BIOTROPICA 37(3): 357363 2005

10.1111/j.1744-7429.2005.00047.x

Pollination Biology of the Exotic Rattleweed Crotalaria retusa L. (Fabaceae) in NE Brazil1

Claudia M. Jacobi2 Departamento de Biologia Geral/ICB, Universidade Federal de Minas Gerais, Brazil Av. Antonio Carlos 6627, 31270-901 Belo Horizonte, MG, Brazil Mauro Ramalho and Maise Silva IBIO-Universidade Federal da Bahia, Brazil

ABSTRACT
The rattleweed Crotalaria retusa was introduced in Brazil from Africa, and combines a series of characters that have ensured its establishment in NE Brazil. We focused on its reproductive biology and pollinator behavior to explain its reproductive success. We performed manual pollination and germination experiments, and monitored the behavior of C. retusas main pollinators in monospecic plots, and in mixed plots where C. retusa occurred together with two congeners, Crotalaria pallida and Crotalaria lanceolata. Crotalaria retusa is self-compatible and capable of automatic selng. Inbreeding depression was expressed at the level of percent seed germination, but not seed set. Few insects visited the inorescences. Legitimate pollinators were two large carpenter bees, Xylocopa frontalis and Xylocopa grisescens which, together, accounted for more than 90 percent of the visits. The former foraged on C. retusa exclusively and has low pollen spread potential. The latter ew longer distances between plants and visited fewer owers per inorescence, potentially increasing the extent of pollen carryover, but at the risk of increasing heterospecic pollen transfer, because it visits other Crotalaria species during the same foraging bout. The different foraging strategies, allied to morphological disadvantages represented by pollen overlap on X. grisescens body, may partially explain the much lower seed germination observed in C. pallida and C. lanceolata. These results are consistent with the hypothesis that a reduction in ower constancy may signicantly depress viable seed set by increasing the chances of self-pollination.

RESUMO
A leguminosa Crotalaria retusa, vulgarmente conhecida como chocalho ou xique-xique, foi introduzida no Brasil pela Africa, e combina uma s erie de caracter sticas que facilitaram seu estabelecimento no nordeste do Brasil. Focalizamos aspectos da biologia reprodutiva e do comportamento dos seu polinizadores para explicar seu sucesso reprodutivo. Para isto realizamos tratamentos de polinizac a a o manual e germinac o de sementes, e monitoramos o comportamento dos principais polinizadores em a cas e em a eneres, C. pallida e C. lanceolata. C. retusa e vel e capaz de autofertilizac a reas monoespec reas onde C. retusa ocorria junto a duas cong autocompat o espont anea. Ocorreu depress ao endog amica no n vel de porcentagem de germinac a ao no n umero. Pouco insetos visitaram as inoresc encias. Os o de sementes, mas n polinizadores leg timos foram duas abelhas de grande porte, Xylocopa frontalis e X. grisescens que representaram mais de 90 por cento das visitas. O primeiro forrageia exclusivamente em C. retusa e tem baixo potencial de dispers ao pol nica. O segundo voa a dist ancias mais longas e visita menos ores por inoresc encia, potencialmente aumentando a extens ao de dispers ao do p olen, mas com o risco de ampliar a transfer encia de p olen heteroespec co, pois visita outras esp ecies de Crotalaria durante o v oo. As diferentes estrat egias de forrageio, junto com a sobreposic a olen no corpo de X. grisescens, explica em parte a baixa taxa de germinac a o de p o de C. pallida e C. lanceolata. Os resultados s ao consistentes com a hip otese de que uma reduc a ancia oral pode deprimir signicativamente a produc a aveis, o na const o de sementes vi ao aumentar as chances de autopolinizac a o. Key words: Crotalaria; exotic weed; oral biology; ower constancy; rattleweed; Xylocopa.

