry fruits or naked seeds (resulting from decay of the pericarp) remain embedded within the tubercles. As the plant grows, the newly developed tubercles displace older ones, forcing them to move lower down the stem. After a few reproductive seasons, and as the stem dries out and shrinks, intact fruits and/or naked seeds embedded within the plant are buried below ground (Fig. 2). These embedded seeds are released when the plant dies and rots away or when herbivores, such as hares and rodents, feed on whole plants (C. Rodrı´guez-Ortega, personal observations).
A total of 46 reproductive individuals from two populations of M. solisioides and 43 reproductive individuals from two populations of M. hernandezii were collected in December 1999. These populations are La Virgen (Oaxaca state) and Petlalcingo (Puebla state) for M. solisioides, and Loma de la Estrella and La Pedrera (both in Oaxaca) for M. hernandezii. For M. napina, 42 reproductive individuals were collected from one population in Azumbilla (Puebla) in May 2000. Sample sizes were constrained by the collecting permit issued by the Mexican authorities, which amounted to 50 for each species, and the reproductive history of the individuals collected; for example, a few individuals reproduced for the first time in the year of collection, which was only revealed after digging them out. In the laboratory, each plant was examined for the number of fruits (empty or with seeds), their condition (intact or fragmented) and their number of seeds. The age of fruits/seeds could be determined accurately because flowers are produced in a ring below the apical zone of the plant and are always separated from the fruits of the previous reproductive season by the shoots (tubercles or ‘mammillae’) produced during the growing season. Although some plants do not produce fruits each year, their fairly constant rate of growth allows estimation of the number of years between reproductive events. Thus, once the most recent reproductive event was identified, seed age could be accurately determined. Seeds were stored in the laboratory at room temperature for 6 months, after which germination tests were conducted.
Dynamics of mature fruits during their first year after production We studied the dynamics of newly produced fruits by calculating their annual probability of (i) remaining intact with all their seeds, (ii) fragmenting and releasing all their seeds, or (iii) fragmenting and retaining one or more seeds. The fruits employed in this analysis were those produced in the previous fruiting season, i.e., 1998 for M. solisioides and M. hernandezii, and 1999 for M. napina.
Germination, viability and photoblastism In order to investigate how germination and viability of seeds change with age, we conducted germination and viability tests employing the seeds collected from the 131 individuals described above.
ARTICLE IN PRESS Seed germination in serotinous cacti Because some ages were represented by few seeds, six seed ages for M. solisioides (2–7 years old), seven for M. hernandezii (2–8 years old) and eight for M. napina (1–8 years old) were tested. Also, because the numbers of seeds obtained for different ages were unequal, particularly for older ages, it was not possible to design an experiment with replicated treatments (seed ages). Instead, we employed a randomised design. A total of 60 randomly selected seeds were sown for those seed ages with a large sample size, whereas for seed ages with smaller sample size all seeds were used. Seeds were randomly sown in Petri dishes containing seeds of individual species. The age and position of each seed in the experiment was recorded. A maximum of 70 seeds was sown per Petri dish in 1% agar. To prevent fungal attack, seeds were disinfected in 5% sodium hypochlorite solution for 5 min and washed in distilled water. Dishes were incubated in a germination chamber at 25 1C with a 12 h day1 photoperiod. Germination (radicle appearance) was recorded daily for 31 d. At the end of the experiment, ungerminated seeds were examined to verify whether they were alive by dissecting them under a stereomicroscope. In dead seeds, endosperm and embryo dry out and only the testa remains, whereas in live seeds the endosperm and embryo completely fill the seed. Embryos were too small and the testa too hard to allow exposure of the embryo without damaging it. This prevented the use of a tetrazolium-chloride test. The possible photoblastic response of seeds was tested employing two levels of light, full light and darkness, on recently produced seeds. Four replicates of 25 seeds per treatment (each combination of species by light) were sown in 1% agar in Petri dishes. The darkness treatment was provided by wrapping the Petri dishes in two layers of aluminium foil. M. solisioides and M. hernandezii seeds used in this experiment were collected in 2001 in the same wild populations mentioned above. Seeds of M. napina could not be collected in 2001 because we missed fruit production in this species that year. Instead, we used seeds produced in 2000. Seeds in this experiment were disinfected in 5% sodium hypochlorite solution for 5 min and washed in distilled water. Dishes were incubated in a germination chamber at constant temperature (25 1C) with a 12 h day1 photoperiod. Germination was recorded after 30 d.
