Comparative demographic analysis of three Neobuxbaumia species (Cactaceae) with differing degree of rarity

In this study we use a demographic approach to analyse the differing abundance of three congeneric columnar cacti: Neobuxbaumia macrocephala (the rarest), Neobuxbaumia tetetzo (intermediate), and Neobuxbaumia mezcalaensis (the most common). Populations of these species were studied in the Tehuacan Valley (Central Mexico) over a 3-year period. We employed traditional models and life table response experiments (LTRE) to explore the association between particular demographic traits and the degree of rarity of each species. Most matrices showed population growth rate () values close to unity; the only exception was N. mezcalaensis in 2001–2002 (=1.091±0.088). In the three species the highest elasticity values corresponded to entries referring to the stasis of pre-reproductive plant and small adults. However, the LTRE indicated that most important differences in the values between years and species were associated with variation in fruit production and seedling recruitment. N. mezcalaensis yielded the highest mean due to its high fecundity in 2001–2002. This result suggests that the variation in demographic behaviour observed between species is sufficient to explain the higher abundance of N. mezcalaensis compared to the rare N. macrocephala. The high fecundity values and recruitment success observed in the former, even if they occur only seldom, may result in higher average values accounting for its high population densities.     

Demography of the columnar cactus Neobuxbaumia macrocephala: a comparative approach using population projection matrices

Neobuxbaumia macrocephala is a long-lived columnar cactus endemic to the Tehuacán-Cuicatlán Valley in south-central Mexico. This plant has a very restricted distribution and few recruitment events have been detected in its populations. In this study, we analyze the N. macrocephala demographic pattern using a projection matrix in order to determine the main limiting factors of this species. To accomplish this goal, we compare our results with those obtained for another species of the same genus, N. tetetzo. Considering that both species inhabit the same valley, we believe that this comparative study will offer insights into the main demographic limitations of N. macrocephala. Results showed that these species of columnar cacti have similar demographic patterns in which survival is the process with the highest relative contribution to λ, followed by growth and reproduction. Of all the life cycle stages, seeds and seedlings have the lowest survival probabilities due to a high mortality caused by seed predation and effects of direct solar radiation on germinated seeds. The estimated growth rates indicate that populations of these species of Neobuxbaumia are in a numerical equilibrium. With respect to reproduction, N. macrocephala produce a lower number of seeds per plant than N. tetetzo. This low level of sexual reproduction may decrease the probability of establishment of new individuals in N. macrocephala populations. It is suggested that pollen limitation and pre-dispersal seed predation could be some factors that limit the distribution and abundance of this columnar cactus. This revised version was published online in June 2006 with corrections to the Cover Date.     

Analysis of the factors that affect the distribution and abundance of three Neobuxbaumia species (Cactaceae) that differ in their degree of rarity

We studied three species of columnar cacti in the genus Neobuxbaumia which differ in their degree of rarity: Neobuxbaumia macrocephala (the rarest), Neobuxbaumia tetetzo (intermediate), and Neobuxbaumia mezcalaensis (the most common). To investigate the ecological factors that limit their distribution and abundance, we surveyed 80 localities within the region of Tehuacan-Cuicatlán, in Central Mexico. At each locality we measured several environmental variables, and the density of the Neobuxbaumia populations present. We used a principal component analysis (PCA) to identify the factors that are associated to the presence/absence of each species. Additionally, we carried out multiple regressions between environmental variables and population density to test whether the variation in these variables was related to changes in abundance. The results show that factors significantly affecting the distribution of these species are mean annual temperature, altitude, rainfall, and soil properties such as texture and organic matter content. N. mezcalaensis reaches maximum population densities of 14,740 plants per ha (average density = 3943 plants per ha) and is associated with localities with relatively abundant rainfall. N. tetetzo shows maximum population densities of 14,060 plants per ha (average = 3070 plants per ha), and is associated with sites located at high latitudes and with high phosphorous content in the soil. The rarest species, N. macrocephala, shows maximum densities of 1180 plants per ha (average = 607 plants per ha) and is associated with localities with high soil calcium content. The distribution of this species is limited to sites with specific values of the environmental variables recorded, conferring it a high habitat specificity which accounts for its rarity.     

