, 3
The Macaronesian bird-flower element and its relation to bird and bee opportunists
JENS MOGENS OLESEN
. Boianical Insiiiuie, Uniuerszp o/ Aarhus, Nordlandsuej 68, D K-8240 Risskov, Denrnark
Xrrrired Jub 1984, accrpirdjnr puhlrrniinn .\ oornrbrr 1984
OLESEN. J. M.. 1983.. The Macaroncrian bud-flower clernent uid ics relation to bird and bee opportuaiscs. Canarina canarirnrir. ihrcc /JO~~CK~Jspccics and Ldiw brrdrlolii, arnong othcr spccics, havc bccn supposcd 10 bc bird pollinatcd. Nonc of ihcir flowcn rcflcci UV lighi and ihc volumc of ncctar produccd ir rclarivcly high with low sugar conccntration. indicating bird pollination. This siudy givcs thc fin ADDITIONAL KEY \\‘OKí)S. -Bird polliriarioi~- Rombur - Canarina - floral biology - /soplcxiJ - LolUS. (‘OSTESTS Introducrion .. . 395 Obscrbaiions and discuwioii ...... 396 Taxonomy. ph>rogrogi~pli\ ciolo~s ,111d disiriI)iiciori ...... 396 Floral biologb ...... 398 Flowcr viriiors or pollinaion .. . 406 Ccncral discussion and conclusion ...... 411 Acknowlcdgcrncnis .. . . 412 Rcfcrcnccs...... 413 .. c I SI K( )DL:C:I.l os \Ve have been awarc for several b’ears of a putative e.xistence of ornithophily in some Macaronesiari species: Cnnnrirm cannriensis (L.) Vatke (Campanulaccac) (Vogel, 1954: 300, 302), isopfexis rnmriensis (L.) G. Don (Scropiiulariaceac) (Vogel, 1954: 252), f. isnbelfiana (lt’ebb) klasf. (Yeo, 1972), Lolus berthefofii Masf. (Fabaceae) (Vogel, 1954: 2 I3), and Jlussrhin woflasionii Lowe (Campanulaceae) (Vogel, 1954: 328). The flowcrs of these species possess some truly ornithophilous characiers: red-orange-yellow corollas, plenty of nectar, and (at least in some of them) absence of scent (Stilcs, 1981). In spite of the appareiit attractivencss of these Macaronesiari bird flowers and iheir relativeiy high energ): rewards tliere secm to be no reports of any visitors 395 0024-4074/85/070395 + 20 803.00!0 0 1985 Thc Linncan Sociciy of London 3% J. M.OLESEN and poliinators. Vogcl ( I 954: 2 13, 328) regards thcse bird fiowers as an cvidcllcc of an earlier presence Nectariniidae on the Macaroriesian archipelq:oi, Today no flower birds are found on the islands, but several other bird sp&iCs found on the Macaroncsian Islands, residents and migrants, are known to occasional flower visitors. For exampie Sylviidae (Ash, 1959; Porsch, 1924 ,, Paridae (Porsch, 1924) and Pioceidae (Passer dornesficus (L.) on Agave americnnn L. in Malaga, S Spain, personal observation) are known to include in their dict nectar from bird-pollinated piants introduced to European gardens, such as Aloe and Hibiscus, and from native European species, such as Prunus, Crocus and Primula. Porsch (1924) cites observations made by Lowe in 1896, that Sylria alricapilla (subspecies airicapilla?) visi ts Hibiscus species on Tenerife, and Parus caeruleus (subspecies fenerzjae?) Abufilon species on Gran Canaria. Extensive and unique areas of natural vegetation of Tenerife (especially), Gran Canaria and hqadeira have disappeared with ever increasing rapidit!, in recent decades, but with the establishment and initiatives of different scr\.ic.c.s aiici institutions. tiic eítorts for natural conservation 1iaL.e been gr-eiiit! intensified. Tlic niost scnsitive type of vegetation on the islands is without doul)i the laurel forest i laurisiiva). This broadleaved evergreen forest characterized 1)). 1,aurus acorica (Scub.) Franco is probably the oldest type of climax vegetation in hfacaronesia (bliocene or Pliocene; Bramwell, 1972, 1976; Dansereau, 1968; Lems, 1960; Meusel, 1965; Sunding, 1970), and during the Tertiary period may have had an enormous area of distribution in S Europe and N Africa. íts survival in Macaronesia may be due to the buffering influence of the oceanic climate (Aldridge, 1976; Dansereau, 1968; Humphries, 1976; Lems. 1960 i. According to Parsons (1981) less than 60 km2 of the laurisil\.a is left o11 tlic foiii- i\:estern islands, nia!-be only iOoí, of its original area. The bird-flou,ci- element belongs to tlie laurel forest, the tree heath ’ I:I) ,iI brezal), and the pine forest (pinar). Today, these types of vegetation are niurc or less threatened f\:oggenreiter. 1974). In recent times pine forests ha\.c hrt-ii niorc or les i-c-c% OBSER\’A’I‘IOSS ASI) DISCUSSIOS Tasoriotqy, phyfogeografihy, ecology and disiribuiion The genus Cariarina L. (Campanulaceae) coniprises three species: C. cannrierrjls (L.) Vatke, C. a6yssinica Engler, and C. euiinii Ascherson es Scliweinf. (Hcdbc1.s el ni., 1961). Canarinn canariensis is known frorn four of the Canary Islands: Tenerife, Gran Canaria, La Palma and Gomera (Bramweli 8r Brarnwell, 1974: >I,.\C:AKOS~:~IASRlRD FLO\VF.KS 397 204). 