baker 1999 sugar composition of nectars and fruits consumed by birds and bats in the tropics and...

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. The 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 full 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 acknowledg- ment that historical factors can strongly influence correlations among characters of species (Harvey & Pagel 1991). As pointed out by others (.g., Felsen- stein 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 en- vironments (Harvey & Pagel 1991).

Received 27 March 1997; revision accepted 12 August

Deceased 9 November 1989 1998.

As an example of how correlations utilizing species data can be misleading, Donoghue (1 989) 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 (1 9 9 9 , however, after controlling for historical effects, found that fruit di- ameter 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 (1 993) found evidence supporting the hypothesis that length of fruits was an adaptation for gape- limited 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-

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560 Baker, Baker, and Hodges

cies were grouped according to their probable in- sect 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 (Microchirop- tera). 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 (rang- ing 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 de- pend on nectar supplies and insects for their nour- ishment. 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; Dan- iel 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 (1 982) provided a general review of relationships between bats and plants. A model treatment of a single species (Carollia perspicillata Microchirop- tera) 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 vol- unteers (see Acknowledgments). Many of these samples were submitted by experts on the taxa con- cerned. 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

Sugar Composition of Nectar and Fruit Pulp 561

TABLE 1 . Mean percent sucrose in nectars o f 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. Using family means a Kruskal-Wallis test and Mann-Whitney U-test between each pair of pollinator classes (I' < "0.05, *"O.OI, ***0.001, *x*xO.OOO1) were calculated.

Pollinator Families f class (N, range, CV)

Genera f Species .t (N, range, CV) (N, range, CV)

H 58.0

Po 7.4

Pn 1.9

co 41.0

en 18.3

(33, 18.0-89.5, 24)

(24, 0-30.9, 99)

( 5 , 0-3.7, 75)

(1 1, 9-93, 60)

(14, 3-51, 68)

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)

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)

Kruskal-Wallis H = 65.0, P << 0.001

Mann-Whitney PO Pn c o c:n

H 790**** 165*** 286** 448**** Po loo* 248**** 272"* Pn 55** 69** c o 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. On 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


TABLE 2. Mean percent sucrose in f iu 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 Kruskal- Wallis test and Mann- Wbitney U-test between each pair ofpollinator classes (P < 70.10, *0.05, *"O.OI) were calculated.

Disperser Families X Genera 2 Species 2 class (N, range, CV) (N> range, CV) (N, range, CV)

"0 7.9

I'n 8.2

<:0 23.5

Cn 8.5

(27, 0-41, 118)

(37, 0-37, 117)

(22, 0-51, 81)

(15, 0-21, 79)

8.0 7.6

7.8 9.9

24.0 21.9

9.1 8.4

(41, 0-41, 118)

(61, 0-58, 137)

(32, 0-55, 84)

(19, 0-27, 91)

(64, 0-41, 122)

(96, 0-77, 156)

(42, 0-63, 91)

(27, 0-33, 107)

Kruskal-Wallis H 8.32, P < 0.05

Mann-Whitney I'n c o Cn

P O 50 1 418* 229 Pn 572** 307 C O 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 Me- gachiroptera 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 fre- quency 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 (4 species 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. Distri- butions 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 Mega- chiroptera 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-


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, bats in the Old World [Co] and 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 H P c o Cn

Acanthaceae 47.6 (6, 1 1 ) 16.0 ( 1 , 1 ) Apocynaceae 55.0 ( 1 , 2) 71.0 (1, 1) Bignoniaceae 66.0 (2, 3) 4.5 (2, 2) 40.0 (1, 1) 24.7 ( 1 , 3) Bombacaceae 17.5 (2, 3) 41.7 (3, 4) 14.8 (5, 6) Bromeliaceae 57.0 ( 1 , 4) 2.3 ( I , 3) Cactaceae 65.0 (1, 1) 13.7 (3, 3) Ericaceae 62.5 (2, 5) 2.0 (1, 3) Euphorbiaceae 42.0 (2, 2) 16.0 ( I , 1) Gesneriaceae 59.4 (5, 14) 3.0 ( 1 , 1) Heliconiaceae 52.2 ( 1 , 6) 4.0 (1, 1) 48.0 ( 1 , 2) Labiatae 68.8 ( 1 , 4) 10.7 (3, 3) Leguminosae 58.2 (4, 31) 3.0 (2, 24) 35.7 (3, 3) 18.4 (4, 9)

Loranthaceae 49.0 (1, 1) 2.8 (3, 5) Liliaceae 63.5 ( 1 , 2) 2.0 (1, 1)

Malvaceae 44.0 ( 1 , 1) 22.2 (5, 10) Marcgraviaceae 2.5 (2, 2) 4.5 (2, 2) Onagraceae 60.0 (3, 9) 6.3 (1, 3) Polemoniaceae 54.0 (2, 3) 23.0 ( 1 , I ) Proteaceae 7.1 (4, 6) Rubiaceae 54.1 (4, 5) 11.0 ( 1 , 1) Scrophulariaceae 46.5 ( 1 , 2) 0 (1, 1) Solanaceae 59.2 (5, 5) 30.0 (2, 2) Sterculiaceae 78.0 (1, 1) 6.0 (1, 1 ) Strelitziaceae 13.5 (1, 2) 20.0 (1, 1)

10.0 (1, 1 )

Pollinator classes comDared

Sign test No. families P

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 outstand- ing low percentages of glucose in the nectars of Gesneriaceae (Appendix 2) appear to be a charac- teristic 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 seed- disperser 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 pro- vide 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 nectar- and fruit-sugar compositions consumed by birds and bats separately.

