Identifying the impacts of chronic anthropogenic disturbance on two threatened cacti to provide guidelines for population-dynamics restoration

Biological Conservation 142 (2009) 1992–2001

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Identifying the impacts of chronic anthropogenic disturbance on two threatened cacti to provide guidelines for population-dynamics restoration Carolina Ureta, Carlos Martorell * Departamento de Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, Circuito Exterior s/n, Ciudad Universitaria, 04510 México, D.F., Mexico

a r t i c l e

i n f o

Article history: Received 17 March 2008 Received in revised form 6 October 2008 Accepted 25 December 2008 Available online 15 May 2009 Keywords: LTRE Overgrazing Land degradation Demography Cactaceae Mexico

a b s t r a c t Species frequently have to be preserved in disturbed areas. Restoring their predisturbance population dynamics may increase their population growth rate (k) while preventing the development of vulnerable genetic- or age-structures in the population. We assessed how population dynamics have been affected by anthropogenic disturbance in the threatened cacti Mammillaria dixanthocentron and Mammillaria hernandezii. We worked in areas exposed to different intensities of disturbance, and applied a retrospective analysis to detect which of the vital rates affected by disturbance were responsible for reductions in k. M. dixanthocentron had lower ks in more disturbed conditions as a consequence of the reduced survival of adults because of livestock trampling and increased predation by hares. M. hernandezii had significantly higher ks with intermediate disturbance. The reduction in k under intense disturbance resulted from reduced reproduction and adult plant mortality. The death of these individuals seemingly was associated to the change in soil conditions due to overgrazing. However, the factor with the greatest influence over both species was temporal variability, which interacted with disturbance sometimes increasing its negative effects. The identification of hypothetical mechanisms reducing k was facilitated by the retrospective analysis, which is then a valuable heuristic tool guiding research. As long as they are not properly tested, these hypotheses should be considered carefully in management plans, but they may provide timely information. Retrospective analysis allows taking initial conservation measures, while suggesting guidelines for future research that may improve such measures. Ó 2009 Elsevier Ltd. All rights reserved.

1. Introduction Anthropogenic disturbance has impacted biodiversity severely (Cuaron, 2000; Dellasala et al., 2004; Liira et al., 2007; Lin and Liu 2006; Martorell and Peters, 2005; Maclean et al., 2006; Wolf, 2005). Depending on their frequency and intensity, anthropogenic disturbances can be classified as acute or chronic (Singh, 1998). The former have a high intensity but low frequency, are highly destructive and easy to identify because of the extreme changes they induce on the structure of ecological systems (Dellasala et al., 2004). Instead, chronic anthropogenic disturbance (CAD) is frequent but subtle and takes place over long time-periods. This kind of disturbance is widespread in developing countries, where low-intensity activities such as branch cutting and extensive cattle raising are very common (Martorell and Peters, 2005; Singh, 1998). Although CAD is frequently overlooked, it may be as destructive as acute disturbance. In drylands or other low-productivity areas where recovery after disturbances is slow, CAD may have a very strong impact over populations because their complete recupera* Corresponding author. Tel.: +52 55 5622 48 35; fax: +52 55 5622 48 28. E-mail address: [email protected] (C. Martorell). 0006-3207/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2008.12.031

tion is not achieved before new impacts occur (Martorell, 2007; Martorell and Peters, 2005; Singh, 1998). Due to the fact that the degradation caused by CAD is not linear, the harm can go unnoticed until its damage becomes nearly irreversible (Cuaron, 2000; Lin and Liu, 2006; McKinney and Lockwood, 1999; Singh, 1998). However, in developing countries where few economic alternatives are available, it is very difficult to suspend the productive activities on which the peasant’s income relies. Consequently, it is necessary to preserve biodiversity in the presence of human disturbance (Brandon et al., 2005; Pedroso-Júnior and Sato, 2005). In order to assess if successful conservation may be achieved in disturbed areas the population growth rate, k, is useful. This parameter provides information on whether a population is able to persist given some environmental conditions, a critical issue when determining if a species is threatened. Accordingly, conservation efforts have frequently been oriented to increasing k. This is achieved by acting upon specific demographic processes or individuals that are recognized as important after applying prospective perturbation analyses (sensitivity or elasticity; Silvertown et al., 1996; Caswell,1997, 2001). Nevertheless, management recommendations based on prospective methods do not necessarily restore the natural dynamics of the population and may even produce

