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Ecology |
Department of Biology, Florida International University, University Park, Miami, Florida 33199 USA
Received for publication November 22, 2002. Accepted for publication February 27, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: breeding system • buzz pollination • Chamaecrista keyensis • Fabaceae • Florida Keys • mosquito control • pesticide spray • pine rocklands • pollination • urban-wildland interface
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; DeMauro, 1993
; Weller, 1994
; Spira, 2001
). Such information may also provide insights into the vulnerability of a species (e.g., Bowlin et al., 1993
; Sipes and Tepedino, 1995
; Carlsen et al., 2002
).
Rarity and endangerment of a plant species may be due to intrinsic (related to the biology of the species) or extrinsic (related to environment) factors (Rabinowitz, 1981
; Fiedler and Ahouse, 1992
). While some extrinsic factors are natural, many others are caused by humans. Anthropogenic habitat fragmentation has been widely cited as a major threat to biodiversity (Simberloff, 1988
). As a result, many studies have evaluated the direct and indirect biotic effects of fragmentation (e.g., Shreeve and Mason, 1980
; Jennersten, 1988
; Aizen and Feinsinger, 1994a
). One of the many changes brought about by habitat fragmentation is increased edge habitat (Murcia, 1995
). Most edge-effect studies have dealt with edge habitats that were created by agricultural fields (Sork, 1983
; Murcia, 1995
; Kapos et al., 1997
; Fortin and Mauffette, 2001
; Tscharntke et al., 2002
). Yet, urban edges are increasingly common as a result of urban sprawl into natural areas. Effects of the urban matrix on natural populations and processes are likely different from those of an agricultural matrix, as effects of edge habitat vary depending on the degree of contrast between the forest and its surrounding matrix (Kapos et al., 1997
). An urban matrix dominated by roads, houses, and artificial gardens is different from agricultural fields in both abiotic and biotic components. Few studies, however, have compared the biology of plants in an urban-edge habitat with those in a pristine habitat.
Another threat to natural populations and processes that comes from agricultural and urban development is the use of pesticides. Aerial pesticides on crop and forestry fields have been shown to negatively affect pollinator populations (Johansen, 1977
; Johansen et al., 1983
; Kearns and Inouye, 1997
; Spira, 2001
). Aerial insecticide spraying that coincides with the flowering of endangered entomophilous species threatens the continued existence of those species (Bowlin et al., 1993
; Sipes and Tepedino, 1995
). Pesticide spray is also used in urban areas to control mosquitos. Despite concerns about the use of mosquito spraying on natural insect populations, these effects on plant species are seldom examined.
Chamaecrista keyensis Pennell (Fabaceae), big pine partridge pea, is a narrowly endemic understory herb of pine rocklands, a fire-dependent ecosystem of the Lower Florida Keys. This species was formerly found on several of the Lower Keys (No Name, Big Pine, and Ramrod Keys [Irwin and Barneby, 1982
]). However, a more recent survey by Ross and Ruiz (1996)
found it only on Big Pine Key, indicating the extirpation of this species from parts of its former range. The most prominent threats to this species include habitat loss and degradation, especially long-term fire exclusion (Snyder et al., 1990
). Although not yet recognized by the U.S. Fish and Wildlife Service (USFWS) as an endangered species, C. keyensis has been recommended for federal listing and is currently listed by the state of Florida (Florida Natural Areas Inventory, 2002
).
Big Pine Key has the largest pine rockland forest of the Lower Florida Keys (Ross and Ruiz, 1996
) and many urban/wildland interface issues. Roads and residential and commercial buildings fragment the once continuous forest on the island. The many parcels of private property within the National Key Deer Refuge, a major site for C. keyensis, also provide many challenges for wildland managers. Peak mosquito season overlaps the flowering peak (June–July) of C. keyensis, and mosquito control includes aerial (1,2-dibromo-2,2-dichloroethyl dimethyl phosphate) and ground [Permethrin (3-phenoxyphenyl) methyl (±) cis, trans-3-(2,2-dichlorethenyl)-2,2-dimethyl-cyclopropanecarboxylate and piperonyl butoxide)] sprayings throughout the island during the summer, even though most of the pine forest is federal property. Mosquito-control agents are sprayed in response to monitoring and resident complaints on no fixed schedule, but sometimes as often as daily.