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


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 gven (no. families) with results of sign tests.

Disperser class

Family Po Pn c o Cn

Anacardiaceae 0 (1, 1) 36.0 (2, 2) 13.5 (2, 2) Annonaceae 0 (1, 1) 0.5 (2, 2) 12.0 (1, 1) Apocynaceae 9.0 (1, 1) 1.0 (2, 2) 30.0 (2, 2) Araliaceae 17.0 (1, 2) 1.5 (2, 3) Araceae 7.8 (2, 3) 0 ( 1 , 1) Arecaceae 4.3 (2, 3) 14.0 (1, 1) 35.0 (1, 1) Dillrniaceae 5.0 (I , 1) 2.0 (1, 1) Elaeocarpaceae 0 (1, 1) 0 (1, 1) 11.0 (I , 1) Flacourciaceae 31.0 (1, 2) 0 (1, 1) Gesneriaceae 1.0 (1, 1) 5.0 (2, 2) Guttiferae 7.0 (1, 1) 51.0 (2, 2) Lauraceae 1.0 (1, I ) 1.0 (1, 1) Liliaceae 6.3 (3, 3) 42.0 (1, I ) Melastomataceae 1.0 (1, 1) 2.3 (6, 12) Moraceae 2.0 (1, 1) 12.1 (3, 10) 8.7 (2, 7 ) Musaceae 41.0 (1, 1) 48.0 ( I , 1) Myrsinaceae 4.8 (2, 4) 1.0 (1, 1) Myrtaceae 2.5 (2, 4) 5,0 (1, 1) 8.0 ( I , 2) 14.5 (2, 2) Piperaceae 25.0 ( I , 1) 1.0 ( I , 1) 2.0 (1, 2) Rubiaceae 11.9 (6, 16) 5.9 (8, 22) 43.0 (1, 1) Sapindaceae 3.0 (2, 2) 45.5 (3, 4) Sapotaceae 37.0 (1, I) 39.0 (1, 1) 21.0 (1, 1) Solanaceae 0 (1, 1) 16.1 (7, 14) 9.3 (2, 3)

Verbenaceae 0.5 (2, 2) 0 (1, 1) Urticaceae 4.0 (1, 1) 5.0 (1, I)

Disperser classes Sign test

P0:Pn 6:5 NS 1’n:Co 1:8 (1 ) <0.05 Pn:Cn 4:5 (1) NS I’0:Co 0:8 <0.01 C0:Cn 3:3 NS

compared No. families P

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. Humming- bird-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 Er- ythrina 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


chemistry may have shifted from a low sucrose content to high more than once, with the repeated evolution of hummingbird-pollinated species (Bru- neau & Doyle 1993, I. Baker & H. G. Baker 1979, 1982, H. G. Baker & I. Baker 1990). Shifts back to low sucrose nectars may also have occurred. Un- fortunately, many of the species analyzed here are not the same as those used for the available phylogenetic reconstruction (Bruneau & Doyle 1993) so we are not able to determine how many times the shift in nectar chemistry has occurred in this genus.

Similar striking shifts in nectar sucrose content are true for other genera. In the genus Puya (Bro- meliaceae), the nectar sugars of five hummingbird- pollinated species averaged 57 percent sucrose, while the contents of nectar from three passerine- bird pollinated species averaged only 2.3 percent sucrose (Table 3; Scogin & Freeman 1984; Baker & Baker 1990). Likewise, in the genus Fuchsia eight hummingbird-pollinated species averaged 50 percent sucrose while three species pollinated by passerines averaged only 5 percent sucrose. Similar intrageneric shifts in sucrose content of nectars have been found in Campsw and Heliconia (Ap- pendix 2). Thus, these shifts are likely to have occurred many times during the evolution of species with contrasting pollination systems.

An important contribution to understanding the difference between nectars consumed by hummingbirds and those consumed by passerines has been provided by the work of Martinez del Rio (Martinez del Rio & Karasov 1990, Martinez del Rio et al. 1992). These authors have shown that many passerines lack or have minimal sucrase in their guts, whereas hummingbird guts are richly provided with sucrase that efficiently hydrolyzes sucrose. Martinez del Rio (1990) has pointed out that hummingbird nestlings will be “imprinted with sucrose when they are fed such a predominantly sucrose diet. As such, hummingbirds may actively seek sucrose-rich food sources. Further- more, these high sucrose nectars will likely deter visitation by passerines that cannot utilize them, resulting in lower competition for resources.

Despite the clear pattern between sucrose content and pollinator class, there are species with nectars that contrast with the norm for a particular bird pollinator class. These apparent “anomalous” cases point to two important caveats. First, as we have tried to control for in our analysis, phylogenetic history may influence the characters of species. Old World passerine flowers, Anapalina cafia, A. nervosa, and AntboLyza ringens, belong to the

Iridaceae and share with other members of that family a tendency for high sucrose content in nectar (Baker & Baker, pers. obs.). Furthermore, Adansonia za var. bozy, although pollinated by passerines, has high sucrose content (34%). This species belongs to a genus that outside of Madagascar is bat pollinated and tends to have high sucrose content. Thus, some species may retain ancestral character states and obscure or enhance general patterns.

