Ted Fleming - Academia.edu (original) (raw)

Papers by Ted Fleming

Journal of Mammalogy, 2004

Annals of Botany, 2009

† Background Most tropical and subtropical plants are biotically pollinated, and insects are the ... more † Background Most tropical and subtropical plants are biotically pollinated, and insects are the major pollinators. A small but ecologically and economically important group of plants classified in 28 orders, 67 families and about 528 species of angiosperms are pollinated by nectar-feeding bats. From a phylogenetic perspective this is a derived pollination mode involving a relatively large and energetically expensive pollinator. Here its ecological and evolutionary consequences are explored. † Scope and Conclusions This review summarizes adaptations in bats and plants that facilitate this interaction and discusses the evolution of bat pollination from a plant phylogenetic perspective. Two families of bats contain specialized flower visitors, one in the Old World and one in the New World. Adaptation to pollination by bats has evolved independently many times from a variety of ancestral conditions, including insect-, bird-and non-volant mammal-pollination. Bat pollination predominates in very few families but is relatively common in certain angiosperm subfamilies and tribes. We propose that flower-visiting bats provide two important benefits to plants: they deposit large amounts of pollen and a variety of pollen genotypes on plant stigmas and, compared with many other pollinators, they are long-distance pollen dispersers. Bat pollination tends to occur in plants that occur in low densities and in lineages producing large flowers. In highly fragmented tropical habitats, nectar bats play an important role in maintaining the genetic continuity of plant populations and thus have considerable conservation value.

Oecologia, 1993

Three species of nectar-feeding bats migrate from tropical and subtropical Mexico into the Sonora... more 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.

Oecologia, 2002

Specialization of a plant on a particular pollinator may not evolve if co-pollinators are effecti... more Specialization of a plant on a particular pollinator may not evolve if co-pollinators are effective and abundant. This is particularly evident if fruit set is resource limited and cannot be increased above the levels produced by the actions of co-pollinators. The pollinating seed-consuming interaction between senita cacti and senita moths in the Sonoran Desert presents a paradox because it exhibits many traits resembling those of the highly specialized yucca/yucca moth system, but also involves co-pollinators. For 6 years, we studied how contributions of nocturnal senita moths and diurnal co-pollinating bees to fruit set depended on resource and pollen limitation, time of flower closing, and the onset and phenology of flowering. Fruit set was typically resource limited. Fruit set of flowers exposed only to senita moths was not different from resource-limited fruit set of control flowers. When only co-pollinating bees were allowed to visit flowers, however, fruit set became pollen limited. Only in one year when fruit set was pollen limited were bees able to increase fruit set beyond the level resulting from senita moth pollination. High temperatures commonly induced flowers to close before sunrise so that diurnal bees were unable to visit flowers. This was particularly important from 1998 to 2000, when flowering did not begin until late in spring when temperatures were already high enough to induce flowers to close before sunrise. Bees were typically functionally redundant with senita moths; excluding bees from visiting flowers did not alter fruit set. Nevertheless, extreme specialization of floral traits to exclude co-pollinators has not evolved in senita, possibly because there are times when bees do increase fruit set. This can occur when senita moths are rare, fruit set is pollen limited, cool temperatures prevent flowers from closing before sunrise, and flowering begins early in spring.

Journal of Biogeography, 2008

Aim We review several aspects of the structure of regional and local assemblages of nectar-feedin... more Aim We review several aspects of the structure of regional and local assemblages of nectar-feeding birds and bats and their relationships with food plants to determine the extent to which evolutionary convergence has or has not occurred in the New and Old World tropics.

Journal of Arid Environments, 2004

Columnar cacti in tropical deserts depend on nectar-feeding bats for their reproduction while spe... more Columnar cacti in tropical deserts depend on nectar-feeding bats for their reproduction while species from extra-tropical deserts show a relatively generalized pollination system with both nocturnal and diurnal pollinators. Pachycereus pecten-aboriginum is a columnar cactus with a broad distribution along the Pacific coast of M! exico, from Oaxaca to Sonora. Along its distribution, the nectar-feeding bat, Leptonycteris curasoae, changes from resident within the tropics to migratory in the Sonoran desert. If bat unpredictability has been an important force in the evolution of pollination systems in columnar cacti, P. pecten-aboriginum is expected to show a relatively generalized system in northern populations. We studied the pollination biology of P. pecten-aboriginum in two northern populations in the state of Sonora. Hand pollination experiments showed that this species has a self-incompatible, hermaphroditic breeding system. Although flowers open at night, they remain open and continue secreting nectar during the morning, allowing visitation by both nocturnal and diurnal pollinators. One population showed evidence of strong pollinator limitation while the results from both populations indicated that diurnal pollinators are more important than nocturnal pollinators. These results are discussed in terms of specialization vs. generalization in the pollination biology of columnar cacti in tropical and extra-tropical deserts.