'rhe otlier tbvo specics are found in highland arcas and rnountains in 1; 1; Africa (Hedberg el al., 1961). This so-called Macaronesian-afrornontane distribution (Hedberg el al., 1961) or Macaronesian-S and E African distribution (Bramwell, 1976) indicates a quite diKerent climatic and \.egetational situation in the past in N Africa. CQnQTZna CQnQYienSiS grows in the rernnants of the iaurei forest, in Erica shrub, at roadsides in the rnountains, in forest rnargins, and in ravines in shaded places. The species has a restricted distribution, locally cornmon on Tenerife but rare ' . on the other islands (Bramwell & Brarnwell, 1974). It flowers frorn November to 34ay (sometimes to June) (Ceballos & Ortui10, 1951; Hedberg el al., 1961; and personal observations). Isoplexis (Lindley) Bentham (Scrophulariaceae) is an endemic Macaronesian genus of four species: I. canariensis (Tenerife, La Palma), I. isabefliana (Webb) Alasf., 1. chalcanfha Svent. & O'Shan. (both endernic to Gran Canaria and very closely related) and 1. scepfrurn (L. fil.) Loudon (Madeira) (Brarnwell 8: l Figurc l. LV photograph of corolla of Conarina ranarirnrir. Filicr: Kodak \Vraticn 18.4, a Ui’- iransrniiiing filter. Lcft pctal is sccn froni ihr insidc: righr pcial frorn rhc outsidc. Crcy scalc aiid techniqucs according io Kevan. Mulligan & Kobcrtson f 19731. f../otnl biolog, General descriptions 01’ riiorpholog\ aiid ptienology of ílowers of niost of the iibove-rnentioiicd spccies tia\.e bccri prescrited by se\.eral authors (Sctiniuckcr, 1936, Canarina; Vogel, 1954, Cannritia, Isoplewis, Lotiis and 1i4usschin; Hedberg et al., 1961, Canarina; Bryndum Christensen, Dalgaard ei Hamann, 1970, Isoplexis; Faegri t3 Pijl, 1971, Isoplewis; Yeo. 1972. Cmiarinn and Isoplexis; Proctor 8r Yeo. 1973, Isoplexis), aiid will not be repeatcd tiere, but a fe\\.additional obser\.ations of anthecological iiiterest are giveii. ?’he stifT corollas of C~tiaritinnrid Lofus ha1.e reddisli colours. Cnrinririo has ~\.tiite-)ielto\v-greeriflower buds, [tic operied flo\vers become red-orange and firiall~~dark red. I,ofus has dcep red flotvers \\*ith a dark niidline on the staridard. These colours have without doubt Oceri thc rnaiii iiidication in the diagnosis of oriiitliophily. ?’he íiowers ot“ Coriarino and Lofiis do iiot secrii to reflect C\.’ light whcn photographed through a L\*-rrarisniittiiig filler (Figs 1, 2) (Ke\vari, 1972; Kevan, Mulligan ei Robertson, 1973). ‘fhis obser\,ation is in accordance with current belief about ornithophil!.. Figure 3 sliows the flower riioi-pliology of Isopíesis species and I’ablc 1 summarizes some differences and siriiilarities in floral characters between ttiree Isoplexis specics. Onl!. Isojdel-is isnbellinna has bccn tisted I'oi. iiii: U\' rellectioii, aiid nonc \vas found (Fig. 2). If the other t\vo Isop1e.i-is spccics ~lsoiack U\: reílection, the shift in corolla colour from red to !.cllou., u.Iicii oiic moves from I. c-anariensis to I. isnbelliclrin to I. sreplriini (Tablc I 1. iiinkcs tlic ílo\\crs (niore) visible to bees. Going agaiii froni the Caiiai-iaii /.iop/e.i-i.( specics to /. sre,~frum in Tablc I the increasc iii Ieiigtli and cross-scctioii:iI arca o!' (tic (x)i.oiia tube creatcs ;t kiiid of landing platforni or 'garage' [o \.isitirig iiisccis , tiic ci-oss-sectional arca of an indi\.idual oí' Lloriiúiis c-ariariensis f'ci.cL ,sce i:i[cr, ic ti0 80 rnni2). Togctliei- \vith chaiigcs iii coiisisteiicy of thc coi-olla arid iii [tic oviciitatioii of thc flower. ttiis vai-iatioii iii ílo\\.ci- structiii-e scciiis [o dociiiiiciit 'III c\.olutioiiai-!. siiift fi-oiii oriiithophily to\\.ai-ds ttie niodei.ii iiielittoptiiioiis /)i,qiioíis species. 111 tliis coiitext an anttiecological stud!. of Ditilalis oú.íciirn \\.otiici I)c \.ci.!. \\.elconie. Isoplexis spccies, Lotits beriheloiii and Cnrinririn rnnnrieiisis have been tested for scent, bui oiii), lsoplexis specics scciii [o Iia\.e a faiiit oni, detectable by Iiurnans onl), after criclosurc of the íloi\*ers for a da!, or so iri airtight jar. The scent is swcet and Freesin-like. 16 V Figure 3. Flowcr morphology of'lroplrirs spccies A. 1. canaricnscs. B. 1. rsabclliana. C. i. sccpirum. 40 I <:olour rcd-oraiiKe orangc-ycllow Corisisrcncy ciifT!iough ICES sriK/rough Prescnce of - (+) landing plarform Arca of cnlrancc 40- 50 90-1 10 hole io nccrar lrnrn') Orientarion of sligtiily uprighr slighrly hanging flowcr Ixiigih (11 , 9riiiii c. 16miti corolla iuli~ Sccni f' f Sugñr coiicrniraiion ?O 22 of nccrar ",, Pcrccntagc oí 19 4 deformcd pollcn Cnnnririn mriaritrisis is able to producc O. 18--0.285 ncctar per flo\\.er duririg a period of 2--3 da!-s, Schniiickcr ' 1936). No estiiiiatcs of nectar \.olunie i\'crc made in tlie present study. bur ilie figures given abo\.e seem ver? high. Xo nectar is preseiit in tlie buds. ?'he sugar is a 2.5",, \\ soliitioii (.