C. Ureta, C. Martorell / Biological Conservation 142 (2009) 1992–2001

further modifications in it which may result detrimental. For example, in Echeverria longissima (Crassulaceae), a management strategy which promotes the vital rates with greater sensitivity may cause changes in the population dynamics that are known to erode genetic variability or reduce the effective population size, all of which in turn may reduce k-values in the long term (Martorell, 2007). On the contrary, the undisturbed population dynamics can be presumed to be compatible with long-term conservation in most cases, as it has allowed the persistence of species for long time periods. However, not all the changes in population dynamics are equally important. Retrospective analysis (LTRE) can be used to determine which vital rates are responsible for the observed reductions, if any, in k under different CAD conditions (Horvitz et al., 1997; Caswell, 1997, 2000, 2001; Tuljapurkar and Caswell, 1997) and thus may provide guidelines to restore the original dynamics of the population while increasing k (Ehrlén and van Groenendael, 1998; Martorell, 2007). In this paper we assessed the impact of CAD on two threatened cacti, Mammillaria hernandezii and Mammillaria dixanthocentron, whose habitat has been disturbed for centuries by livestock, treefelling, change of land use, and extraction of non-timber forest products (Martorell and Peters, 2005). We compared areas that were exposed or isolated from CAD by means of a fence that prevents ongoing disturbance by precluding livestock and people from entering. Analysing the effect of fencing is important because a reduction in the current disturbance intensity may be proposed as a management form. While fencing effectively isolates the population from ongoing disturbance, cacti inside the fences may not resemble closely the undisturbed population dynamics to be restored: disturbances that have been taking place for centuries and have changed the environment through soil compaction, erosion, nutrient loss or reduction of tree cover are unlikely to be reversed by fencing in the short term. In order to assess how these impacts affect the population dynamics, we worked in two sites differing in their initial disturbance intensity. Thus, the sites  exclosure combinations represent four different disturbance conditions in which the population dynamics could be evaluated. We used retrospective analysis to identify the demographic processes and size categories that have been affected by temporal variability and anthropogenic disturbance causing reductions in the population growth rate. In order to do so, we compared populations with different disturbance regimes, using fences and sites with different levels of CAD to elucidate which population dynamics both cacti may have had before disturbance occurred. We also show how this information may be used to design population management plans aimed at population-dynamics restoration, and how LTRE may provide useful information for conservation, an issue that has been in debate over the last decade (Ehrlén and van Groenendael, 1998; Caswell, 2000; Martorell, 2007).

tation (622 mm; historically, 22% of the years were rainier). The midsummer drought became harsher as the years passed, and was extremely severe in the third year, with only 3 days of rain from mid-June to mid-September. M. dixanthocentron Backeb. grows in Quercus forests. It is a globose to approximately cylindric plant that rarely branches, with stems of 5–30 cm tall and 7–25 cm wide. Some flowering occurs throughout the year, but it reaches a marked maximum in February (Arias-Montes et al., 1997). It only grows in south-western Mexico (Puebla and Oaxaca). While it is partially protected by the Tehuacán-Cuicatlán Biosphere Reserve, our study sites lay out of that area. M. hernandezii Glass and R.C. Foster buries its 35–45 mm stem into the ground. Only the flattened top of the plant, some 25 mm in diameter, protrudes from the soil. Flowering occurs from October through December (Arias-Montes et al., 1997). This species grows in Bouteloua short-grass prairies, in a very small, 17.1 km2 area out of any reserve, most of which has been under severe disturbance. Both species are protected by Mexican laws (SEMARNAT, 2008), and are included in the IUCN Red Book (IUCN, 1997). Two locations that differed in CAD intensity as measured through the Martorell and Peters (2005, 2009) index were chosen for each species. This index is based on 14 different metrics accounting for three main agents of disturbance: human activities, livestock raising and land degradation. For M. dixanthocentron, the more preserved site had a disturbance index of 30.4 (on a 0–100 scale) and a density of 1998 individuals/ha, and the more disturbed one had an index of 39.2 and a density of 1200 individuals/ha. The sites for M. hernandezii had indices of 41.8 and 57.2 and densities of 13,455 and 13,800 individuals/ha, respectively. The study sites are representative as the average disturbance experienced by the populations of M. dixanthocentron is 42.5, and by M. hernandezii is 58.5 (Martorell and Peters, 2009). In each site, a 100  100 m area was delimited and half of it was fenced to protect the population from the main human activities occurring in the region. No less than 100 individuals were marked along 50 m long, randomly placed transects in the protected and exposed halves of each study site (Table 1). The diameter of M. hernandezii plants and the diameter and height of M. dixanthocentron plants were measured with a caliper to the closest millimetre between 2001 and 2004. Data were collected between July and August when plants are hydrated and unburied. Transects were meticulously inspected for new seedlings every year. Flower production was recorded in October for M. hernandezii and July and February for M. dixanthocentron. 2.2. Lefkovitch Matrix Construction Matrix population models project the number of individuals in different life-cycle stages at time t (denoted by the vector nt) into time t + 1 through the basic equation

ntþ1 ¼ Ant 2. Method 2.1. Study site and species The study was conducted in Concepción Buenavista, Mixteca Alta, State of Oaxaca, Mexico, at an altitude of 2300 m a.s.l. The climate is semiarid (BS1) with an annual precipitation of 530.3 mm falling mainly from May to September and a strongly dry canicular period in July–August. The annual average temperature is 14.9 °C. The first year of the study had an annual rainfall well below the average (377 mm; only 14% of the years in the historical record were dryer than this one), the second presented a precipitation similar to the average (539 mm) and the third had a high precipi-

1993

ð1Þ

where A is a square matrix whose elements aij are either fecundities or probabilities of transitioning from category j to category i. Thus, aij are the vital rates that characterize population dynamics. Plant size was defined as the diameter in M. hernandezii and as the approximate volume in M. dixanthocentron assuming that its form was cylindrical. Plants were classified into five size categories. Matrix models assume that all the individuals in a size category have the same demographic behaviour (Caswell, 1997), so the categories were defined trying to be congruent with biological criteria while keeping the numbers of individuals in each category as large as possible in order to have accurate estimations (Table 1). The fecundity was estimated assuming that the newly recruited individuals are produced by each size category proportionally to the number of