Our goals in this research were twofold: to elucidate the breeding system and pollinators of C. keyensis and to assess the effects of urban wildland interface on the reproductive biology of C. keyensis. Specifically, we address the following questions: (1) Is C. keyensis self-compatible? (2) Is there inbreeding depression with self-pollination? (3) Does C. keyensis depend on insect pollinators for sexual reproduction? (4) Which insect species are effective pollinators? (5) Are there differences in pollinator visitation and fruit and seed set between forest and urban-edge populations? (6) What is the effect of aerial mosquito control on the pollination biology of C. keyensis?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Because access to the pollen is severely limited by the small terminal pores, pollination of poricidal flowers usually rely on bees that can carry out "buzz pollination" (Buchmann, 1978
). Buzz pollination refers to a bee shivering its indirect flight muscles to generate a specific frequency of vibration that effectively releases the pollen for collection (Buchmann, 1978
). Pollination of C. keyensis is therefore expected to be insect dependent.
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). Habitat destruction, fragmentation, and degradation (i.e., long-term fire exclusion) have made pine rocklands a globally endangered ecosystem (Snyder et al., 1990
). Pine rocklands on Big Pine Key, the only home of C. keyensis, is also an important habitat for the federally endangered key deer. The canopy of pine rocklands is monotypic, composed of slash pine (Pinus elliottii var. densa). The relatively open canopy allows the growth of a diverse shrub and herb layer, with many rare and endemic species (Alexander and Dickson, 1972
). The 665 ha of pine rocklands on Big Pine Key is fragmented into many tracts by roads, houses, and firelanes. Our breeding system study was carried out at two sites, Orchid and Loma Lane. Orchid represents "pristine" pine rocklands located at the northeast end of Big Pine Key in a relatively large (20 ha) continuous piece of pineland (the forest population). This area has burned at various intervals (7–10 yr) during the last two decades; prior to that, its fire history is uncertain. Loma Lane represents degraded pine rocklands in the southwest part of Big Pine Key, adjacent to roads and homes, mowed occasionally and managed by homeowners (the urban-edge population). Pollinator watches were conducted throughout the island, including the Orchid and Loma Lane sites.
Breeding system
To determine the breeding system of C. keyensis, we performed controlled hand-pollination experiments (Kearns and Inouye, 1993
) on plants in their natural environments using five treatments: autogamy (automatic self-pollination), self-pollination, cross-pollination, pollen supplement, and control (Table 1). We did not include emasculation (removal of anthers) to test apomixis because it is difficult to remove all the anthers without damaging the ovary of the flower. We bagged the flowers with fine mesh cloth bags in the early morning, prior to any insect visits and as flowers were just opening. In this way we prevented flower deformation and unwanted insect visits. Hand pollinations began after 0800, when anthers released pollen with tapping (see later). A flower was self-pollinated by applying pollen from another flower of the same plant and then bagging it until dusk to prevent additional pollen deposition by insects. Similarly, a flower was cross-pollinated by applying pollen collected that same morning from one or more plants at least 10 m away. The pollen-supplement (pollen +) treatment was performed by applying pollen from another plant but without bagging the treated flower afterwards (Table 1). This treatment was to test the existence of pollen limitation. For the control treatment, we did nothing to the flower to allow for natural pollination.
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Seed germination
Replicates of 10 seeds from each different pollination treatment (with sites and plants pooled) were used to test seed germination. Seeds were nicked to break seed dormancy and then put in petri dishes with moist filter paper. Seeds with any radicle or cotyledon growth were considered germinated. Percentage germination was compared across treatments with all sites combined.
Floral visitors
We carried out 10-min floral visitor watches at arbitrarily selected patches of C. keyensis at four forest sites (Orchid, Dogwood, Locustberry, and Buttonwood) and two urban-edge sites (Loma Lane and Wilder Road). From preliminary observations, on sunny days, floral visits start around 0800 and peak between 0900 and 1000, then taper off after 1100. We carried out the watches from 0800 to 1200 on sunny days for two consecutive weeks in early July, when aerial mosquito spraying (adulticide) had just started for the season. The number of visits by different insects and the number of flowers of each watched patch were recorded during the watches. Insect behavior on a flower, such as buzz pollination, was noted. Samples of flower visitors were collected for determination. The captured insects were sampled for pollen types by touching fuchsin gel to the insect's body. The gel was then melted onto a slide for examination under a microscope. Dates of aerial mosquito spraying during the floral visitor watches were recorded and confirmed with the Lower Keys Mosquito Control Unit.