\+= 15. raiigc 20 30; 33'C. c.oi.rccted to ?o'(-:: Iull suti: 13clliriqli;iiii & Staiile!. POT~CI Refractoiiirtci-: tlic iiiiicr p'irt (11. i3;itxiico del i IiIit~rtio.S 'Tcnerifc. 9 Fcl)riiai.!. 13.00 IioLtr-s). \\.itlicring flo\\.ers iii,i! Iia\.e c~~ii[.i,t~[t,~iti~~iisabo\.c 50n,. Measurenicrits of nectar voluiiie and coiiccntra[ions of sugar of flowers of f. cnnarierisis are gi\ren iii Fig. 4. .l'lie \.oliinie ol'iicctar pcr flower (al1 age clases) is 1 1.8 pI (.!\'= 23. range 0-27.6; 14°C. cloud).; Parc Forestal, E Tenerife, 5 Februar!;. 17.00 Iiours). ?'he iipper aiid yoitiigcsi 11ou.er-sin each iiiflor-cscciice did not contain iiectar, but oiil!. \\.ater. Tliis pticnonienon tiiay be explaiiicd t>y ttie cliniate prc\.ailing in ttie tiabitats of f. c'nrici)retr.ii.r.: 10s and risiiiz clouds caused by tlie trade-\vind. Tlicsc nio\'emctits 01' \.ci-!. liurnid air iiiasses nia! cause \%ratcrto be trapped in tlie flot\rers. Thc atiioiint of water in tliesc '\\.atcr flowers' \%ras7.0 pl per fio\\.er i,:\'=G. rangc I .2--I3.31. If tlie 'sugar flo\\,ers' are corrected for 7.0 pl water, ttie \.oliirne of ncctai. is oiilb 1.8 pl. Froni Fig. 4 alonc it is not possiblc to tcll anytliing about tlie rli)~tliiii iii ncctar productioti as a function of flotvcr age. Tlie coticeiitration ofsugar in 'sugar ílowcrs' is lo0; w/w (A'= 11, range, 2-15; 14"C, cor-rected to 20°C) aiid the amount of sugar per flower is 0.66 iiig. If tlie conccntration is cor-recrcd Ior water added frorn thc exterior [tic concciitration of siigar becomes 259, \\./\\. (l'able 1). Greeriliousc specimens of f. isabeflinnn and f. .rc-eprm liad 10-20 and 10--46 pI of nectar per flower, respecti\dy, after sc\,cral days of production. Ttie 402 i 2 3 4 5 6 7 8 9 1011 12 13 14 Consecuiive position of flower FiKurr 4. Seciar voiumcs ipl! and sugar concenirations (',, \s.,\s'i of individual flo\\er'i oí lropktir i.arinritriii, as a funciion oí ihcir consccuiivc position on ihr inflorcsccncc. Thc lo\t. nunibcrs reíer io !tic iin\cr posiiions. l'hc '25 ílowcrs beionged to ihr tlirrr Iiiflorrscences (1. 0;11. 0:111. *.oíihc iiidi\i~i~i.iiiinder obsrnation I'Iii. Ilwwrs nos 7 & R iiilli~ir.cxmrr 1. had juii hwii \i.iicd l)v a /'lb: '.. ,.~tin/l~hi/n. conceiiti-ation of sugar \\.as 20°, W/M. (,.\,.= 4, r'iiige 18-22; 2G"C:, corrected to 20°C:; I1.00 hours) and 22", \Y/W (JV= 20. i-aiige 15-40; 22°C. corrected to 20°C: 14.00 hours) respectively. These conceiitrntions are closer to thc correctcd perceiitnge for 1. cannriensis [han to the iiiicoriwred, thus supportiiig [he idea tliat a cniisiderable aniouiit of water is gaiiicd by tlie ílowcrs li-oiii tlie trade- \vi ii d 5. ?'he [\\.o outer stanieiis iii ílowers of 1. srcpirrinr are stroiigl!. S-ciiixed. Wlieii their nrirlici-s open, two drops of iicctar bcgiri to iricrease iri sizc aiid slidc aloiia ttie stanieiis. In the hangirig flowers of f. srepirrint ttie curved staiiiciis sccrn to bc iiiipoi.t;iiit iii preveiitiiig tlic iicctar frorn riiiiiiirig out of the flo\\~-rs. Tlie qiiaiitity of nectai prodiiced per flo\\.ri pei- day, percciitagc sugar iii nectai' aiid sugar produciioii per flower pei. da,.. for a greenhoiisc csarnple of L. berlhdolii are given iii Fig. 5. Tlie floivcrs reach an age of c. 10 days uiipolliiinted and with a tcnipcrature regiiiic ot' niax. 20-30°C ;id iiiin. GOC. Ttie iicctai- data is based oii measurernents ofr. 20 Rowers for a \\.cek; tliese rneasiirciiieiits were rnade at c. 10.00 hours eacti day. The ai'erage \.aliies were constarit from the fifth da). oiiwards. Nectar productioii per flou~rpcr da): is 16 14 12 .. 10 ! 8 6 4 2 I I I 1 II m Ip 12I4l I I 1 1 lr m Ip 1.0 / 3.8 ;-; 1 1.4)l . /123456789 Age of flower (di I It III Ip Age class of flower Figure 5. 'I'hc productivii) of neciar (in pl, H=61)and siisar (in mg, .4.=441 pcr flmser per da? Jiid pcrceniagc of sugar iii [tic ncctar (as mg/100 rng ncci.ir. -,+.=45) in rclaiion 10 flowcr age class 111 I.NUJ-brrhlotii under conirollcd grccnhousc condirions i 'Thc agc classcs are drfincd iii caprion io FIK ti ' 40.1 J 5f 0I.FSES 9.2 ~1 (fl=6i, rangc 3.4.