Serotiny and environment In order to investigate whether climatic variability was related to serotiny in these species,
537 meteorological information for the studied populations was obtained from the Mexican Meteorological Service (National Water Commission, Mexico). Monthly temperature, rainfall and evaporation data were obtained from four stations. These stations were the closest to the five populations studied. The stations (plus the number of years for which records existed) and the species and populations to which climatic records were associated (plus the approximate distance between stations and populations) were: (i) Tepelmeme, Oaxaca state (14 years): M. hernandezii, at La Estrella (10 km) and La Pedrera (6.7 km); (ii) Huajuapan de Leo ´n, Oaxaca (24 years): M. solisioides at La Virgen (2 km); (iii) Acatla ´n de Osorio, Puebla (10 years): M. solisioides at Petlalcingo (18 km); (iv) Chapulco, Puebla (22 years): M. napina at Azumbilla (7.5 km). Missing data were substituted by averages for the corresponding months calculated from the remaining years. Seven percent of monthly records in all three variables were missing in stations associated with M. solisioides, 13% in those for M. napina and 2% in those for M. hernandezii.
Data analyses Degree of serotiny among species, populations and years: The retained seed fraction per plant per observable reproductive lifespan (R, also referred to as the degree of serotiny or seed retention) was calculated as R¼
Sretained , Stotal
where Sretained is the observed number of retained seeds in all the fruits embedded in a plant and Stotal is the expected original number of seeds in those fruits. The latter is the product of the observed number of fruits on the plant (Ftotal) and the average number of seeds per fruit found in the 1999 fruit crop (S1999): Stotal ¼ S1999 F total . Average seed number per fruit in 1999 was obtained from the same populations where the plants/fruits were collected. The use of the average number of seeds per fruit in 1999 was appropriate because only in 1 year (2000) did individuals in one population each of M. solisioides and M. hernandezii exhibited a significantly lower number of seeds per fruit (23% and 36% lower than in 1999, respectively). This difference was tested with a generalised linear model adjusted for overdispersion (see below). Thus, for M. solisioides: F 2;169 ¼ 7:4, Po0:01; for M. hernandezii: F 2;70 ¼ 3:7, Po0:05. The fraction of seeds retained
ARTICLE IN PRESS 538
C. Rodrı´guez-Ortega et al.
per plant per year (Pyear) was calculated as P year ¼
Sretained year , Stotal year
where Sretained year is the number of seeds in a particular year and Stotal year is the estimated number of seeds produced by this plant in the same year. That is, Stotal year is the product of the observed number of retained fruits in a particular year and the average number of seeds per fruit found in the 1999 fruit crop (S1999). To test for differences in degree of serotiny among species, populations and years, we used a generalised linear model (GLM) assuming a proportional response variable (fraction of retained seeds) with a logit link function (Crawley, 1993). In all cases, it was necessary to adjust the w2 statistic to account for overdispersion employing a corrected F test (Crawley, 1993). Germination, viability and photoblastism: We tested for differences in germination and viability among seeds of different ages in all three species. For each dependent variable, we used a GLM with a binary response (germination vs. no germination and live vs. dead seeds, respectively) with a logit link function (Crawley, 1993). In the case of viability, seeds were considered alive when they germinated in germination experiments or when deemed viable (i.e., full) after dissection. In the case of M. napina, it was necessary to adjust the w2 statistic to account for overdispersion in the germination data analysis (Crawley, 1993). Differences in germination between light and dark treatments were also tested using a GLM with a proportional response variable (fraction of germinated seeds) and a logit link function (Crawley, 1993). Serotiny and environment: The degree of serotiny of the five populations was correlated with indirect measures of potential productivity (or its inverse, the harshness of the environment) and measures of environmental variability. A population-level degree of serotiny (Rpopulation) was calculated as the average of the individual R values in each population. Using monthly data, we calculated the mean annual temperature and total annual rainfall and evaporation for the years for which information was available at each station. Annual water deficit was estimated as the difference between mean annual rainfall and mean annual evaporation. The coefficients of variation (CV) of mean annual temperature, total annual rainfall and mean annual evaporation were employed as indices of climatic variability and, therefore, environmental unpredictability.