Interaction between the cactus Neobuxbaumia tetetzo and the nurse shrub Mimosa luisana

Abstract. Pattern analysis and association analysis showed that recruitment of the giant columnar cactus Neobuxbaumia tetetzo in the semi-arid valley of Zapotitlán is largely limited to areas beneath the canopies of perennial shrubs, acting as nurse plants. Chi-square and Haberman tests revealed that young cacti were more frequently found beneath canopies of leguminous shrubs, especially Mimosa luisana, than were older cacti. Segregation analysis indicated a positive association (= negative segregation) of young cacti and M. luisana canopies, but older cacti were randomly distributed with respect to M. luisana. This, and the height class distributions of cacti associated withM luisana or not, suggested the replacement of M. luisana by N. tetetzo. Mimosa luisana plants in association withiV. tetetzo had greater amounts of dead basal area thanM luisana lacking associated N tetetzo. This suggested competition from JV. tetetzo promotes the replacement process. The roots of N tetetzo are ≤ 30 cm deep. Interception of soil water before penetration to deeper roots of M luisana may be the mode of competition between the two species.     

Spatial relationships between cacti and nurse shrubs in a semi-arid environment in central Mexico

Abstract. The Zapotitlán de las Salinas valley, central Mexico, harbours a high diversity of cacti. Pattern analysis indicated that the establishment of two columnar cacti, Neobuxbaumia tetetzo and Cephalocereus hoppenstedtii, and of three small globose cacti, Coryphantapallida, Mammillaria colina andM casoi, is aggregated and associated with perennial nurse shrubs. Some nurse species, Castela tortuosa, Caesalpinia melanadenia and Eupatorium spinosarum have a higher number of cacti beneath their canopies than would be expected by chance. A replacement pattern was found between the columnar cacti and their nurses, an aspect which was not found with the globose cacti. Following the assumption that protection against excessive radiation is the main factor determining the nurse effect, the azimuth orientation of the cacti with respect to their nurses was evaluated. Only Coryphanta pallida presented a non-random distribution with a tendency towards the North and West. The difference in maximum temperature between the soil surface under the different nurse species and of open spaces, which is reached at midday, was 16 °C. No significant differences were found in beneath-canopy temperatures for the three nurse species considered. Soil nitrogen levels were significantly lower beneath the different nurse plants than in open spaces. This result suggests that soil fertility is not an important factor in the nurse-plant phenomenon in Zapotitlán.     

The Diet and Reproductive Schedules of Leptonycteris curasoae curasoae and Glossophaga longirostris elongata (Chiroptera: Glossophaginae) on Curaçao

Two bat species, Leptonyrteris curasoae and Glossophaga longirostris, are the principal pollinators of at least two of the three species of columnar cacti that grow on the semiarid island of Curaçao, Netherlands Antilles. I examined the importance of the cacti in the diets of the bats and found that 85–91 percent of their diet samples contained cactus pollen and seeds. At least 43 percent of the samples from each species contained cactus pollen andlor seeds exclusively. Leptonycteris curasoae consumes nectar and pollen of Ceiba pentandra and Agave spp. at the beginning of the dry season and G. longirostris also consumes a few other plant products in the wet season, but both bat species depend nutritionally on cacti. Female bats give birth to one pup per year, and the periods of parturition and lactation in each species correspond to peaks in the reproductive phenology of the two most abundant columnar cactus species. From personal observations and a review of the literature, I determined that bats were unlikely to fly to the mainland to feed, although L. curasoae may do so. I conclude that the interdependence of bats and cacti is suggestive of coevolution, and that columnar cacti are critical for the survival and persistence of nectar-feeding bats on Curaçao.     