The second caveat that may explain apparently “anomalous” species is that we have necessarily lumped very large and diverse taxa into pollinator classes. For instance, there is a very large number of passerine species with a long evolutionary history. Thus, some clades of passerines may well have evolved different preferences and/or abilities to consume nectars with higher sucrose content. An example from the literature seems to be Hornstedtia scottiana (Zingiberaceae) from Australia where Ippolito and Armstrong (1993) reported that it produced sucrose-rich nectar although pollinated by passerines of the Meliphagidae. Thus, future investigations need to correlate specific clades of passerines with nectar chemistry. Also, because flowers of H. scottiana are borne within a few centimeters of the ground, they also may be visited by mammals that could independently influence sugar composition. Similarly, in Hawaii, Kokia dynarioi- des has nectar of almost pure sucrose although it is thought to be pollinated by passerines; a careful study on the pollination biology of this species is warrented.

NECTAR: BATS.-cOntrast between sugar composition of nectars in species pollinated by Megachi- roptera and Microchiroptera is striking. Nectars produced by microchiropteran-visited flowers are hexose-rich but have a higher sucrose content than passerine flower nectars. Corresponding figures for megachiropteran-visited flower nectars are even higher and bear comparison with those of hummingbird flowers\(Baker & Baker 1983a, Freeman et al. 1991). In all eight comparisons within families containing species pollinated by both hummingbird and Microchiroptera-pollinated flowers, the hummingbird-pollinated species had higher sucrose contents (Table 3). Similarly, in all six comparisons within families for both Megachiroptera and passerine-pollinated species, the Megachirop- tera-pollinated species had higher sucrose contents (Table 3).

Despite shifts in nectar chemistry often being accompanied by morphological changes in floral


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 differ- entiation associated with different major pollinators (Kress 1985). Most species of Heliconia are hummingbird-pollinated in the American tropics. Bat- pollinated 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 is- land 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 hexose- dominant 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 activ- ity can be found in the bats as between the passerines and hummingbirds. For the Microchirop- tera, Hernandez and Martinez del KO (1992) have examined the gut enzymes of five microchiropteran bats: one purely insectivorous (Pteronotus persona- tus), two predominantly frugivorous (Artibeus ja- maicensis and Stumira lilium), and two primarily nectarivorous (Leptonycteris curasoae and Glossoph- aga 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 Megachi- roptera 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 rath- er 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 hexose- dominated; 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. Suc- culent 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


of fruits by bats and passerines. Detailed studies of the utilization of fruits taken by passerines and Mi- crochiroptera would be extremely useful. The in- tensity of effort on a year-round basis necessary to establish dietary principles is described in Fleming (1988) for the short-tailed fruit bat, Carollia per- spicilkzta, 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 Megachirop- tera and those with fruits taken by Microchirop- tera, however, showed no trend. This comparison may be anomalous because the number of families considered is low and that fruits taken by Micro- chiroptera 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 ar- ilate seeds of some gymnosperms (current represen- tatives include Ginkgo biloba, Tdxus spp., and cy- cads). 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. Hexose- rich 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 Chi- roptera is not clear. The earliest bat fossil is Zcaron- ycteris, having occurred during the Paleocene or Eo- cene 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 (1 993) suggested that several life history features of Leptonycteris curasoae show a parallel evolution with the migratory, roosting, and mass foraging habits of Megachirop- tera.

FUTURE INVESTIGATIONS.-ThC structures Of bat- 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.


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-Bu- yulla, 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. Hei- thaus, 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) .

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BAKER, H. G., AND I. BAKER. 1973. Amino acids in nectar and their evolutionary significance. Nature 241: 543-545. , AND - . 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. , AND - . 1979. Sugar ratios in nectars. Phytochem. Bull. V. 12(3): 43-45. , AND - . 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. , AND - . 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. , AND - . 1986. The occurrence and significance of amino acids in floral nectar. Plant Syst. Evol.: 175- 186. , AND - . 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: 385414. , R. W. CRUDEN, AND I. BAKER. 1971. Minor parasitism in pollination biology and its community function: the case of Ceiba acuminata. Bioscience 21: 1127-1129.

BAKER, I., AND H. G. BAKER. 1976a. Analyses of amino acids in flower nectars of hybrids and their parents, with phylogenetic implications. New Phytol. 76: 87-98. , AND - . 1976b. Analysis of amino acids in nectar. Phytochem. Bull. 9: 4-7. , AND - . 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.

BRUNEACJ, A,, AND J. J. DOYLE. 1993. Cladistic analysis of chloroplast DNA restriction site characters in Erythrina L. (Leguminosae: Phaseoleae). Syst. Bot. 18: 229-247.

CIIA.I.EIAT, R. T., E. KLANN, J. W. DEVERNA, S . YELLE, AND A. B. BENNETT. 1993. Inheritance and genetic mapping of fruit sucrose accumulation in Lycopersicon chmielewskii. Plant J. 4: 643-650.

DANIEL M. J. 1979. The New Zealand short-tailed bat, Mystacina tubercukztu: a review of present knowledge. N.Z. J. 2001. 6: 357-370.

DoRxr, K., AND T. PEIKERT-HOLLE. 1985. Bluten und Fledermause. Verlag von Waldemar Kramer, Frankfurt vam Main, Germany.

DONOGIIUE, M. J. 1989. Phylogenies and the analysis of evolutionary sequences, with examples from seed plants. Evolution 43: 1137-1 156.