Two types of analyses were performed. First, assuming taxonomic independence of species and populations, these were treated as independent points (TIPs analyses sensu Silvertown & Dodd, 1996). Because there was only one meteorological station (Tepelmeme) for the two populations of M. hernandezii, its Rpopulation value was calculated as the average of the two populations. This reduced sample size to four populations or points. Second, the phylogenetic differentiation among species and populations was incorporated in an analysis of phylogenetically independent contrasts (PICs sensu Silvertown & Dodd, 1996). The classification employed was that of Hunt (1987) where M. napina and M. hernandezii belong to the series Longiflorae and M. solisioides belongs to the series Lasiacanthae. Populations of the same species were also treated as bifurcating. This produced a 4-tip, completely resolved tree with three contrasts. PIC analyses were conducted with the programme CAIC (Purvis & Rambaut, 1995) with all variables log transformed and assuming constant branch lengths. As is standard with this method, the resulting contrasts were regressed through the origin and the significance of each relationship was tested.
Results Degree of serotiny among species, populations and years There were significant differences in degree of serotiny (R values) among the three Mammillaria species (GLM adjusted for overdispersion: F 2;112 ¼ 29:1, Po0:001). M. solisioides was the most serotinous species, storing on average 24.1% (S.E. ¼ 0.9, n ¼ 32) of its reproductive output. This was between four and five times the percentage of seeds stored by either M. napina or M. hernandezii. The difference between M. napina (6.5%, S.E. ¼ 1.5, n ¼ 40) and M. hernandezii (4.5%, S.E. ¼ 4.0, n ¼ 43) was not significant at the 5% level (GLM F 1;81 ¼ 3, P ¼ 0:09). In addition, important intraspecific variation in R values was observed among species. While many plants of M. solisioides successively released all their seeds, others plants retained up to 80% of the total produced. In M. napina and M. hernandezii this percentage ranged from 0% to 39% and from 0% to 25%, respectively. Interpopulation differences in seed retention were not statistically significant in M. solisioides (GLM F 1;30 ¼ 0:7, P ¼ 0:42) and M. hernandezii (GLM F 1;41 ¼ 0:6, P ¼ 0:46)–for M. napina we only had information from one
ARTICLE IN PRESS Seed germination in serotinous cacti
539 Table 1. Results of generalised linear models of seed germination and seed viability versus seed age in three Mammillaria species Source of variation Seed M. M. M. Seed M. M. M.
Figure 3. Fraction of seeds retained (Pyear averages, 7S.E.) by three Mammillaria species in eight consecutive years. Data were collected in 2000 before M. solisioides and M. hernandezii reproduced. In 1994 M. solisioides had too few fruits/seeds to allow calculation of these figures. The same was true for M. solisioides and M. hernandezii in 1993.
population. No significant differences were found in seed retention (Pyear) among 11 years examined in M. napina (GLM F 10;129 ¼ 0:8, P ¼ 0:65) and 7 years in M. hernandezii (GLM F 6;160 ¼ 1:2, P ¼ 0:31) (Fig. 3). However, significant differences were found among 7 years in M. solisioides (GLM F 6;85 ¼ 2:3, P ¼ 0:04; Fig. 3).
Dynamics of mature fruits during their first year after production The probability of remaining closed for 1 year after production was low for fruits of all species (M. solisioides ¼ 0.06, M. napina ¼ 0, M. hernandezii ¼ 0.02). However, the probability of seed retention (Xone seed) considering both closed and open fruits was X0.24 in all three species (0.64, 0.25 and 0.24, respectively), hence, the highest proportion of fruits loosing all their seeds within 1 year of production was found in M. napina and M. hernandezii (0.75 and 0.74, respectively), whereas in M. solisioides this was 0.3.