1994

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Table 1 Average number of individuals per category. The four rightmost columns are the average number of individuals per category in three years of measurements for each site and exclosure treatment. M: more disturbed; L: less disturbed, E: exposed to disturbance; F: fenced. Species

Category

Size limits

Developmental stage

M/F

M/E

L/F

L/E

Mammillaria hernandeziia

0 1 2 3 4

1–2 2–6 6–9 9–13 >13

Seedling Juvenile Adult Adult Adult Total

36.7 26.7 23.7 52.3 22.7 162

16.3 16.3 21.7 43.3 32.7 130.3

11.3 16.3 41.7 76 17 162.3

8.3 12.7 32.7 43.3 33.7 130.7

Mammillaria dixanthocentronb

0 1 2 3 4

1–37.5 37.5–375 375–3750 3750–37500 >37500

Seedling Juvenile Adult Adult Adult Total

13 17.7 24.7 24.7 23.3 107.8

5 12 29 24.7 31 99.5

10 11.3 22 29 39.3 119.5

9 13.3 29 45 38.3 132

a b

Sizes in mm. Sizes in mm3.

flowers they produced in a year (Menges, 1990). We assumed that there was no seed bank as in other cacti (Rojas-Aréchiga and Batis, 2001). In a few occasions growth from a category into the next one was not observed in the field and had to be estimated. Since transitioning implies that a plant cannot remain in the same category in which it originally was, estimating transition required that the stasis probability was also changed. To do so we used the formulas (Caswell, 2001)

aii ¼ ri ð1  ci Þ

ð2Þ

aðiþ1Þi ¼ ri ci ;

ð3Þ

where aii is the stasis probability of category i after a year, a(i+1)i is the probability of transiting to the next category, ri is the probability of survival of a plant in category i, and ci is the probability of growing to the next category given that the plant survives. ci was calculated as 1/si, where si is the time a plant stays in the ith category, calculated by dividing in each year the average growth of all the individuals in category i by the category’s amplitude (Caswell, 1997). A similar problem arose with the mortality rate of individuals in the last size category (category 4) of both species because it was not observed in some years. This probability was estimated through a binary regression between the probability of death and the size of individual plants, and then interpolating the mortality rate for a plant having the average size of all the individuals in the category 4. For each species, twelve matrices were constructed; one for each site, exclosure and year combination, and k-values were obtained. 2.3. Retrospective analysis In contrast to prospective analyses, which project the consequences of hypothetical changes in vital rates on k (population growth rate) of a single matrix (Caswell, 1997; De Kroon et al., 1986; Gerber and Heppell, 2004), retrospective methods are based on observed differences among matrices obtained under different conditions. The variations in the vital rates among matrices may result in different k-values. Retrospective analysis decomposes the differences in k observed in different conditions into the contributions made by each vital rate. Their results are summarized in a contribution matrix, whose elements indicate how much each vital rate adds to k. Contributions may have positive or negative values, depending on whether the observed changes in each vital rate cause an increase or decrease in k with respect to a reference value, which is usually the population growth rate, k(r), of the average matrix, A(r). Contributions are calculated as

ðmÞ

cij

  ðmÞ ðrÞ ¼ aij  aij SAy ij ðmÞ

ð4Þ ðmÞ

where cij is the contribution of the aij entry in the matrix A(m) of the population experimenting treatment m, and SAy ij is the sensitivity of the vital rate (for details on the calculation on the appropriate sensitivity, see Caswell, 2001). In other words, matrices are compared to a reference matrix to find out which demographic processes and categories contribute to the difference between k(m) and k(r). Contributions are small if the difference between the vital rates among matrices is negligible or if their sensitivity is low. This means that vital rates that are unaffected by the treatments, or that have a low impact on the population growth rate cannot be responsible for the observed differences in k. Given that contributions are additive, the results can be summarized by adding the contributions of the vital rates that correspond to the same processes (fecundity, stasis, growth and retrogression), or to the same size categories (Martínez-Ballesté et al., 2005). For each species we evaluated the effect of three different factors over the population: site, exclosure and time. The first two factors had two levels and there were 3 years under study, so the experiment was a 2  2  3 factorial. When factorial experiments are used, contributions can be decomposed into those corresponding to the main effects and interactions, just as it occurs in statistical procedures such as ANOVA or GLM (Caswell, 2001). Retrospective analysis deals with the observed differences in k, but these may result from random variation. It is important to assess if variations in k among treatments are significantly different from zero before decomposing them into vital-rate contributions through retrospective analysis. The k-values do not necessarily follow a known probability distribution, so statistical inference on k was performed through bootstrapping (Caswell, 2001). Because we have a factorial design, we assessed whether the main effects or their interactions induced significant changes on the population growth rate. To do so, a matrix for each one of the twelve treatments was built by re-sampling the individuals in it. Using these matrices, an average matrix was calculated for each exclosure level, site, and year (main effects), and for every site  year, site  exclosure and exclosure  year combination (two-way interactions). Lacking replicates for each site  exclosure  year combination, differences in the three-way interaction could not be tested for significance. All the matrices were then iterated 200 times in order to estimate the respective k-values. We assumed the usual linear model for factorial designs, which has the form (Venables and Ripley, 2005):

kijk ¼ k111 þ bi xi þ bj yj þ bkð2Þ zkð2Þ þ bkð3Þ zkð3Þ þ bij xi yj þ bikð2Þ xi zkð2Þ þ bikð3Þ xi zkð3Þ þ bikð2Þ yj zkð2Þ þ bikð3Þ yj zkð3Þ þ eijk