-1 j.9). Conceiitratioii of sugar is 12"., \v/w (A'=4.j, rangc 9-20). Thc arnount of sugar produccd pcr flowcr pcr day is 1.24 rna (A'= 44, range 0.35-2.17). Hurnrningbirds and many species of bees seern to prefer nectar with relatively high concentrations of sugar. Laboratory hurnmingbirds choose concentrated sugar solutions of up to 490/0 w/w (Hains\\,orth Pr \.C'olf, 1976; stilcs, 1976). \Vorkers of Apis mefflJera most freqiiently \%it sugar concentrations in the range 30-50% w/w (Corbet, 1978; Heinrich, 197.5). Nectar of below i80/0 sugar w/w is non-profitabie to honey bees, due to the high energy costs to evaporate water to produce honey (see Percival, 1969). The concentrations of sugar in nectar of many hurnrningbird-poilinated flowers are reiatively low, c. 2001~w/w (Baker, 1975). Baker (1975) argues that the higher viscosity of more concentrated ncctar would reduce the foraging.. efficiency of the birds, especialiy under low temperatiire conditions, as iri inontane regions. IIoItcii Pr Feinsinger ( 1978) prescrit arguinents \\.hich suggest the loiver sugar concentrations in rnany hurnmingbird flowers function primarily to exclude bees, and not to attract birds. They find that bird flotvers frorn tropical Arnerica fall into two distinct groups: exclusive and accesible flowers. The first group coniprises flowers which attract birds \\.itli rclatively concentrated nectar (20-33°/0) and exclude bees in their morphological structure. The second group excludes bees on account of their reiatively ttiiri nectar ( 19-240&), thereby leaving larger amounts of sugar to the birds. Iri this group rnorphoiogy does not hinder thc access of bees. ?'he three genera of Macaronesian bird flo\\.crs stiidied fit reasonably \ve11 iiito these two flower categories. The flo\i,ers of Carinriria are without doubt tlie niost cxclusive. Often thc flowers Iiang like bells \\.itli ihc opening of the corolla pointing downwards, though a relatively large portion of the ilowers are turned 11). tlie siipporting plants, Rubus uíniiJolius Scliorr. aiid Eiiphorbia cnrinrierisis L.. in difkrciit directions and niay to soriic cstciiI t)c iicccssible to insects. Tlie li!.potliesis of Baker (1975) of correlatioiis Ixti\ccii iiectai' \.iscosit>. and altitude of Iiabitat could have been tcsted o11 Cnrinririci. hiit \\as iiot. It miglit ha\.e beeii iiiteicstiiig to compare tlie concentrations of iiecrar iii [he (relict?) population of Cnrtnrinn iri Baranco dei Infierno, c. 200 rn, witli thc populations in the rnontane forests of Anaga Peninsula, E Tenerife, c. 900 rn. Both nectar characteristics and, at least to sorne extent, morphology iridicate tliat tlic floic-er of Isopfesis is a bird flo\\.er. Both I. cnnarierisis and 1. isnbefliarin li,i\.c iio landing platforrn, but biiinblcbecs Iiavc been obseivcd \:isitiiig 1. r~nhdiiciria iii thc Botanic Garden iii Coperiliagen. Here they grasp and ciiter tlie flmvcrs sidc\\.a!. betwecn [he uppci- aiid Iot\,cr half of the corolla. In the gaidcii nf (ni-cstr-!.. Ribeiro Frio (860 ni), Lladcira, a large individual of i. sceplriirrr \\.i[li prot)abl>. more thaii 100 iiiflorcsccnccs Iias been observcd to bc visitcd I>\. iridi\%iiials of Borribus rrzaduerisis. -1'iic \.isits wcrc perforrned in tlie 'legitimate' \\.a!. sccii iri Iligilnlis spccics (C.-O. Ot toscii, pcrsonal corn rnu nica t ion). Tlicse observations confirrn the earlier staternciits about tlie closer position of I. scepfrurri' to the bumblebee-pollinated genuc Digifníis (Table 1, Fig. 3). LO~CS has flowrs truly accessible to insects, but secretes a ver). thin nectar, whicli witliout doubt will exclude bees. Burnblebees iiave been observed approaching I,oius pcndants in the Botanical Garden, Copenliagen, but they iiever try tO 405 t Figurc 6. A. A iriplct oTfIowcrs of Lofur bcrfhclotii (thc numbcrs 1-111 rcfcr 10 ihrcc of thc four agc CIASSCS:i. standard íoldcd up (rnax. 2 days old); 11. standard unfoldcd (max. 6 days old); 111. srigrna visihlc on thc tip of ihc kccl (rnax. 8 days old); and l\’. riigma and ¡ir pollcn load visiablc on [he tip of ihc kccl (max. 10 days old). B. Hypothctical siruations: a bird sccks ncttar in fIosr.cn of L. brrfkrlofri, ihc hcad of ihc bird prcrscs thc kccl down, thcrcby purnping ihc pollcn out . 406 J Xl 0I.F.SEN lanci, SO tliis hypothcsis can not bc rxplorcd furthcr (K. E. Auvincn, pcrsolial communication). Finally it has to be stressed that the hypothesis about the two flowcr categories is founded on hummingbirds and their Rowers, and the situation could bc quite differcnt for bird flowers in the OId World. Baker & Baker (1975) have deepened our understanding of the chernical nature of nectar. They used a so-called 'histidine scale' for cornparative studies of amino acid conccntrations in nectar. Every nectar collection was scored against this scale. In this study nectar samples of 1. canariensis and L. berlheforii were treated in the manner described by Baker & Baker (1975). Isopíexis canariensis scored 3 on the scale (N=4), and L. berthelotii scored 4 (J\'= 49, range 3-5). Al1 spots were violet; yellow ones, an indication of presence of proline/hydroxyproline, were not found in the samples. Baker & Baker (1975) gi\.e a table relating score against histidine scale to type of pollinator. The catcgor!. 'OId World bird' has a rnean score of 3.31. This figure fits excellentl!. \\.itli -x.(lrcs of L. berthelotii and I. cnnnriensis. 