Germination, viability and photoblastism There was a statistically significant correlation between seed germination and seed age in all three species and between seed viability and seed age in two of the three species (Table 1). In M. solisioides, germination of 7-year-old seeds was one-fourth that of 2-year-old seeds (0.1 vs. 0.4; Fig. 4A). The fraction of live seeds was not significantly affected
germination solisioides napina hernandezii viability solisioides napina hernandezii
df
w2 or F
P
5 7, 325 6
19.1 3.0 58.0
0.002 0.004 o0.001
5 7 6
6.3 62.2 14.7
NS o0.001 0.02
Due to overdispersion of the germination data in M. napina, a corrected F test was necessary to assess the significance of the models (Crawley 1993). NS ¼ non-significant differences.
by seed age and over 70% of seeds were still alive after 8 years (Fig. 4B). M. hernandezii germination and seed viability were negatively correlated with seed age. Its germination decreased from 0.9 in 2-year-old seeds to 0.38 in 8-year-old seeds, while its seed viability decreased from 0.96 in 2-year-old seeds to 0.8 in 8-year-old seeds. In the case of M. napina, the fitted model indicated that germination actually increased with seed age, from 0.55 in 1-year-old seeds to 0.68 in 8-year-old ones. This was affected by a small decline in the fraction of viable seeds, from 0.82 in 1-year-old seeds to 0.71 in 8-year-old ones (Fig. 4B). The dormant seed fraction (calculated from the fitted models as the difference between surviving seed fraction and germinated seed fraction) for both M. solisioides and M. hernandezii increased with seed age, while that of M. napina decreased (Fig. 4C). Seeds did not germinate in the dark (all species). Germination rates under light were 87% (S.D. ¼ 9.5%) for M. hernandezii, 24% (S.D. ¼ 15%) for M. napina and 23% (S.D. ¼ 13.2%) for M. solisioides. Thus, seeds of all three species are positively photoblastic.
Serotiny and environment The TIPs relationships between environmental variables and degree of serotiny in the studied populations are shown in Fig. 5. Serotiny (Rpopulation) showed a positive trend with mean annual temperature (Fig. 5A) and this relationship was significant in the TIPs analysis (r TIP ¼ 0:96; the critical value for all TIP correlations shown in Fig. 5 is r TIP½0:05 ¼ 0:95), but not in PICs (r PIC ¼ 0:91; PICs critical value is r PIC½0:05 ¼ 0:997). The highest mean annual temperatures were recorded in
ARTICLE IN PRESS 540
C. Rodrı´guez-Ortega et al. solisioides (Fig. 5C; r TIP ¼ 0:98, rPIC ¼ 0:88), while annual water deficit was higher in M. solisioides (about 1580 mm) than in populations of M. napina (1200 mm) and M. hernandezii (1170 mm) (Fig. 5D; r TIP ¼ 0:97, r PIC ¼ 0:89). M. hernandezii populations were subjected to the highest variability in temperature between years, followed by M. napina and M. solisioides populations (Fig. 5E; r TIP ¼ 0:88, r PIC ¼ 0:74). M. napina had the highest among-year variability in annual rainfall, followed by M. hernandezii and M. solisioides populations (Fig. 5F; r TIP ¼ 0:90, rPIC ¼ 0:94).
Discussion The phenomenon of serotiny in cacti
Figure 4. Fitted regression models of the fraction of (A) germinated seeds, and (B) viable seeds versus seed age in three Mammillaria species. The fraction of dormant seeds (C) is the difference between the curves fitted in (B) and (A).
M. solisioides populations (about 7 and 9 1C above those found for M. napina and M. hernandezii populations, respectively). Annual rainfall was highest for M. solisioides populations (about 280 and 140 mm more than for M. napina and M. hernandezii populations, respectively), but this relationship was not significant for either TIPs or PICs (Fig. 5B; rTIP ¼ 0:82, r PIC ¼ 0:56). Mean annual evaporation was lower in populations of M. napina and M. hernandezii than in populations of M.