Statistical analysis
We used chi-square tests to assess the differences in fruit set (proportion of flowers that developed fruits) and percentage fruit with insect predation between sites and among treatments. Individual plants subjected to pollination treatments cannot be used as replicates for the described variables because of the small number of flowers available for each treatment per plant. Two-way ANOVA was used to test the effect of site, treatment, and their interaction on seed set (number of seeds per fruit). However, because the error variances were significantly different (Levene's test, F7,195 = 3.933, P < 0.001), we also used nonparametric tests (Mann-Whitney U and Kruskal-Wallis) to verify and report the differences between sites and among and between treatments in seed set (post-hoc tests). We used nonparametric tests to determine the differences in percentage seed germination among and between treatments because no transformation could improve the data for parametric assumptions. Mann-Whitney U tests were used to test the differences in the number of visitors per watch per flower between forest vs. urban-edge sites. We used SPSS 10.0 (SPSS, Chicago, Illinois, USA) for these tests.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2 = 0.845, df = 1, P = 0.358). Similar results were found between sites for all treatments (2 = 2.088, 0.083, 0.838, 1.430, df = 1; P = 0.148, 0.773, 0.360, 0.232, for control, selfed, crossed, and pollen-supplement treatments, respectively) (Fig. 2). All flowers in the autogamy treatment aborted except for one, the bag of which was removed from the flower by an unknown agent (we suspect a key deer) and was excluded from the analysis. Because there was not a significant site difference, we analyzed the differences among and between treatments with sites pooled. There were significant differences among the treatments, with (Pearson 2 = 100.932, df = 4, P < 0.001) or without the autogamy treatment (Pearson 2 = 10.779, df = 3, P = 0.013) (Fig. 2). The control treatment yielded significantly fewer fruit than the selfed (Pearson 2 = 5.027, df = 1, P = 0.025), crossed (Pearson 2 = 7.819, df = 1, P = 0.05), and pollen-supplement treatments (Pearson 2 = 5.195, df = 1, P = 0.023).
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2 = 89.825, df = 1, P < 0.001). However, there was no significant difference in seed predation among the four pollination treatments that produced fruits (66.7%, 62.5%, 77.8%, and 50% for control, selfed, crossed, and pollen-supplement treatments, respectively, Pearson 2 = 0.810, df = 3, P = 0.847).
Seed germination
Percentage germination differed significantly among seeds produced by different pollination treatments (Kruskal-Wallis 2 = 19.044, df = 3, P < 0.001). Significantly fewer selfed seeds germinated than in the three other treatments (Fig. 4).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Although capable of selfing and probably doing so under natural conditions as suggested by the seed set data, C. keyensis suffers a certain degree of inbreeding depression, as self-pollination resulted in the lowest seed set and percentage germination of all treatments. Inbreeding depression may negatively affect plant demography and thus pose a threat to the conservation of endangered species (Menges, 1991
; Burgman and Lamont, 1992
; Oostermeijer, 2001
). Only inbreeding depression of the very earliest parts of the life cycle was measured in this study. Because the expression of inbreeding depression may vary across a plant's life cycle (Schemske, 1983
; Husband and Schemske, 1996
), more research is needed to quantify the extent of inbreeding depression of C. keyensis throughout its life cycle.
Although there was no difference in fruit set between Loma Lane (urban edge) and Orchid (forest) populations, Loma Lane had significantly lower seed set across all treatments (autogamy treatment excluded). This lower seed set was due to higher insect predation of seeds. We were unable to rear or determine the identity of two species whose larvae and pupae were found in many pods. We cannot make the generalized conclusion that urban-edge populations have lower seed set and higher insect seed predation than forest populations because of our limited quantitative data (the lack of replicate sites for each type of habitat). However, our results from two sites verified field observations that C. keyensis individuals at the urban edge suffer higher seed predation by insects than those inside the forest.
Reduced seed production has been documented in many fragmented plant populations from reduced pollinator services (Jennersten, 1988
; Rathcke and Jules, 1993
; Aizen and Feinsinger, 1994a
; Kearns and Inouye, 1997
; Kearns et al., 1998
; Steffan-Dewenter and Tscharntke, 1999
; Spira, 2001
). In this study, however, the effects of the urban edge on pollinator services were mixed. While the urban-edge habitat had a significantly higher frequency of X. micans (buzz-pollinating bees), it had fewer (but not statistically significant) visits by Melissodes spp. (also buzz-pollinating bees) and by all bees pooled. Thus, the overall effect of urban edge on pollination and seed production of C. keyensis is unclear. Increased visitation frequency by certain bees such as honey bees associated with fragmented habitats has been documented in other studies (Aizen and Feinsinger, 1994b
).
