BlOTROPlCA 30(4):559-586

1998

Sugar Composition of Nectars and Fruits Consumed by Birds and Bats in the Tropics and Subtropicsl
Herbert G. Baker Department of Integrative Biology, University of California, Berkeley, California 94720, U.S.A. Irene Baker2 Department of Integrative Biology, University of California, Berkeley, California 94720, U.S.A. Scott A. Hodges Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, California 93106, U.S.A.

ABSTRACT
Several characteristics of flowers and fruits have been suggested as comprising syndromes of characters that indicate particular classes of pollinators and fruit dispersers. Common phylogenetic history among species, however, may also significantly influence these characters and obscure or enhance perceived patterns of plant syndromes. We analyzed the proportions of glucose, fructose, and sucrose by paper chromatography in the nectar and fruit juice of 525 tropical and subtropical plant species to test whether sugar chemistry was correlated with volant vertebrate pollinator or fruit disperser classes. Samples were taken from Old World and New World species and the calculations kept separate. Kruskal-Wallis tests of family means showed significant deviations in the percent sucrose content among pollinator/ disperser classes. Mann-Whitney U-tests showed significant differences among nectars of all pollinator classes but fruit juices differed only due to the high sucrose content of megachiropteran dispersed fruits. In addition, sign tests of samples occurring within families showed significant correlations between percentage sucrose content and pollinator/ disperser classes. Passerine nectars had low sucrose content. In striking contrast, the nectar of hummingbird flowers had very high sucrose content. T h e Microchiroptera nectars showed hexose richness with a sucrose content somewhat greater than that of passerine flowers. Megachiroptera flowers showed sucrose-rich nectars. The results for fruits were comparable to those for nectars. Passerine fruits were hexose dominated, microchiropteran fruits had a sucrose content similar to passerine fruits, and megachiropteran ftuits were sucrose-rich. We speculate on the evolutionary sequence of changes in nectar and fruit juice sugar composition and suggest that future investigations consider the chemistry of other food sources such as pollen and leaves. Only with these additions and other ecological studies can the f l ul interplay of such plant-animal interactions be anticipated.

Key words: coevolution; Erythrina; j k i t juice; hummingbirds; Megachiroptera; Microchiroptera; nectar; passerine; .sucrose.

GENEML ADAPTATIONS BY Pi.ANTs to specific pollinators and seed dispersers are thought to have produced syndromes of plant characters that reflect these interactions (Hurd 1968, Baker & van der Pijl 1982). More recently, these views have been challenged both because pollination or seed dispersal by a single species is rare and acknowledgment that historical factors can strongly influence correlations among characters of species (Harvey & Pagel 1991). As pointed out by others (.g., Felsenstein 1985, Donoghue 1989, Maddison 1990), calculating correlations among characters using species as independent units can be misleading; species may not represent independent data points due to recent divergence or because they share similar environments (Harvey & Pagel 1991).
Received 27 March 1997; revision accepted 12 August 1998. Deceased 9 November 1989

As an example of how correlations utilizing species data can be misleading, Donoghue (1989) showed that a highly significant association between fleshy fruits and dioecy was ambiguous when correlations of historical changes were tested. In the case of fruit characters and their dispersers, Herrera (1992) found that taxonomic membership was more highly correlated with fruit shape than dispersal mode. Jordan0 (19 9 9 , however, after controlling for historical effects, found that fruit diameter was correlated with the class of bird dispersers, although many other fruit characters, such as mass and energy content, were not significantly correlated. Similarly, Mazer and Wheelwright (1993) found evidence supporting the hypothesis that length of fruits was an adaptation for gapelimited avian seed dispersers in the tropics. Over the last 20 years we have been collecting and analyzing the chemistry of nectars and fruit juices. Summaries of data for nectars of >700 spe-

559

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cies were grouped according to their probable insect or vertebrate major pollinator. Striking patterns of sugar composition with pollinator class were detected (I. Baker & H. G. Baker 1982, H. G. Baker & I. Baker 1983a) based on sugar ratio (sucrose to glucose plus fructose: S/G F) (Baker & Baker 1983a, b, 1990). High sugar ratios characterized some pollination classes such as that by hawkmoths, long-tongued bees, and hummingbirds. Low ratios characterized short-tongued bees, flies, and both Old and New World passerine birds (I. Baker & H. G. Baker 1982, H. G. Baker & I. Baker 1983a; Table 5.10). Thus, these initial data demonstrate a clear agreement between nectars of taxonomically unrelated species and similar pollination biology. This investigation was based on the study of pollination and seed dispersal by volant vertebrate animals. Several of the pollinator categories were represented in 1983 by samples too small for definite conclusions to be drawn. These categories included bats of the Old World (Megachiroptera) that appeared to pollinate flowers with higher sugar ratios than bats of the New World (Microchiroptera). We expanded these studies to include fruit juices and attempted to account for correlations due to common history in our analyses. Non-volant primates are undoubtedly important flower and fruit visitors in many communities; however, there is a shortage of literature and primates (ranging from tiny prosimians to monkeys, apes, and human beings) are too varied for inclusion in this study. They will need consideration in any future ecosystem-based study. The null hypothesis is that no correlation exists between pollinator or seed dispersal class and the chemistry of the sugars involved, after controlling for common history. Birds of many families acquire their food (at least partly) from plant sources. Most frugivorous birds are passerine (perching) birds (super family Passeriformes) and many also take nectar from flowers. Sharply distinct from passerines are hummingbirds (family Trochilidae), which are restricted to the New World (Welty 1982) and depend on nectar supplies and insects for their nourishment. Hummingbirds do not normally visit fruits. Bats belong to the order Chiroptera with two suborders, Megachiroptera and Microchiroptera. The Microchiroptera, present in both hemispheres, have (with one exception from New Zealand; Daniel 1979, Pierson et al. 1986) evolved flower and fruit visiting only in the New World. They belong to the super family Phyllostomidae and eat nectar,

fruit juice, and varying amounts of insects, caught on the wing. The Megachiroptera occur exclusively in the Old World. In both suborders the flower visiting bats also acquire pollen from flowers they visit, and also may chew leaves (folivory) (Kunz & Diaz 1995). Hill and Smith (1985) and Dobat and Peikert-Holle (1985) have provided good comparative treatments of the lifestyle differences between the Megachiroptera and Microchiroptera. Heithaus (1982) provided a general review of relationships between bats and plants. A model treatment of a single species (Carollia perspicillata Microchiroptera) in an ecological and historical setting was provided by Fleming (1988). Fleming (1993) compared a Microchiroptera and Megachiroptera in an ecological context. Marshall (1983) can be a useful starting point for information on Megachiroptera.

MATERIALS AND METHODS

Methods of quantitative paper chromatography for the three sugars, sucrose, glucose, and fructose, are given in Baker and Baker (1983a, p. 120; Appendix 1). Fleshy or juicy fruits were sampled in a similar manner. Juice from fruit pulp was applied to pure cellulose chromatography paper and dried for subsequent analysis. Care was taken to ensure that fruits were ripe, judging by color, texture, softness, and the presence of unripe fruits for contrast. All chemical analyses were carried out by Irene Baker. The survey was restricted to nectars and fruit juices produced by plants growing wild or feral in the tropics or subtropics and pollinated or having their seeds dispersed by birds or bats. Market sources of fruit were not used. Nectar and fruit juice samples were collected by us and a large number of volunteers (see Acknowledgments). Many of these samples were submitted by experts on the taxa concerned. Herbarium specimens were taken from many plants by collectors of nectar and fruit samples. The three sugars, sucrose, glucose, and fructose, are by far the most common and abundant sugars in nectars and fruit juices. As such, we quantified the percentage of each of these three sugars in the total sucrose, glucose, and fructose soluble-sugar pool. Because the percentage of monosaccharides plus percentage of sucrose necessarily equal 100 percent, these percentages are not independent. Therefore, we concentrated our analyses simply on percent sucrose. Species may show similarities in sucrose content because of a common phylogenetic history, thus making species samples nonindependent. For

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TABLE 1 . Mean percent sucrose in nectars of plants with differing classes of pollinators (hummingbirds [HI, passerzne birds in the Old World [Po] and New World (Pn], bats in the Old World [CoJ and New World (Cn]) across species, genera, and families. Calculation of genera and families means are described in the text. Usingfamily means a Kruskal-Wallis test and Mann-Whitney U-test between each pair of pollinator classes (' < "0.05, I *"O.OI, ***0.001, *x*xO.OOO1) were calculated.
Pollinator class Families f (N, range, CV)

(N, range, CV)

57.5 (60, 18.0-89.5, 24) 10.2 (44, 0-98, 185) 2.0 (6, 0-3.7, 67) 40.4 (15, 9-93, 55) 17.8 (24, 2-51, 70)
Pn co

Genera f

Species .t (N, range, CV)