As far as we are aware, this is the first study to describe the ecological features and seed germination responses of serotinous cacti. In Cactaceae, this phenomenon has only been found in ten species of Mammillaria (Rodrı´guez-Ortega & Franco, 2001). Other species of cacti can retain a few seeds on external structures such a spines and apical wool. However, it is not known whether they retain significant amounts of seeds for long periods of time and, more importantly, whether this retention is a regular and significant feature of their life history, as seems to be the case in the Mammillaria species. Some differences between the cacti studied here and other serotinous species exist. First, the release of seeds X2 years old in Mammillaria seems to be triggered by death of whole plants (necriscence, sensu Lamont, 1991) instead of fire (pyriscence) or moisture (hygriscence), which have been described as the most common mechanisms in serotinous species. Second, at first sight our results suggest that these Mammillaria species are only weakly serotinous. Mean annual seed accumulation per plant in the most serotinous species (M. solisioides) did not exceed 35% of seed production in all study years, while in the other two species the respective values were close to 15%. These values are low when compared with those of, for example, pyriscent species such as Banksia (Proteaceae) or Pinus (Pinaceae) whose retention fractions per reproductive season range between 60% and 100% (McMaster & Zedler, 1981; Cowling & Lamont, 1985). Although Banksia and Pinus plants store a higher proportion of their seed crop than do mammillarian cacti, subsequent spontaneous follicle rupture, granivory and seed decay can substantially reduce the number of viable seeds. In
ARTICLE IN PRESS Seed germination in serotinous cacti
541
Figure 5. Relationships between degree of serotiny (Rpopulation) and both mean annual climatic variables (A, temperature; B, rainfall; C, evaporation; D, water deficit) and their variability among years (E, CV of temperature; F, CV of rainfall) in populations of three Mammillaria species. Diamonds correspond to populations of M. solisioides (Petlalcingo being the most serotinous of them), squares to the M. napina population (Azumbilla) and triangles to the average of the M. hernandezii populations.
Banksia hookeriana for example, 50% of seed accumulation may be lost after 10 years (Enright et al., 1996), whereas in P. torreyana only about 5% of total seeds remain in the mother plants after 15 years (McMaster & Zedler, 1981). In contrast, Mammillaria’s sunken fruits prevent seed dispersal and seeds are protected against seed predators because fruits are relatively quickly buried underground. Our field observations suggest that a very small fraction of seeds is damaged after they have been buried in the underground stem. Thus, the most important factor affecting survival of buried seeds in Mammillaria species is seed decay. In consequence, the proportion of the lifetime seed crop retained by Mammillaria species may not be all that different from that of other serotinous species. We are currently evaluating the contribution that this phenomenon may make to population growth rate, as opposed to that of recruitment from current seed production.
Interspecific variation in degree of serotiny Variation in the degree of serotiny was found among the three Mammillaria species. In general, individuals of M. solisioides retain more seeds in each reproductive season and over their lifespan than M. napina and M. hernandezii. Variation in the degree of seed retention has also been shown, for example, in Banksia species (Enright et al., 1998a, b; Lamont & Enright, 2000). In the case of desert species, the evolution of serotiny might be promoted by spatial and temporal variation in water availability (Ellner & Shmida, 1981), constraining seedling recruitment to years when particular favourable conditions occur. It has been suggested that, in order to spread the risk of reproductive failure, delayed germination of desert ephemeral species is an adaptive trait in this environment (Cohen, 1966; Venable & Lawlor, 1980; Venable & Brown, 1988). Spreading the
ARTICLE IN PRESS 542 germination of seeds over time allows exploration of varying environmental conditions from year to year. Death of a small fraction of the seed crop would be compensated by future success of dormant seeds. The result is a bet-hedging strategy in which phenotypes with delayed germination would be favoured over phenotypes with rapid germination (Philippi & Seger, 1989). Although a similar argument has been raised for the presence of dormant seeds in perennial desert plants (e.g. Mandujano et al., 1997; Bowers, 2000; RojasAre´chiga & Va ´zquez-Yanes, 2000), the correlated evolution of traits in the established (vegetative plant) and regenerative (e.g., seed) phases of the life cycle produces a more complex scenario for selection of seed dormancy (Rees, 1994). Thus, although our results suggest a positive correlation between serotiny and harshness of the environment (some of the TIPs analyses in Fig. 5), our small species sample did not provide significant trends employing phylogenetically independent contrasts. Thus, our results (which are based on only four populations/three species) must await confirmation from more detailed demographic analyses.