Increased herbivory associated with habitat fragmentation has also been shown in many studies and is often attributed to small-area or isolation effects (Kruess and Tscharntke, 1994
, 2000
; Lienert et al., 2002
). However, results of edge effects on herbivory are mixed (Sork, 1983
; Fortin and Mauffette, 2001
; Tscharntke et al., 2002
). The increased herbivory has been attributed to reduced parasitism in fragments (Kruess and Tscharntke, 1994
), increased nutrient influx in small sites (Lienert et al., 2002
), and enhanced nutritional quality of edge foliage (Fortin and Mauffette, 2001
). For C. keyensis, increased seed predation may be due to lack of fire, as habitat near the urban edge is rarely burned. More study is needed to understand the mechanism of increased insect seed predation of C. keyensis associated with the urban edge.
Pollinators and the effects of aerial mosquito spraying
Percentage fruit set of the open-pollinated treatment was lower than the three hand-pollinated treatments (selfing, crossing, and pollen supplement) at both sites, suggesting that fruit production in natural populations of C. keyensis was pollen/pollinator limited. Pollinator limitation is widespread in natural plant populations (Bierzychudek, 1981
) and may be due to natural factors such as stochasticity in flower visits by insects, low insect numbers, or low floral rewards (Burd, 1994
; Johnson and Bond, 1997
).
Pollinator limitation in C. keyensis may also be due to natural causes. While many species of bees visit C. keyensis flowers, only three (Xylocopa micans and two Melissodes spp.) are capable of buzz pollination. Visits from the buzz pollinators constituted only 50% of the total flower visits. The floral morphology of C. keyensis (poricidal anthers and stigma held well above the anthers; Fig. 6) calls for buzz pollination behavior of the bees for effective pollination. The relatively large size of the flowers limits the range of bee sizes that can transfer pollen to the stigmas. The relatively low number of available bee species that are capable of buzzing in C. keyensis habitat may contribute to pollinator limitation. In addition, although the most abundant type of pollen carried by C. keyensis visitors was that of C. keyensis, all C. keyensis visitors, especially Megachile spp. (the most frequent, but nonbuzzing, bees) carried pollen of several other plant species. The lack of fidelity may also reduce the pollination efficiency of the pollinators and may even lead to stigma clogging by foreign pollen (Waser, 1978a
, b
), but this possibility has not yet been examined.
On the other hand, the pollinator limitation experienced by C. keyensis may, in part, be due to aerial mosquito control. Mosquito spray seems to have suppressed the number of visits by insects, especially Melissodes spp. and X. micans, the only buzz-pollinating bees. All these species are solitary bees. Solitary bees are more susceptible to insecticides than social bees because of the lower fecundity of the former (Tepedino, 1979
; Spira, 2001
). Even if aerial mosquito spray is not the primary cause, it may exacerbate existing pollinator limitation.
Less frequent aerial mosquito spraying (no more than once a week) may be more pollinator-friendly than the spray frequency (every second day) during this study. Nevertheless, caution should be taken in interpreting short-term observational data, such as these, as factors other than mosquito spray (e.g., weather and the intrinsic biology of the bees) could have influenced the activities and abundance of insects (Frankie et al., 1998
). Clearly, more research is needed to determine the effects of mosquito spray on C. keyensis pollinators and population dynamics.