Heredity, 2001

We examine seven geographically separate subpopulations of Heliconius charithonia, a butter¯y wit... more We examine seven geographically separate subpopulations of Heliconius charithonia, a butter¯y with well-documented home range behaviour, in Miami±Dade County, Florida, for genetic dierentiation using cellulose acetate electrophoresis. These subpopulations exhibit little genetic variation (percent polymorphic loci 27, average heterozygosity 0.103) especially in comparison to populations of the same and related species from mainland South America. Allele frequencies do not dier among the subpopulations in south Florida and estimates of Wright's ®xation index (F ST) support that there is no detectable genetic dierentiation among them. This result supports an earlier ®nding that the dispersal ability of Heliconius butter¯ies may be underestimated. However, it is unlikely that increased dispersal ability alone could account for the lack of genetic dierentiation observed among subpopulations separated by almost 80 km. Given the likely eective population size of these subpopulations (N e 205) and the average generation time of this species in the subtropics (in the range of 30±90 days), this lack of genetic dierentiation is best explained by current or very recent gene¯ow following a stepping-stone model. Furthermore, this result provides evidence that the current extensive degree of habitat fragmentation surrounding the city of Miami does not limit genē ow among urban subpopulations of Heliconius charithonia.

PLoS ONE, 2011

Observed patterns of genetic structure result from the interactions of demographic, physical, and... more Observed patterns of genetic structure result from the interactions of demographic, physical, and historical influences on gene flow. The particular strength of various factors in governing gene flow, however, may differ between species in biologically relevant ways. We investigated the role of demographic factors (population size and sex-biased dispersal) and physical features (geographic distance, island size and climatological winds) on patterns of genetic structure and gene flow for two lineages of Greater Antillean bats. We used microsatellite genetic data to estimate demographic characteristics, infer population genetic structure, and estimate gene flow among island populations of Erophylla sezekorni/E. bombifrons and Macrotus waterhousii (Chiroptera: Phyllostomidae). Using a landscape genetics approach, we asked if geographic distance, island size, or climatological winds mediate historical gene flow in this system. Samples from 13 islands spanning Erophylla's range clustered into five genetically distinct populations. Samples of M. waterhousii from eight islands represented eight genetically distinct populations. While we found evidence that a majority of historical gene flow between genetic populations was asymmetric for both lineages, we were not able to entirely rule out incomplete lineage sorting in generating this pattern. We found no evidence of contemporary gene flow except between two genetic populations of Erophylla. Both lineages exhibited significant isolation by geographic distance. Patterns of genetic structure and gene flow, however, were not explained by differences in relative effective population sizes, island area, sex-biased dispersal (tested only for Erophylla), or surface-level climatological winds. Gene flow among islands appears to be highly restricted, particularly for M. waterhousii, and we suggest that this species deserves increased taxonomic attention and conservation concern.

Oecologia, 1998

We report a new obligate pollination mutualism involving the senita cactus, Lophocereus schottii ... more We report a new obligate pollination mutualism involving the senita cactus, Lophocereus schottii (Cactaceae, Pachyceereae), and the senita moth, Upiga virescens (Pyralidae, Glaphyriinae) in the Sonoran Desert and discuss the evolution of specialized pollination mutualisms. L. schottii is a night-blooming, self-incompatible columnar cactus. Beginning at sunset, its¯owers are visited by U. virescens females, which collect pollen on specialized abdominal scales, actively deposit pollen on¯ower stigmas, and oviposit a single egg on a¯ower petal. Larvae spend 6 days eating ovules before exiting the fruit and pupating in a cactus branch. Hand-pollination and pollinator exclusion experiments at our study site near Bahia Kino, Sonora, Mexico, revealed that fruit set in L. schottii is likely to be resource limited. About 50% of hand-outcrossed and open-pollinated senita¯owers abort by day 6 after¯ower opening. Results of exclusion experiments indicated that senita moths accounted for 75% of open-pollinated fruit set in 1995 with two species of halictid bees accounting for the remaining fruit set. In 1996,¯owers usually closed before sunrise, and senita moths accounted for at least 90% of open-pollinated fruit set. The net outcome of the senita/senita moth interaction is mutualistic, with senita larvae destroying about 30% of the seeds resulting from pollination by senita moths. Comparison of the senita system with the yucca/yucca moth mutualism reveals many similarities, including reduced nectar production, active pollination, and limited seed destruction. The independent evolution of many of the same features in the two systems suggests that a common pathway exists for the evolution of these highly specialized pollination mutualisms. Nocturnal¯ower opening, self-incompatible breeding systems, and resource-limited fruit production appear to be important during this evolution. Key words Pollination á Sonoran Desert á Lophocereus schottii á Upiga virescens á Yucca/yucca moths Oecologia (1998) 114:368±375

