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A Fossil Fuchsia (Onagraceae) Flower and an Anther Mass with in Situ Pollen from the Early Miocene of New Zealand 1

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A Fossil Fuchsia (Onagraceae) Flower and an Anther Mass with in Situ Pollen from the Early Miocene of New Zealand 1 American Journal of Botany 100(10): 2052–2065. 2013. A FOSSIL FUCHSIA (ONAGRACEAE) FLOWER AND AN ANTHER MASS WITH IN SITU POLLEN FROM THE EARLY MIOCENE OF NEW ZEALAND 1 D APHNE E. LEE 2 , J OHN G. CONRAN 3,6 , J ENNIFER M. BANNISTER 4 , U WE K AULFUSS 2 , AND D ALLAS C. MILDENHALL 5 2 Department of Geology, University of Otago, P.O. Box 56, Dunedin, New Zealand; 3 Australian Centre for Evolutionary Biology and Biodiversity & Sprigg Geobiology Centre, School of Earth and Environmental Sciences, Benham Bldg DX 650 312, The University of Adelaide, SA 5005 Australia; 4 Department of Botany, University of Otago, P.O. Box 56, Dunedin, New Zealand; and 5 GNS Science, P.O. Box 30-368, Lower Hutt, New Zealand • Premise of the study: Fuchsia (Onagraceae) anthers, pollen, and an ornithophilous Fuchsia -like fl ower from an earliest Mio- cene lacustrine diatomite deposit at Foulden Maar, southern New Zealand confi rm a long record for Fuchsia in New Zealand and probably an equally long history for its distinctive honeyeater pollination syndrome. The anthers contain in situ pollen of the fossil palynomorph previously assigned to Diporites aspis Pocknall et Mildenh. (Onagraceae: Fuchsia L.). • Methods: We undertook comparative studies of the fl ower and anther morphology of the newly discovered macrofossils and compared the in situ pollen grains from the anthers with dispersed pollen grains from extant species. • Key results: The anther mass is referred to a new, extinct species, Fuchsia antiqua D.E.Lee, Conran, Bannister, U.Kaulfuss & Mildenh. (Onagraceae), and is associated with a fossilized Fuchsia -like fl ower from the same small mining pit. Because Dipo- rites van der Hammen is typifi ed by a fungal sporomorph, the replacement name for D. aspis is Koninidites aspis (Pocknall & Mildenh.) Mildenh. gen. & comb. nov. Phylogenetic placement of the fossils agrees with a proximal position to either sect. Skinnera or sect. Procumbentes. These are the oldest macrofossils of Fuchsia globally. • Conclusions: The fl oral structures are remarkably similar to those of modern New Zealand Fuchsia . They suggest that the distinctive honeyeater bird-pollination syndrome/association seen in modern New Zealand was already established by the late Oligocene–earliest Miocene. The implications for the biogeography and paleoecology of Fuchsia in Australasia are discussed. Key words: anthers; biogeography; fl ower; Fuchsia antiqua ; in situ pollen; Koninidites aspis ; Miocene; Oligocene; Onagraceae. In contrast to the fl ora of neighboring landmasses of Austra- plants include Alepis Tiegh. and Peraxilla Tiegh. (Loranthaceae), lia and New Caledonia, the present-day fl ora of New Zealand is Alseuosmia A.Cunn. (Alseuosmiaceae), Fuchsia L. (Onagraceae), characterized by a depauperate array of fl owering plants, many Knightia R.Br. (Proteaceae), Metrosideros Banks ex Gaertn. monotypic woody genera, a predominance of white-fl owered (Myrtaceae), Phormium J.R.Forst. & G.Forst. (Xanthorrhoeaceae), taxa and unspecialized fl oral structures for generalist pollina- Rhabdothamnus A.Cunn. (Gesneriaceae), and Sophora L. tion by small birds and insects ( Lloyd, 1985 ; Lee et al., 2001 ). (Fabaceae) ( Kelly et al., 2010 ). Of the 29 species of fl owering trees and shrubs in New Zealand Relatively little is known about the antiquity of the fl oral that possess ornithophilous fl owers, most are mainly pollinated structures and syndromes that relate to bird pollination in New by honeyeaters (Meliphagidae), including tūī ( Prosthemadera Zealand (and elsewhere). Lloyd (1985) postulated that the de- novaeseelandiae ) and bellbirds ( Anthornis melaneura ). These velopment of simplifi ed fl oral structures in New Zealand plants was related to a depauperate insect and bird fauna, although he did not speculate on the cause or antiquity of this general biotic 1 Manuscript received 20 December 2012; revision accepted 5 July 2013. The authors thank the Gibson family, Dr. Alan Walker, and Featherston impoverishment. Similarly, Kelly et al. (2010) showed that de- Resources Ltd for kindly allowing us access to the site. Liz Girvan (Otago pendence on bird pollination is unexpectedly high, with 85 na- Centre for Electron Microscopy) provided valuable assistance with the tive species (including 30% of the tree fl ora) having reports of SEM photographs. Jack Lamb of the World living collection of Fuchsia visits to fl owers, despite the very small number of nectarivorous species for BGCI, Fuchsia Species Conservation and Research, U.K. is bird species. They concluded that bird pollination in New Zealand thanked for the photo of F. cyrtandroides . Dr. Jamie Wood helped with is widespread and important for numerous taxa, including many pollination and dispersal information on modern Fuchsia in New Zealand. lacking apparently ornithophilous fl owers. The Departments of Geology and Botany, University of Otago, Dunedin Recent research in richly fossiliferous lagerstätten