FELSENSTEIN, J. 1985. Phylogenies and the comparative method. Am. Nat. 125: 1-15. FLEMING, T. H. 1988. The short-tailed fruit bat. University of Chicago Press, Chicago, Illinois.

. 1993. Plant-visiting bats. Am. Sci. 81: 460467. FREEMAN, C. E., AND R. D. WORTHINGTON. 1985. 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.


, R. D. WORTHINGTON, AND K. D. CORRAL. 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, I? H., AND M. D. PAGEL. 1991. The comparative method in evolutionary biology. Oxford University Press, Oxford, England.

HEI.I.HAUS, E. R. 1982. Coevolution between bats and plants. In T. H. Kunz (Ed.). Ecology of bats, pp. 327-367. Plenum Press, New York, New York.

HERNANDEZ, A., AND C. MART~NEZ DEL Kio. 1992. Intestinal disaccharidases in five species of phyllostomoid bats. Comp. Biochem. Physiol. 103B: 105-1 11.

HERRERA, C. M. 1992. Interspecific variation in fruit shape: allometry, phylogeny and adaptation to dispersal agents. Ecology 73: 1832-1841.

HILL, J. E., AND J. D. SMITII. 1985. Bats: a natural history. British Museum (Natural History), London, England. HOWELL, D. J. 1974. Bats and pollen: physiological aspects of the syndrome of chiropterophily. Comp. Biochem.

IPPOLITO, A,, AND J. E. ARMSTRONG. 1993. Floral biology of Hornstedtiu scottiunu Zingiberaceae in a lowland rain forest

JEPSEN, G. L. 1970. Bat origins and evolution. In W. A. Wimsatt (Ed.). Biology of bats, pp. 1-64. Academic Press,

JORDANO, P. 1995. Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints

KRESS, W. J. 1985. Bat pollination of an Old World Heliconiu. Biotropica 17: 302-308. 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, W. F! 1990. A method for testing the correlated evolution of two binary characters: are gains or losses

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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 ap- propriate 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 dis- tilled water and the solution concentrated in a vac- uum desiccator. Respotting on Whatman No. 1 chromatography paper was followed by separation of sugars by single-direction descending paper


jl 20

/;; .P 0

- -0 - - Fructose - e- -Glucose P‘m 0

0 20 40 60 80 1 % 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 . lX , 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-pro- pano1: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 com- pacted 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 re- agent consisting of two solutions mixed just prior to use. Solution A was 75 mg of oxalic acid dis- solved in 15 ml of ethanol; Solution B contained 150 mg of p-aminobenzoic acid in 25 ml of chlo- roform and 2 ml of acetic acid. Again after air- drying the papers were held at 110°C 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 correlat- ing 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-


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.

APP

END

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bore

a 76

, 2

Thm

etia

ner

iifol

ia

Z o

vatu

Ik

x an

omak

z An

thur

ium

mac

rolo

bium

Spat

hiph

yllu

m sp

. Xz

ntho

som

a sp

.*

Cbeir

oden

dron

helle

ri

Den

drop

anax

arb

oreu

s D

. zon

atop

odis

Scbe

fira

digi

tata

G

eono

ma s

p.

Licu

ala

spino

sa

Phoe

nix

&cty

l+ra

Pg

chos

perm

a ele

gans

l?

sp.

Base

lla r

ubra

Ca

mps

k gra

ndiJo

ra

C. r

adica

ni

Cres

centi

a al

ata

C. c

ujete

C.

dac

tylon

D

istict

is bu

ccin

ator

ia

D. s

p.

Kige

lia s

p.

Teeo

maria

cap

ensis

N s

p. 2

15

, 71

A. s

p.

c. m

gyna

u1

-l

P

APP

END

IX 2

. Co

ntin

ued.

W %

Po

Pn

co

C

n Po

Pn

c

o

Cn

me

Bom

baca

ceae

Ad

anso

nia

za b

ar.

bozy

54

, 34

% A.

dig

itata

36

, 48

"C

Nec

tar

Frui

t

Fam

ily

Spec

ies

H

W

P, 3

Bonz

baco

psis

quin

atum

40

, 25

Bom

bax

buon

oaoz

ensis

61

, 2

P

Bor

agin

acea

e

Bro

mel

iace

ae

Cac

tace

ae

Cam

panu

lace

ae

Cap

parid

acea

e C

anna

ceae

B. s

p.

Ceib

a ac

umin

ata'

C. pe

ntan

dra

Cbor

isia

peri

od

Dur

io m

ahcc

ensis

D

. zib

etbi

nw

Ocb

rom

a Ia

gopu

s Q

uara

ribea

aste

riolep

is Q.

SP

. Co

rdia

pana

men

sis

c. sp

. Pu

ya a

lpes

tris

l? c

hilen

sis

I? co

riace

a l?

ha

l?

mac

rura

I! r

aim

ondi

i I!

viola

rea

Carn

egiea

giga

ntea

Lm

aire

ocer

ew t

brub

eri

Opu

ntia

sp.

Sc

blum

berg

era

sp.

Burm

eister

a sp

. Ce

ntro

pogo

n so

lani

faliu

so

C. ta

lama

ncen

sis"

C. v

akri

P c.

sp. 1

c.

sp. 2

c.

sp. 3

c

sp. 4

Cr

ateu

a ta

pia

Cann

a in

dica

c.

sp.