THE COLONIZATION ABILITY OF A PLANT SPECIES depends on combined aspects of its reproduction and life history attributes. Growth form, longevity, size, mating system, oral allocation strategies, seed set and germination, as well as modes of dispersal, phenotypic plasticity, and tolerance to environmental changes are among the most important characteristics correlated with successful establishment in new environments (Baker 1974). A decisive factor for the success of many of these attributes is the presence of suitable pollinators in new environments, either to effect pollination in the case of selfincompatible plants, or to reduce the levels of inbreeding in selffertile species. Inbreeding depression is a widespread mechanism to prevent self progeny, reected in the poor performance frequently observed in the progeny derived from self or close relative crosses (Lande & Schemske 1985, Husband & Schemske 1996, Richards

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Received 6 February 2003; revision accepted 27 November 2004. Corresponding author; e-mail: jacobi@icb.ufmg.br 357

1997, Husband & Gurney 1998, Culley et al. 1999). In many circumstances, however, self-fertilization is not so strongly prevented, or is even favored by selective forces. The higher the level of uncertainty of cross-pollination, the stronger the effect of reproductive assurance in favor of self-fertilization (Ramsey & Vaughton 1996, Barrett et al. 1997, Petanidou et al. 1998). The supply of suitable pollination services grants good levels of both pollen quantity and quality. Pollination services depend on aspects such as the degree of oral constancy of pollinators, a behavior that is still the focus of ample debate regarding its causes and consequences, but is generally associated positively with reproductive success (Waser 1986, Kwak & Bergman 1996, McLernon et al. 1996, Chittka et al. 1999). Many legumes (Fabaceae) are among the most widely spread exotic plants and, besides presenting self-compatibility, they benet from either exotic (Stout et al. 2002) or native pollination services (Etcheverry et al. 2003), although the rates of spread within the family vary considerably (Wu et al. 2003). In this study, we will

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focus on the causes for the colonization success of a member of this family. Species of Crotalaria are annual herb native to old-world tropics, ranked as pantropical weeds well adapted to colonize open elds, roadsides, cattle pastures, and other human-altered areas (Moore 1978, Polhill 1982, Lewis 1987). They produce hepatotoxic alkaloids (Culvenor & Smith 1957) and are known to be toxic to farm animals (Hooper & Scanlan 1977, Alfonso et al. 1993) and insects (Panizzi & Slanski 1991). Approximately 40 species of Crotalaria occur in Brazil, of which ten are exotic, introduced from Africa (Oliveira 1992). In the Atlantic coast of NE Brazil the most abundant exotics are the common rattleweed Crotalaria retusa L., followed by the smooth rattlebox Crotalaria pallida Ait., and the lanceleaf rattlebox Crotalaria lanceolata E. Mey. The genus has several self-compatible examples (Moore 1978, Almeida 1986, Etcheverry et al. 2003), concurring with the high rates of selfcompatibility of Fabaceae (Endress 1996). Seed dispersal is explosive and the small reniform seeds are scattered a few meters from the mother plant (Almeida 1986), making gene ow highly dependent on pollination services. Inorescences are composed of bright yellow ag-owers (papilionate owers), which offer nectar to visitors. Pollen is concealed and presented secondarily when legitimate pollinators, typically large bees strong enough to depress the keel, expose the stigma and push out a mass of pollen grains (Endress 1996, Westerkamp 1997). Because of their predominance in disturbed sites and poor performance in unaltered environments, exotic Crotalaria may be considered noninvasive colonizers according to Davis and Thompsons (2000) classication of invasive species. However, their success may vary among populations, and depends on the behavior of native or exotic pollinators they encounter in the new environment. We evaluated the reasons for the colonization success of C. retusa with respect to two less abundant exotic congeners in NE Brazil, C. lanceolata and C. pallida, focusing on reproductive aspects, with emphasis on the role of visitors. We hypothesized that C. retusa benets from a better pollen supply, both in quality and quantity, derived from pollinator services, and that this partially explains its higher abundance in the region, given that the taxonomic and ecological status, and time of introduction in NE Brazil is similar among the three species.

