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Hovering Sunbirds in the Old World: Occasional Behaviour Or Evolutionary Trend?

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Hovering Sunbirds in the Old World: Occasional Behaviour Or Evolutionary Trend? Oikos 120: 178–183, 2011 doi: 10.1111/j.1600-0706.2010.18612.x © 2011 Th e Authors. Oikos © 2011 Nordic Society Oikos Subject Editor: Jan van Gils. Accepted 28 May 2010 Hovering sunbirds in the Old World: occasional behaviour or evolutionary trend? Š t eˇ p á n Jane cˇ ek , Eli š ka Pat á cˇ ov á , Michael Barto š , Eli š ka Pady š á kov á, Luk á š Spitzer and Robert Tropek Š . Jane č ek ([email protected]) , E. Pat á č ov á , M. Barto š and E. Pady š á kov á , Inst. of Botany, Academy of Sciences of the Czech Republic, Dukelsk á 135, CZ – 379 82 T ř ebo ň , Czech Republic. – EPat, MB, EPad, L. Spitzer and R. Tropek, Faculty of Science, Univ. of South Bohemia, Brani š ovsk á 31, CZ – 370 05 Č esk é Bud ě jovice, Czech Republic. – LP and RT also at: Inst. of Entomology, Biology Centre, Academy of Sciences of the Czech Republic, Brani š ovsk á 31, CZ – 370 05 Č esk é Bud ě jovice, Czech Republic. Th e nectarivory of sunbirds in the Old World and hummingbirds in the New World evolved independently. While both groups are specialised in their feeding apparatuses, hummingbirds are moreover famous for their adaptations to sustained hovering fl ight. Recently, an example of a pollination system of the invasive plant Nicotiana glauca has been used to show that less adapted sunbirds also are frequently able to hover. Nevertheless, the question has remained why plants adapted to bird hovering pollination do not occur outside the New World. In this paper we show that the long-peduncle Cameroonian Impatiens sakeriana is not capable of autonomous selfi ng and can be pollinated only by two often hovering sunbirds, the Cameroon sunbird Cyanomitra oritis and the northern double-collared sunbird Cinnyris reichenowi . Our study revealed that this plant is highly specialised for pollination by C. oritis . Cinnyris reichenowi hovers less frequently and often thieves nectar by piercing the fl ower spur when perching. Th is study shows that pollination systems occurring in the Old World follow similar evolutionary trends as systems including hovering hummingbirds in the New World. Convergence and divergence of an organism ’ s character dur- studies on their pollination ecology, and after the discovery ing natural selection is among the fundamental principles of fossil hummingbirds in the Old World it was hypoth- of Darwin ’ s evolutionary theory (Darwin 1859). One of esised that these plants co-evolved with hummingbirds ’ the most famous examples of convergent adaptation stud- ancestors (Mayr 2004). ied since Darwin ’ s time is comprised of the morphological Th e view of sunbirds as perching birds was also sup- and behavioural adaptations of nectarivorous birds in rela- ported by many plant adaptations which have been studied tion to their feeding activity. Moreover, recent molecular mainly in southern Africa. Some ornithophilous spe- studies have showed that the two largest groups of necta- cies (e.g. Erica spp. (Siegfried et al. 1985), Satyrium spp. rivorous birds (Old World sunbirds and New World hum- (Johnson 1996) and many Iridaceae species (Goldblatt and mingbirds) are members of two superordinal phylogenetic Manning 2006) have thick stems to support avian pol- clades and represent morphologically convergent forms linators in perching. Syncolostemon densifl orus (Lamiaceae) of nectarivorous birds (Fain and Houde 2004). While the has a compact terminal infl orescence that enables feeding feeding apparatus adaptations of the two groups appear to from a single perching position (Ford and Johnson 2008). be very similar, they evidently diff er in their adaptations for Strelitzia nicolai (Musaceae) creates a perch from anther- hovering fl ight (Schuchmann 1999, Altshuler and Dudley sheath and stigma (Frost and Frost 1981) and Babiana rin- 2002). Sunbirds, which are not capable of sustained hover- gens (Iridaceae) facilitates perching by an unusual sterile ing fl ight as are hummingbirds, are considered to be mainly infl orescence axis (Anderson et al. 2005). In other African perching birds and observations of hovering sunbirds dur- regions pollination studies have been less frequent, but ing nectar feeding are rare (Ley and Classen-Bockhoff have also showed pollination systems including the perch- 2009). However, Westerkamp (1990) suggested that ing behaviour of sunbirds – e.g. in East Africa, Nectarinia attention should be directed to the actual functioning of johnstoni perch on Lobelia telekii (Evans 1996) and sev- fl owers rather than to systematic affi liation of birds. He eral sunbird species perch on Leonotis nepetifolia (Gill and also supposed some plants in the Old World (including Wolf 1978). Impatiens sakeriana, which is the focus of our study) have More recently, an example of a pollination system of blossoms oriented into free space which could be adapted the invasive plant Nicotiana glauca has been used to show to hovering birds. Nevertheless, there have been no detailed that less adapted sunbirds also are frequently able to hover. 