H
Po
Pn

co
en
Kruskal-Wallis H Mann-Whitney
=

58.0 (33, 18.0-89.5, 24) 7.4 (24, 0-30.9, 99) 1.9 ( 5 , 0-3.7, 75) 41.0 (1 1, 9-93, 60) 18.3 (14, 3-51, 68) 65.0, P << 0.001
PO

57.6 (137, 18-97, 29) 8.1 (88, 0-98, 193) 2.8 (14, 0-5, 51) 41.2 (19, 9-93, 51) 16.9 (38, 2-51, 70)
cn :

790****

Po Pn co

165*** loo*

286** 248****

55**

448**** 272"* 69** 121"

example in our data set, 75 percent of the genera with more than one species sampled had only one pollinator/disperser type represented. Thus, characters of species within these genera may be similar simply because they share characters of their recent common ancestors or because they share similar habitam, resulting in the species being nonindependent. O n the other hand, among families with more than one genus sampled, only 20 percent had a single pollinator/disperser type represented. This indicates that shifts in pollinator/disperser type are more common among genera within families than among species within genera. Therefore, samples at the family level are more likely to be independent. To reduce the problem of nonindependence of data, we calculated the mean percent sucrose within each family for each pollinator or disperser class. To reduce the effect of different intensities of sampling within genera, a mean of the species in each genus sharing a common pollinator/disperser class was first calculated. A mean of the genus means was then calculated for common pollinator/disperser classes within each family. Because the data were not normally distributed, the family means among pollinator/disperser classes were subjected to a Kruskal-Wallis test. Mann-Whitney U-tests were used to determine which classes differed from one another. Because some data points may still have been nonindependent due to common history, even after

calculating family means, a second set of tests was performed. In families with at least two pollinator or two disperser classes represented, at least one shift in pollinator/disperser class must have occurred. Therefore, we used sign tests on the means within families to determine if particular pollinator/disperser classes had greater sucrose content than an alternate class. Examining the data in this manner is quite conservative because it assumes only a single shift in pollinator/disperser class per family when there may have been multiple shifts.

RESULTS
In total, 296 species from 55 families were analyzed for nectar sugar composition and 229 species from 64 families were analyzed for fruit juice sugar composition (Appendix 2). Overall means differed little whether calculated from all species, from genera means, or from family means (Tables 1 and 2 ) . Kruskal-Wallis tests of the distribution of family means for percent sucrose in nectars and fruits indicated significant variation among both pollinator classes (P< 0.001) and seed disperser classes (P< 0.05). Mann-Whitney U-tests revealed significant differences in sucrose content between each pair of pollinator classes, while fruit juices differed only due to fruits taken by Megachiroptera (Tables 1 and 2). Sign tests were limited to contrasts in which at

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TABLE 2. Mean percent sucrose in f i u i t juices of plants with differing classes of dispersers (passerine birds in the Old
World [Po] and New World [Pn], bats in the Old World [Co] and New World [Cn]) across species, genera, andfamilies. Calculation ofgenera andfamilies means are described in the text. Usingfamily means a KruskalWallis test and Mann- Wbitney U-test between each pair ofpollinator classes (P < 70.10, *0.05,*"O.OI) were calculated.

Disperser class
"0

(N, range, CV)

7.9 (27, 0-41, 8.2 (37, 0-37, 23.5 (22, 0-51, 8.5 (15, 0-21, 8.32, P < 0.05
I'n
118)

Families X

(N> range, CV)

8.0 (41, 0-41, 7.8 (61, 0-58, 24.0 (32, 0-55, 9.1 (19, 0-27, 118) 137) 84)

Genera 2

Species 2

(N,range, CV)
7.6 (64, 0-41, 9.9 (96, 0-77, 21.9 (42, 0-63, 8.4 (27, 0-33,
Cn

122) 156) 91) 107)

I'n
<0 :

117) 81) 79)

Cn Kruskal-Wallis H

91)

Mann-Whitney
PO

co

Pn
CO

50 1

418* 572**

229 307 221t

least 5 families had both pollinatorldisperser classes represented. Means for samples pollinated by hummingbirds were always higher than means for samples pollinated by passerines (Table 3; P < 0.001). Likewise, the means for samples pollinated by hummingbirds were always higher than means for samples pollinated by Microchiroptera (Table 3; P < 0.01). Species with flowers pollinated by Megachiroptera had a larger proportion of sugar as sucrose than those species in the same families with flowers pollinated by passerines (Table 3; P < 0.05). For the sucrose content of fruit juices, two comparisons were significant or nearly so. Fruits taken by Megachiroptera had higher mean percent sucrose than passerine taken fruits from both the New World (P< 0.05) and the Old World (Table 4;P < 0.01). To test whether further possible relationships between sugar chemistry and pollinator/disperser classes existed, we conducted sign tests for the frequency that fructose or glucose was in greater quantity. For nectars from plants pollinated by hummingbirds, 102 had greater fructose content and 31 had greater glucose content (4species had equal percentages) (P < 0.001). Likewise, fruits dispersed by Megachiroptera had 28 species with greater fructose content and 12 with greater glucose content (P < 0.02). Nectars with passerine pollinators in the Old World had more species with higher glucose content (52 species with greater glucose content and 33 species with greater fructose

content; P < 0.05). All other comparisons were not significant (data not shown).

DISCUSSION
Data presented here strongly support the hypothesis that the composition of soluble sugars in nectar and fruit juices has been influenced by the pollinators and frugivores that consume them. Distributions of percent sucrose in nectars and fruit juices were significantly different among families when separated by pollinator and frugivore class (Tables 1 and 2). Nectars of flowers visited by hummingbirds or Megachiroptera, tended to have high levels of sucrose while nectars of flowers consumed by passerines had very low levels of sucrose. Nectars taken by Microchiroptera were intermediate (Table 1). Similarly, the juices of fruits taken by Megachiroptera were relatively high in sucrose while passerine consumed fruits had low sucrose content. While we did not have the necessary phylogenetic information to perform independent contrast tests with all of the available data, contrasts of samples within families broadly support the overall findings (Tables 3 and 4). Stiles and Freeman (1993), in their survey of hummingbird flowers in Costa Rica, noticed some correlative relationships between the sucrose and fructose content of some nectar taxa. Nectar having higher sucrose content tended to show slightly higher F/G ratios. This was not, however, statisti-

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563

TABLE 3. Fami4 means (no. genera, no. species) of the percent sucrose content in nectarsfor families in which more than one pollinator class was represented (hummingbirds [HI, passerine birds [PJ, in the Old World [Co] and bats New World [Cn]). Below are comparisons among pollinator classes within families for sucrose content. The number offamilies in which the mean sucrose content of one class was higher than the alternate class is given (no. families) with results of sign tests. Pollinator class Family Acanthaceae Apocynaceae Bignoniaceae Bombacaceae Bromeliaceae Cactaceae Ericaceae Euphorbiaceae Gesneriaceae Heliconiaceae Labiatae Leguminosae Liliaceae Loranthaceae Malvaceae Marcgraviaceae Onagraceae Polemoniaceae Proteaceae Rubiaceae Scrophulariaceae Solanaceae Sterculiaceae Strelitziaceae Pollinator classes comDared

H
47.6 (6, 1 1 ) 55.0 ( 1 , 2) 66.0 (2,3) 57.0 ( 1 , 4) 65.0 (1, 1) 62.5 (2,5) 42.0 (2,2) 59.4 (5, 14) 52.2 ( 1 , 6) 68.8 ( 1 , 4) 58.2 (4, 31) 63.5 ( 1 , 2) 49.0 (1, 1) 44.0 ( 1 , 1)

co

Cn

4.5 (2,2) 17.5 (2,3) 2.3 (I, 3) 2.0 (1,3) 3 0 ( 1 , 1) . 4.0 (1, 1) 10.7 (3,3) 3.0 (2,24) 2.0 (1, 1) 2.8 (3,5) 22.2 (5, 10) 2.5 (2,2) 6.3 (1, 3) 11.0 ( 1 , 1)
0
7.1

71.0 (1, 1) 40.0 (1, 1) 41.7 (3,4)

16.0 ( 1 , 1 ) 24.7 ( 1 , 3) 14.8 (5, 6) 13.7 (3,3) 16.0 ( I , 1)

48.0 ( 1 , 2) 35.7 (3,3) 18.4 (4, 9)

60.0 (3,9) 54.0 (2, 3)

4.5 (2,2) 10.0 (1, 1 ) 2 . ( 1 , I) 30

54.1 (4, 5) 46.5 ( 1 , 2) 59.2 (5,5) 78.0(1, 1)

(4, 6)
(1, 1)

13.5 (1, 2)
No. families

20.0 (1, 1)

30.0 (2, 2) 6.0 (1, 1 )

Sign test

H:P H:Cn P:Co

13:O 8:O 0:6

<0.001
<0.01

<0.05

cally significant. Our data indicate that nectars and fruits with high sucrose content are significantly more likely to have more fructose than glucose. These determinations, however, did not explicitly control for phylogeny. For example, the outstanding low percentages of glucose in the nectars of Gesneriaceae (Appendix 2) appear to be a characteristic of the family, as was noted by Stiles and Freeman (1993). The overall patterns of the relative proportions of fructose and glucose, however, appear to be much less robust than patterns of the proportion of sucrose among pollinator and seeddisperser classes. Therefore, fructose/glucose content cannot be relied upon as evidence of pollination and seed-disperser syndrome in any nectar or fruit juice sample. Consequently, although we provide the hexose data in each nectar and fruit juice sample, we do not focus attention on them. In contrast to the present study, Freeman et al.

