Data Paper |
Corresponding author: Cynthia M. Morton ( mortoncm100@gmail.com ) Academic editor: Sylvain Razafimandimbison
© 2015 Cynthia M. Morton.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Morton CM (2015) Phylogenetic relationships of Zieria (Rutaceae) inferred from chloroplast, nuclear, and morphological data. PhytoKeys 44: 15-38. https://doi.org/10.3897/phytokeys.44.8393
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Zieria Sm. (Rutaceae, Boronieae) is predominantly native to eastern Australia except for one species, which is endemic to New Caledonia. For this study, sequence data of two non-coding chloroplast regions (trnL-trnF, and rpl32-trnL), one nuclear region (ITS region) and various morphological characters, based on
Zieria , Rutaceae , Boronieae , Australia, conservation
Zieria Sm. (Rutaceae, Boronieae) comprises 42 species. Six major taxonomic groups were defined based on non-molecular characters, according to the most recent classification by
Zieria consists of prostrate shrubs to small trees, with opposite and trifoliolate, or rarely unifoliolate leaves. Inflorescences are axillary, with four-merous, white or pink flowers. The fruits are comprised of one to four basally connate cocci, which dehisce explosively along the adaxial and apical margins. The seeds are usually one (often by abortion of one ovule) per fruit, with a thin brittle testa that is irregularly sculptured. In general, Zieria is distinguished from other genera of the Australian Rutaceae by the combination of opposite leaves, the conspicuous and 4-merous flowers, free petals, four stamens, free filaments, a deeply four-lobed disc, and dry, dehiscent fruits. This genus is predominantly native to eastern Australia, with the exception of the one species, Z. chevalieri Virot., which is endemic to New Caledonia. The distribution in eastern Australia extends from northeastern Queensland to Tasmania and as far west as Kangaroo Island in South Australia.
Sir James E. Smith first described the genus in
Zieria, Group A |
Z. adenodonta (F. Muell.) J.A. Armstr. |
Z. adenophora Blakely |
Z. buxijugum J.D. Briggs & J.A. Armstr. |
Z. collina C.T. White |
Z. floydii J.A. Armstr. |
Z. formosa J.D. Briggs & J.A. Armstr. |
Z. furfuracea R.Br. ex Benth. |
Z. granulata C. Moore ex Benth. |
Z. hindii J.A. Armstr. |
Z. obcordata A. Cunn. |
Z. parrisiae J.D. Briggs & J.A. Armstr. |
Z. robusta Maiden & Betche |
Z. tuberculata J.A. Armstr. |
Z. verrucosa J.A. Armstr. |
Zieria, Group B |
Z. arborescens Sims |
Z. caducibracteata J.A. Armstr. |
Z. lasiocaulis J.A. Armstr. |
Z. oreocena J.A. Armstr. |
Z. southwelli J.A. Armstr. |
Zieria, Group C |
Z. chevalieri Virot |
Z. fraseri Hook. |
Z. laevigata Bonpl. |
Z. laxiflora Domin |
Zieria, Group D |
Z. montana J.A. Armstr. |
Z. prostrata J.A. Armstr. |
Z. robertsiorum J.A. Armstr. |
Z. smithii Andrews |
Zieria, Group E |
Z. aspalathoides A. Cunn. ex Benth. |
Z. citriodora J.A. Armstr. |
Z. ingramii J.A. Armstr. |
Z. minutiflora (F. Muell.) Domin |
Z. obovata (C.T. White) J.A. Armstr. |
Z. odorifera J.A. Armstr. |
Z. pilosa Rudge |
Z. rimulosa C.T. White |
Zieria, Group F |
Z. baeuerlenii J.A. Armstr. |
Z. covenyi J.A. Armstr. |
Z. cytisoides Sm. |
Z. involucrata R.Br. ex Benth. |
Z. littoralis J.A. Armstr. |
Z. murphyi Blakely |
Z. veronicea (F. Muell.) Benth. |
A subfamilial phylogenetic analysis was completed for Rutaceae by
Molecular studies can produce effective and practical solutions for conservation biology to taxonomic uncertainties with respect to rare and threatened taxa and, in light of the high proportion of endangered taxa and overlying distribution patterns for a number of these taxa, examinations should be conducted on Zieria.
