baker 1999 sugar composition of nectars and fruits consumed by birds and bats in the tropics and...
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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 polli- nators and seed dispersers are thought to have pro- duced 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 dis- persal 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), cal- culating correlations among characters using spe- cies 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 be- tween 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 dis- persal mode. Jordan0 (1 9 9 9 , however, after con- trolling for historical effects, found that fruit di- ameter was correlated with the class of bird dis- persers, 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 pat- terns 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 char- acterized some pollination classes such as that by hawkmoths, long-tongued bees, and humming- birds. 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 polli- nation biology.
This investigation was based on the study of pollination and seed dispersal by “volant” verte- brate 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-vo- lant 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 (su- per family Passeriformes) and many also take nectar from flowers. Sharply distinct from passerines are hummingbirds (family Trochilidae), which are re- stricted 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 compar- ative 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 pro- vided by Fleming (1988). Fleming (1993) com- pared 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 sub- sequent 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 sam- ples.
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 con- tent 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, char- acters 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 nonindepen- dent. 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 with- in each family for each pollinator or disperser class. To reduce the effect of different intensities of sam- pling 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/dis- perser 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 oc- curred. Therefore, we used sign tests on the means within families to determine if particular pollina- tor/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 com- position (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 in- dicated 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
562 Baker, Baker, and Hodges
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 hum- mingbirds were always higher than means for sam- ples 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 glu- cose content (P < 0.02). Nectars with passerine pollinators in the Old World had more species with higher glucose content (52 species with greater glu- cose 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 hypoth- esis that the composition of soluble sugars in nectar and fruit juices has been influenced by the polli- nators and frugivores that consume them. Distri- butions of percent sucrose in nectars and fruit juic- es were significantly different among families when separated by pollinator and frugivore class (Tables 1 and 2). Nectars of flowers visited by humming- birds 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 pas- serine 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-
Sugar Composition of Nectar and Fruit Pulp 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, 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, ap- pear to be much less robust than patterns of the proportion of sucrose among pollinator and seed- disperser classes. Therefore, fructose/glucose con- tent cannot be relied upon as evidence of pollina- tion 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
564 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 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 ex- ception, 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 sam- ples of both hummingbird- and passerine-pollinat- ed 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 con- sumed 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 passer- ine-pollinated species in both hemispheres where they are uniformly hexose-rich; New World hum- mingbird-pollinated species, however, are uniform- ly rich in sucrose. Most likely, the ancestral con- dition 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- tent 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 phy- logenetic 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 oc- curred many times during the evolution of species with contrasting pollination systems.
An important contribution to understanding the difference between nectars consumed by hum- mingbirds 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 su- crose. Martinez del Rio (1990) has pointed out that hummingbird nestlings will be “imprinted with sucrose when they are fed such a predomi- nantly 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 con- tent and pollinator class, there are species with nec- tars 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, phyloge- netic history may influence the characters of spe- cies. 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 nec- tar (Baker & Baker, pers. obs.). Furthermore, Adansonia za var. bozy, although pollinated by pas- serines, has high sucrose content (34%). This spe- cies 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 his- tory. 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 in- vestigations need to correlate specific clades of pas- serines with nectar chemistry. Also, because flowers of H. scottiana are borne within a few centimeters of the ground, they also may be visited by mam- mals 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 composi- tion 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 hum- mingbird flowers\(Baker & Baker 1983a, Freeman et al. 1991). In all eight comparisons within fam- ilies containing species pollinated by both hum- mingbird and Microchiroptera-pollinated flowers, the hummingbird-pollinated species had higher su- crose contents (Table 3). Similarly, in all six com- parisons 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
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 differ- entiation associated with different major pollinators (Kress 1985). Most species of Heliconia are hum- mingbird-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 pol- lination, 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 spe- cies span these values with a range of 28-73 per- cent sucrose. An interesting variation is H. paka from Fiji, judged by Kress (1985) on morpholog- ical 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 sub- order 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 pas- serines 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 insectivo- rous 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 sug- gests 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 com- positions 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 pas- serine-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 re- markable similarity exists between the sugar com- position of passerine fruit juices and passerine nec- tars. 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 accu- mulation 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 ecolog- ical 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 pas- serines (New World) or Microchiroptera. There was no significant trend between the sugar com- position of fruits taken by these disperser classes (Table 4). It is interesting that data for percent su- crose 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 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 passer- ine 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 con- taining 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 com- position (see above).
CoNcLusIoNs.-Speculation is possible on the de- velopment of changes in sugar composition for nectar and fruit juice producing plants. The se- quence 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 su- crose 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 be- tween 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 ex- amples of “hummingbird flowers” with hexose-rich
or hexose-dominated nectar. But there is no evi- dence 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 trop- ical 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 hab- its.
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 adap- tive to bats of this suborder. The adaptive signifi- cance of greater sucrose content in the megachi- ropteran nectar and fruit juices is unknown; how- ever, it is interesting that Fleming (1 993) suggested that several life history features of Leptonycteris cur- asoae 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 con- siderable 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. ap- parently 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 pollina- tion 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.
568 Baker, Baker, and Hodges
ACKNOWLEDGMENTS Many people collected and sent samples of nectar and fruit juice for our analyses. Several persons also were ex- tremely 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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. 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.
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.
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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.
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, 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.
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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
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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 in- volved sampling freshly produced nectar with a finely drawn out micropipette, spotting the nectar immediately onto chromatography paper and dry- ing 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
570 Baker, Baker, and Hodges
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 pri- mary 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 val- ues 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 su- crose may be broken down, increasing glucose and fructose concentrations; this may be caused by nat- ural acidity of nectar or fruit pulp, be due to en- zymes 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 meth- ods, 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 pat- terns 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
IX 2
. Su
gar
com
posit
ion
of ne
ctars
andf
rtlit
s )om
tro
pica
l and
subt
ropi
cal r
egion
s wor
h'wid
e. Pe
rcen
tages
of t
otal
solub
le su
gars
due
to fru
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follo
wed
by s
ucro
se ar
e gi
ven
[valu
es fo
r per
cent
gluc
ose
can
be o
btai
ned
by 1
00 - (%
Fru
ctose
+ %
Suc
rose
)]. V
alues
are
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rated
acc
ordi
ng to
their
maj
or po
llina
tor o
r disp
erse
r clas
ses
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min
gbird
s [H
I, pa
sser
ine
bird
s in
the
Old
Wor
ld [Po] an
d N
ew W
orld
[Pn]
, bat
s in
the
Old
Wor
ld [C
o] a
nd N
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[Cn]
), *p
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nd b
atpo
llina
ted
fhum
min
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d an
d ba
t pol
linat
ed).
Whe
n m
ultip
le d
eterm
inat
ions
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ugar
com
posit
ion
were
mad
e fir
a p
artic
ular
spec
ies, t
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vera
ges
are
repo
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Spe
cies -'
inde
pend
ently
colle
cted
and
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by
HPL
C (F
reem
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1983
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5, 1
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APP
END
IX 2
. Co
ntin
ued.
Nec
tar
Frui
t Fa
mily
Sp
ecie
s H
Po
Pn
c
o
Cn
Po
Pn
co
C
n
Apo
cyna
ceae
Ca
rissa
edu
lis
51, 9
Ne
isosp
emza
sp.
1 56
, 20
Ochr
osia
sp.
13, 4
0 St
emm
aden
ia do
nnel
l-sm
ithii
62, 0
Ta
bern
aem
onta
na ar
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
Sugar Composition of Nectar and Fruit Pulp 575
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