(1991) reported data for nectars from flowers with the full range of pollinators from short-tongued bees to bats. Where known, the specific results of Freeman et al. (1991) are consistent with our own (Appendix 1). We consider the findings for nectarand fruit-sugar compositions consumed by birds and bats separately.

NECTAR: BIms.-Despite a statistically significant difference between Old and New World passerinepollinated species (Table l ) , low sucrose content predominates in both groups. The test was marginally significant and may be spurious due to the multiple comparisons made. Furthermore, hexose dominance of nectars consumed by passerines occurs both in more derived families (e.g., LobeliMyrtaceae). aceae) and more basal families (g., There is every reason to believe that low sucrose

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Baker, Baker, and Hodges

TABLE 4.

Family means (no. genera, no. species) of the percent sucrose content in fruit juicesf0rfamilies in which more than one disperser class was repesented (passerine birds in the Old World [Po], and New World [Pn], bats in the OU World [Co] and New World [Cn]). Below are comparisons among pollinator cla.aes within familie3 f i r sucrose content. The number offamilies in which the mean sucrose content of one class was higher than the alternate class (no. ties) is g v e n (no. families) with results of sign tests.
Disperser class

Family Anacardiaceae Annonaceae Apocynaceae Araliaceae Araceae Arecaceae Dillrniaceae Elaeocarpaceae Flacourciaceae Gesneriaceae Guttiferae Lauraceae Liliaceae Melastomataceae Moraceae Musaceae Myrsinaceae Myrtaceae Piperaceae Rubiaceae Sapindaceae Sapotaceae Solanaceae Urticaceae Verbenaceae Disperser classes compared

Po
0
0 (1, 1) 9.0 (1, 1) 17.0 (1, 2)

Pn
(1, 1)

co
36.0 (2, 2) 0.5 (2, 2) 30.0 (2, 2) 35.0 (1, 1)
0

Cn 13.5 (2, 2) 12.0 (1, 1)

0
( 1 , 1)

4.3 (2, 3) 5.0 (I, 1)

1.0 (1, 1) 7.0 (1, 1)

1.0 (2, 1.5 (2, 7.8 (2, 14.0 (1, 2.0 (1, 0 (1, 31.0 (1, 5.0 (2,

2) 3)
1) 1)

3)
1)

2) 2)

(1, 1) (1, 1)

11.0 (I, 1)

6.3 (3, 3)

1.0 (1, I ) 2.3 (6, 12) 2.0 (1, 1) (1, 1) (1, 1) ( I , 1) (8, 22) (2, 2) 37.0 (1, I) 16.1 (7, 14) 0.5 (2, 2) 1.0 5,0 1.0 5.9 3.0

51.0 (2, 2) 42.0 (1, I ) 12.1 (3, 10) 48.0 ( I , 1) 8.0 ( I , 2) 43.0 (1, 1) 45.5 (3, 4) 39.0 (1, 1)
0

1.0 (1, 1)

1.0 (1, 1)

41.0 (1, 1) 4.8 (2, 4) 2.5 (2, 4) 25.0 ( I , 1) 11.9 (6, 16)

8.7 (2, 7 )
14.5 (2, 2) 2.0 (1, 2) 21.0 (1, 1) 9.3 (2, 3) 5.0 (1, I) Sign test P

0 (1, 1) 4.0 (1, 1)

(1, 1)

No. families
6:5 1:8 (1) 4:5 (1) 0:8

P0:Pn 1n:Co Pn:Cn C0:Cn

I0:Co

3:3

NS <0.05 NS <0.01 NS

content in nectar represents the ancestral condition for taxa pollinated by volant vertebrate animals. The sucrose content of nectars from species pollinated by hummingbirds is in stark contrast to those species pollinated by passerines. Hummingbird-taken nectars are tabulated from 137 species in 33 families and many more are listed in previous publications (Baker & Baker 1983a, Freeman & Worthington 1985, Freeman et al. 1985, Stiles & Freeman 1993). They are high, almost without exception, and average above 50 percent of the total soluble-sugar pool. The distinction between sucrose contents of passerine- and hummingbird-taken nectars is very robust. In every family where samples of both hummingbird- and passerine-pollinated species have been analyzed, the sucrose content

of the nectar from the hummingbird-pollinated species was higher than that for species pollinated by passerines (Table 3). Comparisons within families of nectars consumed by hummingbirds or passerines are likely to be conservative because significant shifts in sucrose content between the two kinds of nectar also can be seen within genera. For instance, the genus Erythrina exemplifies the agreement between passerine-pollinated species in both hemispheres where they are uniformly hexose-rich; New World hummingbird-pollinated species, however, are uniformly rich in sucrose. Most likely, the ancestral condition of nectars with low sucrose content was breached by species in the New World where they were in contact with hummingbirds. The nectar

Sugar Composition of Nectar and Fruit Pulp

565

chemistry may have shifted from a low sucrose con- Iridaceae and share with other members of that tent to high more than once, with the repeated family a tendency for high sucrose content in necevolution of hummingbird-pollinated species (Bru- tar (Baker & Baker, pers. obs.). Furthermore, neau & Doyle 1993, I. Baker & H. G. Baker 1979, Adansonia za var. bozy, although pollinated by pas1982, H. G. Baker & I. Baker 1990). Shifts back serines, has high sucrose content (34%). This speto low sucrose nectars may also have occurred. Un- cies belongs to a genus that outside of Madagascar fortunately, many of the species analyzed here are is bat pollinated and tends to have high sucrose not the same as those used for the available phy- content. Thus, some species may retain ancestral logenetic reconstruction (Bruneau & Doyle 1993) character states and obscure or enhance general so we are not able to determine how many times patterns. the shift in nectar chemistry has occurred in this The second caveat that may explain apparently genus. anomalous species is that we have necessarily Similar striking shifts in nectar sucrose content lumped very large and diverse taxa into pollinator are true for other genera. In the genus Puya (Bro- classes. For instance, there is a very large number meliaceae), the nectar sugars of five hummingbird- of passerine species with a long evolutionary hispollinated species averaged 57 percent sucrose, tory. Thus, some clades of passerines may well have while the contents of nectar from three passerine- evolved different preferences and/or abilities to bird pollinated species averaged only 2.3 percent consume nectars with higher sucrose content. An sucrose (Table 3; Scogin & Freeman 1984; Baker example from the literature seems to be Hornstedtia & Baker 1990). Likewise, in the genus Fuchsia scottiana (Zingiberaceae) from Australia where eight hummingbird-pollinated species averaged 50 Ippolito and Armstrong (1993) reported that it percent sucrose while three species pollinated by produced sucrose-rich nectar although pollinated passerines averaged only 5 percent sucrose. Similar by passerines of the Meliphagidae. Thus, future inintrageneric shifts in sucrose content of nectars vestigations need to correlate specific clades of pashave been found in Campsw and Heliconia (Ap- serines with nectar chemistry. Also, because flowers pendix 2). Thus, these shifts are likely to have oc- of H. scottiana are borne within a few centimeters curred many times during the evolution of species of the ground, they also may be visited by mamwith contrasting pollination systems. mals that could independently influence sugar An important contribution to understanding composition. Similarly, in Hawaii, Kokia dynarioithe difference between nectars consumed by hum- des has nectar of almost pure sucrose although it is mingbirds and those consumed by passerines has thought to be pollinated by passerines; a careful been provided by the work of Martinez del Rio study on the pollination biology of this species is (Martinez del Rio & Karasov 1990, Martinez del warrented. Rio et al. 1992). These authors have shown that many passerines lack or have minimal sucrase in NECTAR: BATS.-cOntrast between sugar compositheir guts, whereas hummingbird guts are richly tion of nectars in species pollinated by Megachiprovided with sucrase that efficiently hydrolyzes su- roptera and Microchiroptera is striking. Nectars crose. Martinez del Rio (1990) has pointed out produced by microchiropteran-visited flowers are that hummingbird nestlings will be imprinted hexose-rich but have a higher sucrose content than with sucrose when they are fed such a predomi- passerine flower nectars. Corresponding figures for nantly sucrose diet. As such, hummingbirds may megachiropteran-visited flower nectars are even actively seek sucrose-rich food sources. Further- higher and bear comparison with those of hummore, these high sucrose nectars will likely deter mingbird flowers\(Baker & Baker 1983a, Freeman visitation by passerines that cannot utilize them, et al. 1991). In all eight comparisons within famresulting in lower competition for resources. ilies containing species pollinated by both humDespite the clear pattern between sucrose con- mingbird and Microchiroptera-pollinated flowers, tent and pollinator class, there are species with nec- the hummingbird-pollinated species had higher sutars that contrast with the norm for a particular crose contents (Table 3). Similarly, in all six combird pollinator class. These apparent anomalous parisons within families for both Megachiroptera cases point to two important caveats. First, as we and passerine-pollinated species, the Megachirophave tried to control for in our analysis, phyloge- tera-pollinated species had higher sucrose contents netic history may influence the characters of spe- (Table 3). cies. Old World passerine flowers, Anapalina cafia, Despite shifts in nectar chemistry often being A. nervosa, and AntboLyza ringens, belong to the accompanied by morphological changes in floral