The goals of this study are (1) to test the monophyly of the genus Zieria and to identify its closest relatives; (2) to evaluate the six taxonomic groups within Zieria as recognized in the most recent revision (
For this study, two non-coding chloroplast regions (trnL-trnF, and the rpl32-trnL) were selected, as well as the Internal Transcribed Spacer (ITS) of the nuclear region and various morphological characters. The trnL-trnF region consists of the trnL intron and the trnL-trnF intergenic spacer (
Vouchers for the 33 species used in this study along with the GenBank accession numbers are listed in the
The rpl32-trnL gene in 33 species was amplified using the primer pair rpl32F/trnL (
The trnL intron and the trnL-trnF intergenic spacer for 33 species were PCR-amplified using the universal primers trn-c, trn-d, trn-e, and trn-f as described by
The amplification of the ITS was performed successfully on 33 species using oligonucleotide primers ITS1/ITS4 (
The PCR products were cleaned using the QIAGEN QIAquick PCR purification kit (QIAGEN Inc., Chatsworth, California, USA) following the protocols provided by the manufacturer. Cleaned products were then directly sequenced using the ABI PRISM Dye Terminator Cycle Sequencing Ready Kit with AmpliTaq DNA Polymerase (Applied Biosystems Inc., Foster City, California, USA). Unincorporated dye terminators were removed using the QIAGEN DyeEx dye-terminator removal system (QIAGEN Inc.) following the manufacturer’s recommendations. Samples were then loaded into an ABI 3100 DNA Sequencer. The sequencing data was analyzed and edited using the
A morphological dataset of 48 characters was constructed. Twenty-eight characters were coded as unordered binary and 20 as multistate. All but two characters (4-types of pubescence on young branches and 12-presence or absence of revolute lamina margins) were variable within Zieria. The invariant characters were included because they were thought to be important in testing the monophyly of the genus. All analyses were conducted as stated in the analysis section. Character states of taxa were taken from
Boundaries of the trnL intron, rpl32-trnL, and the ITS nuclear gene were determined by comparison with sequences in GenBank. The following two alignment criteria and methodology were used: (1) when two or more gaps were not identical but overlapping, they were scored as two separate events and (2) phylogenetically informative indels (variable in two or more taxa) were scored as one event at the end of the data set. All DNA sequences reported in the analyses have been deposited in GenBank (
Maximum-parsimony (MP) analyses of all single markers as well as the combined datasets were performed in PAUP* 4.0b8 (
The Bayesian analysis of the combined molecular and morphological analysis used a mixed-model approach (Mr Bayes 3.1.2
To determine the combinability of the data sets, their data structure was compared using methods outlined by
This study examined the following 15 of the 21 endangered or vulnerable species (Z. adenophora, Z. baeuerlenii, Z. buxijugum, Z. citriodora, Z. collina, Z. convenyi, Z. formosa, Z. granulata, Z. ingramii, Z. murphyi, Z. obcordata, Z. parrisiae, Z. prostrata, Z. verrucosa, and Z. tuberculata). An examination for similarity was made using the distribution patterns and the number of bp changes within all three genes for the taxa in clades that had strong posterior probabilities.
The inclusion of gap coding in all data sets containing molecular data resulted in more homoplasy and lack of resolution; therefore, gap coding was not used in the following results. GenBank sequences EU281855–EU281953 were specifically generated for this study.
Multiple sequence alignment of Zieria and Neobyrnesia with 44 other Rutaceae and closely related taxa resulted in a data matrix of 1038 characters. No regions were excluded. Of the 1038 positions constituting the aligned trnL-trnF sequences, 357 (34%) were variable and 408 (39%) were parsimony-informative. The analysis recovered 4,383 equally optimal trees of 1037 steps (CI = 0.57, RI = 0.72; Fig.
Zieria are supported as a monophyletic clade in the strict consensus tree (BS 100%). Sister to six species of Zieria is the genus Neobyrnesia (BS 94%). Sister to this grouping is (((Medicosma and Euodia (BS 96%)) Boronia (BS100%)) (Sarcomelocope and Melicope (BS 100)) (BS 87%)) followed by the remaining taxa. Neobyrnesia was therefore selected as the outgroup for this study.