'Bat', 'Hurnmingbird', 'Ceneralized fl!.. iiiicl 'Sliort-tongued bec' have scores of 3.75, 4.86, 4.35 and 4.59 respectively, the rest of the categories lie above these figures. But it has to be stressed that tlicrc could be a rather i\,ide range of scores intraspecifcally, as with Jnsminum oJicirinlt rcported by Baker Br Baker (1 975). ,411 ttie species studied are protandrous. Canarina has flowers with a kind of sccoiidary pollen presentation comparable with what is known from Campanula. lsoplesis species expose their pollen from anthers situated iinder the upper corolla lip. Pollen grains are spheroid witti a diameter of 20-24 prn. According to data given in Table 1 the individual of 1. isabellinna studied liad an unusuall!. tiigti friiction of deformed polien. The cause of tliis high figure is unkiio\\m. Lofirs brrihtdotii piesents its pollcii by a pumpiiig riieclianisrn kn0u.n iii other species of I-oiuj. .-\ pressure on ttie keel sends the pollen out in big clouds (Fig. 61. ELiropraii species of I.otiis erude small doses of sticky pollen \\.hen \.isited. There czict iio r-ccords of \.isitiiig ariinials, btit iii Fiy. G it is demoristiarcd Iio~.a bird prohiii': 101.iicctar niigtit pius tlic keel iiiid priiiip pollen graiiij out ai-ound the [llroat 'irid foiehead. Tlic Iinbitat of I,. bur.iírt~íoíiisugcests its polliiintois could be groiiiid-íoragiiig birds. Tliis is knoit-ii ti)!. sonie Austi-aliari ground-le\-el flm criiig Fabaceae (Baker-, 1979). Fforoer uisiiors or /)ollitiniors Duririg a stay o11 tlic Caiiaiy Islaiids iii Jaiiiiar!.-Fet>i.iiai-). 1982, sonie obsci.\.ntioiis of flo\vei. \.isirors or polliiiatni..; 01' 1. rnrinrien.ri.i aiid í,.. cnrinrierisi.c \\.crc iii'idc at [\\'O localitics. IJo/Jlt,i/i IXIM/.~MS~S:Pniw Forestal, ..\iiag;i. 'í'ciicrite. Aii iiidi\-idcinI :, I .5 rn iii Iici~lii\\.¡[ti tliree iiiflort.scciiccs aiid [tic pre\ ioiis !.ear's iiifructcsceiicc) \\.as kcpt iinder nbo;cr\,atioii for 2 days at tlie bcgiiiiiirig of Fcbruai).. Otlici. flo\vcriiig species. \\.liich rnight compete for the sersices of polliiiating aniiiials. \vere: Ericn atboirci L., Gernniuni rnirntierise Reuter, Hlperirirttr grtrndl/oliiitri Cliois!., Senecio n/ipeiidiriiln!iis (L. fil.) ScIi. Bip., Sonchits ncnir/is Diiin.-Cours. and Ilbilrriirni rigidum Veiit. (rionienclature according to Brainwdl & Bramwell, 1974'1. Oii 5 February at 14.00 tiours a Bonibiis rnrinriensis \vas obser-\.cd sc\,eral timcs .\f ,A( :.4 K 0 N 1:s I A N II I K i 1 c' I ,( 1 \i'E K S 407 \cry fIcar[lic /.to/dtxis plarit arid ai oric tirnc it sccrncd [o ir?. [o iarid ori oric of [tic irifloresccrices, but was probably scared away. A[ 17.00 tiours on the sarne day a brown bird was scen visiting one of the iriflorcsccnces for 5-7 s, probing for ncctar in two flowers. It carne out frorn the Krica shrub and disappeared again in the same direction. It perched under one of [tic inflorescenccs on the leafless pari of the stern (observation 1). The Rowers t.isitcd were checked for remains of nectar, and in contrast to the rest of the flowers contained no nectar (Fig. 4). On 8 February at 15.00 hours a bird with a faint yellow colour on the breast, * and light dark stripes down along the Ranks, c. 100 rnrn in length, perched on two or three flowers, with a visiting time of 6-9 s (observation 2). At 15.20 hours, probably the same bird came back, perching as it had 20 min carlier, and probing two flowers. The visiting time was t. 6 s (observation 3). Ai 15.50 hours, a blue-ashy coloured bird with a sornewhat darker cap, white breas[. a dark line ttirough the eye and a red eye-ring, c. 1.50 rnrn in length, carne flyiiig frorn the nearby trecs and visited thc lsupferis plant. It probcd for nectar iri thrce or four flowers for 12-15 s (observatiori 4, Fig. 7). tigurc 7. An individual oí'Sylria rnclanoccphala Irucogarh probing lor ncctar in thc obrcrvcd lroplcxir ranarrrnrrs . 408 .j x1. OLESE8 At 16.00 hours the Same species carne back. Again it probed for neC[ar i,, three of four flowers for c. 10 s (observation 5)'. No other anirnals were seen visiting the Isoplexis plant or found iiisidc its flowers. This could have been due to rather cloudy, rainy and cold weather, The birds seerned to know the flower-type from previous visits. The birds in observations 1, 2 and 3 were identified as Phyl1osco/ws colIybiia cannrienjis (Hartwig), and the birds in observations 4 and 5 were identified as S,duia melanocephala leucogasire (Ledru) following the descriptions given by Bannerman (1963: 233 & 22 1, respectively). Canarina canariensis: The innermost part of Baranco del Infierno, Adeje, Tenerife. This deep and narrow gorge is dominated in its inner part by trees and bushes, especiaily Salix canariensis Chr. Sm. and Rubus ulmi/olius. On 9 February at 13.00 hours one certain and one uncertain observation of birds visiting ttie Canarina flowers were made. The bird was rather small, secmed diiIIy brown on thc back, sandy or dark crearny on the breast. It perched on rhc stems of Rubus ulml/olius. It was probably too heavy [O perch on the C'atinriirn itself. On 10 February at 08.50 hours an observation of a bird visit was made at the same site. This bird was more unifor-in brown on the back and the bell!