Resource availability, population dynamics and diet of the nectar-feeding bat Leptonycteris curasoae in Guaymas, Sonora, Mexico

Nectar-feeding bats play important roles in the pollination of columnar cacti. Migratory bats such as Leptonycteris curasoae are vulnerable to extinction due to their migratory behavior and cave-roosting habit. The conservation of migratory bats requires the identification and protection of key roosting sites and their floral resources. In this paper we describe the availability of resources, the population dynamics and the diet of L. curasoae in the Guaymas region, and its diet at three additional sites in coastal Sonora, Mexico. Our results indicate that L. curasoae is a seasonal resident in the Guaymas area, with local occupation of around 4 months. Seasonal occupation seems to be determined by the availability of flowers and fruits of columnar cacti as peak abundance and peak availability coincide in time. The analyses of fecal and fur samples revealed that columnar cacti constitute the major food source during their seasonal occupation of coastal Sonora. The frequency of pollen from Agave and Bombacaceae in fecal samples was generally low but increased in importance in lower latitudes. Our results suggest that the availability of resources provided by columnar cacti determine seasonal occupation of L. curasoae in Sonora. Given that we detected newborns in the studied colony, we suggest active cave protection for the conservation of the maternity roosting site in Guaymas, Sonora, Mexico.     

Effects of mixed-species pollen load on fruits,seeds, and seedlings of two sympatric columnar cactus species

Ecological Research - Two sympatric species of columnar cacti on Curaçao, Netherlands Antilles, share bat pollinators, overlap in flowering phenology, and are floral homologues. Leptonycteris...     

Comparative pollination biology of Venezuelan columnar cacti and the role of nectar-feeding bats in their sexual reproduction

The floral biology, reproductive system, and visitation behavior of pollinators of four species of columnar cacti, Stenocereus griseus, Pilosocereus moritzianus, Subpilocereus repandus, and Subpilocereus horrispinus, were studied in two arid zones in the north of Venezuela. Our results support the hypothesis that Venezuelan species of columnar cacti have evolved toward specialization on bat pollination. Additional information on the floral biology of a fifth species, Pilosocereus lanuginosus, was also included. All species showed the typical traits that characterize the pollination syndrome of chiropterophily. All species but Pilosocereus moritzianus were obligate outcrossers. Nectar and pollen were restricted to nocturnal floral visitors. Two species of nectar-feeding bats, Leptonycteris curasoae Miller and Glossophaga longirostris Miller, were responsible for practically all the fruit set in these cacti. Frequency of bat visitation per flower per night was highly variable within and between species of cactus, with average frequencies varying between 27 and 78 visits/flower/night. In general terms, the pattern of floral visitation through the night was significantly correlated with the pattern of nectar production and nectar sugar concentration for all species of cactus. Under natural pollination, fruit:flower ratios varied from 0.46 in Subpilocereus repandus to 0.76 in Stenocereus griseus. The efficiency of bat pollination in terms of seed:ovule ratio was high in all species, varying between 0.70 and 0.94.     

Impact of climate change on the distribution of populations of an endemic Mexican columnar cactus in the Tehuacán-Cuicatlán Valley,Mexico

In this paper, we present a bioclimatic approach to (1) differentiate populations of the endemic Mexican columnar cactus Neobuxbaumia tetetzo within the Tehuacán-Cuicatlán Valley and (2) evaluate, under two possible future scenarios (years 2050 and 2080), the effects of climate change on the total species distribution in this area, as well as on groups of populations defined by their bioclimatic models. Four population groups were identified, and principal component analysis showed that the variables that explained more than 40% of the climatic variation were precipitation of the wettest quarter and temperature seasonality. Bioclimatic models under the different scenarios indicated that when the overall species distribution was analyzed, this area will probably have contracted by 19.5% by the year 2050 and 47.05% by the year 2080, whereas the separate analysis of population groups projected area contractions of 18.4% by the year 2050 and 51.95% by the year 2080. These results demonstrate the importance of exploring new approaches for evaluating and predicting current and future distribution of plant species.     

Spatial Associations, Size–Distance Relationships and Population Structure of Two Dominant Life Forms in a Semiarid Enclave of the Venezuelan Andes