Multiple sequence alignment of Zieria and Neobyrnesia resulted in a matrix of 1035 characters. A total of 10 gaps were required for proper alignment of the trnL-trnF sequences. These gaps ranged from one to 15 bps. No regions were excluded. Mean percentage G + C content was 56%. Of the 1035 positions, 127 (12.3%) were variable and 33 (3.2%) were parsimony-informative. The analysis recovered 35,458 equally optimal trees of 71 steps (CI = 0.59, RI = 0.69).
Zieria was supported as monophyletic in the strict consensus trees (BS 100). Most of Zieria consists of an unsupported grade or small polytomies except for one minor clade with bootstrap support of 75% (Z. furfuracea R.Br. ex Benth. and Z. laxiflora Domin).
Multiple sequence alignment of Zieria and Neobyrnesia resulted in a matrix of 1180 characters. Approximately 14 gaps were required for proper alignment of the rpL32-trnL sequences. These gaps ranged from one to 49 bps. No regions were excluded. Mean percentage G + C content was 30%. Of the 1180, 236 (20%) were variable and 46 (3.9%) were parsimony-informative. The analysis recovered 87,213 equally optimal trees of 77 steps (CI = 0.69, RI = 0.90).
Zieria was supported as monophyletic in the strict consensus trees (BS 100). The tree mainly consists of a polytomy except for one minor clade with bootstrap support greater than 75% (Z. furfuracea and Z. laxiflora (BS 95%)).
Multiple sequence alignment of Zieria and Neobyrnesia resulted in a data matrix of 714 characters. Approximately five gaps were required for proper alignment of the ITS sequences. These gaps ranged from one to 16 bps. No regions were excluded. Mean percentage G + C content was 36%. Of the 714, 207 (29%) were variable and 82 (11.5%) were parsimony-informative. The analysis recovered 7,259 equally optimal trees of 169 steps (CI = 0.72, RI = 0.84). Zieria is supported as a monophyletic clade in the strict consensus tree (BS 100%). Basal within this clade is Z. citriodora J.A. Armstr., which is sister to Z. aspalathoides A. Cunn. Ex Benth. and Z. ingramii J.A. Armstr. (BS 88%). The backbone phylogeny of the genus remained unresolved, however a number of minor clades were inferred. Clades that contain bootstrap support greater than 75% starting from the base of the tree include: 1) a clade containing Z. arborescens Sims sister to a polytomy of Z. covenyi J.A. Armstr., Z. murphyi Blakely and Z. odorifera J.A. Armstr. (BS 88%); 2) a clade containing Z. montana J.A. Armstr. and Z. southwelli J.A. Armstr. (BS 100%); 3) a clade containing a polytomy of Z. adenophora Blakely, Z. furfuracea and Z. laxiflora (BS 100%); 4) a clade containing Z. fraseri Hook. and Z. laevigata Bonpl. (BS 100%); 5) a clade containing Z. pilosa Rudge and Z. verrucosa J.A. Armstr. (BS 100%); and 6) a clade containing ((Z. collina C.T. White and Z. prostrata J.A. Armstr. (BS 89%)) sister to Z. adenodonta (F. Muell.) J.A. Armstr. (BS 77%)).
The respective numbers of variable and potentially phylogenetically informative characters in each dataset, the consistency indices and the numbers of branches with bootstrap support above 75% can be found in Table
Genetic statistics for genes and genic regions utilized in the individual genic analyses, and in the combined molecular and morphological datasets.
Results | trnL | rpl32 | ITS | molecular | morphology | Total data |
---|---|---|---|---|---|---|
Gaps | 10 | 14 | 5 | 957 | ||
Range of Gaps | 1–15 | 1–49 | 1–16 | |||
Excluded | none | none | none | none | none | none |
56 | 30 | 36 | 40 | |||
Length | 1035 | 1180 | 714 | 2929 | 48 | 2977 |
Informative characters | 33 | 46 | 82 | 161 | 45 | 209 |
Variable characters | 127 | 236 | 207 | 570 | 48 | 618 |
Trees | 35458 | 87213 | 7259 | 2301 | 591 | 555 |
Steps | 71 | 77 | 169 | 378 | 278 | 1177 |
CI (consistency index) | 59 | 69 | 72 | 57 | 30 | 62 |
RI (retention index) | 69 | 90 | 84 | 74 | 57 | 59 |
BB (branch and bound) above 75% | 2 | 2 | 9 | 7 | 0 | 6 |
Following the methods outlined by
Multiple sequence alignment of Zieria and Neobyrnesia resulted in a matrix of 2929 characters, of which (32.7%) include at least one accession with a gap. Mean percentage G + C content is 40%. Of the 2929, 570 (19.5%) were variable and 161 (5.5%) were parsimony informative. The analysis recovered 2,301 equally optimal trees of 378 steps (CI = 0.57, RI = 0.74; Fig.