49, 0

48, 4

49

, 2

26, 5

2 9,

78

16. 6

1 50

, 1

37,3

7

29, 6

5 33

, 36

17, 8

0 48

, 42

38, 5

3 33

, 57

2, 9

7 4,

96

39, 5

3

25, 5

1 26

, 50

38, 3

3

53, 2

42

, 37

35, 3

1 32

, 49

48, 9

41

, 5

49, 5

39,2

0 36

, 17

39, 4

39, 3

I

0 P

0

lD v)

41, 4

3 45

, 3


rn Ln Ln

2 2 d v ; w r n

0

6 Ln

0

w w"

3 3

0 l n 2 00" 0- r n m

m 4

ul m

APP

END

IX 2

. Co

ntin

ued

% -c Sp

ecies

H

Po

Pn

co

Cn

Po

Pn

co

C

n m

% Er

ythr

oxyl

acea

e Er

ythro

xylu

m m

atto

s-silv

ii 52

, 1

-2 2

Hur

a cr

epita

ns

53, 1

6 P

24, 5

5 5 I

Nect

ar

Frui

t

Fam

ily

Euph

orbi

acea

e Eu

phor

bia p

ulch

errim

a 26

, 9

Pedi

lant

hw c

arin

atus

Pe

ra s

p.

64, 3

Rypa

rosu

java

nica

68

, 0

Gen

tiana

ceae

Sy

mbo

lant

hus s

p.*

32, 5

1 G

esne

riace

ae

Allo

plec

tus t

etrug

onus

" 32

, 57

Besk

ria c

olumn

eoide

s"

54, 3

9

Dry

mon

ia ga

yana

52

, 1

D. s

erru

lata

5,

3

Colu

mne

a vir

gini

ca

24, 7

6 c.

sp.

1 45

,46

c. sp

. 2

21, 7

4 c.

sp. 3

27

, 70

Dry

mon

ia F

mbr

iatu

22

, 57

D. s

erru

lata

11

, 82

D. s

pecta

bilis

32

, 48

D. s

p. 1

24

, 58

D. s

p. 2

18

, 61

D. s

p. 4

14

, 58

Koh

kria

eleg

ans

27, 6

9 Rh

abdo

tham

nus s

olan

deri

50, 3

P

(P

Flac

ourt

iace

ae

Case

aria

acul

eata

40

, 10

C. y

lves

tris

30, 5

2

B. s

p.

50, 7

D. s

p. 3

4,

94

Goo

deni

acea

e Sc

aevo

la ga

udic

haud

iana

S.

kila

ueae

S.

molli

s S. ta

ccaa

h G

rey i

acea

e Gr

eyia

suth

erla

ndii

Gut

tifer

ae

Gar

cinia

man

gosta

na

G. x

anth

ocLy

mw

Mam

mea

odo

rata

71, 7

52, 7

54, 1

61

, 4

51, 4

49

, 1

23, 5

0

25, 5

2

APP

END

IX 2

. Co

ntin

ued.

Nec

tar

Frui

t

H yd

rang

eace

ae

Icac

inac

eae

Irid

acea

e

Labi

atae

Laur

acea

e

Lecy

thid

acea

e Le

gum

inos

ae

21, 5

8 3,

88

28, 4

2 63

, 1

52, 6

55

, 1

53, 6

10

, 15

38,

16

9, 8

7 13

, 82

22, 7

2 43

,34

63, 1

21, 5

5 10

,81

24, 3

9

17, 5

7

49, 1

39

, 0

47, 6

Fam

ily

Spec

ies

H

Po

Pn

co

C

n Po

Pn

c

o

Cn

Hae

mod

orac

eae

Anig

omnt

bos

mang

lesii

40, 5

H

elic

onia

ceae

He

licon

ia bi

bai

0, 7

3 H

. birs

uta

26, 3

3 H

. nut

ans

26, 2

8

H. p

apua

na

H. i

ostra

ta 22

, 70

H. s

olomo

nemi

s H

. sub

ulat

a 0,

70

H. t

ortuo

sa"

28, 3

9

H. p

aka

51, 4

Brou

ssaisi

a arg

uta

Penn

antia

corym

bosa

M

appi

a ra

cemo

sa

Anap

alin

a ca

fia

A. n

ervo

sa

Antb

olyz

a rin

gens

Kl

attia

&va

K

piat

ula

K sto

koei

Wits

enia

mau

ra

Leon

otis l

eonu

rus

Pycn

ostac

bys

retic

ulata

Salvi

a ae

tbiop

is S.

divin

orum

S. ka

rwin

skii

S. sp

lende

ns

Sten

ogyn

e min

utifo

ra

Beils

chmi

edia

pend

ula

Ocote

a sp

. Ba

rririg

tonia

miati

ca'

Bauh

inia

acu

leata

B. e

marg

inata

B. g

hbra

B.

rnu

ltine

rvia

B.

pau

leltia

B.

rut

ilans

B.

ung

uhta

4, 9

3 42

, 1

36, 2

9

40, 2

1 41

, 19

40.

10

5 2 g 49

, 1

Q 9

5. - U 7J

5

ul

4

4

22, 4

6 35

, 19

Baker, Baker, and Hodges

4 d

m m

m T 00- d

APP

END

IX 2

. Co

ntin

ued.