178 Nevertheless, the question has remained why plants adapted Reproductive system of I. sakeriana to bird hovering pollination do not occur outside the New World (Geerts and Pauw 2009a). In our fi rst experiment, we studied the reproductive system In our study, we focused on the pollination ecology of of I. sakeriana to assess the importance of sunbirds on its Impatiens sakeriana . Th is plant has a bird-pollination syn- pollination and to better understand the pollination ecology drome including red fl owers, a spur up to 25 mm long of this species. Th e experiment was realised from November (Grey-Wilson 1980), and produces a high volume (38 μ l 2008 to January 2009 and was performed on eight popu- per fl ower) of dilute nectar (31% of sugar w/w); (Barto š lations of I. sakeriana . In this experiment we established et al. unpubl.). Moreover, I. sakeriana have fl owers on long- fi ve treatments: parthenogenesis: fl owers bagged and emas- peduncles oriented into free space (Grey-Wilson 1980) and culated; autogamy: fl owers bagged; geitonogamy: fl owers so seem to be pollinated by hovering birds (Westerkamp bagged and hand pollinated from fl owers of the same plant; 1990, Mayr 2004). While the pollination system of this outcrossing: fl owers bagged and hand-pollinated by the pol- plant has not so far been studied, it has been the object of len of a distant population; control: natural pollination. evolutionary hypotheses, which we tested: 1) Impatiens sake- Th ese treatments were performed in seven replicates in each riana represents a plant which is adapted to sunbird hovering population. Emasculation was performed after fl ower open- pollination (Westerkamp 1990). 2) Floral traits of I. sakeri- ing before thecae dehiscence. One replicate of treatments ana have evolved in the past in co-evolution with extinct was performed on one plant if possible, but as we were often hovering hummingbirds and, nowadays, it is pollinated by unable to fi nd enough numbers of plants with suffi cient insects (Mayr 2004) or is dependent on autonomous self- numbers of fl owers we used for one replicate more plants ing. Th e fi rst hypothesis can be supported by the occurrence growing close together. of indications that this plant could specialise for the long- billed (25 – 33 mm) sunbird Cyanomitra oritis (Cheke et al. Sunbird effectiveness 2001). Impatiens sakeriana and C. oritis have an identical dis- tribution area (occurring only in the Cameroonian moun- In our second experiment, which was realised simultane- tains and on Fernando Po), they occupy the same habitats ously with the fi rst one in the same I. sakeriana popula- at higher altitudes and I. sakeriana is a predictable nectar tions, we tested the pollination eff ectiveness of both sunbird resource, as it fl owers continuously throughout the year species with respect to their behaviour. Randomly selected (Grey-Wilson 1980, Cheke et al. 2001). Th e second hypoth- fl owers were bagged during their fl owering, except to be esis can be supported by the fact that no African pollination exposed for a single sunbird visit. In this way, we tested the system including frequent hovering bird pollination has so eff ect on both male (pollen removal) and female (seed yield) far been described. plant functions. To estimate sunbird eff ectiveness on male function, the fl owers in the male period, when the pollen is exposed, were uncovered and after one sunbird visit the Methods rest of the pollen was collected into Eppendorf tubes. In parallel, we collected pollen from seven unvisited (bagged) Study site fl owers in each population to estimate pollen production. Th e pollen removal was then determined as the diff erence Th e study was carried out in the Mendong Buo area between mean pollen production in the population and (6 ° 5 ’ N, 10 ° 18 ’ E; 2100 – 2200 m.a.s.l.); Bamenda Highlands, the pollen left remaining by the sunbird in this population. NorthWest Province, Cameroon. Th e vegetation of this Pollen grains were counted in a laboratory with a micro- area is a mosaic of high Hypparhenia grasslands, pas- scope using a haemocytometer (Roulston 2005). To assess tures dominated by Sporobolus africanus and Pennisetum eff ectiveness of sunbirds on female function, the fl owers cladestianum , Gnidia glauca woodlands, often burned were uncovered in the female period, when the stigma is forest clearings dominated by Pteridium aquilinum, and exposed. After visitation, the fl owers were again bagged and remnants of species-rich montane tropical forests domi- left until fruit maturation. Sunbird behaviour was noted in nated mainly by Scheffl era abysinica , S. manii , Bersama both the female and male parts of the experiment. As it is abyssinica , Syzigium staudtii , Carapa grandifl ora and Ixora impossible to achieve well-balanced numbers of visited fl ow- foliosa .
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