ð5Þ

1995

C. Ureta, C. Martorell / Biological Conservation 142 (2009) 1992–2001

Table 2 Population growth rates (mean and 95% CI) of Mammillaria dixanthocentron and Mammillaria hernandezii in different disturbance conditions for three years. Less: less disturbed site; More: more disturbed site. Boldface shows rates that are significantly different from one. Site

M. dixanthocentron Less More

M. hernandezii Less More

Fence

Year 1

2

3

Yes No

0.975 (0.915–1.035) 1.032 (0.998–1.074)

0.946 (0.872–1.007) 0.931 (0.844–0.974)

1.008 (1.001–1.025) 0.853 (0.760–0.946)

Yes No

1.066 (1.023–1.136) 0.958 (0.914–0.997)

0.943 (0.863–1.014) 0.882 (0.798–0.958)

0.856 (0.771–0.947) 0.893 (0.825–0.956)

Yes No

0.858 (0.776–0.932) 0.984 (0.945–1.008)

0.776 (0.630–0.999) 0.947 (0.844–1.008)

0.980 (0.952–1.004) 0.976 (0.936–0.999)

Yes No

1.138 (1.042–1.234) 1.006 (0.961–1.059)

0.912 (0.840–0.971) 0.981 (0.944–1.013)

1.007 (0.976–1.030) 0.971 (0.927–0.998)

where i is the site number (conserved site = 1 disturbed site = 2), j is the exclosure treatment (inside the exclosure = 1, out of it = 2), and k is the year number (1, 2 or 3). Variables x and y have a value of 0 if i or j are equal to 1, and a value of 1 otherwise. zk(2) and zk(3) have values of one only when k = 2 or k = 3, respectively. The error eijk is assumed to have a mean of 0. The b coefficients are the main effects or interaction effects depending on the terms involved. For example, bi, which is only multiplied by the site coefficient xi, is the site main effect, but bik(2), altogether with bik(3), corresponds to the site  year interaction since it is multiplied by both the site and year coefficients. Let  stand for the average, so that, for example, k11 is the eigenvalue of the transition matrix obtained for the exclosure in the more conserved site by averaging the bootstrapped matrices for the 3 years. From Eq. (5), it can be shown that the interaction coefficients can be calculated from the eigenvalues as bij = k11 + k22  k12  k21, bik(2) = k11 + k22  k12  k21, bik(3) = k11 + k33  k13  k31, bjk(2) = k11 + k22  k12  k21, and bjk(3) = k11 + k33  k13  k31. Notice that we are assuming that the error terms cancel out when data are averaged and thus that E(eijk) = 0 as mentioned earlier. This would occur, for example, if k-values were approximately normally distributed as it has been found in some studies (see data in Caswell, 2001 for population growth rate’s distributions obtained from a procedure similar to the one used here and Martorell, 2007). The main effects coefficients can then be estimated as bi = k2  k1  bij/2  (bik(2) + bik(3))/3, bj = k2  k1  bij/2  (bjk(2) + bjk(3))/3, bk(2) = k2  k1  bik(2)/2  bjk(2)/2, and bk(3) = k3  k1  bik(3)/2  bjk(3)/2. It must be noted that the significance of the year and its interactions was assessed through two b-coefficients, which is the result of having two degrees of freedom for this three-level factor. We considered that the year or its interactions had a significant effect if at least one b was significant. This corresponds to the usual statistical approach when categorical explanatory variables with more than two levels are involved (such as ANOVA) in which the alternate hypothesis being tested is usually stated in the form ‘‘at least one of all the possible differences is significant”. The whole procedure from bootstrapping and matrix construction to the estimation of b coefficients from k-values was repeated 1000 times. The estimates for each b coefficient were sorted, and the number of positive or negative ones (whichever was smaller) was counted and divided by 1000. The result is the P-value for the null hypothesis that b = 0, or, in other words, that there is a significant main effect or interaction effect (Venables and Ripley, 2005). At this point we must bear in mind that significant b-coefficients mean that k-values differ, and that contributions regard those the differences in population growth rates. In order to account only for those differences that we are sure enough that

are non-random, we analysed only the contribution matrices that corresponded to significant main or interaction effects. 3. Results Significantly negative population growth rates were frequently observed for both species. The bootstrapped k-values of the interaction between the 3-year average matrix and the site, as well as the years and the exclosure, show that the population under those conditions did not reach population growth rates significantly greater than one with the exception of M. hernandezii in the first year inside the fence in the more disturbed site (Table 2). In M. dixanthocentron, the largest values of k were recorded inside the exclosure in the less disturbed site. The population growth rate did not significantly differ from one inside the exclosures at both sites, while the areas exposed to disturbance had significantly smaller k-values (Table 2). In M. hernandezii no clear pattern was observed in terms of the k of individual matrices (Table 2). In M. dixanthocentron the highest sensitivity values corresponded to the stasis of categories 2–4. In M. hernandezii the highest sensitivities were observed in stasis of individuals of the categories 3 and 4 and growth of category 3 (Table 3). 3.1. M. dixanthocentron Population growth rate of this species showed a trend to be reduced by disturbance. We observed significantly higher k-values in the less disturbed site (P = 0.021) as a result of increased stasis, even though reduced growth and retrogression had a negative impact on k (Fig. 1c–d). Category 4 stood out for its positive contribuTable 3 Sensitivity matrices for Mammillaria dixanthocentron and Mammillaria hernandezii. Sensitivities were estimated from the mean matrix for all the sites and years for each species. The three largest values are typed in boldface. For the sake of clarity, sensitivity values were multiplied by 1000. 0 Mammillaria 0 1 2 3 4