METHODS
The study took place at the campus of the Federal University of Bahia, NE coast of Brazil (12 56 S, 38 21 W) from January to May 2001. The area is characterized by large patches of open elds and small fragments of secondary forest (Queiros 2001). The climate is typically tropical wet and lacks a dry season. Crotalaria retusa plants grow in patches that ower year round, as a result of ve to six asynchronous annual life cycles within the population. Crotalaria retusa pods are approximately 40-mm long, brown, and dry when ripe. They explode easily when manipulated, propelling most of the seeds within 12 m of the mother plant. While most areas of the campus are colonized exclusively by this

species, in some areas it grows mixed with two congeners, C. pallida and C. lanceolata. In the monospecic patches, C. retusa can reach high densities (up to 1.0 individual/m2 ). In most heterospecic areas, any of the other two Crotalaria species reach only a quarter of the density of C. retusa. The three species share most of their oral visitors and their owering phenologies overlap. Each C. retusa inorescence has typically few (04) owers open at any given time, a small number compared to the other two species, which can carry three to four times that amount. Still, C. retusas inorescences appear more attractive because of the owers larger size, in particular the ag, which is ca 20-mm long, more than double the size than the other two species. To determine the ability to set fruit and seed in the absence of pollinators, we performed three pollination treatments, each one in a different inorescence from 52 plants: (1) agamospermy (N = 28 buds), by emasculating buds; (2) spontaneous self-pollination (N = 34); and (3) manual cross-pollination (N = 38), by emasculating buds and smearing the stigma when the ower opened with pollen from at least two different plants distant about 100 m from the focal plant. Other buds and old owers were removed from all the treatment inorescences, which were immediately bagged with ne mesh cloth to prevent visits, and remained covered until seeds were fully developed or the fruits aborted. The ratio spontaneous selng/hand outcrossing of mean seed number was used as a selffertility index, following Lloyd and Schoen (1992). In addition, 104 unbagged owers were used as control (free pollination) to check for natural abortions. All the seeds produced by the self and cross-pollinated fruits were sown in a greenhouse, kept moist, and monitored during 50 d. Stigma receptivity was determined in the eld in ten open and preanthesis owers by testing the reaction (bubble production) of the stigmatic surface to hydrogen peroxide at 3 percent (Dafni 1992) with a hand lens. Anther dehiscence in preanthesis owers was checked by removing part of the keel. Natural seed production and viability in the three genera was established by counting seeds from naturally pollinated fruits taken from 3140 plants of each species, as well as ovules of ten buds from different plants of each species. All seeds from 40 fruits of C. retusa, 9 fruits of C. pallida, and 9 fruits of C. lanceolata were sown and allowed to germinate for 60 d. We devoted 240 h to observe the foraging behavior of ower visitors of the three species in different parts of the campus, in particular their success in exposing the reproductive structures. Observations started before anthesis, around 0700 h, and ended at dusk, around 1900 h. After establishing the role of each visitor, the oral constancy of the effective pollinators, two large carpenter bees (Xylocopa spp.), was monitored in an area where the three species of Crotalaria grew intermingled. In this plot, C. pallida and C. lanceolata reached their highest density, which nevertheless was half or less than that of C. retusa. Twenty-six individuals of Xylocopa frontalis (Olivier) and 32 of Xylocopa grisescens Lepeletier were followed from the moment they entered the study plot (approximately 300 m2 ) until they ew away from the patch. We recorded the number of owers available and visited per plant, as well as the sequence of interplant movements.

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The length and thorax width was obtained from ten individuals of each species, and the region of pollen deposition in their body was noted. To compare potential pollen spread by the two Xylocopa species, we monitored their foraging ight behavior in a large patch (approximately 1000 m2 ) colonized exclusively by C. retusa. We calculated the density of oral resources at the time of the observations from ten 4-m2 quadrats, and registered the number of owers available and visited by individual bees for all visited plants. Sixteen individuals of X. grisescens and 22 of X. frontalis were followed from plant to plant for up to 17 steps (plant switches). To characterize their foraging behavior, we measured the beeline between visits to successive plants and the angle formed by these segments. Signicant differences in the frequency distributions of these two ight variables between pollinators were evaluated with a KolmogorovSmirnov two-sample test (Sokal & Rohlf 1981). To compare the expected distance own by each species, we incorporated these data in an equation that estimates the expected net squared displacement after n segments E(Rn2 ), as proposed by Kareiva and Shigesada (1983). In this approach, E(Rn2 ) depends on the mean segment length and on the mean turning angle between segments. Large segments and small turning angles result in large displacements (large inertia). Assuming that the organism exhibits the same probability of turning left or right (independently of the value of the angle), the expected net squared displacement is
2 E Rn = n E (l 2 ) + E (l )2

FIGURE 1. Germination of Crotalaria retusa seeds resulting from natural (N = 714), spontaneous self-pollination (N = 291), and manual cross-pollination (N = 174).

c 1c

1 cn 1c

(1)

where l is the mean segment length, c is the mean cosine of the turning angle, and n is the number of steps.