566

Baker, Baker, and Hodges

form, large shifts in floral morphology need not indicate changes in nectar chemistry. For instance, in the genus Heliconia (Heliconiaceae) there exists considerable morphological and behavioral differentiation associated with different major pollinators (Kress 1985). Most species of Heliconia are hummingbird-pollinated in the American tropics. Batpollinated species occur in the South Pacific islands (including the Solomon Islands and Papua New Guinea) that are adapted to megachiropteran pollination, both morphologically and phenologically (Kress 1985). It is notable that the two Pacific island species investigated for sugar constituents of their nectars have shown high sucrose content (39 and 57%) while the hummingbird-pollinated species span these values with a range of 28-73 percent sucrose. An interesting variation is H. paka from Fiji, judged by Kress (1985) on morphological grounds to be pollinated by passerines. It is with acclamation that our data show it has hexosedominant nectar (sucrose 4%). Analyses of gut enzymes from bats of each suborder would be extremely useful. It would thus be possible to test if similar shifts in gut sucrase activity can be found in the bats as between the passerines and hummingbirds. For the Microchiroptera, Hernandez and Martinez del KO(1992) have examined the gut enzymes of five microchiropteran bats: one purely insectivorous (Pteronotuspersonatus), two predominantly frugivorous (Artibeusjamaicensis and Stumira lilium), and two primarily nectarivorous (Leptonycteriscurasoae and Glossophaga soricina). Sucrase was lacking in the insectivorous bat but was present in sufficient concentration in the nectar and fruit devouring bats to suggest that nectar and fruit juices containing sucrose could be digested quite comfortably by these bats. The similarity between the sucrose content of hummingbird and megachiropteran flowers suggests that there will be plentiful sucrase in the guts of the latter. For Megachiroptera, analyses by Ogunbuyi and Okon (1976) on African Eidolon heluum found sucrase to be present. There are a few species pollinated by Megachiroptera that have quite different nectar sugar compositions from the norm. Barringtonia asiatica has a vast preponderance of sucrose and is, according to Polunin (1988), pollinated by large moths as well as by bats. This is consistent with the high sucrose content typical of moth-pollinated flowers (Baker & Baker 1983a). In contrast, there are rather low concentrations of sucrose in Daniellia sp. (16%), Grevillea robwta (lo%), and Cananga odor-

ata (9%). We predict that these species will be passerine-visited.

FRUITS: BIRDS.-oUT results clearly indicate that passerine fruits from the Old World are hexosedominated; out of 65 samples from 27 families, only two were really aberrant; Coffea robusta and Musa coccinea. Both possibly attract primates. There is another item of note in our results; a remarkable similarity exists between the sugar composition of passerine fruit juices and passerine nectars. This similarity with nectar sugar composition suggests that passerines select fruits and nectars they can readily digest with a low sucrase digestive system. Sugar composition for passerine fruits from the New World are predominantly hexoses and their agreement with passerine fruits from the Old World is clear. This similarity is important evidence that hexose dominance is an ancient attribute of temperate and tropical angiosperms. One exception to these results is evident in some wild species of Lycopersicon (Solanaceae). Very recent studies on this genus have identified a gene for sucrose accumulation in the fruit of L. chemielewskii that is present in other species (including L. peruvianum and L. pimpinellifolium) Chatelat et al. 1993). It appears to be absent from L. pennellii. The ecological importance on the high sucrose content in these Lycopersicon species may be in their being an adaptation to mammalian taste preferences. Succulent fruits utilized by birds are liable to be eaten by mammals as well. FRUITS: BAx-Fruits taken by Microchiroptera had low percent sucrose and were very similar to the sugar composition of fruits taken by passerines in both the Old and New Worlds. The range of sucrose content for fruits taken by passerines was larger and completely overlapped the measurements for fruits taken by Microchiroptera, although it should be noted that sample sizes for fruits taken by passerines was about two- to three-fold larger than those for fruits taken by Microchiroptera. Furthermore, there were nine plant families with data for species having fruits taken by either passerines (New World) or Microchiroptera. There was no significant trend between the sugar composition of fruits taken by these disperser classes (Table 4). It is interesting that data for percent sucrose content of nectars is nearly double that for fruits taken by Microchiroptera (compared Tables 1 and 2). One explanation for this pattern is that there may be considerable overlap in the utilization

Sugar Composition of Nectar and Fruit Pulp

567

of fruits by bats and passerines. Detailed studies of the utilization of fruits taken by passerines and Microchiroptera would be extremely useful. The intensity of effort on a year-round basis necessary to establish dietary principles is described in Fleming (1988) for the short-tailed fruit bat, Carollia perspicilkzta, in Costa Rica. Fruits, like nectars taken by Megachiroptera, have higher percent sucrose than those taken by passerines or Microchiroptera. Again, similar to data for fruits and nectars taken by passerines, these data suggest Megachiroptera actively seek food sources with a specific sucrose content. The family comparisons with both Megachiroptera and passerine dispersed fruits showed significantly (New World passerine, P < 0.05; Old World passerine, P < 0.01) higher sucrose content for fruits taken by Megachiroptera (Table 4). The six families containing both taxa with fruits taken by Megachiroptera and those with fruits taken by Microchiroptera, however, showed no trend. This comparison may be anomalous because the number of families considered is low and that fruits taken by Microchiroptera and passerines are similar in sugar composition (see above).
CoNcLusIoNs.-Speculation is possible on the development of changes in sugar composition for nectar and fruit juice producing plants. The sequence of events may begin with the fleshy or arilate seeds of some gymnosperms (current representatives include Ginkgo biloba, Tdxus spp., and cycads). These species show low percentages of sucrose in their juices and could have set the stage for subsequent development of rewards for birds seeking nutriment from early angiosperms. Hexoserich fruit juice or pulp would have been a chemical search image for these early frugivores and there would have been an advantage to plants with this search image for both nectar and fruit juices. In any case, nectarivorous passerines are frequently frugivorous as well, so a similar search image might apply to both kinds of rewards. This may explain the similarity in patterns of sugar proportions between fruits and nectars of passerine birds. There is evidence that the switch to sucrose dominance in hummingbird flowers is correlated with changed morphological features of flowers as well as with the chemistry of nectars. It remains to be discovered whether these morphological changes preceded or followed the chemical evolutionary switch. If the morphological change precedes the chemical change, we would expect to see some examples of hummingbird flowers with hexose-rich

or hexose-dominated nectar. But there is no evidence for this in the data lists of Stiles and Freeman (1993) or in this investigation. The origin and early development of the Chiroptera is not clear. The earliest bat fossil is Zcaronycteris, having occurred during the Paleocene or Eocene in Wyoming (Jepsen 1970); however, other bats are known from the Eocene and later deposits in Europe (Hill & Smith 1985). The earliest tropical microchiropteran fossil is from the Miocene in the Magdalena Valley, Colombia (Savage 1951). The undertaking of flower and fruit visitation was probably later in development for Microchiroptera than for Megachiroptera; the flora feeding them may be more closely related to the original hexose search image than that of Megachiroptera, which became rapidly specialized in their vegetarian habits. The agreement between the sucrose percentage in fruits and nectars of Megachiroptera-visited flowers is further evidence for the chemical nature of these two nutritional sources being equally adaptive to bats of this suborder. The adaptive significance of greater sucrose content in the megachiropteran nectar and fruit juices is unknown; however, it is interesting that Fleming (1993) suggested that several life history features of Leptonycteris curasoae show a parallel evolution with the migratory, roosting, and mass foraging habits of Megachiroptera.