-. Suddenly it carne out from the shrub, sat on a brarnble branch just under a Canarina fower and thrust its head into the bell. The head of the bird nearly disappeared. The situation has been reconstructed in Fig. 8. The light Figure 8. An indibidual of Syluia conrpirillaío or6ríalis probing for ncciar in a Canorina rnnorirnsri flowcr. 1t pcrchcd on a Rubur stcrn. . 1I ,ACAKO S LS 1 A S II 1 K D FLOiV I-: R S 409 co1,ciitioi1s iri tlie gorge were too bad for piiotographing. After just one visit it agaili rctur.ned into thc thickct. This bird was, by the aid of thc ctcscription gi\,cn bb, Bannerrnan ( 1963: 227), identified as the species Sylvia corispiciliaia orbilails íki'halberg). No insects were ever seen in the Rowers of C. tanarietisis. At least 50 flowers were closcly exarnined for tiny insects and other srnall anirnals hidden in the interior of the corolla, but none was found. , ?'he bee Bombus canariensis has only recently received recognition as a species (Erlandsson, 1979). It is endernic to the Canarian archipelago, and it seerns to be the only representative of the genus. The bumblebee is almost entirely black, with only the apex of the abdomen white. However, some individuals according to Erlandsson (1979) have a mixture of yellow and black hairs revealing the relationships of the species to B. ierreslris L., which has its nearest localities in Algeria. During ni! sta?. a fe\\. individuals of B. canariensis i\.crc observed and caiiglit: 29 Januar),, I I .O0 liours; one specimen caught in Saioia canariensis L. ,E of Güirnar, *I'erierife, c. 200 rn); 30 January, 13.00 hours; one specimen observed iii shrub of Riibus dml/oiius (abo\re El Rejo, Gomera, c. 700 m); 2 February, 14.00 hours; one spccimen observed visiting the big capitula of Sonchus acaulis Dum.- Cours.; and oiic specirnen caught foraging in the vegetation of SpQr!O abie/itia !NiIs.;oii 1 ..Joliariseri, 16471. Tlie-first two of tlicsc lia\.e becii Iiiiiiicl as winter visitor.q iii ttie casterii Cnnary Islands (Bnriiiernian, 1963: 237 '. P/$iosropii.i ~~~d/i~/~//oibrrira I>rccds iii S Europeaii loi\.laiid foi-ests 01' cink. P/!vllosrol>ir.r c-ol!;+iía íol!rbi/a is ii N \\'-Gen t ral Europea ii su bspecies espa iid i rig rapidly iii iiii~cdIbi-est arcas. k'iiiall!,, Phylloscopris coi!ybi/n abiulitia is a taiga-bii-d coiifined to SE Eiiropcaii coiiifcroiis forcsts (Dybbro 1976: 248-219; I.ack. 1971; 293 2-1 . 'l'lir n.iiitcr qii;ii-tcrs are, accordiiig to Lack (1971. %ti. restricted 10 S :\l.rica. Phrliosro/ins coi(ybiia is not kiio\\.ii to breed iii N :lli.ica. Joliarisen ( 19-17 i considered P. rolb-bila to be a specics of i\.estern palaroai-ciic origin, \viiicli mtlicr receiitly in tlie last interglacial pci-iod has expandrd its breeding raiigc liorii Stk' Europc to E Europe. Baiincrman ( 1920), piirtl?. opposing iliis Ii>.potliesis, regai-ds tlie Canarian cliiffciiaffs to be Europeaii migrants. Argiiriiciits against ttiis view are found in Volsoe (1955). Accordiiig to Johansen ( 1947) tlie Canarian Píyiioscopus species comprise the niost aiicient 410 J. >I OI.I:SIN populations of al1 rccent cliiffchaffs. This vicw was furtticr cxplorcd by \'olsoc ( 1955), who calculated the Canarian avifauna to be tiighly dorninatcd species of palaeoarctic origin (89%). Phylloscopus collybiia canariensis is extrernely nurnerous in most habitats frorn Euphorbia serni-desert to the Retama, nesting even in gardens. 1t occupies a range of Iiabitats, which in Europe is shared by several Ph~llosco~usspccics and subspecies. fhyfloscopus collybifa canariensis has a total body length of 105 rnrn (JV = 10, range 95-120; skins frorn the Zoological Museum, Copenhagen), and a bill length oí9 mm (range 9-10). Food preferences seem to be insects íHald- . iMortensen, 1969), but an indication of a much wider range of food iterns in winter and in surnmer quarters is given by Pettett (1975). He reports an observation of chiffchaffs consurning acacia gurn in [he Sudan. In thc most ,e eastern Danish island, Christiansa, the spring is substantially delased in cornparison with the rnain and more oceanic parts of the country. hligrants of [tic gcnera Ph-dloscopus and Sylvia rnay thus experience a shortagc of animal food iri tlic spring on tliis island. Several