Internally, Zieria consists of mainly a polytomy except for several minor clades with bootstrap support greater than 75%. Clades that contain bootstrap support greater than 75% starting from the base of the tree include: 1) a clade containing Z. prostrata and Z. smithii (BS 94%); 2) a clade containing Z. fraseri and Z. laevigata (BS 100%); 3) a clade containing a polytomy of Z. arborescens, Z. covenyi, Z. murphyi Blakely and Z. odorifera A. Cunn. (BS 76%); 4) a clade containing Z. furfuracea and Z. laxiflora (BS 99%) sister to Z. adenophora (BS 99%); and 5) a clade containing Z. collina and Z. adenodonta (BS 95%).
Of the 48 characters constituting the non-molecular dataset, 48 were variable and 45 (93.8%) were parsimony-informative. The analysis recovered 591 equally optimal trees of 278 steps (CI = 0.30, RI = 0.57). Zieria was monophyletic in the strict consensus of these trees (BS 100%). The in-group topology consisted of a large grade with only one clade that contained bootstrap support greater than 75% (Z. laxiflora and Z. laevigata (BS 75%)).
Following the methods outlined by
Multiple sequence alignment of Zieria and Neobyrnesia resulted in a matrix of 2977 characters, of which 28% include at least one accession with a gap. Of the 2977 positions constituting the aligned sequences, 618 (%) were variable and 209 (%) were parsimony informative. The analysis recovered 555 equally optimal trees of 1177 steps (CI = 0.62, RI = 0.59; Fig.
Zieria was supported as monophyletic in the strict consensus trees (BS 100).
Zieria consists mainly of grades except for several minor clades with bootstrap support greater than 75%. Clades that contain bootstrap support greater than 75% starting from the base of the clade include: 1) a clade containing Z. furfuracea and Z. laxiflora (BS 76%); 2) a clade containing Z. fraseri and Z. laevigata (BS 100%); 3) a clade containing Z. prostrata and Z. smithii (BS 95%); 4) a clade containing a polytomy of (Z. buxijugum J.D. Briggs & J.A. Armstr., Z. formosa J.D. Briggs & J.A. Armstr.), Z. granulata C. Moore ex Benth., Z. littoralis J.A. Armstr., Z. parrisiae J.D. Briggs & J.A. Armstr., Z. tuberculata J.A. Armstr., and Z. verrucosa (BS 93%); and 5) a clade containing Z. collina and Z. adenodonta (BS 92%).
In the Bayesian analysis (Fig.
This study examined 15 of the 21 endangered or vulnerable species found in Zieria for similarity in their distribution patterns and for the number of bp changes within all three genes inside clades that had strong posterior probabilities.
The first clade containing Z. adenodonta and Z. collina (BPP 100 and BS 92%) have similar distribution patterns, however two of the three genes indicated had numerous bp changes (over 10 bps), indicating the taxa are distinct species.
The second clade contains eight species, one species being Z. buxijugum (BPP 100 and BS 93%), and although the species all occurred mostly in the southeastern territory (New South Wales, Victoria and Tasmania), they had numerous bp changes between taxa.
Within the clade consisting of Z. aspalathoides, and Z. ingramii (BPP 100), there is distributional overlap, however there are over 30 bp changes among the taxa.
Although Z. adenophora has a non-overlapping distribution pattern from Z. furfuracea, and Z. laxiflora, the latter two taxa are very similar in distribution pattern. All three taxa have numerous bp differences, however Z. furfuracea and Z. laxiflora only had 2 solid bp differences.
The third clade consisted of Z. prostrata and Z. smithii (BPP 100 and BS 76%) these taxa have non-overlapping distribution patterns and two of the three genes had numerous bp changes (over 10 bps).
Z. covenyi and Z. murphyi (BPP 83), are from the same area and only had 3 bp changes among all three genes.
We assembled a trnL-F dataset including 44 taxa of Rutaceae to determine the outgroup relationship of Zieria (Fig.