deposits and the School of Earth and Environmental Sciences, The University of of late Oligocene–early Miocene age in southern New Zealand Adelaide are thanked for the provision of resources to undertake this has revealed a wide variety of particularly well-preserved plant research. Funding for this study was provided by a Marsden Grant from the Royal Society of New Zealand. Prof. Bill Lee (Landcare Research, NZ) is fossils, including a fertile fern ( Conran et al., 2010 ), leaves with thanked for comments on the manuscript. cuticle (e.g., Conran et al., 2009 ; Carpenter et al., 2010a , b ; 6 Author for correspondence (e-mail: [email protected]) Ferguson et al., 2010 ; Jordan et al., 2010 ; Lee et al., 2010 ; Bannister et al., 2012 ), fruits and seeds, and importantly, fl ow- doi:10.3732/ajb.1200643 ers with in situ pollen ( Bannister et al., 2005 ; Lee et al., 2010 ). American Journal of Botany 100(10): 2052–2065, 2013 ; http://www.amjbot.org/ © 2013 Botanical Society of America 2052 October 2013] LEE ET AL.—NEW ZEALAND FOSSIL FUCHSIA 2053 Taken in conjunction with the extensive, continuous palyno- 1999 ; Martin, 2003 ), is considered to represent the modern morph record for the New Zealand Cenozoic ( Mildenhall, 1980 ; semiaquatic genus Ludwigia L. (including Jussiaea L.), which Pocknall and Mildenhall, 1984 ; Mildenhall and Pocknall, 1989 ), is now extinct in New Zealand, possibly indicating climatic these macrofossils make it possible to investigate and clarify change to more open and drier ecosystems ( Macphail, 1999 ). aspects of the history of angiosperms in New Zealand in some The affi nity of C. oculusnoctis was listed in Bannister et al. detail. Of particular interest is the antiquity of ecological inter- (2005 , p. 517) as “Onagraceae, cf. Epilobium .” actions relating to pollination and dispersal in relation to the Onagraceae appears to have diverged from its sister family evolution of the distinctive modern New Zealand fl ora. Lythraceae ~93 Ma in the early Cenomanian, while Fuchsia is One notable genus is Fuchsia, which is widespread through- thought to have differentiated from Circaea L. ~40 Ma in the out New Zealand today and has distinctively colored fl owers Eocene ( Conti et al., 1993 ; Berry et al., 2004 ; Sytsma et al., and pollen and specialized fl oral structures for bird pollination 2004 ; Wagner et al., 2007 ; Xie et al., 2009 ). The presence of a ( Robertson et al., 2008 ). Similarly, the fruits display a bird- well-dated 23 Ma Fuchsia fossil fl ower and pollen-bearing an- dispersal syndrome ( Armesto and Rozzi, 1989 ; Robertson et al., thers at Foulden Maar provides new information on the fl oral 2008 ). structure of early Fuchsia , in particular the shape of the fl oral Fuchsia also displays an unusual biogeographic pattern. Of tube and arrangement of the anthers. Furthermore, as macrofos- the 107 species in 12 sections ( Heywood et al., 2007 ; Wagner sil records for Onagraceae are extremely rare, these fl oral mac- et al., 2007 ; Mabberley, 2008 ), three species (and a natural hy- rofossils are very important for an improved understanding of brid) in two sections are endemic to New Zealand: sect. Skinnera the fossil record of Fuchsia and unraveling the molecular phy- (J.R.Forst. & G.Forst.) DC.: F. excorticata (J.R.Forst. & G.Forst.) logenetics and biogeographic history of Onagraceae. L.f. ( Fig. 1A ), F. perscandens Cockayne & Allan ( Fig. 1B ) and F. × colensoi Hook.f. ( Fig. 1C ); and sect. Procumbentes Godley & P.E.Berry: F. procumbens R.Cunn. ex A.Cunn. ( Fig. 1E ). The MATERIALS AND METHODS remaining species in sect. Skinnera , F. cyrtandroides J.W.Moore ( Fig. 1D ), is confi ned to Tahiti ( Godley and Berry, 1995 ). The Fossil preparation — The fossils were recovered from small mining pits remainder of the genus is found throughout South and Central near Middlemarch in Otago, southern New Zealand. The plant fossils occur in America as far north as Mexico, but Fuchsia is notably absent the Foulden Hills Diatomite ( Lee et al., 2007 ; Lindqvist and Lee, 2009 ), a fi nely from present-day Australia, New Caledonia, and other Pacifi c laminated biogenic lake deposit comprised mainly of pennate diatom frustules, islands ( Berry et al., 2004 ). siliceous chrysophycean algal stomatocysts, sponge spicules, insects, articu- The global fossil record of Onagraceae has until now been lated fi sh skeletons, and plant material ( Pole, 1996 ; Lee et al., 2007 ). The fossil based almost entirely on distinctive pollen, with macrofossils macrofl ora comprises numerous leaf compressions, typically with well-pre- served cuticle, fruits, occasional bark and wood fragments, and rare fl owers. (seeds and fruits) rare for the family ( Grímsson et al., 2011 and The anthers and fl ower described here, as with other fl ower parts from the site references therein) and none reported for Fuchsia ( Martin, ( Bannister et al., 2005 ), were preserved on light-colored layers in the varved 2003 ). Within the family, Fuchsia pollen is highly recognizable diatomite ( Lindqvist and Lee, 2009 ). ( Erdtman, 1952 ; Balme, 1995 ). Distinctive diporate pollen as- The Foulden Hills Diatomite was deposited in a small maar crater lake Diporites aspis ( Lindqvist and Lee, 2009 ).
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