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Nectar As Food for Birds: the Physiological Consequences of Drinking Dilute Sugar Solutions

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Nectar As Food for Birds: the Physiological Consequences of Drinking Dilute Sugar Solutions http://tweaket.com/CPGenerator/?id=4725 MURDOCH RESEARCH REPOSITORY http://researchrepository.murdoch.edu.au This is the author's final version of the work, as accepted for publication following peer review but without the publisher's layout or pagination. Nicolson, S.W. and Fleming, P.A. (2003) Nectar as food for birds: The physiological consequences of drinking dilute sugar solutions. Plant Systematics and Evolution, 238 (1-4). pp. 139-153. http://researchrepository.murdoch.edu.au/4725 Copyright © Springer Verlag It is posted here for your personal use. No further distribution is permitted. 1 of 1 2/08/2011 1:44 PM PS&E/0276 FOR AUTHOR’S CORRECTION ONLY Plant Syst. Evol. (2003) DOI 10.1007/s00606-003-0276-7 Nectar as food for birds: the physiological consequences of drinking dilute sugar solutions S. W. Nicolson and P. A. Fleming Department of Zoology and Entomology, University of Pretoria, Pretoria, South Africa Received November 28, 2002; accepted January 26, 2003 Published online: xxx Ó Springer-Verlag 2003 Abstract. Nectarivory has evolved many times in also characterised as diurnal, unscented, and birds: although best known in hummingbirds, frequently possessing tubular corollas which sunbirds and honeyeaters, it also occurs on an match the narrow bills of their pollinators opportunistic basis in a varied assortment of birds. (Endress 1994). Alternatively, birds visit less We present a phylogenetic analysis of the distribu- specialised brush-like flowers with conspicuous tion of nectarivory in birds. Specialised avian stamens, grouped in inflorescences, like those nectarivores are generally small, with an energetic of Eucalyptus and other Australian Myrtaceae. lifestyle and high metabolic rates. Their high degree of dependence on nectar as a food source has led to The energetic requirements of bird pollinators convergence in morphological, physiological and are met by abundant nectar which represents a behavioural adaptations. We examine the constit- significant investment by the plant, not only in uents of nectar which are most important to bird terms of nectar production but also the consumers, and how the birds deal with them in substantial floral structures required to pro- terms of physiology and behaviour. There are still duce and contain it. unanswered questions: for example, the dichotomy Convergent evolution is illustrated by three between sucrose-rich nectars in hummingbird- major radiations of nectarivorous birds on pollinated plants and predominantly hexose-rich different continents: the Neotropical hum- nectars in sunbird-pollinated plants appears to mingbirds (Trochilidae), and two passerine have little to do with bird physiologies and may families, the Meliphagidae (honeyeaters) in rather reflect patterns of nectar secretion. Australasia and Nectariniidae (sunbirds) in Keywords: Nectarivory, pollination, humming- Africa and Asia. Hummingbirds and their birds, sunbirds, sugar digestion, water balance, tubular flowers show the most specialised osmoregulation. interactions; sunbirds occupy an intermediate position; and honeyeaters are the least specia- lised, foraging on accessible brush flowers and depending more on insects (Stiles 1981). Of the Nectar feeding is widespread in birds three main nectarivore lineages, hummingbirds Many bird-pollinated (ornithophilous) flowers are the oldest, dating back to some 33 million are spectacular because of their large size and years ago. Consequently, throughout the bright colours, often red or orange. They are Americas, nearly 8,000 plant species of >60 SW020276 Dispatch: 21.3.2003 Journal : Plant Syst. Evol. No. of pages: 15 Journal number Manuscript number B Author’s disk received 4 Used 4 Corrupted Mismatch Keyed SW02/0276/2 S. W. Nicolson and P. A. Fleming: Nectar as food for birds families have evolved flowers whose principal highly susceptible to energetic stress. In terms pollinators are hummingbirds, and humming- of studying digestive physiology, they eat bird pollination has sometimes evolved nu- sugar solutions, a deceptively simple food. merous times within a single genus (e.g. And finally, these sugar solutions are dilute, so Erythrina, Baker and Baker 1982b, Bruneau that water fluxes through the bodies of avian 1997). Body sizes support the idea that nectar- nectarivores may be extraordinarily high (Beu- dependant species are in general smaller than chat et al. 1990; Martı´ nez del Rio et al. 2001; those with more varied or non-nectarivorous Nicolson and Fleming 2003). diets (Brown et al. 1978, Pyke 1980). Hum- We will examine the constituents of nectar mingbirds weigh 2–20 g (331 species, Cotton which are most important to bird consumers, 1996), sunbirds 5–22 g (102 species, Cheke et al. and how the birds deal with them in terms of 2001) and honeyeaters are the largest, ranging physiology and behaviour. from 8–250 g (169 species, Frith 1977, Pyke 1980). Sugars Numerous other families, mostly