Sister to this grouping is a clade containing the following taxa: Medicosma, Euodia, Boronia, Sarcomelicope and Melicope (see results for BS values and clade arrangements). We therefore used Neobrynesia as the outgroup for this study.
Both independent and combined analyses of the molecular and morphological data supported the monophyly of Zieria (Figs
On the basis of
The MP trees (strict-consensus trees from the independent, the combined molecular, and the non-molecular datasets) are poorly resolved and thus do not allow conclusive evaluation of the classification of
Characters that support the six major taxon groups defined by
Group A contains 14 species and is characterized by having distinctly tuberculate younger branches, peduncles, petioles, midveins, and fruits.
Group B contains five species. The characteristics include younger branches slightly ridged or terete, primary inflorescence bracts boat-shaped and deciduous leaving a scar, and the abaxial surface of the calyx lobes with stellate hairs.
Group C consists of four species defined by having younger branches distinctly ridged with prominent glabrous leaf decurrencies, lower lamina surface velvet like, midveins glabrous with pellucid glands, inflorescences equal to or longer than the leaves, apex of calyx lobes curved inward adaxially, anthers prominently sharply pointed, and fruits with pellucid glands.
Group D comprises four species with the following characteristics: younger branches distinctly ridged with prominent glabrous leaf decurrencies; lower lamina surface glabrous and with pellucid glands that turn black on drying and become sunken; petiole either with pellucid glands or tuberculate; midvein glabrous with pellucid glands; and fruit with pellucid glands.
Group E is composed of eight species with younger branches densely pubescent, upper lamina surface with simple hairs, lamina lower surface and midvein hirsute, filaments warty towards the apex, anthers prominently sharply pointed, ovary pubescent, cocci sharply pointed, and fruits glabrous or pubescent.
Group F, the final group, consists of seven species. The characteristics include upper lamina surfaces that are velvet like, inflorescences equal to or longer than the leaves, primary bracts that are boat-shaped and fruits that are pubescent.
In examining the Bayesian clade the following three mixed clades indicate that none of
On the basis of the combined Bayesian analysis based on three genes (two-cholorplast and one-nuclear) and a morphological matrix (48 features), eight major taxon groups are distinguishable within Zieria. All of these informal groups, except for Groups 1 and 8, correspond to the clades with posterior probability values of 100 (Fig.
The examination of the 48 morphological characters within the Bayesian tree revealed no unambiguous synapomorphies. However, sets of morphological synapomorphies in combination provide unique groups of characters to define a clade.
Z. cytisoidesGroup 1: four species — Z. adenodonta, Z. baeuerlenii J.A. Armstr., Z. collina, and Z. cytisoides Sm. This group contained the following synapomorphies: young branches densely pubescent and abaxial lamina surface not tuberculate.
Z. granulataGroup 2: eight species — Z. buxijugum, Z. caducibracteata, Z. formosa, Z. granulata, Z. littoralis, Z. parrisiae, Z. tuberculata, and Z. verrucosa. Morphological characters that were found to be synapomorphic for this clade include: abaxial lamina surface and midvein tuberculate.
Z. laevigataGroup 3: two species — Z. fraseri and Z. laevigata. These taxa had a number of morphological synapomorphies including: young branches, petioles and midveins not tuberculate, lamina suface and filaments pubescent, and calyx lobes glaucous and apex inflexed adaxially.
Z. smithiiGroup 4: two species — Z. prostrata and Z. smithii. Morpholoigcal characters that were found to be synapomorphic for this clade include: lamina surface and peduncles glabrous, lamina surface without black pellucid glands, midveins with pellucid oil glands, and inflorescences containing 10–50 flowers.
Z. aspalathoidesGroup 5: two species — Z. aspalathoides and Z. ingramii. Several morphogical characters are shared by these taxa such as: young branches distinctly ridged and densely pubescent, lamina surface with simple hairs, lamina margins revolute, filaments prominently dilated at base and anthers slightly apiculate.
Z. furfuraceaGroup 6: three species — Z. adenophora, Z. furfuracea, and Z. laxiflora. Only one morphological synapomorphy was found for this grouping: filaments not prominently dilated at base.
Z. montanaGroup 7: two species — Z. montana and Z. southwelli. One synapomorphy was found for these taxa: pubescence consisting of stellate trichomes.