1

dixanthocentron 1.47 0.29 2.93 4.46 0.34 1.87 0.05

Mammillaria hernandezii 0 0.02 1 0.11 2 3 4

0.02 0.10 0.14

2

0.50 5.50 1.39

0.04 0.19 0.27 0.32

3

4

0.08

2.65

0.40 6.14 1.14

0.55 7.19

0.05 0.25 0.34 0.41 0.46

0.021 0.15 0.18 0.20

1996

C. Ureta, C. Martorell / Biological Conservation 142 (2009) 1992–2001

tion to k in the less disturbed site and negative in the more disturbed area (Fig. 1p–q). Also, the population growth rate was larger inside the exclosures (P < 0.001), where all demographic processes contributed in a positive way to k, growth being the one with the largest values (Fig. 1a–b). Again, category-4 plants were the ones contributing the most to the observed difference between the protected and exposed areas (Fig. 1n–o). However, among all the factors that we assessed, temporal exerted the greatest influence on k-values. From the first year of study—which presented the moister canicular period—until the last, ks-values decreased gradually and significantly (P < 0.001) as the midsummer drought became harsher. During the first year, growth and stasis made considerably high positive contributions, while in the third year—which had the harshest canicular period—all demographic processes contributed negatively (Fig. 1e–g). The same pattern was observed when summarizing data through the categories. All of them contributed positively in the first year and negatively in the third one. As it occurred in the exclosure and site main effects, categories 3 and 4 were the greatest contributors to the differences among years (Fig. 1r–t). There was a marginally significant interaction between site and year. In the third year the differences between the disturbed and the less disturbed areas became significantly greater than in the previous 2 years (P = 0.057) as a result of a very large negative contribution of growth and of plants in the categories 0, 2 and 3 (Fig. 1h–m and u–z). 3.2. M. hernandezii In terms of population growth rate, M. hernandezii presented greater values in the more disturbed locality (P = 0.023). The

exclosure’s main effect was not significant, but its interaction with the site was (P = 0.001). Consequently, it could be seen that intermediate levels of disturbance (inside the fence in the more disturbed site and outside the fence in the less disturbed site) presented higher values of k. The demographic processes that stand out for their contributions to the differences between k-values were stasis and growth (Fig. 2a–f) from almost every size category (Fig. 2p–u). The highest sensitivity values were also located in these demographic processes. Consequently, in order to increase k-values, plants need to stay and grow (Table 3). As in M. dixanthocentron, the factor that had the largest effect on M. hernandeziis population growth was temporal variation. Both the second and third years of study had a significant effect on k (P = 0.0462 and P = 0.010, respectively). In the second year, which presented typical annual precipitation and a relatively severe canicular period, the population had the lowest population growth rate. In contrast to M. dixanthocentron, the third year had a higher k than the second year, even though it was the year with the strongest canicular period. The interaction between years and site was significant only for the third year (P < 0.001), and the years  exclosure interaction was significant for the second (P = 0.014). In the third year, almost all demographic processes and categories contributed negatively to k in the disturbed site. Similarly, in the second year, negative contributions of categories and demographic processes were observed in the exclosures (Fig. 2v–d, and Fig. 3l–v). The interaction between years and sites shows that in the first year, almost all demographic processes and categories contributed negatively in the less disturbed site and positively in the more disturbed site. The opposite was observed in the third year (Fig. 3a–v).

Fig. 1. Site, exposition to disturbance, and year contributions to the population growth rate (k) in Mammillaria dixanthocentron. The average population growth rate value was k(r) = 0.9779. The left panel shows demographic process’ contributions (R: retrogression; S: stasis; G: individual growth; and F: sexual reproduction), and the right one corresponds to contributions made by size categories 0 through 4. Graphs a–b and n–o correspond to the main effect of the exposition to disturbance, c–d and p–q, to the site’s main effect, and e–g and r–t to the year’s main effect. Graphs h–m and u–z show the contributions of the marginally-significant site  year interaction. Notice the differences in the contribution’s scale among left and right panels.