Heredity, 1994

The mating system of the Mexican subdioecious columnar cactus, Pachycereus pringlei (Cardón), was... more The mating system of the Mexican subdioecious columnar cactus, Pachycereus pringlei (Cardón), was examined by allozyme analysis. Tetrasomic patterns of inheritance were found for all polymorphic loci, indicating that the species is an autotetraploid. A model is presented that expands Ritland's (1 990a) mixed mating model for autotetraploids to incorporate an arbitrary number of alleles per locus. This model is applied to the progeny arrays of several female and hermaphroditic individuals of P. pringlei. P. pringlei exhibited a complex breeding system; the multilocus estimate of outcrossing, tm, for female cacti was 0.949 and for hermaphrodites was 0.30 1. These results are discussed in the context of inbreeding depression and the evolution of the breeding system of this species.

Florida Entomologist, 2005

BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access t... more BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses.

Ecological Monographs, 2001

We studied variation in flowering phenology, fruit and seed set, and the abundance of the pollina... more We studied variation in flowering phenology, fruit and seed set, and the abundance of the pollinators of four species of night-blooming Sonoran Desert columnar cacti for up to eight years at one site in Mexico and one year at one site in Arizona. We determined how spatiotemporal variation in plant-pollinator interactions affects the evolution of generalized pollination systems. We conducted pollinator exclusion and hand pollination experiments to document annual variability in pollinator reliability and to determine whether pollination systems were redundant (different species are partially or totally substitutable) or complementary (different species have an additive effect on fruit set). The cacti we studied included three species with generalized pollination systems involving bats, birds, and bees (cardon, Pachycereus pringlei; saguaro, Carnegiea gigantea; and organ pipe, Stenocereus thurberi) and one specialized moth-pollinated species (senita, Lophocereus schottii). We predicted that the migratory lesser long-nosed bat, Leptonycteris curasoae, is a less reliable pollinator than birds and bees, and that cacti with generalized pollination systems have more variable flowering phenologies than the specialized species. Annual time of peak flowering and mean size of flower crops were relatively invariant in saguaro and organ pipe. Time of peak flowering in cardon varied by as much as six weeks, and mean flower crop size varied threefold over six years. In senita, peak flowering varied by as much as 5-8 wk among years. Peak numbers of the nectar bat L. curasoae varied among years, and bat density (0.9/ha) was an order of magnitude lower than that of cactus-visiting birds at both study sites. The abundance of migratory hummingbirds was also highly variable among years. Pollinator exclusion experiments indicated that bats were major pollinators of cardon, whereas diurnal visitors accounted for most fruit set in saguaro (except in 1995 when bats were most important) and organ pipe at our Mexican site; honeybees accounted for 64-87% of diurnal fruit set in these species. Annual variation in the contribution to fruit set by bats was substantially higher than that of diurnal pollinators in saguaro and organ pipe, but not in cardon. There was little geographic variation in the relative importance of nocturnal vs. diurnal pollinators in saguaro and senita, but bats were much more important for fruit set in organ pipe in Arizona than in Mexico. We generally detected no effect of different pollinators on number of seeds per fruit in any species. Annual variation in fruit set was lowest in saguaro, the species with the most diurnal pollination system, and highest in organ pipe, the species with the most generalized pollination system. Fruit set was strongly pollen limited only in females of cardon (a trioecious species) and in organ pipe (at both sites). The ''missing'' pollinators in both species are likely Leptonycteris bats. The pollination systems of saguaro and cardon were partially redundant, whereas that of organ pipe was complementary. The four species of cactus that we studied occur at the northern geographic limits of Mexican columnar cacti where many vertebrate pollinators are seasonal migrants. In the Sonoran Desert, variation in rainfall and spring temperatures affects timing of flowering and the extent of competition between cacti for pollinator visits and causes the relative importance of particular pollinators, especially Leptonycteris bats, for fruit set to vary annually. Under such conditions, selection has favored generalized pollination systems (as seen in organ pipe) or shifts from reliance primarily on nocturnal pollinators (as seen in cardon) to reliance primarily on diurnal pollinators (as seen in saguaro). Nonetheless, as exemplified by the senita-senita moth system, highly specialized pollination mutualisms can also evolve in this habitat in plants that rely on sedentary insects rather than migratory bats and birds for pollination.