Intraspecific variation in degree of serotiny Important intraspecific variation in the degree of seed retention was found in all three Mammillaria species. Similar variation has been found in other serotinous species, including pines (Muir & Lotan, 1985; Gauthier et al., 1996). These authors have pointed out that spatial and temporal variability in environmental conditions, such as intensity, frequency and spatial distribution of disturbance, could promote phenotypic variation in the degree of serotiny (McMaster & Zedler, 1981; Cowling & Lamont, 1985; Lamont et al., 1991; see also Mathias & Kisdi, 2002). Although germination fractions seem to be low after 8 years in two species (M. solisioides and M. napina), their viability points to long-lived seeds. Seventy-per cent of retained seeds in all three Mammillaria species were still alive after 8 years. Indeed, longlived seeds may not be uncommon in the Cactaceae (Mandujano et al., 1997; Rojas-Are ´chiga & Va ´zquezYanes, 2000).
Dormant seed fractions and photoblastism One interesting result concerning serotiny in Mammillaria seeds refers to the size of the dormant fraction as seeds age. These fractions increased in M. solisioides and M. hernandezii, but decreased in M. napina (Fig. 5C). Dormant seeds have been
C. Rodrı´guez-Ortega et al. reported in several species of desert ephemerals, for which germination could be prolonged over a period of 2 years, even when conditions for germination were favourable each year (Philippi, 1993a). Both theoretical and empirical work suggest that (monocarpic) populations subject to high environmental variability produce higher fractions of dormant seeds than populations inhabiting places with more stable or favourable environmental conditions (Cohen, 1966; Venable & Lawlor, 1980; Venable & Brown, 1988; Philippi, 1993b; Pake & Venable, 1996). Of interest here is that larger dormant fractions were found in M. solisioides (the most serotinous species), whose seeds also exhibited the highest survival fraction after 8 years. In contrast, species with lower seed retention had smaller dormant fractions. Positive photoblastism has been suggested to be an important mechanism to build persistent seed banks in many species (Pons, 1992). For example, seeds of Ferocactus wislizeni, which develops persistent soil seed banks in the Sonoran Desert, did not germinate when incubated in the dark (Bowers, 2000). The same occurred in the three Mammillaria species studied here. The ecological significance of photoblastic seeds in species with persistent seed banks seems clear. In the case of serotinous Mammillaria, the germination of seeds buried in the soil would lead to the death of the seedlings if they were not able to reach the ground surface. Because growth rates in the Cactaceae are low, particularly in the early stages of the life cycle (Nobel, 1988), growth alone would limit the recruitment success of buried seeds. Seeds would therefore only be exposed after being dispersed by herbivores (endozoochory) or after disintegration of the plant after death.
Conclusions The correlative evidence of retention, germination, viability and dormancy of seeds in these three species of Mammillaria suggests that serotiny is not a fortuitous attribute, but one that may confer some advantage under the harsh environments where they live. Although these attributes would seem to allow the plants to spread the risk of reproductive failure in both time and space, adequate quantification of their ecological and evolutionary significance is necessary before we can reject alternative hypotheses. All three species are rare and endangered and it is possible that their rarity is due to their inability to recruit successful offspring more often than they do. Presently, we
ARTICLE IN PRESS Seed germination in serotinous cacti are therefore conducting a detailed demographic study to assess the consequences of serotiny under different environmental scenarios. Coupling the information on seedling recruitment with an analysis of prevailing environmental conditions will allow us to appraise the demographic and evolutionary consequences of seed retention in these plants.
Acknowledgements The authors thank Teresa Valverde, Arturo Flores-Martı´nez and Jordan Golubov for guidance and support throughout the course of this study and useful criticism of earlier versions of the manuscript. We particularly thank Rube´n Pe ´rez-Ishiwara for his help with fieldwork and overall technical assistance. We also thank the anonymous reviewers and the editorial team of BAE whose suggestions greatly improved the quality of the presentation. This work was financed by grants IN205500 of DGAPA-UNAM to M.C.M. and M.F. and W031 of CONABIO to M.C.M. C.E.R.O. thanks CONACyT and DGEP-UNAM for a Ph.D. scholarship, and the Posgrado en Ciencias Biolo ´gicas (UNAM) for financial support to complete this work at the University of Plymouth. Permit to collect specimens (DOO 024152) was granted by the Ministry of the Environment, Natural Resources and Fisheries (SEMARNAP), Mexico.
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