The role of three thorny legume species as nurse plants and competitive relationships with columnar cacti were evaluated in a semiarid enclave of the Venezuelan Andes. Abundance and size of three columnar cacti species (Stenocereus griseus, Cereus repandus and Pilosocereus tillianus) under isolated shrubs of three thorny legumes species (Prosopis juliflora, Acacia farnesiana and A. macracantha) were recorded and compared with open areas. Using size–distance data we inferred the intensity of intra- and interspecific competition between both life forms in a “cardonal” (xeric zone) and “espinar” (mesic zone) of the enclave. Sixty-one columnar cacti were found beneath the three thorny legume species (92%), while only 5 cactus individuals were found in open areas (8%). Comparison of observed and expected number of cactus individuals shows that S. griseus and C. repandus are significantly associated with isolated shrubs of A. farnesiana and A. macracantha. Although P. juliflora contributed more than 40% of the total legume plant cover, the number of columnar cacti under its isolated shrubs was significantly lower than would be expected by chance. In all, 19 of 21 possible plant–plant combinations between and within columnar cacti and legume shrubs were recorded (espinar: 18, cardonal: 13, common combinations: 12). In both zones, intra- and interspecific combinations among columnar cacti species were relatively high (positive correlation between the sum of neighbour plant sizes and the distances separating them). Our results strongly suggest, at least for case of S. griseus and C. repandus, that these columnar cacti species require nurse plants for their establishment. The results on interference need still support from further research. We discuss the effects of plant–plant positive interactions on natural regeneration of these columnar cacti.     

Digestibility of columnar cacti pollen grains in the glosophagine bats Glossophaga longirostris and Leptonycteris curasoae (Chiroptera: Phyllostomidae)

We examined the protoplasmic assimilation of columnar cacti pollen grains in two species of Venezuelan desert glosophagine bats, Glossophaga longirostris and Leptonycteris curasoae, by determining the amount of empty (digested) pollen grains found in their fecal samples. To determine the amount of empty pollen grains, the fecal samples were stained to differ between empty and full (non-digested) pollen grains. The number of empty and full pollen grains observed in the fecal samples were corrected using the amount of aborted pollens present (before anthesis) in flowers of the columnar cacti species (Subpilocereus repandus, Stenocereus griseus and Pilosocereus tillianus) used by bats as food in the study site; G. longirostris and L. curasoae digested 64.2% and 71.3% of all the pollens fed, respectively. These high values confirm the importance of pollen in the diet of these bats, given its high nitrogen level.     

Seasonal changes in the diets of migrant and non-migrant nectarivorous bats as revealed by carbon stable isotope analysis

Three species of nectar-feeding bats migrate from tropical and subtropical Mexico into the Sonoran and Chihuahuan deserts during the spring and summer months. We examined geographic and seasonal changes in the diet of one migrant species, Leptonycteris curasoae, using carbon stable isotope techniques to determine the relative importance of C3 and CAM (Cactaceae, Agavaceae) plants in its diet. We also examined the diet of a non-migratory nectar-feeding bat, Glossophaga soricina, from southern Mexico using the same techniques. We found that L. curasoae feeds extensively or exclusively on CAM plants during migration and in the northern part of its range and feeds mostly on C3 plants in southern Mexico. This bat is a year-round resident on Baja California where it is a CAM specialist. The non-migrant G. soricina feeds mostly on C3 plants year-round. Phenological data suggest that certain species of columnar cacti and at least one group of paniculate Agaves on the Mexican mainland provide a spatio-temporally predictable nectar corridor along which nectarivorous bats may migrate in the spring and fall, respectively. Different flowering schedules of Agaves in Baja California appear to promote year-round dietary specialization and perhaps non-migratory behavior in nectar-feeding bats living there.     

Reproductive biology of Oreocereus fossulatus (Cactaceae), a long‐lived columnar cactus endemic to the tropical Andes

The geographic dichotomy hypothesis suggests that columnar cacti inhabiting the tropics depend on flower visitors (birds and bats) for their pollination, showing highly specialized animal‐pollinated systems. This pattern has been demonstrated for the northern hemisphere; however, our knowledge of the species of columnar cacti growing in the southern tropics is still scarce. In this study, we studied the reproductive biology of Oreocereus fossulatus (Cactaceae, Tribe Trichocereae), an endemic, columnar cactus of the tropical Andes, to determine if its pollination system tends to be more generalized (mixed systems of autogamy and xenogamy) than specialized (xenogamy) as a consequence of the geographic position of where it lives. Observations of the frequency of visits showed that Patagona gigas (Trochillidae) is its main pollinator. It visits the flowers when they are open, coinciding with the periods of greater floral reward (dusk and dawn of the first day of anthesis). The treatments of autogamy, xenogamy and geitonogamy produced fruits, showing that O. fossulatus exhibits a generalized pollination system, in the same way as its congeneric species O. celsianus, which is distributed farther south in the Prepuna biogeographical region. Our results suggest that species partially specializing in pollination by hummingbirds and, besides, capable of autopollination, could be common in the tropical and subtropical Andes, probably as a response to the unpredictable environments present in their ecosystems.     