Nec

ror

Frui

t -

Fam

ily

Spec

ies

H

Po

Pn

co

Cn

Po

Pn

co

C

n

Lilia

ceae

Loas

acea

e Lo

belia

ceae

Loga

niac

eae

E. s

andw

ichen

sis

E. se

nega

lensis

E

sigmo

idpa

E. s

rnitb

iana

E.

spec

iosa

E. s

ubur

nbra

ns

E. s

tand

leyan

a E.

tabi

tensis

E.

taju

rnuc

ensis

E.

uer

na

E. u

espe

rtilio

H

yrne

naea

cour

baril

In

ga to

nduz

ii I.

Vera"

I.

Vera

In

ocar

pus j

zgqe

r M

ucun

a an

dreu

na

M. p

rurie

ns

M. r

ostra

td

Park

ia b

iglob

osa

Pbas

eolus

sp.

Scbo

tia b

rahy

peta

la

Sesb

aniu

form

osa

Aspa

ragu

s spr

enge

ri As

telia

ner

uosa

Bo

mar

ea ro

starir

ense

Cliu

ia r

nini

ata

Collo

spen

num

bas

tatu

rn

Doi

yant

bes

exce

lra

Eucn

idp

aure

a Cl

erm

ontia

kak

cune

B. sp

.

C. pe

rsici

folia

c.

sp.

Cyan

ea a

ngus

tifol

ia

Fagr

aea

berte

riana

37, 5

49

, 2

46, 4

28

, 49

19, 5

7

26, 5

1

30, 4

3

41, 2

41, 4

37, 4

36

, 4

36, 3

1 19

, 72

35, 1

9

46,2

0

48, 4

35

, 33

48, 1

5 33

, 36

21, 6

6 58

, 2

35, 5

5 70

, 5

52, 0

20

, 72

44,5

5

49, 2

34, 5

33

, 1

44, 6

35

, 2

12, 8

5

32, 4

1

48, 1

4 48

, 42

43, 3

6

!3 3 a

9

E. -

47, 0

Lyth

race

ae

Mdv

acea

e

ul

03 0

APP

END

IX 2

. Co

ntin

ued.

m

Nec

tar

Frui

t e,

Lora

ntha

ceae

Am

yem

a m

ique

lii

60, 2

e,

5 Ile

ostyl

us m

icran

tbus

5

2 5

Ory

ctant

bus s

p.

59, 0

8

Fam

ily

Spec

ies

H

Po

Pn

co

C

n Po

Pn

c

o

Cn

“6

A. p

endu

lum

59

, 1

-6 W

A. q

uand

zng

47, 1

(I a

Psin

aran

tbus

sp.

26, 4

9 Tu

peia

ant

arcti

ca

56, 7

Cu

phea

caec

ilae

21, 4

6 C

. spe

ctabi

lis

13, 8

0 Ab

utilo

n m

enzie

sii

39, 0

Hib

iscad

elpbu

s dist

ans

47, 6

Hib

iscus

elat

us

61, 3

H

. firr

cella

tus

41, 1

2 H

. kok

ia

48, 4

H

. St.

jobn

ianu

s 42

, 3

H. w

aim

eae

40, 1

Ko

kia d

tynar

ioid

es

1, 9

8 M

alva

viscu

s arb

oreu

s 39

, 44

Mar

cgra

via b

rown

ii 50

, 3

Gos

sypi

um sa

ndvic

ense

45

, 0

H. g

iffar

dian

w

43, 1

1

M. n

epen

tboi

des

Mar

cgra

viac

eae

Mel

asto

mat

acea

e

M. s

< No

rant

ea s

p.

Clid

emia

birt

a C.

sept

uplin

ervia

Co

noste

gia c

inna

mom

ea

Lean

dra

cons

imili

s M

elasto

ma

mal

abat

bric

um

Mic

onia

afin

is

M. c

entro

desm

a M

. bon

dure

nsis

M. i

mpe

tiola

ris

M. s

p.

Mou

riri

myr

tillo

ides

Os

saea

micr

antb

a 0. qu

inqu

iner

vis

48, 2

53, 6

40, 4

68

, 5

49, 3

44

, 4

43, 1

46

, 2

40, 6

38

, 6

58, 3

62

, 1

55, 2

49

, 0

46, 6

48

, 1

61, 1

APP

END

IX 2

. Co

ntin

ued.

Nec

tar

Frui

t

Fam

ily

Spec

ies

H

Po

Pn

co

C

n Po

Pn

c

o

Cn

Mel

iace

ae

Agkz

ia sp

. 45

, 1

Mel

iant

hace

ae

Mel

iant

hw c

omos

us

51, 2

M

. mjo

r 55

, 1

Mor

acea

e Ar

toca

rpw

altil

is"

38, 2

4 A.

het

erop

hyhd

34

, 34

Bros

imum

alic

astru

m

59,

14

Ficw

cap

ensis

44

, 14

E co

staric

ana

45, 2

E

duga

ndii

21, 3

E in

ripi

dz

47, 3

E

g-of

ii 41

, 20

E ob

liqua

50

, 3

E po

peno

ei 52

, 0

E sc

abra

58

, 2

E tin

ctor

ia

47, 3

E

trigo

natd

t 36

, 3

E yo

pone

nsis

34, 4

E

sp. 1

48

, 7

P E

sp. 2

e s

E sp

. 3

G. 2 3 M

oms

alba

M

usa

balb

isian

a '0

rr

M. c

occin

ea

M. t

exti

h M

. sap

ient

um

M. s

p.