obcervations niacic 1)) Laursen 8r I-iolni ( 1981) indicate that the birds rnay eat pollen and other floral parts as a dietary supplernent. Rased on the observations of foraging in [he flowers of fsoplexis carinriensis and tIic rneasurements of bill Iength Phylfosropus coflybiia cannrierisis jhould be able botli to act as pollinator and to extract nectar frorn thc flowers (Table 1 ). Phyífoscopus collybifa canariensis is probably also able to visit Cnnarina cnnariensis successfu I I y. The Canary sardinian warbler (Sylvia melanocephala leucogaslre) and thc Cariar). spectacled \vart>lcr (S.conspicillala orbiralis) together r\.ith the dusky blackcap :S. nlricnpiiln obscilrn Tschusi) are the only breedina rncnibers of the faniily Syl\.iidac in [he Cariary Islands (Bacallado, 1976). Bacallado ( 1976) belie\.is tlie Cariaiian Syl\.iidac to be postglacial irnrnigrants. If tlie Syl\.iidae lia\.c esperienced succecsive invasions the time of their first arrival rnay lie far back in riiiic. iii spitt. of tticir weak differcritiation. The tlircc .;pecies of Si'/i./ti iii;i\ ~r*cwiitlai-il!.ti:i\ C. .;prcad to the arid parts of the ijl,liidG \\'tien ttiew t)cIi.< \\ idciicd. Iio~\c\ci~.according to \'oisoc ( 1955) aiid Bncallado , 1976 tlic .l'ei.tiar!. rclicr ii\.iliiiiia beloriging to tlie laurel forest coiijisrj only of t\\a 'Iaiiix-I pigeon' spccics today. The Pinus forest has probably csisted during thc \\.tiole I'lcistoceiie aiid together with this vegetation type \\.e find the first niassive nppearancc 01' se\.cral bird species. Botti the saidiiiian and the spectacled warbler iiic Ibiind al1 c~t'rtlic. arctiipclago \Bnc;illado, 1976). Batiricrniaii (1963: 224 \\ i.itcs: '.Iii Teiicrifc ilic Siirdinian \\'ai.l)lci. nscends to a grciiicr altitude . . . ttici.t' ij little doiibt ili,ir it IiCsts in [tic ti-cc-licntli zone where it is probably niore 1)lciitiI.iil thaii aii\.\\ Iici.c clsc in tlir iii-ctiipelago". It nia). also be obser\.cd iii [tic Oarrancos. .Si,I[,/o rorr.r/~icilla/n is nIw n \'cry comrnon bird, especially iii S 'l'ciicrife. It is iiicxil! obscr\.cd iii tlic wiiii-dcsert bclt aloiig tlic whole rtinritiiiic 7.one, and iii ilic barraricos. 11 scciiis [o be abscnt li-oiii tlic forests. It is liiiiiici in coriticctiori \\ iili rnariy diflerclit piaiit species sucli as ttiose of Euphorbin. 'l-lic one obscr\,cd oii 10 Februar!., prol)abl}*a fernale, \vas diving in and out of ilic bramble slii.itl). iri accordancc \\,iili oiie of its rnany comnion narnes 'zai-zalcro', the one in [tic branibies. Tlic ioral body length of thc sardinian warbler is c. 140 rnni (.\. = 3, range 135- 140'1,niid tlie length of bill c. 10 rnrn (JV = 2); ttie aiialogous íigiires for tlie spectñclcd \\.arbler are 120 rnni (.N=8, range 110 .125i, aiid 9 ni111 ',\-=8. hlA(:AR(),VESIAK UlKD FL()\\EKS 41 1 ranyc 8 9,. According to Jordano (1982) Sylvia melanocephala in Spairi cats Rubus fruits. *I'tiedict was cornposcd ofaiiirnal and vegetable matter in equal aniounts. in stomachs of Syluia melanocephala, Herrera ( 198 1 ) found fruit remains and seeds in 83O/, and 28% of the stornachs, respectively. Nine difTerent plant species were represented. Sylvia melanocephala is a typical bird species of the Mediterranean region. Sylvia conspicillata was rarely observed eating Rubus fruits (jordano, 1982). According to Hald-Mortensen (1969) its preferred food seerns to be insects. Syluia atricapilla probably also prefers a mixed diet. I The data on habitat preferences and bill length support the conclusion that Syluia melanocephala rnay be an irnportant poliinator of lsoplexis and probably also of Canarina. On the other hand, Sylvia conspicillata, due to its more narrow habitat choice, is only a possibie pollinator of Canarina in its southern localities on Tenerifc. In Ash (1959) an oid phenomenon often observed has found its solution. Migrating birds frorn S and NW Europe have frequently been found \\rith a substance adticring to their bills. Ash (1959) estirnates tliat no more than i -2O., of the spring rnigrants carry this substance, which he identifies as Cifrus pollen. Arnong the bird species were Syluia atricapilla and Phylloscopus collybita. In order further to reveal any posible flower-visiting habits by Canarian hirds the bilis arid feathers of head and neck of al1 specirnens of Canarian Sylviidae, Phylloscopus and several other genera in the skin coiiections of the Zoological Museurn, Copenhagen, were brushed for any residual pollen grains. The material frorn the birds was brushed onto a glass slide mounted with a 'Scotch' double-sided tape. The rnethod was adopted and modified frorn Iwarsson (19791,wtio examined the skins of African Nectariniidae. I found no pollen grains of any kind. The reason may be