Z. robustaGroup 8: four species — Z. covenyi, Z. murphyi, Z. odorifera and Z. robusta Maiden & Betche. This group had several synapomorphies including the lamina surface containing pellucid oil glands, and the few flowered inflorescences being equal to or longer than the leaves.
Because of the lack of resolution, five taxa, Z. citriodora, Z. arborescens, Z. minutiflora, Z. obcordata and Z. pilosa, will remain unplaced until additional studies are completed. DNA for the following species were not examined and therefore these taxa will not be placed into groups until sequencing and analysis is completed: Z. chevalieri, Z. floydii, Z. hindii, Z. involucrata, Z. lasiocaulis, Z. obovata, Z. oreocena, Z. rimulosa, Z. robertsiorum, and Z. veronicea. Although six of the eight groups have strong posterior probabilities the relationships between these clades remain uncertain. The monophyly of the genus and of six of these groups appears unamibiguous; however, additional molecular and morphological studies are needed to further define the groupings and internal relationships.
Many Zieria taxa are considered endangered or vulnerable (
This study examined 15 of the 21 endangered or vulnerable taxa found in Zieria for similarity in their distribution patterns and for the number of bp changes within all three genes inside clades that had strong posterior probabilities.
Z. covenyi and Z. murphyi (BPP 83), are from the same area and only had 3 bp changes among all three genes. Both taxa have several solid morphological differences such as leaves pubescent or glabrous, inflorescence numerous or few and filaments dilated or not dilated respectively. Because of these solid morphological differences these species appear distinct.
Z. furfuracea, and Z. laxiflora, (BPP 100) were very similar in pattern and had only 2 bp differences. Once again an examination of the non-molecular features revealed a number of differences such as the leaves having stellate-pubescence vs. being glabrous; flowers ranging from 21–125 vs. commonly 9; petals valvate vs. imbricate; and flowering from spring to early summer vs. late winter to spring, to name a few.
Taxa in clades with strong posterior probabilities, with similar distribution patterns and low genetic variation, need to be closely examined before conservation management decisions are made to assure that they are unique species.
Zieria as currently circumscribed (
Based on the number of informative characters and the number of branches with supported, ITS is an excellent candidate for higher-level analysis. In addition, ITS produced very few alignment difficulties within the ingroup and outgroup, and its tree topology remained consistent with that of the other genes.
Of the 32 taxa used in this study, 21 are considered endangered or vulnerable according to the EPBC. Several taxa grouped together and formed clades with strong posterior probabilities. Further examination revealed that two of these groups had similar distribution patterns and low genetic variation but solid differences in non-molecular characters. The taxonomic relationships of these taxa should be closely examined as further conservation management decisions are made.
The phylogenetic analysis presented here provides the first study within Zieria using both chloroplast and nuclear datasets, as well as a morphological dataset. Topics to be addressed in a future study include the determination of tribal and subtribal groupings and the use of additional taxa and genes to elucidate the biogeographic history of the genus.
We would like to thank anonymous reviewers for their helpful comments.