C. Ureta, C. Martorell / Biological Conservation 142 (2009) 1992–2001

4. Discussion 4.1. Disturbance impact The response of both species of study under different levels of CAD varied greatly: in M. dixanthocentron’s case, the largest k-values were observed under conditions where CAD was low, that is, in the less disturbed site and in areas that were protected by the fence. Thus, this species resembles other cacti which have been found to be vulnerable to CAD conditions (Dubrovsky et al., 1998; Godínez-Álvarez et al., 2003; Hernández and Godínez, 1994; Méndez et al., 2004; Valverde et al., 2004). This has been explained in terms of cactus’ life-history traits such as their slow growth, long life cycles, and low recruitment of new individuals, which are supposed to diminish their capability to recover after a disturbance (Anderson, 2001; Arias-Montes, 1993; Godínez-Álvarez et al., 2003; Hernández and Godínez, 1994). However, it is interesting to note that M. hernandezii has much lower individual growth rates than M. dixanthocentron and yet was found to be less vulnerable to disturbance, as indicated by its higher population growth rates in the presence of CAD. We believe that differences in disturbance intensity (instead of intrinsic biological differences among species) were not responsible for the differences among species response to CAD, because then it would be expected that the species experiencing more disturbance—M. hernandezii—would have shown a larger negative impact of disturbance, which was not the case. These results highlight that the response of species to disturbance is idiosyncratic. Not even two species in the same genus behave similarly. Thus, extrapolating our results to other plants may lead to erroneous management planning. Even though M. dixanthocentron had larger ks in the fence and the less disturbed site, this pattern was the result of different processes in each case. The fence affected all demographic processes,

1997

but stasis was the only factor contributing to differences among sites. We must bear in mind that even the less disturbed site had some disturbance. This might have prevented some demographic processes from contributing positively to k as it occurred in the exclosure, where CAD was completely eliminated. Growth, which was the factor contributing most to the increase in k inside the fences, did not do so in the less disturbed site, and the same was observed in terms of fecundity. This may suggest that both processes were very sensitive to ongoing disturbance. The category 4 made the greatest contribution to the differences between k among sites and exposure levels. Very little variation was observed in the vital rates of this category, but its contribution was very large because of its high sensitivity. Even small changes in this category’s vital rates resulted in a significant change in kvalues (Caswell, 2001). Thus, identifying and controlling the factors that affected the plants in this category seems critical for conservation. Among these we observed trampling and lagomorphs. In the most disturbed site, lagomorphs ate large numbers of adult plants during the dry seasons. As it has been observed for other lagomorphs (Fa et al., 1998; Lombardi et al., 2003), hares are very abundant in the grasslands of Concepción Buenavista. The proximity of anthropic pastures in disturbed areas may increase hare incursions into the forest, thus posing a problem to M. dixanthocentron. Adult individuals out of the fence were frequently found detached from their substrate, seemingly as a result of kicking and trampling by rambling livestock. Other category-4 plants in disturbed areas gradually dried out maybe as a result of the increased solar radiation and the reduced soil humidity that are associated to overgrazing (Komatsu et al., 2007; McDonald and Glen, 2007; Savadogo et al., 2007). A similar result was observed in the succulent plant E. longissima (Crassulaceae), in which CAD causes a decrease in k due to increased drought and mortality (Martorell, 2007).

Fig. 2. Site, exposition to disturbance, and year contributions to the population growth rate (k) in Mammillaria hernandezii. The average population growth rate value was k(r) = 0.9637. The left panel shows demographic process’ contributions (R: retrogression; S: stasis; G: individual growth; and F: sexual reproduction), and the right panel corresponds to contributions made by size categories 0 through 4. Graphs in the leftmost column of each panel correspond to the main effects of the site (a–b and p–q), and year (g–i and v–x). The graphs in the remaining columns show the site  exposure to disturbance (c–f and r–u) and year  exposure to disturbance (j–o and y–D) interaction contributions. The main effect of exposure to disturbance was not significant and thus is not presented. Notice the differences in the contribution’s scale among left and right panels.

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The positive effect of disturbance on M. hernandezii’s population growth rates is similar to the pattern observed for Echinocactus platyacanthus (Jiménez-Sierra et al., 2007) and five other species in the genus Mammillaria which have greater population densities in intermediate levels of disturbance (Martorell and Peters, 2005, 2009). This response seems to be related to some M. hernandezii’s attributes that increase its tolerance to disturbance. For example, it buries itself into the ground, which reduces the impact of cattle trampling and the chance of being eaten by livestock (pers. obs.). This species also presents physiological traits such as succulence and CAM (Crassulacean Acid Metabolism) photosynthetic pathway that allow it to prosper in the increased aridity that characterizes overgrazed grasslands (van de Koppel et al., 1997). It has been evaluated that cacti can be negatively impacted when interacting with grasses or bushes (Briones et al., 1996, 1998; Jiménez-Sierra et al., 2007; Mandujano-Sánchez et al., 2001, 2007; Reyes-Olivas et al.,

2002). Inside the fence in the less disturbed site, grass density was higher and we observed many M. hernandezii individuals being stiffly squeezed by growing tussocks. Consequently, intermediate levels of disturbance where grass cover is regulated by grazing may be favourable for M. hernandezii. The same occurs in Echinocactus platycanthus, which is not negatively affected by disturbance but by competition when livestock disturbance is reduced (Jiménez-Sierra et al., 2007). However, there seems to be a disturbance threshold that should not be exceeded. The interaction between site and exclosure shows that all demographic processes contributed negatively in extreme disturbance conditions. Outside the fence in the more disturbed site k was greatly reduced as a result of decreased survival and growth. As in M. dixanthocentron, this apparently was the result of plants becoming dehydrated, as the increased retrogression rates and our field observations suggest. Severe retrogression in this species may lead individuals to get

Fig. 3. Site  year interaction contributions to the population growth rate (k) in Mammillaria hernandezii. The average population growth rate value was k(r) = 0.9637. The upper panel shows demographic process’ contributions (R: retrogression; S: stasis; G: Individual growth; and F: Sexual reproduction), and the lower panel corresponds to contributions made by size categories 0 through 4. Graphs in the upper row (a, b, l and m) of each panel correspond to the main effects of the site, and those in the leftmost column (c–e and n–p) are the main effect of the year. The remaining graphs show the site  year interaction contributions. Notice the differences in the contribution’s scale among the upper and lower panels.