FUTURE INVESTIGATIONS.-ThC structures O batf pollinated flowers are such that there may be considerable contamination of nectar by pollen, which is abundantly produced in the flower. Over 20 years ago, Donna Howell (1974) suggested that flowers visited by Microchiroptera, particularly of the genus Leptonycteris, used pollen as a primary source of protein-building amino acids. Baker et al. (1971) photographed a bat of Leptonycteris sp. apparently biting an anther of a Ceiba acuminata flower in Mexico. Pollen contamination probably is also an important source of protein building in the diet of Megachiroptera. The magnitude of the contribution of pollen grains to the nutrition of nectarivorous taxa will be difficult to assess, but ultimately be essential before ecosystem analyses are possible. Soluble amino acids in nectar have been shown as being related to taxonomy and pollination syndromes in a mixed tropical and temperate sample (Baker 1977, 1978; Baker & Baker 1973, 1975, 1977, 1986; I. & H. G. Baker 1976a, b, 1979, 1982). It is possible that chemical analyses of other food sources will lead to similar patterns.

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Baker, Baker, and Hodges

ACKNOWLEDGMENTS
Many people collected and sent samples of nectar and fruit juice for our analyses. Several persons also were extremely helpful in handling of the literature search and discussion. We thank them all sincerely. Those aiding in the collection of samples, alphabetically: E. Alvarez-Buyulla, B. Alversum, D. Baum, P. Bernhardt, S. Bullock, P. Cox, P. DeVries, H. Dobson, l? Fiedler, T. Fleming, G. Frankie, I? Goldblatt, W. Haber, D. Harder, E. Heithaus, l? Hobdy, C. Jones, l? Kevan, S. Koptur, W. Kress,

D. Levey, C. Martinez del Rio, K. Milton, B. Mitchell, ? L. Newstrom, I Opler, J. Patton, 0. Pearson, E. Pierson, C. Quibell, I. Radkey, W. Rainey, N. Ramirez, C. Rick, D. Savage, D. Schemske, K. Steiner, W. Tang, T. Vaughan, C. Webb, and M. Weiss. They do not hold responsibility for the speculations included here. We would also like to thank J. Jones, F. Kim, 0. Miranda, K. Nguyen-Tan, and C. White for their help in preparing this paper for publication. This work was partially funded by the National Science Foundation (DE8-9726272 to SAH).

LITERATURE CITED
BAKER, . G. 1977. Non-sugar constituents of nectar. Apidologie 8: 349-356. H . 1978. Chemical aspects of the pollination biology of woody plants in the tropics. In P. B. Tomlinson and M. H . Zimmermann (Eds.). Tropical trees as living systems, pp. 57-82. Cambridge University Press, New York, New York. 1973. Amino acids in nectar and their evolutionary significance. Nature 241: 543-545. BAKER, G., AND I. BAKER. H. , A N D -1975. Studies of nectar constitution in pollinator-plant coevolution. In L. E. Gilbert and P H. . Raven (Eds.). Co-evolution of animals and plants, pp. 100-140. University of Texas Press, Austin, Texas. , AND - 1977. Intraspecific constancy of floral nectar amino acid complements. Bot. Gaz. 138: 183. 191. , A N D - 1979. Sugar ratios in nectars. Phytochem. Bull. V. 12(3): 43-45. . , A N D - 1982. Chemical constituents in nectar in relation to pollination mechanisms and phylogeny. . In M. H . Nitecki (Ed.). Biochemical aspects of evolutionary biology, pp. 131-171. University of Chicago Press, Chicago, Illinois. , A N D - 1983a. Floral nectar-sugar constituents in relation to pollinator type. In C. E. Jones and R. J. . Little (Eds.). Handbook of experimental pollination biology, pp. 117-141. Van Nostrand Reinhold, New York, New York. , AND - 1983b. A brief historical review of the chemistry of Aoral nectar. In B. Bentley and T. Elias . (Eds.). The biology of nectaries, pp. 126-152. Columbia University Press, New York, New York. , A N D -1986. The occurrence and significance of amino acids in floral nectar. Plant Syst. Evol.: 175. 186. , A N D - 1990. The predictive value of nectar chemistry to the recognition of pollinator types. Israel J. . Bot. 39: 157-166. , AND P. D. H u m JR. 1968. Intrafloral ecology. Annu. Rev. Entomol. 13: 3 8 5 4 1 4 . , R. W. CRUDEN, I. BAKER. AND 1971. Minor parasitism in pollination biology and its community function: the case of Ceiba acuminata. Bioscience 21: 1127-1129. I., 1976a. Analyses of amino acids in flower nectars of hybrids and their parents, with BAKER, A N D H. G. BAKER. phylogenetic implications. New Phytol. 76: 87-98. , AND - 1976b. Analysis of amino acids in nectar. Phytochem. Bull. 9: 4-7. . , A N D - 1979. Chemical constituents of the nectars of two Eytbrina species and their hybrid. Ann. . Mo. Bot. Gard. 66: 446-450. , AND - 1982. Some chemical constituents of the floral nectars of Eytbrina in relation to pollinators . and systematics. Allertonia 3: 25-38. 1993. Cladistic analysis of chloroplast DNA restriction site characters in Erythrina L. BRUNEACJ, A N D J. J. DOYLE. A,, (Leguminosae: Phaseoleae). Syst. Bot. 18: 229-247. CIIA.I.EIAT,T., E. KLANN, W. DEVERNA, YELLE,N D A. B. BENNETT. R. J. S. A 1993. Inheritance and genetic mapping of fruit sucrose accumulation in Lycopersicon chmielewskii. Plant J. 4: 643-650. DANIEL J. 1979. The New Zealand short-tailed bat, Mystacina tubercukztu: a review of present knowledge. N.Z. J. M. 2001.6: 357-370. DoRxr, K., AND T. PEIKERT-HOLLE. Bluten und Fledermause. Verlag von Waldemar Kramer, Frankfurt vam 1985. Main, Germany. DONOGIIUE, J. 1989. Phylogenies and the analysis of evolutionary sequences, with examples from seed plants. M. Evolution 43: 1137-1 156. J. 1985. Phylogenies and the comparative method. Am. Nat. 125: 1-15. FELSENSTEIN, FLEMING, H. 1988. The short-tailed fruit bat. University of Chicago Press, Chicago, Illinois. T. . 1993. Plant-visiting bats. Am. Sci. 81: 4 6 0 4 6 7 . C. 1985. FREEMAN, E., A N D R. D. WORTHINGTON. Some floral nectar-sugar compositions of species from southeastern Arizona and southwestern New Mexico. Madroiio 32: 78-86. , W. H. REID, AND J. E. BECVAR. 1983. Nectar sugar composition of species from southeastern Arizona and southwestern New Mexico. Madrofio 32: 78-86.