passerine or perching birds, include species that show Nectar sugars are derived from sucrose trans- varying dependence on nectar. These include located in phloem sap, and the final compo- the Hawaiian honeycreepers, flowerpiercers, sition of nectar is determined by nectary and lorikeet parrots, as well as opportunistic invertase which hydrolyses sucrose to glucose nectar feeders such as white-eyes, weavers, Old and fructose. The extent of this hydrolysis, and New World orioles, barbets, louries, and the resulting sugar composition, vary mousebirds, starlings, Darwin’s finches and dramatically between the nectars of hum- some babblers and warblers (Fig. 1, Oatley mingbird- and passerine-pollinated plants and Skead 1972, Wolf and Gill 1986). Around (Baker and Baker 1983). Hummingbird nec- 10% of all bird species may use nectar as a tars show a left-skewed normal distribution, resource at some time (Wolf and Gill 1986). with an average of 64.4 ± 18.5% (S.D.) of Even in Europe, which lacks ornithophilous the nectar sugar being present in the form of flowers (Ford 1985), opportunistic nectar con- sucrose (Fig. 2B, n ¼ 278plant species). A sumption can be energetically important for very different bimodal pattern emerges for Sylvia warblers returning after long-distance sugarbird- and sunbird-pollinated plants in migratory flights (Schwilch et al. 2001). The southern Africa (n ¼ 259 species), the majority relationship between bill length and corolla of these producing nectar that is hexose length determines whether nectar-feeding birds dominant (37.0 ± 39.3% sucrose). About are legitimate pollinators or nectar robbers, half (47%) of sunbird/sugarbird plants pro- although the distinction between the two duce nectar with <10% of the sugar present categories is becoming less clear (Maloof and as sucrose (Fig. 2D). Many produce sucrose- Inouye 2000). rich nectars, with almost a quarter of species Aside from the fascination of bird-flower (24%) producing >80% sucrose nectars. The associations, nectar-feeding birds are excellent sucrose-hexose dichotomy is pronounced even models for ecophysiological research because within genera, with Erica, Protea and Leuco- their energetics and water turnover are extreme spermum nectars being either sucrose- or and inseparable (Beuchat et al. 1990; Martı´ nez hexose-dominated and showing few species del Rio et al. 2001). They are generally small, with mixed sugar compositions (Barnes et al. and consequently have high mass-specific met- 1995, Nicolson and Van Wyk 1998, Nicolson abolic rates: hummingbirds are the smallest 2002). Nectars from plants pollinated by endotherms and their hovering flight is espe- honeyeaters and honeycreepers demonstrate cially expensive. Small body size also means a an even more dramatic bimodal pattern low capacity for energy storage, so they are (Fig. 2F, n ¼ 83 species) with almost half S. W. Nicolson and P. A. Fleming: Nectar as food for birds SW02/276A/3 Fig. 1. Phylogenetic distribution of avian nectarivory; phylogeny based on Sibley and Ahlquist (1990). Specialised nectarivores are indicated in bold, opportunistic or occasional nectar-feeders are indicated in italics (Oatley and Skead 1972, Wolf and Gill 1986, Schwilch et al. 2001). Some non-nectarivorous birds have been tested for the presence of sucrase and these are included in plain text. The presence of sucrase is indicated as: Ppresent,-notexamined,trtrace,and**absent¼ sucrose intolerant species (Martı´nez del Rio et al. 1988, Martı´nez del Rio et al. 1989, Martı´nez del Rio and Stevens 1989, Martı´nez del Rio 1990a, Malcarney et al. 1994, I. G. van Tets, A. Green, T. McWhorter, B. Pinshow unpubl. data) (46%) of plant species recorded with <10% hexose dichotomy is also pronounced within sucrose and a third (37%) of species with genera (e.g. Banksia and Grevillea, Nicolson >90% sucrose. In these plants, the sucrose- and Van Wyk 1998). SW02/0276/4 S. W. Nicolson and P. A. Fleming: Nectar as food for birds 70 70 A. B. 60 60 50 50 40 40 30 30 20 20 10 10 0 0 5 10 15 20 25 30 35 40 45 50 55 10 20 30 40 50 60 70 80 90 50 140 100 C. D. 120 % sucrose 40 100 30 80 20 60 40 10 20 0 0 Number of plant species 5 s 10 15 20 25 30 35 40 45 50 55 10 20 30 40 50 60 70 80 90 40 100 E. F. 10 30 20 5 10 0 0 <5 <10 <20 <30 <40 <50 <60 <70 <80 <90 <10 <15 <20 <25 <30 <35 <40 <45 <50 <55 <100 Nectar concentration (% w/w) % total sugar as sucrose Fig. 2. Nectar concentration (% w/w sugar) and sugar composition (% total sugar as sucrose) for plant species pollinated by hummingbirds in America (A & B), sunbirds/sugarbirds in southern Africa (C & D) and honeyeaters/honeycreepers in Australia and Hawaii (E & F). Values are unpublished data (S. W. Nicolson) as well as from the literature (Percival 1965; Skead 1967; Hainsworth and Wolf 1972a, b; Hainsworth 1973, 1974; Baker 1975; Gill and Wolf 1975a, b; Stiles 1975; Wolf 1975; Hainsworth and Wolf 1976; Wolf et al. 1976; Cruden and Toledo 1977; Hainsworth 1977; Bolten and Feinsinger 1978; Bond and Brown 1979; Brown and Kodric-Brown 1979; Waser 1979; Pyke 1980; Corbet and Willmer 1981; Frost and Frost 1981; Pyke and Waser 1981; Baker and Baker 1982a, b; Feinsinger et al.
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