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completely buried in the soil, preventing photosynthesis and reproduction. We have observed that plants may remain buried for several years, but eventually die. It seems that the increasing dryness of the soil caused by overgrazing (van de Koppel et al., 1997) together with the higher erosion and silting in the more disturbed site may be responsible for dehydration and plant burying and thus of reduction in k-values. 4.2. Temporal variability and disturbance Although our main goal was to evaluate CAD impacts on the population dynamics, the factor having the greatest influence over both species’ k was temporal variability, which nevertheless interacted with CAD. For M. dixanthocentron, there was a close correspondence between the intensity of the canicular period and negative contributions resulting in lower k-values. The first year of study, which was the driest in terms of annual precipitation, presented a gentle midsummer drought and the highest k (the only one above one) among years. In contrast, k decreased strongly in the third year, which—although having the greatest annual precipitation—had the most severe canicular period. These results suggest that this species resists reductions in annual precipitation but not during the rainy season, maybe because it is the time when growth and recruitment occurs (Drezner, 2005; Dubrovsky et al., 1998). Actually, the growth and reproduction contributions in the third year were strongly negative. The categories 0 and 4 were the ones most affected by the severe canicular period of 2004. Because of their low water-storage capacity, seedlings are very susceptible to drought (Godínez-Álvarez et al., 2003; Jiménez-Sierra et al., 2007; Valiente-Banuet and Ezcurra, 1991). Germination takes place at the beginning of the rainy season (May–June), so survival becomes difficult during harsh canicular periods in July–August (Briones et al., 1998). On the other hand, high predation rates of adults by lagomorphs were observed in the third year, maybe because cacti represent a water source. Predation of adults was greater in the more disturbed site and caused a larger (although only marginally significant, as evinced by the site  year interaction) fall in k. This suggests that there is a synergism between the canicular period intensity and disturbance as it occurs in the succulent E. longissima (Martorell, 2007). Instead, it was harder to find a pattern response of M. hernandezii to canicular period. There was only a significant interaction between year 3 and site, indicating that in this year the population in the less disturbed site showed relatively better performance compared to the one in the more disturbed site (see the positive contributions in Fig. 3h and s). This may suggest a moderate synergism between harsh midsummer droughts and disturbance as in M. dixanthocentron and E. longissima (Martorell, 2007), but the pattern is not completely clear from the data and was not observed in the exclosure  year interaction. 4.3. Implications for management It is important to mention that, while we have replicates for the exclosure treatment, logistic restrictions precluded replication for the site, as the two portions (fenced and exposed) of each site are not completely independent. Thus, differences in population growth rates among sites may be confounded with other factors. Besides, the techniques required for statistical analysis of k in nested designs such as this one are yet unavailable. Therefore, management based on our conclusions for sites needs to be carefully monitored and corrected using tools such as adaptive management. In terms of the species’ response to CAD, it is clear that there are large differences between species. For instance, small plants made large negative contributions in M. hernandezii, but were relatively

1999

irrelevant in M. dixanthocentron. Even when the same categories or processes were affected similarly by CAD in both species, the management options may be very different. Prospective perturbation analysis (sensitivity matrices) suggests almost the same conservation strategy for both species, promoting the stasis of plants in categories 2–4 and in M. hernandezii also promoting growth of category 3. Nevertheless, the way to achieve this seems to be different in each species. To increase the population growth rate for M. dixanthocentron, it is crucial to reduce cattle and goat grazing. However, excluding livestock may be insufficient to achieve an increase in the more disturbed sites, as the predation by lagomorphs seems to have a large impact on this cactus, and thus excluding them may be required. Maybe the reforestation of anthropic grasslands close to forests where M. dixanthocentron grows may reduce the impact of hares. For M. hernandezii it seems possible to maintain a higher, but still moderate, intensity of productive activities. However, the intensity of human activities in the area seems difficult to control or monitor. A possible solution is to set a rotation system in which M. hernandezii´s populations are protected with fences for some years and then exposed to livestock. To set the appropriate fencing periods it is necessary to evaluate experimentally the negative impact of the interspecific competition in preserved conditions. Assessing the CAD intensity that increases soil aridity and sets on erosion and silting that seem responsible for reductions in k will set the amount of time that populations can be exposed to disturbance. For both species it would be of paramount importance to continue with this study for more years. This would help to average out the effects the temporal variability and clarify those of CAD. Also, given the importance of temporal variability, it would be relevant to understand how climate change may affect cacti if the canicular periods become harsher, or if meteorological variability increases (Boyce et al., 2006; IPCC, 2008). Under changing climatic conditions CAD should be kept below those intensities in which the populations are able to abate the effect of temporal variability. 4.4. The use of retrospective analysis in conservation biology In the case of these Mammillaria species, prospective and retrospective analysis suggested different management options. For example, even though M. hernandezii presented small sensitivity values for reproduction, this process made large negative contributions in both the disturbed site and the exposed areas. Basing management plans only on prospective methods would not take into account reproduction and promote survival of older plants, which would eventually result in a population dominated by old individuals and thus to the loss of genotypic variability and the reduction of effective population size (Balloux et al., 2003; Martorell, 2007; Rossetto et al., 1995). Using information obtained from both prospective and retrospective methods may help us to avoid the loss of relevant information. Retrospective perturbation analysis has been proposed as a useful tool in conservation because it detects stages in the life cycle that are prone to manipulation (Ehrlén and Van Groenendael, 1998) and allows for an assessment of how anthropic influence affects a population in order to restore its dynamics while increasing k (Martorell, 2007). Nevertheless, management based on this method may fail to produce the largest increases in population growth rate (Caswell, 2000), which may be the main objective when designing conservation strategies for critically endangered species. In this work we have emphasised other assets of retrospective analysis when it is used to assess the impacts of any factor that poses a threat for a species. This method may direct conserva-