Biological Reviews, 2007

Discussion of successional change has traditionally focused on plants. The role of animals in pro... more Discussion of successional change has traditionally focused on plants. The role of animals in producing and responding to successional change has received far less attention. Dispersal of plant propagules by animals is a fundamental part of successional change in the tropics. Here we review the role played by frugivorous bats in successional change in tropical forests. We explore the similarities and differences of this ecological service provided by New and Old World seed-dispersing bats and conclude with a discussion of their current economic and conservation implications. Our review suggests that frugivorous New World phyllostomid bats play a more important role in early plant succession than their Old World pteropodid counterparts. We propose that phyllostomid bats have shared a long evolutionary history with small-seeded early successional shrubs and treelets while pteropodid bats are principally dispersers of the seeds of later successional canopy fruits. When species of figs (Ficus) are involved in the early stages of primary succession (e.g. in the river meander system in Amazonia and on Krakatau, Indonesia), both groups of bats are important contributors of propagules. Because they disperse and sometimes pollinate canopy trees, pteropodid bats have a considerable impact on the economic value of Old World tropical forests; phyllostomid bats appear to make a more modest direct contribution to the economic value of New World tropical forests. Nonetheless, because they critically influence forest regeneration, phyllostomid bats make an important indirect contribution to the economic value of these forests. Overall, fruiteating bats play important roles in forest regeneration throughout the tropics, making their conservation highly desirable.

American Journal of Botany, 2003

We conducted allozyme surveys of three Venezuelan self-incompatible chiropterophilous columnar ca... more We conducted allozyme surveys of three Venezuelan self-incompatible chiropterophilous columnar cacti: two diploid species, Stenocereus griseus and Cereus repandus, and one tetraploid, Pilosocereus lanuginosus. The three cacti are pollinated by bats, and both bats and birds disperse seeds. Population sampling comprised two spatial scales: all Venezuelan arid zones (macrogeographic) and two arid regions in northwestern Venezuela (regional). Ten to 15 populations and 17-23 loci were analyzed per species. Estimates of genetic diversity were compared with those of other allozyme surveys in the Cactaceae to examine how bat-mediated gene dispersal affects the population genetic attributes of the three cacti. Genetic diversity was high for both diploid (P s ϭ 94.1-100, P p ϭ 56.7-72.3, H s ϭ 0.182-0.242, H p ϭ 0.161-0.205) and tetraploid (P s ϭ 93.1, P p ϭ 76.1, H s ϭ 0.274, H p ϭ 0.253) species. Within-population heterozygote deficit was detected in the three cacti at macrogeographic (F IS ϭ 0.145-0.182) and regional (F IS ϭ 0.057-0.174) levels. Low genetic differentiation was detected at both macrogeographic (G ST ϭ 0.043-0.126) and regional (G ST ϭ 0.009-0.061) levels for the three species, suggesting substantial gene flow among populations. Gene exchange among populations seems to be regulated by distance among populations. Our results support the hypothesis that bat-mediated gene dispersal confers high levels of genetic exchange among populations of the three columnar cacti, a process that enhances levels of genetic diversity within their populations.