Distribution and morphology of columnar cacti in tropical deciduous woodland,Jalisco, Mexico

The distribution and branching morphologies of four species of columnar cactus species in tropical deciduous woodland in Jalisco, western Mexico, are examined. Two species, Stenocereus marginatus and especially Pachycereus pecten-aboriginum, are taller and extend through the woodland canopy, and only these two species occupy habitats where the woodland vegetation is taller, on N- and NE-facing aspects where incident radiation levels are lowest. Two species, Stenocereus standleyi and Cephalocereus purpusii, are shorter, subcanopy species, and are more restricted to low-angle slopes and slopes with S- to W-aspects, where the woodland vegetation is shorter and more open, with a greater penetration of radiation into the vegetation. Branching morphology is affected by the vegetation cover in all species, but in different ways between the two taller and the two shorter species. Ecological segregation in these four species is achieved apparently by differences among the light regimes of subhabitats correlated to the morphology of the cacti. This contrasts to segregation in Sonoran Desert columnar cactus species, which segregate by different strategies of water uptake and utilization, and in columnar cacti in woodlands in Oaxaca further south in Mexico, where adult individuals are very similar in branching morphology, but the younger individuals differ in this respect and presumably become established in different sorts of light gaps.Nomenclature follows Gibson & Horak (1978).     

Pollination ecology of Stenocereus queretaroensis (Cactaceae), a chiropterophilous columnar cactus, in a tropical dry forest of Mexico

Flowers of columnar cacti are animal-pollinated, often displaying a chiropterophylic syndrome. This study examined if the columnar cactus Stenocereus queretaroensis, a tropical species endemic to western Mexico, is bat-pollinated, by studying its pollination biology and the foraging behavior of potential pollinators. Flowers were produced in winter through spring, peaking in April. Anthesis was nocturnal, and stigma and anther turgidity began around 2200 hours. Production of nectar secretion and highest sugar concentration and energy supply were nocturnal, peaking between 2200 and 2400 hours. Manual auto-pollination and exclusion experiments showed that self-pollination yielded no fruits, while nocturnal pollinators resulted in high fruit set and seed set compared to diurnal pollination treatments. The nectar-feeding bat Leptonycteris curasoae (Phyllostomidae) was the main nocturnal pollinator with the highest effective pollination. Peak bat visitation coincided with peaks in nectar production. The high abundance of L. curasoae throughout the 4-yr study, suggests that it is a seasonally reliable pollinator for this columnar cactus. While pollination syndromes have been increasingly called into question in recent years, this study suggests that at least for this system, there is a fairly close fit between pollinator and pollination syndrome.     

Pollination system of the Pilosocereus leucocephalus columnar cactus (tribe Cereeae) in eastern Mexico

It has been suggested that there is a geographic dichotomy in the pollination systems of chiropterophilous columnar cacti: in intra‐tropical areas they are pollinated almost exclusively by bats, whereas in extratropical areas they are pollinated by bats, birds and bees. However, currently the studies are clumped both taxonomically (mainly Pachycereeae species) and geographically (mainly in the Tehuacan Valley and the Sonoran Desert). This clumping limits the possibility of generalising the pattern to other regions or cactus tribes. Only four of the 36 chiropterophilous cacti in Pilosocereus have been studied. Despite the tropical distribution of two Pilosocereus species, bees account for 40–100% of their fruit set. We examined how specialised is the pollination system of P. leucocephalus in eastern Mexico. As we studied tropical populations, we expected a bat‐specialised pollination system. However, previous studies of Pilosocereus suggest that a generalised pollination system is also possible. We found that this cactus is mainly bat‐pollinated (bats account for 33–65% of fruit set); although to a lesser degree, diurnal visitors also caused some fruit set (7–15%). Diurnal visitors were more effective in populations containing honeybee hives. P. leucocephalus is partially self‐compatible (14–18% of fructification) but unable to set fruit without visitors. Despite the variation in pollination system, P. leucocephalus shows more affinity with other columnar cacti from tropical regions than with those from extratropical regions. Although we report here that a new species of tropical Pilosocereus is relatively bat‐specialised, this Cereeae genus is more flexible in its pollination system than the Pachycereeae genera.     