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tion-oriented research, because it detects which vital rates or individuals are responsible for population decline, it allows us to establish hypotheses on the mechanisms of that declination. These hypotheses might later be studied in more detail to achieve a better understanding or to prove them experimentally. For instance, in the case of M. dixanthocentron we observed that the greatest reductions in k could be more closely linked with lagomorphs rather than with other impacts such as trampling; future research may include hare exclusions in order to measure their impact on k experimentally. In M. hernandezii further research should focus on competition with other species and on the impacts of disturbance on soil attributes. When proposing management plans, these hypotheses should be taken carefully as long as they are not properly tested. However, they may provide timely information. Postponing management recommendations until the most robust and detailed information is available may keep our hands out of the problem for many invaluable years. Retrospective analysis may lead a combined action plan in which some conservation measures are applied as early as possible and research is conducted simultaneously in order to improve them. Acknowledgements We are grateful to Adrián Quintero, Bianca Santini, David Ramírez and Andrea Martínez-Ballesté who helped us in the fieldwork, and to José Llanos at the Servicio Meteorológico Nacional who provided us the meteorological data for the study period. Agradecemos a la comunidad de Concepción Buenavista por su invaluable apoyo y entusiasmo para conservar las plantas de su pueblo. This research was funded by Fondo Mexicano para la Conservación de la Naturaleza A.C., Project A1-00-054, and by Semarnat-CONACyT Project 2002-C01-059. References Anderson, E.F., 2001. The Cactus Family. Portland, Oregon USA. Arias-Montes, S., 1993. Cactaceae: conservation and diversity in Mexico. Revista de la Sociedad Mexicana de Historia Natural 44, 109–115. Arias-Montes, S., Gama-López, S., Guzmán-Cruz, L.U., 1997. Flora del Valle de Tehuacán-Cuicatlán. Cactaceae A.L. Juss, México, DF. Balloux, F., Lehmann, L., de Meenus, T., 2003. The population genetics of clonal and partially clonal diploids. Genetics 127, 429–437. Boyce, M.S., Haridas, C.V., Lee, C.T., 2006. Demography in an increasingly variable world. Trends in Ecology and Evolution 21, 141–148. Brandon, K., Gorenflo, L.J., Rodrigues, A.S.L., Waller, R.W., 2005. Reconciling biodiversity conservation, people, protected areas, and agricultural suitability in Mexico. World Development 33, 1403–1418. Briones, O., Montaña, C., Ezcurra, E., 1996. Competition between three Chihuahuan Desert species: evidence from plant size-distance relations and root distribution. Journal of Vegetation Science 7, 453–460. Briones, O., Montaña, C., Ezcurra, E., 1998. Competition intensity as a function of resource availability in a semiarid ecosystem. Oecologia 116, 365–372. Caswell, H., 1997. Methods of matrix population analyses. In: Tuljapurkar, S., Caswell, H. (Eds.), Structured-Population Models in Marine, Terrestrial, and Freshwater Systems. Chapman and Hall, New York, pp. 19–58. Caswell, H., 2000. Prospective and retrospective perturbation analyses: their roles in conservation biology. Ecology 81, 619–627. Caswell, H., 2001. Matrix Population Models: Construction, Analysis and Interpretation. Sunderland, Massachusetts, USA. Cuaron, A.D., 2000. A global perspective on habitat disturbance and tropical rainforest mammals. Conservation Biology 14, 1574–1579. De Kroon, H.A., Plaisier, J., Van Groenendael, H., Caswell, H., 1986. Elasticity: the relative contribution of demographic parameters to population growth rate. Ecology 67, 1427–1431. Dellasala, D., Williams, J., Williams, C., Franklins, J., 2004. Beyond smoke and mirrors: a synthesis of fire policy and science. Conservation Biology 18, 976– 980. Drezner, T.D., 2005. Saguaro (Carnegiae gigantae, Cactaceae) growth rate over its American range and the link to summer precipitation. The Southwestern Naturalist 50, 65–68. Dubrovsky, J.G., Contreras-Burciaga, L., Ivanov, V.B., 1998. Cell cycle duration in the root meristem of Sonoran Desert Cactaceae as estimated by cell-flow and rateof-cell-production methods. Annals of Botany Company 81, 619–624.

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