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, R. D. WORTHINGTON, K. D. CORRAL. AND 1985. Some floral nectar-sugar compositions from Durango and Sinaloa, Mexico. Biotropica 17(4): 309-313. , R. D. WomHiNaaN, AND M. s. JACKSON. 1991. Floral nectar sugar compositions of some south and southeast Asian species. Biotropica 23(4b): 568-574. HARVEY, H., AND M. D. PAGEL. I? 1991. The comparative method in evolutionary biology. Oxford University Press, Oxford, England. HEI.I.HAUS, R. 1982. Coevolution between bats and plants. In T. H. Kunz (Ed.). Ecology of bats, pp. 327-367. E. Plenum Press, New York, New York. HERNANDEZ, AND C. MART~NEZ Kio. 1992. Intestinal disaccharidases in five species of phyllostomoid bats. A., DEL Comp. Biochem. Physiol. 103B: 105-1 11. HERRERA, M. 1992. Interspecific variation in fruit shape: allometry, phylogeny and adaptation to dispersal agents. C. Ecology 73: 1832-1841. HILL, E., AND J. D. SMITII. J. 1985. Bats: a natural history. British Museum (Natural History), London, England. HOWELL, J. 1974. Bats and pollen: physiological aspects of the syndrome of chiropterophily. Comp. Biochem. D. Physiol. 4 8 A 236-276. 1993. Floral biology of Hornstedtiu scottiunu Zingiberaceae in a lowland rain forest IPPOLITO, AND J. E. ARMSTRONG. A,, of Australia. Biotropica 25: 281-289. JEPSEN, L. 1970. Bat origins and evolution. In W. A. Wimsatt (Ed.). Biology of bats, pp. 1-64. Academic Press, G. New York, New York. JORDANO, 1995. Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints P. in plant-animal interactions. Am. Nat. 145: 163-191. KRESS, J. 1985. Bat pollination of an Old World Heliconiu. Biotropica 17: 302-308. W. KUNZ,T. H., AND C. A. DIAZ. 1995. Folivory in fruit-eating bats, with new evidence from Artibeusjumuicensis (Chiroptera: Phyllostomidae). Biotropica 27: 106-120. MADDISON, F 1990. A method for testing the correlated evolution of two binary characters: are gains or losses W. ! concentrated on certain branches of a phylogenetic tree? Evolution 44: 539-557. MARSHALL,J. 1983. Bats, flowers and fruit: evolutionary relationships in the Old World. Biol. J. Linn. Soc. 20: A. 115-135. MARTfNEZ DEL KIO,C. 1990. Sugar preferences in hummingbirds: the influence of subtle chemical differences on food choice. Condor 92: 1022-1030. , H. G. BAKER, I. BAKER. AND 1992. Ecological and evolutionary implications of digestive processes: bird preferences and the sugar constituents of floral nectar and fruit pulp. Experientia 48: 544-45 1. , AND W. H. KARASOV. 1990. Digestion strategies in nectar- and fruit-eating birds and the sugar composition of plant rewards. Am. Nat. 136: 618-637. MAZER, J., AND N. T. WHEELWRIGHT. Fruit size and shape: allometry at different taxonomic levels in birdS. 1993. dispersed plants. Evol. Ecol. 7: 556-575. OCUNLKJYI, AND E. E. OKON.1976. Studies on the digestive enzymes of the African fruit bat Eidolon helvum 0. A,, (Kerr). Comp. Biochem. Physiol. 55A: 359-361. PIEKSON, D., V. M. SARICH, M. LOEWENSTEIN,J. DANIEL, W. E. RAINEY. E. J. M. AND 1986. A molecular link between the bats of New Zealand and South America. Nature 323: 60-63. POIUNIN, 1988. Plants and flowers of Malaysia. Times Editions, Singapore, Malaysia. I. SAVAGE, E. 1951. A Miocene phyllostomid bat from Colombia, South America. University of California Publ. D. Bull., Geol. Sci. 28: 367-365. SCOGIN, AND C. E. FISEEMAN. K., 1984. Floral pigments and nectar constituents in the genus Puyu (Bromeliaceae). Aliso 10: 617-619. SMITH, 1969. Chromatographic and electrophoretic techniques, Vol. I. Chromatography, 3rd edition. W. HeineI. mann, London, England. STILES, G., AND C. E. FREEMAN. F. 1993. Patterns in floral nectar characteristics of some bird-visited plant species from Costa Rica. Biotropica 25: 191-205. VAN DER PIJL,L. 1982. Principles of dispersal in higher plants. Springer-Verlag, New York, New York. WELTY, C. 1982. The life of birds, 3rd edition. CBS College Publishing, New York, New York. J.

APPENDIX 1.
Previous studies on sugar composition of floral nectars have been numerous (reviews in Baker and Baker [1983a] and Stiles and Freeman [1993]). Our method of analysis for sugars in nectars involved sampling freshly produced nectar with a finely drawn out micropipette, spotting the nectar immediately onto chromatography paper and drying it promptly to await analysis. If kept perfectly

dry, the spot will not change in composition for many years. To analyze sugar in fruit pulp, the appropriate part of the ripe fruit was smeared onto chromatography paper to produce a spot that could be analyzed by the same method as the nectar. In the laboratory, the spot was eluted with distilled water and the solution concentrated in a vacuum desiccator. Respotting on Whatman No. 1 chromatography paper was followed by separation of sugars by single-direction descending paper

570

Baker, Baker, and Hodges

jl
20

/; ;
. P
0

Pm 0

- - 0 - - Fructose - e- -Glucose

20

40

60

80

% Sugar Baker et al.

APPENDIX FIGURE 1. Comparison of percent sugar in the total sugar pool of nectars analyzed independently by both HPLC (Freeman et al. 1983, 1985, 1991) and by paper chromatography (this paper). Lines indicate best-fit linear regressions (sucrose y = 9.0 + l . l X , R2 = 0.75; P < 0.0001; fructose y = 2.7 + 0.71X; R2 = 0.45, P < 0,001, glucose y = -6.2 2 l.Ox, R2 = 0.79, P < 0.0001; N = 26). Species sampled and analyzed independently by both groups of workers are indicated in Appendix 2.

chromatography. The solvent system used n-propano1:ethyl acetate:water (14:4:2, v/v/v), a slight modification ofthat given in Smith (1969;p. 134). The increased proportion of ethyl acetate compacted the individual sugar spot considerably. The running time was usually 65-72 h; several nectars could run at a time. A standard mixture of known sugars was run on each paper as a control. After air drying, the papers were dipped in staining reagent consisting of two solutions mixed just prior to use. Solution A was 75 mg of oxalic acid dissolved in 15 ml of ethanol; Solution B contained 150 mg of p-aminobenzoic acid in 25 ml of chloroform and 2 ml of acetic acid. Again after airdrying the papers were held at 110C for 20 min, by which time pentoses became red, and all other sugars produced a brown color. Under ultraviolet illumination, all sugars fluoresce, and each spot could be outlined in pencil. In this manner, spots could be detected even when the amount of sugar in question was too small to produce detectable color in visible light. After cutting out individual sugar spots, the stained sugars were eluted into 4 ml of 50 percent methanol, and their fluorescence was measured in

a filter fluorometer (Turner model 111 with primary filter Kodak 12). Calibration curves correlating fluorescence values with amounts of sugar were obtained for each sugar using chromatography of known quantities to obtain their fluorescence values in the same manner. Because correlations are linear only in dilute solutions, it was necessary on occasion to dilute the stained sugar solution further with 50 percent methanol. By this method, sugar amounts from 0.5 mg upwards could be estimated quantitatively. An important technical point is that nectar and fruit pulp must not be allowed to stand in the liquid condition. If it does, large amounts of sucrose may be broken down, increasing glucose and fructose concentrations; this may be caused by natural acidity of nectar or fruit pulp, be due to enzymes occurring naturally in nectar or fruit pulp, or is brought in by microorganisms (especially yeasts). For the record, most nectars are acidic (the lowest in our experience being pH 2.8 in Strehzia reginu), although alkaline nectars do occur (up to pH 10 in Kburnum costaricanum [Baker & Baker, pers. obs.]). Freeman and collaborators used high perfor-

Sugar Composition of Nectar and Fruit Pulp

571

mance liquid chromatography (HPLC) to quantify nectar composition to one-tenth of a percent. There are relatively few occasions when Freeman et a/. (1983, 1985, 1991) worked with the same species nectar that we investigated. For those species in which both laboratories independently investigated, however, the results were quite similar (Fig. 1). Our percentages were calculated to the nearest whole number and we believe remarkable agreement exists between the data derived from two different methods, especially when considering that nectars were from different localities and without controls. It is very encouraging that different workers can produce comparable data. We suggest that the cruder paper

chromatography is quite capable of revealing patterns in nectar and fruit juice composition. HPLC apparatus can yield more sensitive results and should be used when available; however, the increasing need for studies of reproductive biology to be carried out by indigenous investigators means that the highly sophisticated machinery may not be available to many workers. We hope this paper shows that the biology of plant/animal relations can progress with the increasing number of investigators and reveals the need for information of a naturalistic kind to work in conjunction with chemical analyses of plant products and studies of animal preferences.

APPENDIX 2. Sugar composition o f nectars andfrtlits )om tropical and subtropical regions worh'wide. Percentages o f total soluble sugars due to fructose followed by sucrose are

given [values for percent glucose can be obtained by 100 - (% Fructose + % Sucrose)]. Values are separated according to their major pollinator or disperser classes (hummingbirds [HI, passerine birds in the Old World [Po]and New World [Pn], bats in the Old World [Co] and New World [Cn]), *passerineand batpollinated fhummingbird and bat pollinated). When multiple determinations of sugar composition were made f i r a particular species, the averages are reported. Species independently collected and analyzed by HPLC (Freeman et al. 1983, 1985, 1991) are indicated

c).

% !
Cn

Fruit co Cn P O Pn co

Family

Species

H
P O

Nectar Pn

-' -' 2
Q

Acanthaceae

5
( P

v)

C D

7.
38, 36, 48, 54, 50, 16 1 7 9 3 12

35, 42 44, 37 31, 62 30, 60 41, 32 36, 45 29, 49 33, 36 35, 49 23, 55 29, 48

Agavaceae

Aloeaceae

Anacardiaceae

43, 5 34, 0 29, 13 42, 5 53, 2

55, 0
48. 0 59, 9

35, 55 42, 17 54, 1 43, 0

48, 19

Annonaceae

47, 8

Aphelandra aurantiaca A. deppeana" A. sp. Dicliptera iopus' D. sp. Hansteinia blepharorachis' Iwticia aurea' J. oerstedii sp. Poikalacantbw marranthus Razisea picata" Eicanthera gigantea Agave havardiana" A. palmen*" A. pawyP A. sbawii Aloe arboresrens A. aristata A. bumilis A. parvula Kniphofia sp. Anacardium excelsum Mangifera indica Scbinw mollis Spondias dulcis S. mombin Annona cberimola A. sqtlamata Cananga odorata Cymbopetalum baillonii Guamia sp.