Ardi

sia c

ompr

essa

A.

rev

olut

a C

ybia

nthw

sp.

9 8 e 2

Myr

sine

ksse

rtian

a Q

3 G

allis

temon

sp.

A

Euca

lyptu

s f;.

;f.l

ia

73

Euge

nia j

ambo

s u

2

M. s

andw

icens

e G

L

E. n

esio

tica

59, 2

M. e

xceh

a M

etros

ider

os co

llina

u1

??

Mus

acea

e 20

, 57

25, 4

9

36, 2

6

33, 4

1

66, 1

38

, 1

51,

1

24, 4

8

Myr

sinac

eae

Myr

tace

ae

58, 3

51

, 5

62, 8

39

, 1

48.

13

46; 3

42

, 1

63, 1

80

, 2

57, 1

Nyc

tagi

nace

ae

Ola

cace

ae

Ona

grac

eae

Oxa

lidac

eae

Pand

anac

eae

Papa

vera

ceae

Pa

ssifl

orac

eae

Phyt

olac

cace

ae

22, 5

0 12

, 83

49, 4

48

, 6

36,4

0 14

, 84

31, 6

0 24

, 46

38, 3

6 34

, 62

21. 6

1

44, 7

6, 8

7 6,

92

29, 4

3

46, 0

41, 1

1 35

, 1

41, 5

54, 1

48, 1

5

APP

END

IX 2

. Co

ntin

ued.

m

Fr

uit

e,

Nec

tar

4 M

. ker

made

cens

is 46

, 9

-F m

e,

Spec

ies

H

Po

Pn

co

CIl

Po

Pn

co

Cn

Fam

ily

P, 3

L1

0

M. p

olym

orph

a 44

, 3

M. u

mbe

llata

44

, 2

I! c

anle

ianu

m

Q

Syzy

gium

flori

bund

um

u3

50, 2

7 I

Psid

ium

guaj

ava

S. in

opby

lloid

es

!2 S. pa

nicu

latu

m

S. sa

ndwi

cens

e s.

sp.

Neea

sp.

H

eister

ia a

cum

inat

a Fu

chsia

abr

upta

E:

boliv

iana

E

colen

soi

E ex

corti

cata

E

jimen

ezii

E m

agell

anica

E

proc

umbe

ns

E re

gia

E vu

lcani

cola

E

sp.

Lope

zra

lang

man

iae

Xylo

nagr

a ar

bore

a Av

errb

oa c

aram

bola

Fr

eycin

etia

rein

ecke

i E

scan

dens

Pa

ndun

us te

ctor

iw

Sara

rang

a sp

. Bo

ccon

ia s

p. Pa

sszf2o

ra in

carn

ata

I! m

ollis

sima

I! ni

tida

Pbyto

lacc

a riv

inoi

des

I? sp

. 1

I! s

p. 2

42, 5

27

, 23

41, 9

45, 8

24

, 23

51, 2

6 51

, 2

49, 1

72

, 0

37, 1

7 43

, 2

52, 1

2

APP

END

IX 2

. Co

ntin

ued.

Nec

tar

Frui

t

Fam

ily

Spec

ies

H

Po

Pn

co

C

n Po

Pn

c

o

Cn

Pipe

race

ae

P+er

auri

tum

I?

dota

rum"

I?

silvi

vagu

m

I? sp

. Po

lem

onia

ceae

Ca

ntua

can

delil

la

C. p

yr fo

lia

Coba

ea sc

ande

ns

Loes

elia

cilia

ta

Poly

gala

ceae

M

onni

na sp

. Po

lygo

nace

ae

Cocc

olob

a car

acas

ana*

C

. pad

ifomi

s' Pr

otea

ceae

Ba

nksia

eric

ifolia

B.

spin

ulos

a Gr

evill

ea ro

bwta'

Pr

otea

ryn

aroi

des

Sten

ocav

pm si

nuat

us

Telop

ea o

reah

I:

pecio

sissir

na

Rubw

rosit

fooliu

s Al

berta

mag

na

Bobe

a ek

ztior

Ca

ntbi

um o

dora

tum

Ce

phae

lis ax

ilkzr

is

Cbio

ne co

staric

ensis

Co

ffea

arab

ica"

C. li

beric

a C.

rob

usta

C. g

rand

iflor

a C.

mon

tana

C.

parv

zjlor

a C

pro

pinq

ua

C. r

bync

ocav

pa

C. r

obus

ta

C. r

otun

difo

lia

C. ru

gosa

C.

wai

meae

C. e

lata"

Copr

osma

ern

ohoi

hs

31, 5

6 22

, 72

44,4

4

44, 1

3 41

. 22

Ros

acea

e R

ubia

ceae

48, 1

8 46

, 33

12, 6

3

44, 2

3

51, 1

0 54

, 2

40, 6

40

, 2

53, 4

34, 1

1

54, 1

45

, 25

53, 4

60, 1

6

49, 2

38

, 22

37, 3

46

, 1

47, 6

40

, 43

60, 2

5 40

, 41

35, 1

41

, 0

48, 2

47

, 12

40, 5

46

, 6

43, 3

30

, 7

47, 4

31

, 2

51, 1

47

, 3

30,

17

36, 1

9

I

Q ? c.

c

cn

03

W

CJl

03

P

APP

END

IX 2

. Co

ntin

ued.

m

N

ecta

r Fr

uit

% -2

Fara

mea

occid

enta

lis

44, 1

1 %

Gon

zahg

ulni

a ro

sea

61, 6

-2

41, 1

1 5

Nerte

ra d

epre

ssa

38, 7

0

Palic

oure

a sp

. 35

, 1

$ Ps

ycho

tria

acum

inat

a 35

, 12

I! g

racil

ifolia

39

, 7

I! g

racil

is 33

, 12

I! g

rand

istip

ula

43, 7

I!

hor

izont

alis

43, 3

I!

mac

rodo

n 45

, 7

I! m

apou

rioid

es

59, I

I!

mar

gina

ta

61, 3

I!

ojic

inal

is

38, 1

I!

tond

uzii

49, 7

I!

sp.