due to a non-existence of ans flower-visiting habits, to a rneticulousness of the collectors in cieaning the skins, or due to the birds thernselves cleaning their bili and forehead. In view of the stiidy of I\\,arssori ' 1979) on sunbirds, which are regular flo\\.er birds. arid iri faci are deperidcric oii tlic existencc of bird flowers, u.licrx- he found less tliiiri 10 giairis per prcl)'ir GENERAL DISCI'SSIOX AND C0SC:l.l SiOS Conclusinris drat\.ri frorn data o11 nectar, corolla coloiirs. scent and otlicr rnorphological cliaiacteristics confirni the supposed oriiithophilous naturc of .. lsoplexis spccics. l.otris bcrthelofii, aiid Cmiarina canarierisis. rhese species Iia\.c t ticir origin in tiir l'crtiary Period, whiic flowcr-visiting birds do riot appear as fossils iintil ttic Plcistoccrie, but iIndoiibtedly originated considerably carlier. l'lierefore. tlic stoi!' of Old \\'orld bird-flower coc\.oiutioii probabi!. bcgiris at sorne time iii tlic carly to rnid-Tcrtiary. \\'ithout doiibt tlie hlacaroncsiaii bid- flower eleniciit bclongs to a rictier bird-flower flora once distributed in ttie tiumid forcsts iri [tic hlediterrancan arid N Africa. Recerit African taxa riia). be remnants of tlic saiiie flora, such as, the E African spccies of Canarina arid Erica. Sorne rnoderri S African species of Erica have bird flowers. This study giim exarnples oí' three different modes of Old \\'orld bird 412 J. Al. OLESEN pollination: Ground foraging, Lotus; perching arid nectar drinking on rtie same plant, fsoplexis; and perching and nectar drinking on different plants, Rubus and Canarina. These piants might have been pollinated by different sunbirds in the past. With changes in ciimate and vegetation in S Europe and N Africa new plant species appeared: the bee-pollinated Digitalis and Lotus species. They have different corolla coiours, lower nectar volurne per flower, and higher sugar concentrations than their bird-pollinated relatives. The relation Can- nrina-Campanula might be the third exarnple. The concentrations of sugar, as in , Digifafis, iie between 21 and 40% (Percival & Morgan, 1965) and in European Lotus between 30 and 50% (Percival, 1969). The concentration of sugar in Macaronesian species of Lotw other than L. berfhelotii is not known. 9 Macaronesia has, cornpared wi th the Mediterranean region, a relativeiy poor Hyrnenoptcran fauna. The sea has acted as a dispersa1 barrier. The irnportance of bee pollination on the Macaronesian Islands is not known, but is probably low. The Macaronesian bird-flower elernent has both in the past and in the present relied on birds, whether sunbirds or other groups. If sunbirds ha\,e been present in the past, they probably disappeared when the arid zones widencd and ultirnateiy resulted in a shortage of their food plants. Some time in the past the two species of Sylvia, Phylloscopus colbbita, Bombus canariensis, and probabiy other animal groups too, have included nectar from these bird flowers in their diet. These anirnals harvest a wide variety of food items witti a low predictability in time. They have thus been narned opportunists in this context (hlcKey, 1975). This plastic way of foragirig might have been fa\.ourcd and intensified after their colonization of the islands due to a lack of congciieric cornpetition. ?'he idea of niche tvidening on islands rclati\.e to nearby continents has been a rnatter of dispute (McArthur & \\'ilsoii, 1967; \t'iliiamsori. 1981 !. Since red flowcr-s generally seem to attract opportiiriistic niid pollinatiiig I)ir.ds, tlie supposed csiiiiction of 1,. berlheiotii in natiiic iiiiylit I)c csplained 1)). Iici-bivorcs aiidlor iiian. Of al1 [tic Iliiropean species 01' Uottibus, it was a Bortibirs close to tlit' fh1ihu.i kmesfris-type which reached llacaronesia. Bombirs /erresfris and a 1u oilier European aiid Americari Bom!~sspecies are, compared with most I>uinblcbce species: niore often nectar robbeis; use more non-flower food sources c.g. lione!- dew, juice froiii iipen fruits aiid nricmophilous polleiij; Iiave a brond-~l)~*ciiwi use of food plaiits; possess stroii3ci iiiandibles and slioitei- probosces: XIX. IIKII'C abundant ni ;I Iiabitat; tiave widci. gcographicai arid aliitiidinal raiiggc.;. t.iiici-~c earlier frorri IiiI>crnation; are 1iioi.c long-distancc dispersers; aiid m;I? I>c aggressi\.e. 'l'ogeilici-, these cliaiacters constitutc a kiiid of opl)oi-iiiiiisi syndrorne. fjorribirs ratinrienszs \\'as ablc to reach tlie Canaries and to ot)i;iiri rood frorn a w%ic \.nriet). of plarits li-oiii diflcrent \*egctaiion typcs and ~~Iiii~idiii~iI zones. .-\~:~XO\\.l.~DGEh~E~.~S 1 ani \.ery grateful to Dr Petcr F. Yeo for his helpful suggestioiis aiid cornrnents. 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