38, 12

APPENDIX 2.
Nectar Species
Po Pn

Continued.

Fruit co Cn

Family

H
Po
Pn co

Cn

Apocynaceae

51, 9

56, 20 62, 0 76, 2 13, 40

15, 71

Aquifoliaceae Araceae

36, 52 21, 58 48, 7

Araliaceae

Carissa edulis Neisospemza sp. 1 N sp. 2 Ochrosia sp. Stemmadenia donnell-smithii Tabernaemontana arborea Thmetia neriifolia Z ovatu Ikx anomakz Anthurium macrolobium A. sp. Spathiphyllum sp. Xznthosoma sp.* Cbeirodendron helleri

47, 6 38, 3 54, 11 53, 8 28, 26

51, 0 28, 6 21, 0 51, 0 45, 14 42, 4 23, 4 30, 5 34, 20 38, 35

c. mgyna

Arecaceae

Basellaceae Bignoniaceae

18, 7 3

45, 2 43, 20 34, 26 33, 28 36, 40 42, 7

Dendropanax arboreus D. zonatopodis Scbefira digitata Geonoma sp. Licuala spinosa Phoenix &ctyl+ra Pgchosperma elegans l? sp. Basella rubra Campsk grandiJora C. radicani Crescentia alata C. cujete C. dactylon Distictis buccinatoria D. sp. Kigelia sp. Teeomaria capensis

13, 81 34,37

u1 l

APPENDIX 2.
Nectar Species Fruit co Cn

Continued.
Po Pn

Family

H
54, 34 36, 48 40, 25 38, 33 53, 2 48, 9 41, 5 49, 5

Po
Pn co

Cn

% me % "C
P , 3

Bombacaceae

61, 2 49, 0 42, 37 35, 31 32, 49

I
0 0

P
v)

Adansonia za bar. bozy A. digitata Bonzbacopsis quinatum Bombax buonoaozensis B. sp. Ceiba acuminata' C. pentandra Cborisia p e r i o d Durio mahccensis D. zibetbinw Ocbroma Iagopus Quararibea asteriolepis

l D

Boraginaceae

Q. SP.
48, 4 49, 2

41, 43 45, 3

Bromeliaceae

26, 52 9, 78 16. 61 37,37

50, 1

Cactaceae

39,20 7 36, 1 39, 4

Campanulaceae

Capparidaceae Cannaceae

Cordia panamensis c. sp. Puya alpestris l? chilensis I? coriacea l?h a l? macrura I! raimondii I! violarea Carnegiea gigantea Lmaireocerew tbruberi Opuntia sp. Scblumbergera sp. Burmeistera sp. Centropogon solanifaliuso C. talamancensis" C. vakriP c. sp. 1 sp. 2 c. sp. 3 sp. 4 Crateua tapia Canna indica sp. 29, 65 33, 36 17, 80 48, 42 38, 53 33, 57 2, 97 4 , 96 39, 53 25, 5 1 26, 50 39, 3

c. c

c.

Sugar Composition of Nectar and Fruit Pulp

575

rn
Ln Ln

6 Ln

w r n

d v ;

w" w

3 3

0 l n 2 0" 0

0 -

u l

APPENDIX 2. Continued
Nectar Species
co

m
Fruit Cn 52, 1 53, 16 64, 3 40, 10 30, 52 32, 51 50, 7 52, 1 24, 76 45,46 21, 74 27, 70 22, 57 11, 82 32, 48 24, 58 18, 61 4, 94 14, 58 27, 69 50, 3 5, 3

Family Erythroxylaceae Euphorbiaceae 26, 9 24, 55

H
Pn

Po

Pn

co
Po

Cn

-c

% -2

5
68, 0

P
P
( P

Flacourtiaceae

Gentianaceae Gesneriaceae 32, 57 54, 39

Goodeniaceae

Greyiaceae Guttiferae

71, 7

54, 1 61, 4 51, 4 49, 1 52, 7 23, 50 25, 52

Erythroxylum mattos-silvii Euphorbia pulcherrima Hura crepitans Pedilanthw carinatus Pera sp. Casearia aculeata C. ylvestris Ryparosu javanica Symbolanthus sp.* Alloplectus tetrugonus" Beskria columneoides" B. sp. Drymonia gayana D. serrulata Columnea virginica c. sp. 1 c. sp. 2 c. sp. 3 Drymonia Fmbriatu D. serrulata D. spectabilis D. sp. 1 D. sp. 2 D. sp. 3 D. sp. 4 Kohkria elegans Rhabdothamnussolanderi Scaevola gaudichaudiana S. kilaueae S. mollis S. taccaah Greyia sutherlandii Garcinia mangostana G. xanthocLymw Mammea odorata

APPENDIX 2.
Nectar Species H Fruit co Cn

Continued.

Family

Po
Pn co

Po

Pn

Cn

Haemodoraceae Heliconiaceae

0, 73 26, 33 26, 28

40, 5

51, 4 22, 70 28, 39 49, 1 39, 0

0, 70

24, 39 17, 57

Hydrangeaceae

Icacinaceae Iridaceae

47, 6

Labiatae

9, 87 13, 82 22, 7 2 43,34 63, 1

21, 58 3, 88 28, 42 63, 1 52, 6 55, 1 53, 6 10, 1 5 38, 16

Lauraceae

42, 1 21, 5 5 10,81 4, 93

49, 1 36, 29

5 2
g
Q

Lecythidaceae Leguminosae

5. 40, 21 41, 19 40. 10 35, 19

7J

9 -

5
u l

Anigomntbos manglesii Heliconia bibai H. birsuta H. nutans H. paka H. papuana H. iostrata H. solomonemis H. subulata H. tortuosa" Broussaisia arguta Pennantia corymbosa Mappia racemosa Anapalina cafia A. nervosa Antbolyza ringens Klattia &va K piatula K stokoei Witsenia maura Leonotis leonurus Pycnostacbys reticulata Salvia aetbiopis S. divinorum S karwinskii . S splendens . Stenogyne minutifora Beilschmiedia pendula Ocotea sp. Barririgtonia miatica' Bauhinia aculeata B. emarginata B. ghbra B. rnultinervia B. pauleltia B. rutilans B. unguhta
22, 46

Baker, Baker, and Hodges

4
d

m
T

m
00-

APPENDIX 2.
Necror -

Continued.
Fruit

Family
co

Species

H
Po
Cn

Pn

c o
Po Pn

Cn

28, 49 19, 57 26, 51 41, 4 36, 4 36, 31 19, 7 2 46,20 35, 19 37, 4 30, 43 41, 2

37, 5 49, 2 46, 4

21, 66 58, 2

33, 36 35, 55

48, 4 35, 33 48, 15

32, 41

Liliaceae

20, 7 2 44,55 49, 2 34, 5 33, 1 44, 6 35, 2

70, 5 52, 0 48, 14

48, 42

! 3

Loasaceae Lobeliaceae

E. sandwichensis E. senegalensis E sigmoidpa E. srnitbiana E. speciosa E. suburnbrans E. standleyana E. tabitensis E. tajurnucensis E. uerna E. uespertilio Hyrnenaea courbaril Inga tonduzii I. Vera" I. Vera Inocarpus jzgqer Mucuna andreuna M. pruriens M. rostratd Parkia biglobosa Pbaseolus sp. Scbotia brahypetala Sesbaniu formosa Asparagus sprengeri Astelia neruosa Bomarea rostarirense B. sp. Cliuia rniniata Collospennum bastaturn Doiyantbes excelra Eucnidp aurea Clermontia kakcune C. persicifolia
12, 85

E.

43, 36

Loganiaceae

c. sp. Cyanea angustifolia Fagraea berteriana

ul

APPENDIX 2.
Fruit co Cn Species

Continued.

03 0

m e,
Cn

Family

H
Po
Pn

Nectar Pn

Po
co

Loranthaceae

60, 2 59, 1 47, 1 59, 0 56, 7 39, 0 45, 0 47, 6 43, 1 1 61, 3 41, 12 48, 4 42, 3 40, 1 1 , 98 50, 3 48, 2 40, 4 68, 5 49, 3 44, 4 43, 1 46, 2 61, 1 47, 0

-6
5
5 2

W e,

26, 49 21, 46 13, 80

( I

Lythraceae

Mdvaceae

Marcgraviaceae

39, 44

53, 6

Melastomataceae

Amyema miquelii A. pendulum A. quandzng Ileostylus micrantbus Oryctantbus sp. Psinarantbus sp. Tupeia antarctica Cuphea caecilae C. spectabilis Abutilon menziesii Gossypium sandvicense Hibiscadelpbus distans H. giffardianw Hibiscus elatus H. firrcellatus H. kokia H. S .jobnianus t H. waimeae Kokia dtynarioides Malvaviscus arboreus Marcgravia brownii M. nepentboides M. s< Norantea sp. Clidemia birta C. septuplinervia Conostegia cinnamomea Leandra consimilis Melastoma malabatbricum Miconia afinis M. centrodesma M. bondurensis M. impetiolaris M. sp. Mouriri myrtilloides Ossaea micrantba 0. quinquinervis

40, 6 38, 6 58, 3 62, 1 55, 2 49, 0 46, 6 48, 1

APPENDIX 2.
Nectar Species Fruit

Continued.