RESULTS
The percentage of seeded fruits obtained from the different pollination experiments indicate that C. retusa is self-compatible and capable of spontaneous selng. No fruits developed from agamospermy, while spontaneous self-pollination had 50 percent success in fruit production. In comparison, 82.7 percent of the 104 free-pollinated owers reached maturity. The rate of aborted cross-pollinated fruits was high (only 10 fruits lasted, i.e., 26%). This poor maturation rate was probably the consequence of heavy manipulation during anther removal from inside the keel. This procedure was mandatory since we conrmed that stigma receptivity and anther dehiscence may occur before anthesis. Seeds of C. retusa are brown, reniform (4.2 0.1 mm, N = 10), and small (16.8 2.4 mg, N = 10). There was no difference in the mean number of seeds per pod produced by either spontaneous autogamy or manual cross-pollination, which was 17.1 3.9 (N = 17) and 17.4 7.1 (N = 10), respectively, and these did not differ from the number of seeds in control pods (17.9 3.1, N = 40). The self-fertility value was 0.98. There was a striking difference in seed germination, however, according to their paternity (Fig. 1). Those sired by cross-pollen had a fast germination response and attained

97 percent of germination after 50 d, while those sired by selfpollen reached only 44 percent in the same period. Control seeds had the same germination rate of cross-seeds after 20 d of sowing, but decreased their germination rate after that. Indeed, after the initial 3 weeks, only cross-seeds showed a substantial increase in percent germination. Under natural conditions, 80 percent of the ovules of C. retusa developed into seeds, a lower rate than the other two Crotalaria species, which have approximately twice the number of ovules per pod (Table 1). Seed germination after 2 mo, however, was different among the species, and much higher in C. retusa, resulting in the highest rate (66%) of ovules that developed into viable seeds. In the study area C. retusa owers opened by lifting the ag around 1000 h and wilted by 1800 h. Two native carpenter bees (Xylocopini) accounted for more than 90 percent of all visits recorded (N = 214). These bees visited the inorescences before anthesis, forcing the buds in search of nectar, and remained active all day. Xylocopa frontalis accounted for 49 percent of the visits, followed closely by X. grisescens, with 44 percent. Other than these, few insects visited the inorescences. Occasional visitors were the

TABLE 1.

Ovule and seed number (mean SD), and 60-d percent germination of Crotalaria retusa and two sympatric congeners. Seeds were obtained from naturally pollinated fruits.

Germination C. lanceolata C. pallida C. retusa

Ovule number 45.02 2.12 (N = 10) 51.60 1.67 (N = 10) 22.42 1.52 (N = 10)

Seed number 42.29 3.00 (N = 31) 48.45 4.15 (N = 31) 17.85 3.13 (N = 40)

Percent 14.9 (57/383) 57.0 (245/430) 83.0 (593/714)

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digger bee Centris leprieuri (Spinola), a legitimate pollinator, and the stingless bee Trigona spinipes (Fabricius), a robber who perforated the base of the corolla to obtain nectar. Butteries of the families Hesperiidae and Pieridae behaved as thieves, collecting nectar with their proboscis without pushing the keel down. The two carpenter bees were considered the only effective pollinators because of their high visiting frequency and behavior in the inorescence. Their large size allowed them to manipulate the ower mechanism and expose the reproductive structures. Xylocopa frontalis is 29.9 1.1 mm long, with a thorax width of 12.0 0.4 mm (N = 10). X. grisescens is slightly smaller, 28.5 1.8 mm long and a thorax width of 11.2 0.5 mm (N = 10). Both embraced the ower when they landed on the keel, and pressed it down while pushing the ag upward to introduce the proboscis between them, forcing the emergence of the stigma and squirting pollen onto the thorax. Pollen was deposited around the insertion of the third pair of legs in both species. Because of their owers smaller size, pollen of the other two rattlebox species is deposited closer to the insertion of the rst pair of legs. The resources in the monospecic C. retusa plot were of 3.5 2.4 owers/m2 during the observations. The number of owers per