We have provided evidence here that the endemic Big Pine partridge pea is self-compatible but requires insect visitation for pollination. Effective pollination can be performed by buzz-pollinating bees, though many kinds of bees collect pollen from their flowers. Plants may be pollinator limited, and urban-edge habitats have fewer bees visiting flowers (though X. micans, one of the buzz pollinators, is more common there) and lose more seed to insect predators. Bee numbers are depressed with aerial mosquito spraying (affecting both urban-edge and "pristine" woods habitats). Prevention of further fragmentation by limiting urban sprawl and more careful use of aerial insecticides are essential to maintain reproductive populations of this plant species.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Aizen M. A. P. Feinsinger 1994b Habitat fragmentation, native insect pollinators, and feral honey bees in Argentine Chaco Serrano. Ecological Applications 4: 378-392[CrossRef][ISI]
Alexander T. R. J. D. Dickson 1972 Vegetational changes in the National Key Deer Refuge. II. Quarterly Journal of the Florida Academy of Sciences 35: 85-96
Bierzychudek P. 1981 Pollination limitation of plant reproductive effort. American Naturalist 117: 838-840[CrossRef][ISI]
Bowlin W. R. V. J. Tepedino T. L. Griswold 1993 The reproductive biology of Eriogonum pelinophilum (Polygonaceae). In R. Sivinski and K. Lightfoot [eds.], Southwestern rare and endangered plants, 296–302. Miscellaneous publication No. 2. New Mexico Forestry and Resources Conservation Division, Santa Fe, New Mexico, USA
Buchmann S. L. 1978 Vibratile "buzz" pollination in angiosperms with poricidally dehiscent anthers. Ph.D. dissertation, Department of Entomology, University of California, Davis, California, USA
Buchmann S. L. 1983 Buzz pollination in angiosperms. In C. E. Jones and R. J. Little [eds.], Handbook of experimental pollination biology, 73–113. Scientific and Academic Editions. Van Nostrand Reinhold, New York, New York, USA
Burd M. 1994 Bateman's principal and plant reproduction: the role of pollen limitation in fruit and seed set. Botanical Review 60: 83-139[CrossRef][ISI]
Burgman M. A. B. B. Lamont 1992 A stochastic model for the viability of Banksia cuneata populations: environmental, demographic, and genetic effects. Journal of Applied Ecology 29: 719-727
Carlsen T. M. E. K. Espeland B. M. Pavlik 2002 Reproductive ecology and the persistence of an endangered plant. Biodiversity and Conservation 11: 1247-1268[CrossRef][ISI]
DeMauro M. M. 1993 Relationship of breeding system to rarity in the lakeside daisy (Hymenoxys acaulis var. glabra). Conservation Biology 7: 542-550[CrossRef][ISI]
Fiedler P. L. J. J. Ahouse 1992 Hierarchies and cause: toward an understanding of rarity in vascular plant species. In P. L. Fiedler and S. K. Jain [eds.], Conservation biology: the theory and practice of nature conservation, preservation and management, 23–47. Chapman & Hall, New York, New York, USA
Florida Natural Areas Inventory. 2002 . Http://www.fnai.org
Fortin M. Y. Mauffette 2001 Forest edge effects on the biological performance of the forest tent caterpillar (Lepidoptera: Lasiocampidae) in sugar maple stands. Ecoscience 8: 164-172[ISI]
Frankie G. W. R. W. Thorp L. E. Newstrom-Lloyd M. A. Rizzardi J. F. Barthell T. L. Griswold J. Y. Kim S. Kappagoda 1998 Monitoring solitary bees in modified wildland habitats: implications for bee ecology and conservation. Environmental Entomology 27: 1137-1148[ISI]
Hamrick J. L. M. J. W. Godt D. A. Murawski M. D. Loveless 1991 Correlations between species traits and allozyme diversity: implications for conservation biology. In D. A. Falk and K. E. Holsinger [eds.], Genetics and conservation of rare plants, 75–86. Oxford University Press, New York, New York, USA
Husband B. C. D. W. Schemske 1996 Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50: 54-70
Irwin H. S. R. C. Barneby 1982 The American Cassiinae, a synoptical revision of Leguminosae, tribe Cassieae, subtribe Cassiinae in the New World. Memoirs of the New York Botanical Garden 35: 1-918
Jennersten O. 1988 Pollination in Dianthus deltoides (Caryophyllaceae): effects of habitat fragmentation on visitation and seed set. Conservation Biology 2: 359-366
Johansen C. A. 1977 Pesticides and pollinators. Annual Review of Entomology 22: 177-192[CrossRef][ISI]
Johansen C. A. D. F. Mayer J. D. Eves C. W. Isious 1983 Pesticides and bees. Environmental Entomology 12: 1513-1518[ISI]
Johnson S. D. E. J. Bond 1997 Evidence for widespread pollen limitation of fruiting success in Cape wildflowers. Oecologia 109: 530-534[CrossRef][ISI]