Family

H
Po
Pn

Pn
co

co 45, 1

Cn
Po

Cn

Meliaceae Melianthaceae

Moraceae

51, 2 55, 1

38, 24 34, 34
44, 14 45, 2 41, 20

59, 14 21, 3 47, 3

50, 3
58, 2 47, 3

52, 0 36, 3 34, 4 48, 7 66, 1 38, 1 51, 1 33, 41

P
'0

Musaceae

20, 57

s 3
25, 49 36, 26 24, 48 48. 13 46; 3 63, 1 80, 2

G. rr 2
9
42, 1

Myrsinaceae

8 e

2 Q
57, 1

Myrtaceae

58, 3 51, 5

3
G A

59, 2 62, 8 39, 1

L u
u1

Agkzia sp. Melianthw comosus M. m jo r Artocarpw altilis" A. heterophyhd Brosimum alicastrum Ficw capensis E costaricana E dugandii E g-ofii E inripidz E obliqua E popenoei E scabra E tinctoria E trigonatdt E yoponensis E sp. 1 E sp. 2 E sp. 3 Moms alba Musa balbisiana M. coccinea M. textih M. sapientum M. sp. Ardisia compressa A. revoluta Cybianthw sp. Myrsine kssertiana M. sandwicense Gallistemon sp. Eucalyptus f;.;f.lia Eugenia jambos E. nesiotica Metrosideros collina M. exceha

73

??

APPENDIX 2.
Nectar Species Fruit

Continued.
e,

m
Cn

Family

H
Po

Pn

c o

CIl

Po

Pn
c o

4 m -F
e,
P ,

M. kermadecensis M. polymorpha M. umbellata

41, 5 46, 0 41, 1 1 35, 1 42, 5 27, 23 22, 50 12, 83 36,40 14, 84 44, 7 49, 4 48, 6

46, 9 44, 3 44, 2

L1

50, 27 54, 1 48, 15

I 0 Q u3

2 !

Nyctaginaceae Olacaceae Onagraceae

Psidium guajava I! canleianum Syzygium floribundum S inopbylloides . S paniculatum . S sandwicense . s. sp. Neea sp. Heisteria acuminata Fuchsia abrupta E: boliviana E colensoi E excorticata E jimenezii E magellanica E procumbens E regia E vulcanicola 41, 9 31, 60 24, 46 38, 36 34, 62 21. 61

E sp.

Oxalidaceae Pandanaceae

Papaveraceae Passifloraceae

6, 87 6 , 92

72, 0

45, 8 24, 23 51, 26 51, 2 49, 1

Phytolaccaceae

37, 1 7 43, 2 52, 12 29, 43

Lopezra langmaniae Xylonagra arborea Averrboa carambola Freycinetia reineckei E scandens Pandunus tectoriw Sararanga sp. Bocconia sp. Passzf2ora incarnata I! mollissima I! nitida Pbytolacca rivinoides I? sp. 1 I! sp. 2

APPENDIX 2.
Nectar
Fruit

Continued.

Family

Species

H
Po
Pn co Cn Pn co

Po

Cn

Piperaceae

51, 1 47, 3 45, 25 44, 23 53, 4 44, 13 41. 22 54, 2 40, 6 40, 2 53, 4 34, 1 1 48, 18 46, 33 12, 63 5 1 , 10 30, 17 36, 19 54, 1 31, 56 22, 7 2 44,44

Polemoniaceae

Polygalaceae Polygonaceae

Proteaceae

Rosaceae Rubiaceae

60, 16 49, 2 38, 22

37, 3 46, 1 47, 6

40, 43

I Q c.
c

P+er auritum I? dotarum" I? silvivagum I? sp. Cantua candelilla C. pyrfolia Cobaea scandens Loeselia ciliata Monnina sp. Coccoloba caracasana* C. padifomis' Banksia ericifolia B. spinulosa Grevillea robwta' Protea rynaroides Stenocavpm sinuatus Telopea o r e a h I: peciosissirna Rubw rositfoolius Alberta magna Bobea ekztior Cantbium odoratum Cephaelis axilkzris C. elata" Cbione costaricensis Coffea arabica" C. liberica C. robusta Coprosma ernohoihs C. grandiflora C. montana C. parvzjlora C propinqua C. rbyncocavpa C. robusta C. rotundifolia C. rugosa C. waimeae 60, 25 40, 41 35, 1 41, 0 48, 2 47, 12 40, 5 46, 6 43, 3 30, 7 47, 4 31, 2

cn

03
W

03 P

Cl J

APPENDIX 2.
Fruit
co
co

Continued.

Family
44, 1 1 61, 6 38, 3 38, 7 46, 5 41, 1 1 35, 1 35, 12 66, 1 48, 1 39, 7 33, 12 43, 7 43, 3 45, 7 59, I 61, 3 38, 1 49, 7 37, 6 41, 4 57, 1 43, 33 25, 50 26, 44 20, 63 51, 5 33, 37 53, 0 23, 30 24, 58 21, 66

Species

Po

Nectar Pn

Cn

Po

Pn

Cn

% -2 % -2
Q

Q 0

5
$

Sapindaceae

22, 62

Sapotaceae

40, 39

43, 21

Scrophulariaceae
36, 48 33, 45

Simaroubaceae

Faramea occidentalis Gonzahgulnia rosea Gouldia teminalis Hamelia patens' Hofmannia sp. Nertera depressa Palicourea sp. Psychotria acuminata I! de&a I! Prcata I! gracilifolia I! gracilis I! grandistipula I! horizontalis I! macrodon I! mapourioides I! marginata I! ojicinalis I! tonduzii I! sp. 1 I? sp. 2 Xerococm nubosea Cupania sylvatica Cupaniopsis sp. Litchi chinensis Nephelium lappaceurn N.bngana Paullinia sp. Manilkara achras M. zapota Planchonella torricellensis Hebe speciosa Russelia samentosa R. verticellata Picramnia catpinterae Quassia amara'

APPENDIX 2. Concinued.
Nectar Species
16, 7 2 33, 3 52, 3 69, 6 41, 2

Fruit co Cn

Family

H
Po
Pn

Po
Pn

co

Cn

Smilacaceae

Solanaceae
26, 5 5 25, 71 29, 55

54, 2
74, 9 72, 8 71, 15 17, 67 17, 61 23, 25 19, 77 20, 60

40, 1

55, 14
38, 47 24, 46 59, 0

34, 2 40, 33
46, 7 38, 43 41, 33 28, 39 56, 20

cn.

28. 68

Sonneratiaceae Strelitziaceae

54, 3
43, 2 32, 25

Lapageria rosea Smilax sp. 1 s. sp. 2 s. sp. 3 Acnistus arborescens Brugmansia sanguinea Capsicum anuum Cestrum diurnum C. purpureum C. racernosum Iochroma jkbsioides Lycianthes amatitlanensis L. mu~h;flora Lycopersicon chilense L. chmiekwskii L. pennellii L. peruvianum L. pimpinellifolium Markea neurantha Nzcotiana glauca N. otophora? Solanum brenesii" S. corakvense S. laciniatum S. nr. ciliatum S quitoase . s. sp. Streptosolenjamesonii Witheringia solanacea Sonneratia sp. Ravenala mahgascariensis* Strelitzia nicolai S. regina

APPENDIX 2.
Nectar Species

Continued
Fruit co Cn

0 P UY

I
cn a l

Family

H
Po
Pn

Po

Pn

co
52, 3

Cn

Sterculiaceae

S ymplocaceae

14, 78 18, 68

50, 6

Theophrastaceae Thyrnelaeaceae

Tiliaceae Urticaceae 8, 84

Chiranthodendronpentadactyln Helicteresguazumaefolia Symplocos sp. Chu;ia integrzjdia Wikstroemiafircata sp. Luehea speciosa Urera caracarana' 47, 25

36, 16 47, 9
70, 4

Verbenaceae

u. sp.
25, 50
0, 79 17, 76

37, 5
28, 1 55, 0

Xanthorrhoeaceae Zingiberaceae

Cleroa'endrum speciosissimum Lantana camara Staclytaqbeta fianzii Premma sp. Xzntborrboea australis Cosm puluerulenhlp 41, 1 1

73, 0

c. sp.