plant varied from zero to 35 (mean = 6.6 5.3). A comparison of the two Xylocopa species foraging behavior in this area indicated that X. grisescens is capable of spreading pollen farther from the mother plant than the other species. The rst important foraging difference is that X. grisescens visited fewer owers per inorescence (35%) than X. frontalis (47%), potentially increasing pollen carryover. Other differences were exposed by interplant foraging parameters. Although both bees responded to the dense landscape described above by ying short distances between plants (more than 67% of the interplant ight distances of both species were within 3 m, Fig. 2a), ight segments larger than 10 m represented only 4 percent in X. frontalis but reached 9 percent in X. grisescens. About 80 percent of the turning angles between plants in both species ranged between 0 and 90 , either to the left or right, indicating a strong forward directionality (Fig. 2b). There were no signicant differences in the ight behavior of the bee species, when comparing the distribution of either interplant distances ( D = 0.073 < D .05 = 0.130) or turning angles ( D = 0.100 < D .05 = 0.136). This suggests a similar range of pollen spread. However, the potential pollen spread evaluated by the expected net squared displacement after

FIGURE 2. Frequency of interplant distances (a) and turning angles (b) of the foraging paths of 16 Xylocopa frontalis and 22 X. grisescens individuals, obtained from 282 and 178 interplant segments, respectively.

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TABLE 2.

Mean interplant foraging parameters used to calculate the expected squared displacement Rn2 of Xylocopa frontalis and Xylocopa grisescens, obtained from 282 and 178 interplant segments, respectively. See Figure 2 for more details. X. frontalis X. grisescens 3.67 37.13 0.27 651.93 t-test P < 0.05 P < 0.05 NS

C. lanceolata, respectively, reecting the higher number of available owers per inorescence in the last two species.

DISCUSSION
The high frequency of self-compatibility in annual herbs has been interpreted as a response to the degree of uncertainty of pollination during owering (Endress 1996, Ramsey & Vaughton 1996, Barrett et al. 1997). In this scenario, reproductive assurance in C. retusa is reected in its ability to spontaneously self-pollinate, considering that its annual life cycle and ample geographical distribution might expose the species to the risk of temporary absence of pollinators. The high rate of spontaneous self-pollination in C. retusa and other congeners (Etcheverry et al. 2003) is probably associated with the absence of a membrane in the stigma, characteristic of tribe Crotalarieae (Shivanna & Owens 1989). In most self-compatible Fabaceae, however, there is usually no spontaneous germination of a self-pollen tube, because the stigma is covered by a membrane that needs to be abraded rst. This is achieved during the process of exposing the reproductive organs by a legitimate pollinator (Endress 1996). Although seed set in Crotalaria is granted even in the case of absence of visits, and involves delayed selng, as pointed out for C. micans (Etcheverry et al. 2003), the low germination rate of selfseeds in C. retusa is a clear indication that appropriate pollinators are needed to prevent inbreeding depression. Papilionate owers demand specic pollinators that combine strength and behavior to expose the reproductive structures. In our study, only two carpenter bees conformed to these specications: X. frontalis and X. grisescens. Although these native bees were frequent visitors of C. retusa and its two congeners, these last two showed considerably lower germination rates. A partial explanation for the low seed viability of C. pallida and C. lanceolata is the difference in the oral constancy of the bees. Stigma obstruction by heterospecic pollen may occur in the three Crotalaria species since X. grisescens is promiscuous and visited the three species during the same feeding bout. This would reduce the percentage of available cross-pollen, intensifying the germination of self-pollen tubes and leading to inbreeding depression.