Plant Systematics and Evolution, 1999

We studied seed germination and the growth and survivorship of seedlings of females and hermaphro... more We studied seed germination and the growth and survivorship of seedlings of females and hermaphrodites of Pachycereus pringlei (cardon), a Mexican columnar cactus whose geographically variable breeding system includes trioecy and gynodioecy. Results of a two-year field experiment conducted near Bahia Kino, Sonora, Mexico and a ten-month laboratory experiment were similar and did not support the hypothesis that seedlings of females outperform those of hermaphrodites. In the field, percent seed germination and 2-yr seedling survivorship averaged 66% and 95%, respectively and did not differ among six treatment classes. Seedlings of hermaphrodites generally were larger than those of females at the end of both experiments. Selfed seedlings of hermaphrodites did not grow more slowly than outcrossed seedlings of hermaphrodites or females. Hermaphrodite seedlings performed best when pollinated with hermaphrodite pollen; female seedlings performed best with male pollen. We conclude that superior seedling performance cannot explain why females are able to coexist with hermaphrodites in populations of this cactus. Instead, we postulate that greater annual seed production, which averaged 1.6 times higher in females than in hermaphrodites in two years, may be sufficient to allow females to co-occur with hermaphrodites in this large, longlived plant, especially if sex determination involves cytoplasmic-nuclear inheritance.

Oecologia, 1999

Interspecific interactions can vary within and among populations and geographic locations. This v... more Interspecific interactions can vary within and among populations and geographic locations. This variation can subsequently influence the evolution and coevolution of species interactions. We investigated population and geographic variation in traits important to pollinating seed-consuming interactions between the senita cactus (Lophocereus schottii) and its obligate pollinating moth (Upiga virescens), both of which are geographically restricted to the Sonoran Desert. Female moths actively pollinate senita flowers and oviposit onto flowers. Their larvae consume developing seeds and fruit of flowers pollinated by females. Traits important to this interaction include fruit set from moth pollination, fruit survivorship, and costs of fruit consumption by larvae. We studied these traits for five populations at two widely separated geographic locations. On average, 37% of flowers set fruit, 22% of flowers produced mature fruit, and larvae consumed 25% of immature fruit pollinated by female senita moths. Senita cactus and senita moth interactions were strongly mutualistic in all populations that we studied. Although one population had statistically lower fruit set and fruit production than the other four, all five populations were qualitatively similar in fruit production, costs, and patterns of fruit survivorship. Hand-pollination experiments suggested that fruit set was resource-limited in all but this one population. Apparent pollen limitation in the one population explains the quantitative differences in fruit set and fruit survivorship among the populations. As predicted by theory and exemplified by the senita mutualism, specialized and/or obligate interactions vary little among populations and geographic locations.

Journal of Mammalogy, 2002

The Mexican free-tailed bat (Tadarida brasiliensis mexicana) is primarily a nonhibernating, migra... more The Mexican free-tailed bat (Tadarida brasiliensis mexicana) is primarily a nonhibernating, migratory, spring-breeding subspecies. Our study considers the anatomical structure, function, and seasonal cyclicity of testes and accessory sex glands. Unlike temperate, hibernating, sperm-storing vespertilionid bats, Tadarida does not store sperm, and its spermatozoa differ from spermatozoa of species with prolonged sperm storage. Recrudescence of the male reproductive tract occurs in late winter and early spring. Mating behavior of males and function of secondary sex glands are in synchrony with an activation of the male reproductive tract (spermatogenesis). These events, which take place in the spring, during and immediately following northward migration, lead to insemination of estrogenic, receptive females.

American Zoologist, 1979

SYNOPSIS. In this paper I ask two questions: Is fruit ever limiting to vertebrate frugivores and,... more SYNOPSIS. In this paper I ask two questions: Is fruit ever limiting to vertebrate frugivores and, if so, do frugivores presently compete for food, either with closely-or distantly-related species? A brief review of the fruiting strategies of tropical plants indicates that fruit can occasionally be superabundant, but it is often produced at low rates and in low quantities. Variation in fruit abundance results from several biotic selective pressures, including variation in the density, diversity, and reliability of potential dispersal agents. To judge from the size structure, dietary similarities, habitat preferences and foraging behaviors of taxonomically-restricted guilds of frugivorous birds and mammals, members of these guilds have competed for food in the past and must occasionally do so today. Unusual climatic conditions can occasionally "upset" phenological patterns and can create food shortages that promote competition among closely-related species of frugivores. Avian and mammalian frugivores, however, probably seldom compete with each other for food in present-day tropical ecosystems. A major reason for this is that many tropical plants have evolved fruits that are attractive to only a limited subset of frugivores (e.g., only birds or only bats). Plants apparently "perceive" qualitative differences in the dispersal services of birds and mammals and attempt to attract members of one group but not the other.