Zieria species sequenced for the present study, with Neobyrnesia as outgroup. Collection data for accession vouchers and GenBank accession numbers are given below (see Materials and Methods). The country of origin for all specimens is Australia and specimens were collected from the associated botanical garden
Species | Herbarium voucher | GenBank Accession Numbers | ||
---|---|---|---|---|
rpl32-trnL | trnL-trnF | ITS | ||
Neobyrnesia suberosa J.A. Armstr. |
R. Mueller s.n. Dec. 2 1982 (CBG-8316286) |
EU281888 | EU281921 | EU281855 |
Zieria adenodonta (F. Muell.) J.A. Armstr. |
F. A. Zich 453 (CANB 653334) |
EU281889 | EU281922 | EU281856 |
Zieria adenophora Blankly |
J. A. Armstrong et al. 5097a (CBG-8805884) |
EU281890 | EU281923 | EU281857 |
Zieria arborescens Sims. |
I. R. Telford 3134*(CBG-54528) S. R. Donaldson & S. Golson 3594 **(CANB-748530) |
EU281891 | EU281924 | EU281858 |
Zieria aspalathoides A. Cunn. ex Benth |
D. L. Jones & C.H. Broers 7814 (CBG-9109508 |
EU281892 | EU281925 | EU281859 |
Zieria baeuerlenii J.A. Armstr. |
S. Donaldson 111A CBG-9104885 |
EU281893 | EU281926 | EU281860 |
Zieria buxijugum J.D. Briggs & J.A. Armstr. |
M. Parris et al. 9018a CBG-8602343 |
EU281894 | EU281927 | EU281861 |
Zieria caducibracteata J.A. Armstr. |
J. A. Armstrong & R. Coveny 744 CBG-8208729 |
EU281895 | EU281928 | EU281862 |
Zieria citriodora J.A. Armstr. |
I.R. Telford & S. Corbett 7346 CBG- 8001161 |
EU281896 | EU281929 | EU281863 |
Zieria collina C.T. White |
M. Parris 8847 (CBG- 8413675 |
EU281897 | EU281930 | EU281864 |
Zieria covenyi J.A. Armstr. |
P. Beesley et al. 285 (CBG-8411672) |
EU281898 | EU281931 | EU281865 |
Zieria cytisoides Sm. |
F. A. Zich 405 CANB-643984 (CANB-629784) |
EU281899 | EU281932 | EU281866 |
Zieria formosa J.D. Briggs & J.A. Armstr. |
M. Parris & N. Fisher 9151a CBG-8604998 |
EU281900 | EU281933 | EU281867 |
Zieria fraseri Hook. |
I.R. Telford & S. Donaldson 12120 (CANB-9613250) |
EU281901 | EU281934 | EU281868 |
Zieria furfuracea R.Br. ex Benth. |
A. M. Lyne et al. 2143 (CBG-9705354) |
EU281902 | EU281935 | EU281869 |
Zieria granulata C. Moore ex Benth. |
K. Mills 2A CBG-8501509 (CBG-9505133) |
EU281903 | EU281936 | EU281870 |
Zieria ingramii J.A. Armstr. |
K. M. Groeneveld 89 A CBG-8800001 |
EU281904 | EU281937 | EU281871 |
Zieria laevigata Bonpl. |
F. A. Zich 448 CANB 653329 |
EU281905 | EU281938 | EU281872 |
Zieria laxiflora Domin |
S. Fethers et al. 11 (CANB-617460) |
EU281906 | EU281939 | EU281873 |
Zieria littoralis J.A. Armstr. |
M. Parris & N. Fisher 9240 CBG-8703977 |
EU281907 | EU281940 | EU281874 |
Zieria minutiflora (F. Muell.) Domin |
P. Beesley & P. Ollerenshaw 959 CBG-8604299 |
EU281908 | EU281941 | EU281875 |
Zieria montana J.A. Armstr |
F. A. Zich 462 CANB 653343 |
EU281909 | EU281942 | EU281876 |
Zieria murphyi Blakely |
A. M. Lyne et al. 325 CBG-9101073 |
EU281910 | EU281943 | EU281877 |
Zieria obcordata A. Cunn. |
J. D. Briggs 2376 CANB-389372 |
EU281911 | EU281944 | EU281878 |
Zieria odorifera subsp. williamsii Duretto & P.I. Forst. |
I. Southwell H85-039 CBG-8505944 |
EU281912 | EU281945 | EU281879 |
Zieria parrisiae J.D. Briggs & J.A. Armstr. |
M. Parris 9145B CBG-8604990 |
EU281913 | EU281946 | EU281880 |
Zieria pilosa Rudge |
D. L. Jones & C. Broers 6063 CBG-9010362) |
EU281914 | EU281947 | EU281881 |
Zieria prostrata J.A. Armstr. |
S. Myers ANGB 2134a (CBG-8802463) |
EU281915 | EU281948 | EU281882 |
Zieria robusta Maiden & Betche |
M. D. Crisp 4397 CBG-7809037 |
EU281916 | EU281949 | EU281883 |
Zieria smithii Andrews |
S. Pedersen 16 CBG-9705152 |
EU281917 | EU281950 | EU281884 |
Zieria southwelli J.A. Armstr. |
I. R. Telford 3298 CBG- 54531 |
EU281918 | EU281951 | EU281885 |
Zieria tuberculata J.A. Armstr. | J. D. Briggs 2344 CANB 387032 |
EU281919 | EU281952 | EU281886 |
Zieria verrucosa J.A. Armstr. |
P. Beesley & P. Ollerenshaw 970A CBG-8604310 |
EU281920 | EU281953 | EU281887 |