Mean interplant distance (m) Mean squared interplant distance (m2 ) Mean cosine Expected Rn2 after 15 steps (m2 )

2.80 17.82 0.28 326.43

visits to 15 consecutive plants was much higher for X. grisescens (around 650 m2 ) than for X. frontalis (326 m2 ). This difference is explained by the higher mean interplant ight distance of X. grisescens (t-test; P < 0.05; df = 271), given that the mean cosine of the turning angles was not signicantly different between species (t-test; P = 0.37; df = 256, Table 2). The degree of ower constancy, measured in the heterospecic plot, was markedly different between pollinators (Table 3). The density at the time of the observations was of 15 8 owers/m2 . The mean number of owers/inorescence was 7.3 4.1, 5.2 3.4, and 2.4 2.0, in C. lanceolata, C. pallida, and C. retusa, respectively. However, the proportion of plants favored a higher oral density of C. retusa, as mentioned before. All 26 X. frontalis bees approached but gave up visits to species of Crotalaria other than C. retusa. Therefore, all 575 owers visited by this bee belonged to C. retusa, resulting in a mean of 2.4 owers visited per plant. On only one occasion, outside of our study, an individual of X. frontalis was seen visiting a plant of C. pallida. In comparison, of the 32 X. grisescens individuals studied, only eight visited C. retusa exclusively, and the rest foraged on the three species of Crotalaria indiscriminately. From a total of 1121 visits to owers, 47 percent were made to C. retusa, 41 percent to C. pallida, and 12 percent to C. lanceolata. These percentages are in accordance with the proportion of inorescences available in the study plot, where C. lanceolata was under-represented. The mean number of owers per plant visited by X. grisescens was 2.3, 4.2, and 5.3 for C. retusa, C. pallida, and

TABLE 3.

Floral constancy: interplant foraging ights among three species of Crotalaria performed by their two most frequent pollinators: Xylocopa frontalis (N = 26) and Xylocopa grisescens (N = 32). Pairs of letters indicate plant switch, either to the same species or a different one. L: C. lanceolata; P: C. pallida; R: C. retusa. The total number of owers visited and their relative percentage are also shown. Interplant switches RR RL 0 0 7 2.0 RP 0 0 26 7.4 PP 0 0 56 15.9 PL 0 0 1 0.3 PR 0 0 34 9.6 LL 0 0 23 6.5 LP 0 0 6 1.7 LR 0 0 6 1.7 R 575 100 528 47.1 Flowers visited P 0 0 462 41.2 L 0 0 131 11.7

X. frontalis (%) X. grisescens (%)

240 100 194 55.0

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However, the chances of C. retusa receiving cross-pollen are higher compared to the other two exotics, because the percentage of visits from the promiscuous pollinator is diluted with the visits of X. frontalis, which foraged on this plant exclusively. In addition, since its ower is larger, C. retusa pollen is spatially segregated, reducing the chance of stigma contamination. The advantage of a constant pollinator, however, may not be continuous over time, since it has been shown that pollinators may reduce their specicity according to overall resource densities (Kunin 1993, Kunin & Iwasa 1996). In the study site, the presence of two other Crotalaria species may have enhanced attractiveness and beneted all species by pollination facilitation, even at the risk of reduced seed set due to heterospecic pollen transfer, as suggested by theoretical models (Feldman et al. 2004). Whereas their combined oral display may have enhanced attraction of visitors to the three species, the behavior of the pollinators suggests it produced a bias that has favored C. retusas chances of outcross progeny. Another difference in pollinator behavior was related to pollen carryover. Xylocopa grisescens is potentially capable of transporting pollen from a focal plant farther away than X. frontalis, because of its larger mean interplant ight distances and lower percentage of owers visited per plant. Considering the short-distance seed dispersal, a larger area of pollen spread is benecial because it reduces the chances of inbreeding as a consequence of mating with siblings, as already pointed out. The association between large carpenter bees and Crotalaria is common. Xylocopa bees constitute a guild of pollinators active all year round, with ample geographical distribution in the wet tropics (Hurd & Moure 1963, Gerling et al. 1989, Minckley 1998). This makes them relatively predictable in space and time. Even so, their visitation rates are probably lower when the density of oral rewards is low. Also, the ample geographical distribution of Crotalaria (Polhill 1982) expose individuals to the risk of a temporary or local lack of pollinators, in the boundaries of its geographical or population expansion and, evidently, in regions where they are exotic. In both cases, or during unpredictable drop in pollination services, automatic self-pollination increases the chances of seed production. The subsequent establishment of C. retusa in the study area and, likewise, in other portions of the coastal landscape seems to depend, fundamentally, on the successful attraction of its main pollen vector, Xylocopa species. Potentially different roles in the reproductive success of C. retusa were recognized for each pollinator; X. frontalis shows ower constancy favoring outcrossing, but would spread pollen over a smaller area, while X. grisescens is capable of larger pollen carryover favoring genetic variability, but at the risk of reaching the wrong Crotalaria species.