The influence of cactus size and previous infection on bird deposition of mistletoe seeds

Abstract Tristerix aphyllus (Loranthaceae) is a bird-dispersed mistletoe that infects several cactus species in central and north-central Chile. At Las Chinchillas National Reserve it parasitizes two species of columnar cacti (Echinopsis chilensis and Eulychnia acida) and its seeds are dispersed exclusively by the Chilean mockingbird Mimus thenca. The prevalence of T. aphyllus on cacti depended on host species and size. Echinopsis chilensis was parasitized at a higher, and E. acida at a lower, frequency than expected from their relative abundances. In both species, the incidence of T. aphyllus parasitism increased with cactus height. Birds perched and deposited seeds primarily on parasitized cacti, which resulted in an aggregated distribution of seeds. By preventing bird perching and thus reducing seed deposition, the long spines of E. chilensis and E. acida may help protect cacti against T. aphyllus infestation. However, the seeds of T. aphyllus produced a slow-growing radicle that reached up to 91 mm long in 43 days. Radicles of this length are unique among mistletoe species and may have evolved to overcome the barrier posed by cactus spines.     

Columnar cacti-shrub relationships in an Andean semiarid valley in western Venezuela

Spatial associations between columnar cacti and mimosoid shrubs were evaluated in an Andean semidesert enclave. An analysis on the capacity of other deciduous shrub species and medium-sized ephemeral plants to modify the spatial distribution of cacti was also included. The number of Stenocereus griseus (Haw.) F. Buxb., Cereus repandus (L.) Backeb. and Pilosocereus tillianus Gruber & Schaftzl that grow below the canopies of perennial plants were assessed and compared with open areas. Comparison of observed and expected number of cactus individuals shows a positive spatial association between S. griseus and Prosopis juliflora DC. Moreover, abundance of C. repandus and P. tillianus under the canopies of mimosoid shrubs were not statistically different from what was expected by chance. Positive spatial association between S. griseus and Capparis odoratissima Jacq., Cassia emarginata L., Cordia curassavica (Jacq.) Roem. & Schult., Croton rhamnifolius H.B.K. and Jatropha gossypifolia L. was also found. Evidence suggests that positive columnar cacti-shrub spatial association may occur either in the cactus thickets or in the thornscrubs. Due to the clumped distributions of S. griseus beneath P. juliflora and other perennial plants, we here postulate that S. griseus is the primary nursed columnar cactus of the enclave. The presence of cacti in open areas suggests that facilitation may be less important for establishment of columnar cacti species in this Andean semidesert landscape than in other temperate and tropical semiarid zones. We here discuss the importance of the nurse syndrome phenomenon for recruitment of S. griseus and for the conservation of this Andean semiarid environment.     

Specialization clines in the pollination systems of agaves (Agavaceae) and columnar cacti (Cactaceae): A phylogenetically controlled meta-analysis

The biogeography of plant-animal interactions is a novel topic on which many disciplines converge (e.g., reproductive biology, biogeography, and evolutionary biology). Narrative reviews have indicated that tropical columnar cacti and agaves have highly specialized pollination systems, while extratropical species have generalized systems. However, this dichotomy has never been quantitatively tested. We tested this hypothesis using traditional and phylogenetically informed meta-analysis. Three effect sizes were estimated from the literature: diurnal, nocturnal, and hand cross-pollination (an indicator of pollen limitation). Columnar cactus pollination systems ranged from purely bat-pollinated in the tropics to generalized pollination, with diurnal visitors as effective as nocturnal visitors in extratropical regions; even when phylogenetic relatedness among species is taken into account. Metaregressions identified a latitudinal increase in pollen limitation in columnar cacti, but this increase was not significant after correcting for phylogeny. The currently available data for agaves do not support any latitudinal trend. Nectar production of columnar cacti varied with latitude. Although this variation is positively correlated with pollination by diurnal visitors, it is influenced by phylogeny. The degree of specificity in the pollination systems of columnar cacti is heavily influenced by ecological factors and has a predictable geographic pattern.