1

37, 6

I?

sp. 2

41

, 4

m

Fam

ily

Spec

ies

H

Po

Pn

co

C

n Po

Pn

c

o

Cn

Gou

ldia

tem

inal

is

38, 3

H

amel

ia pa

tens'

21, 6

6 46

, 5

Hof

man

nia

sp.

Q

Q

I! d

e&a

66, 1

I!

Prca

ta

48, 1

Xero

cocm

nub

osea

Cu

pani

a sylv

atica

57

, 1

Cupa

niop

sis sp

. 43

, 33

Litc

hi c

hine

nsis

25, 5

0 Ne

phel

ium

lapp

aceu

rn

26, 4

4 N. bn

gana

20

, 63

Paul

linia

sp.

51

, 5

Man

ilkar

a ac

hras

33

, 37

Plan

chon

ella

torr

icelle

nsis

40, 3

9 H

ebe

spec

iosa

Russe

lia s

amen

tosa

R.

ver

ticell

ata

Picr

amni

a ca

tpin

terae

Qu

assia

ama

ra'

M. z

apot

a 43

, 21

Sapi

ndac

eae

22, 6

2

Sapo

tace

ae

Scro

phul

aria

ceae

Sim

arou

bace

ae

53, 0

36

, 48

33, 4

5

24, 5

8 23

, 30

Sola

nace

ae

40, 1

APPE

NDIX

2.

Conc

inue

d.

Nec

tar

Frui

t Fa

mily

Sp

ecie

s H

Po

Pn

c

o

Cn

Po

Pn

co

C

n

Smila

cace

ae

Lapa

geria

rosea

16

, 72

Smila

x sp

. 1

33, 3

s.

sp. 2

52

, 3

s. sp

. 3

69, 6

Ac

nistu

s arb

ores

cens

41

, 2

Brug

man

sia sa

ngui

nea

26, 5

5

Cestr

um d

iurn

um

Caps

icum

anu

um

54, 2

C. pu

rpur

eum

25

, 71

C. ra

cern

osum

74

, 9

Ioch

rom

a jkb

sioi

des

29, 5

5 Ly

ciant

hes a

mat

itlan

ensis

72

, 8

L. m

u~h;

flora

71

, 15

Lyco

persi

con

chile

nse

17, 6

7 L.

chm

iekw

skii

17, 6

1 L.

pen

nelli

i 23

, 25

L. p

eruv

ianu

m

19, 7

7 L.

pim

pine

llifo

lium

20

, 60

Mar

kea

neur

anth

a Nz

cotia

na g

lauc

a N

. otop

hora

? So

lanu

m b

rene

sii"

S. co

rakv

ense

S.

laci

niat

um

S. n

r. ci

liatu

m

S. q

uito

ase

38, 4

7 55

, 14

24, 4

6

Sonn

erat

iace

ae

Stre

litzi

acea

e

s. sp

. St

rept

osol

en ja

mes

onii

With

erin

gia s

olana

cea

Sonn

erat

ia sp

. Ra

vena

la m

ahga

scar

iensis

* St

relit

zia n

icola

i S. re

gina

28. 6

8

43, 2

32

, 25

28, 3

9 56

, 20

59, 0

46

, 7

38, 4

3 41

, 33

54, 3

U 0 cn.

34, 2

g

40, 3

3

I

0 P

UY al cn

APP

END

IX 2

. Co

ntin

ued

Nec

tar

Frui

t

Fam

ily

Spec

ies

H

Po

Pn

co

C

n Po

Pn

co

Cn

Ster

culia

ceae

Ch

irant

hode

ndro

n pen

tada

ctyl

n 50

, 6

Heli

ctere

s gua

zum

aefo

lia

14, 7

8 S y

mpl

ocac

eae

Symp

locos

sp.

18, 6

8 Th

eoph

rast

acea

e C

hu;ia

inte

grzjd

ia

Thyr

nela

eace

ae

Wik

stroe

mia

firca

ta

Tilia

ceae

Lu

ehea

spe

ciosa

U

rtic

acea

e Ur

era

cara

cara

na'

Ver

bena

ceae

Cl

eroa

'endr

um sp

ecio

sissim

um

8, 8

4 La

ntan

a ca

mar

a St

acly

taqb

eta

fianz

ii 25

, 50

Prem

ma

sp.

w sp

.

u. sp

.

Xan

thor

rhoe

acea

e Xz

ntbo

rrbo

ea au

stral

is 41

, 11

Zing

iber

acea

e C

osm

pul

ueru

lenh

lp

0, 7

9 c.

sp.

17, 7

6

52, 3

36

, 16

47, 9

47

, 25

37, 5

70

, 4

28,

1 55

, 0

73, 0

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