LITERATURE CITED
ALFONSO, H. A., L. M. SANCHEZ, M. D. FIGUEREDO, AND B. C. GOMEZ. 1993. Intoxication due to Crotalaria retusa and C. spectabilis in chickens and geese. Vet. Human Toxicol. 35: 539. ALMEIDA, E. C. 1986. Biologia oral e mecanismo de reproduc a o em Crotalaria mucronata Desv. Revta. Ceres 33: 529540. BAKER, H. G. 1974. The evolution of weeds. Annu. Rev. Ecol. Syst. 5: 124. BARRETT, S. C. H., L. D. HARDER, AND A. C. WORLEY. 1997. The comparative biology of pollination and mating in owering plants. In J. Silvertown, M. Franco, and J. L. Harper (Eds.). Plant life histories. Ecology, phylogeny and evolution, pp. 5776. Cambridge University Press, Cambridge. CHITTKA, L., J. D. THOMSON, AND N. M. WASER. 1999. Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86: 361377. CULLEY, T. M., S. G. WELLER, A. K. SAKAI, AND A. E. RANKIN. 1999. Inbreeding depression and selng rates in a self-compatible, hermaphroditic species, Schiedea membranacea (Caryophyllaceae). Am. J. Bot. 86: 980987. CULVENOR, C. C. J., AND L. W. SMITH. 1957. The alkaloids of Crotalaria retusa L. Aust. J. Chem. 10: 464473. DAFNI, A. 1992. Pollination ecology: A practical approach. Oxford University Press, New York. DAVIS, M. A., AND K. THOMPSON. 2000. Eight ways to be a colonizer; two ways to be an invader: A proposed nomenclature scheme for invasion ecology. Bull. Ecol. Soc. Am. 81: 226230. ENDRESS, P. K. 1996. Diversity and evolutionary biology of tropical owers. Cambridge University Press, Cambridge. ETCHEVERRY, A. V., J. J. PROTOMASTRO, AND C. WESTERKAMPP. 2003. Delayed autonomous self-pollination in the colonizer Crotalaria micans (Fabaceae: Papilionoideae): Structural and functional aspects. Plant Syst. Evol. 239: 1528. FELDMAN, T. S., W. F. MORRIS, AND W. G. WILSON. 2004. When can two plant species facilitate each others pollination? Oikos 105: 197207. GERLING, D., H. H. W. VELTHUIS, AND A. HEFETZ. 1989. Bionomics of the large carpenter bees of the genus Xylocopa. Annu. Rev. Entomol. 34: 163190. HOOPER, P. T., AND W. A. SCANLAN. 1977. Crotalaria retusa poisoning of pigs and poultry. Aust. Vet. J. 53: 109114. HURD, P. D. JR, AND J. S. MOURE. 1963. A classication of the large carpenter bees (Xylocopini) (Hymenoptera, Apoidea). Univ. Calif. Publ. Entomol. 29: 1365. HUSBAND, B. C., AND J. E. GURNEY. 1998. Offspring tness and parental effects as a function of inbreeding in Epilobium angustifolium (Onagraceae). Heredity 80: 173179. , AND D. W. SCHEMSKE. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50: 5470. KAREIVA, P. M., AND N. SHIGESADA. 1983. Analyzing insect movement as a correlated random walk. Oecologia 56: 234238. KUNIN, W. 1993. Sex and the single mustardPopulation density and pollinator behavior effects on seed-set. Ecology 74: 21452160. , AND Y. IWASA. 1996. Pollinator foraging strategies in mixed oral arrays: Density effects and oral constancy. Theor. Pop. Biol. 49: 232263. KWAK, M. M., AND P. BERGMAN. 1996. Early owers of Bartsia alpina (Scrophulariaceae) and the visitation by bumblebees. Acta Bot. Neerl. 45: 355366.