Kapos V. E. Wandelli J. L. Camargo G. Ganade 1997 Edge-related changes in environment and plant responses due to forest fragmentation in central Amazonia. In W. F. Laurance and R. O. Bierregaard, Jr. [eds.], Tropical forest remnants, 33–44. University of Chicago Press, Chicago, Illinois, USA
Kearns C. A. D. W. Inouye 1993 Techniques for pollination biologists. University of Colorado Press, Niwot, Colorado, USA
Kearns C. A. D. W. Inouye 1997 Pollinators, flowering plants, and conservation biology—much remains to be learned about pollinators and plants. Bioscience 47: 297-307[CrossRef][ISI]
Kearns C. A. D. W. Inouye N. M. Waser 1998 Endangered mutualisms: the conservation of plant–pollinator interactions. Annual Review of Ecology and Systematics 29: 83-112[CrossRef][ISI]
Kruess A. T. Tscharntke 1994 Habitat fragmentation, species loss, and biological control. Science 264: 1581-1584
Kruess A. T. Tscharntke 2000 Species richness and parasitism in a fragmented landscape: experiments and field studies with insects on Vicia sepium. Oecologia 122: 129-137
Lienert J. M. Diemer B. Schmid 2002 Effects of habitat fragmentation on population structure and fitness components of the wetland specialist Swertia perennis L. (Gentianaceae). Basic and Applied Ecology 3: 101-114[CrossRef][ISI]
Menges E. S. 1991 Seed germination percentage increases with population size in a fragmented prairie species. Conservation Biology 5: 158-164[CrossRef][ISI]
Murcia C. 1995 Edge effects in fragmented forests: implications for conservation. Trends in Ecology and Evolution 10: 58-62
Oostermeijer J. G. B. 2001 Population viability analysis of the rare Gentiana pneumonanthe: importance of demography, genetics, and reproductive biology. In A. Young and G. Clark [eds.], Genetics, demography, and viability of fragmented population, 313–334. Cambridge University Press, Cambridge, UK
Rabinowitz D. 1981 Seven forms of rarity. In H. Synge [ed.], The biological aspects of rare plant conservation, 205–217. Wiley, New York, New York, USA
Rathcke B. E. S. Jules 1993 Habitat fragmentation and plant–pollinator interactions. Current Science 65: 273-277[ISI]
Ross M. S. P. Ruiz 1996 A study of the distribution of several South Florida endemic plants in the Florida Keys. Report to the U.S. Fish and Wildlife Service. Florida International University, Southeast Environmental Research Program, Miami, Florida, USA
Schemske D. W. 1983 Breeding system and habitat effects on fitness components in three neotropical Costus (Zingiberaceae). Evolution 37: 523-539[CrossRef][ISI]
Shreeve T. G. C. Mason 1980 The number of butterfly species in woodlands. Oecologia 45: 414-418[CrossRef][ISI]
Simberloff D. 1988 The contribution of population and community biology to conservation science. Annual Review of Ecology and Systematics 19: 473-511
Sipes S. D. V. J. Tepedino 1995 Reproductive biology of the rare orchid, Spiranthes diluvialis: breeding system, pollination, and implications for conservation. Conservation Biology 9: 929-938[CrossRef][ISI]
Snyder J. R. A. Herndon W. B. Robertson 1990 South Florida rockland. In R. L. Myers and J. J. Ewel [eds.], Ecosystems of Florida, 230–277. University of Central Florida Press, University Presses of Florida, Orlando, Florida, USA
Sork V. L. 1983 Distribution of pignut hickory (Carya glabra) along a forest to edge transect, and factors affecting seeding recruitment. Bulletin of the Torrey Botanical Club 110: 495-506
Spira T. P. 2001 Plant–pollinator interactions: a threatened mutualism with implications for the ecology and management of rare plants. Natural Areas Journal 21: 78-88
Steffan-Dewenter I. T. Tscharntke 1999 Effects of habitat isolation on pollinator communities and seed set. Oecologia 121: 432-440[CrossRef][ISI]
Tepedino V. J. 1979 The importance of bees and other insect pollinators in maintaining floral species composition. Great Basin Naturalist Memoirs 3: 139-150
Tscharntke T. I. Steffan-Dewenter A. Kruess C. Thies 2002 Contribution of small habitat fragments to conservation of insect communities of grassland-cropland landscapes. Ecological Applications 12: 354-363[ISI]
Waser N. M. 1978a Competition for hummingbird pollination and sequential flowering in two Colorado wildflowers. Ecology 59: 934-944[CrossRef][ISI]
Waser N. M. 1978b Interspecific pollen transfer and competition between co-occurring plant species. Oecologia 36: 223-236[CrossRef][ISI]
Weller S. G. 1994 The relationship of rarity to plant reproductive biology. In M. L. Bowles and C. J. Whelan [eds.], Restoration of endangered species, 90–117. Cambridge University Press, Cambridge, UK
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