ACKNOWLEDGMENTS
The authors wish to thank Marcos M.A. Mons ao and Camila M. Pigozzo for their help during eldwork. CMJ thanks CAPES for the fellowship that made possible a 3-mo stay at the Federal University of Bahia. The comments of two anonymous reviewers greatly improved an early version of the manuscript.

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LANDE, R., AND D. W. SCHEMSKE. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39: 2440. LEWIS, G. P. 1987. Legumes of Bahia. Royal Botanical Gardens, Kew, 369 p. LLOYD, D. G., AND D. J. SCHOEN. 1992. Self- and cross-fertilization in plants, I. Functional dimensions. Int. J. Plant. Sci. 153: 358369. MCLERNON, S. M., S. D. MURPHY, AND L. W. AARSEN. 1996. Heterospecic pollen transfer between sympatric species in a midsuccessional old-eld community. Am. J. Bot. 83: 11681174. MINCKLEY, R. L. 1998. A cladistic analysis and classication of the subgenera and genera of the large carpenter bees, tribe Xylocopini (Hymenoptera: Apidae). Nat. Hist. Museum 9: 147. MOORE, L. R. 1978. Seed predation in the legume Crotalaria. Oecologia 34: 185202. OLIVEIRA, A. L. P. C. 1992. Evoluc a pica no g enero Crotalaria L. (Leguo cariot minosae). Ph.D. Dissertation. Escola Superior de Agricultura Luis de Queiros, S ao Paulo, Brazil. PANIZZI, A. R., AND F. SLANSKI. 1991. Suitability of selected legumes and the effect of nymphal and adult nutrition in the Southern green stink bug (Hemiptera, Heteroptera, Pentatomidae). J. Econ. Entomol. 84: 103 113. PETANIDOU, T., A. C. ELLIS-ADAMS, J. C. M. DEN NIJS, AND J. G. B. OOSTERMEIJER. 1998. Pollination ecology of Gentianella uliginosa, a rare annual of the Dutch coastal dunes. Nord. J. Bot. 18: 537548.

POLHILL, R. M. 1982. Crotalaria in Africa and Madagascar. A. A. Balkema, Rotterdam. QUEIROS, E. P. 2001. A subfam lia Faboideae (Leguminosae) nas restingas da costa Norte do Estado da Bahia. M.Sc. Thesis. Universidade Federal da Bahia, Salvador, Brazil. RICHARDS, A. J. 1997. Plant breeding systems. Chapman & Hall, London. RAMSEY, M., AND G. VAUGHTON. 1996. Inbreeding depression and pollinator availability in a partially self-fertile perennial herb Bladfordia grandiora (Liliaceae). Oikos 76: 465474. SHIVANNA, K. R., AND S. J. OWENS. 1989. Pollen-pistil interactions (Papilionoideae). In C. H. Stirton and J. L. Zaruchi (Eds.). Advances in legume biology. Monogr. Syst. Bot. Gard. 29, pp. 157182. SOKAL, R. R., AND F. J. ROHLF. 1981. Biometry. W. H. Freeman, San Francisco. STOUT, J. C., A. R. KELLS, AND D. GOULSON. 2002. Pollination of the invasive exotic shrub Lupinus arboreus (Fabaceae) by introduced bees in Tasmania. Biol. Conserv. 106: 425434. WASER, N. M. 1986. Flower constancy: Denition, cause, and measurement. Am. Nat. 127: 593603. WESTERKAMP, C. 1997. Keel blossoms: Bee owers with adaptations against bees. Flora 192: 125132. WU, S. H., S. M. CHAW, AND M. REJMANEK. 2003. Naturalized Fabaceae (Leguminosae) species in Taiwan: The rst approximation. Bot. Bull. Acad. Sin. 44: 5966.