Lasiocroton trelawniensis (Euphorbiaceae), a critically endangered species from the Cockpit Country of Jamaica, belongs to Bernardia (Euphorbiaceae).
Conservation without clear knowledge of the taxonomy and phylogenetic status of the target taxa can be deceptive. Phylogenetic reconstructions constitute a necessary aspect of the framework required for assigning conservation priorities (Rodrigues et al., 2005), and phylogenetic trees are fundamental for understanding the taxonomy of endangered species (Sinclair et al., 2005). A species misplaced in a particular genus can have a definite impact on the establishment of conservation and management strategies (Rodrigues et al., 2005). A case in point takes place in the Cockpit Country of Jamaica. This region consists primarily of mesic forest over steep limestone hills and is well known as a major "hot spot" for endemic plant species in the West Indies (Iremonger, 1997). While the Cockpit Country only accounts for 4% the landmass of Jamaica, approximately 60% of the island-endemic vascular plants occur in the region (Iremonger, 1997). Lasiocroton Griseb., a genus of euphorbiaceous trees, is diverse on Jamaica, with four of the six species endemic to the island (Adams, 1972). All species found on Jamaica are listed by the IUCN (2007) from the Endangered (E) to the Lower Risk (LR) categories. Lasiocroton trelawniensis C.D. Adams, the species of discussion for this paper, is endemic to a single hilltop, "Island View Hill", in the Cockpit Country (Adams, 1970), and we consider it to be in the Critically Endangered category (CR, based on criteria B1 + D, i.e. present flora only one locality with a population size estimated to number fewer than 50 mature individuals) of the red list guidelines of the World Conservation Union (IUCN, 2001). Lasiocroton trelawniensis was incorrectly assigned to the Endangered category by the IUCN (2007).
Webster (1994) placed Lasiocroton in the tribe Adelieae s.1. (subfamily Acalyphoideae) based on morphology. Recently, Wurdack et al. (2005) and DeNova et al. (2006) published molecular phylogenies of the Euphorbiaceae. The study by Wurdack et al. (2005) was based on the chloroplast regions rbcL and trnL-F and proposed a new circumscription for the Acalyphoideae s.s. This taxon has two major lineages, named as the "core acalyphoids" and the "alchorneoids". The core acalyphoids comprise eight distinct clades, which were labeled from Al to A8. Lasiocroton belongs to A6, and this clade is sister to a monophyletic assemblage composed of Clades A7 and A8. Clade A5 is sister to the group formed by Clades A6, A7, and A8. The genus Bernardia belongs to Clade A7 (Fig. 3).
These previous molecular studies also changed the tribal placements of some genera within the Acalyphoideae. The tribe Adelieae no longer contains the genera Enriquebeltrania Rzed. and Crotonogynopsis Pax, results also supported by recent palynological data (Nowicke et al., 1999). The removal of these two genera restricts the Adelieae to the New World. Philyra Klotzsch, a monotypic South American genus treated by Webster (1994) in the tribe Chrozophoreae subtribe Ditaxinae, was found to be closely allied to the Adelieae. Therefore we consider the Adelieae s.s. to include four genera: Adelia L., Lasiocroton, Leucocroton Griseb., and Philyra. These genera form a monophyletic group, which represent hall of the genera of Clade A6 from Wurdack et al., (2005). In addition, we also propose that Adenophaedra (Mull. Arg.) Mull. Arg., Bernardia Houst. ex Mill., and Caryodendron H. Karst. comprise the tribe Bernardieae s.s. (Clade A7 from Wurdack et al., 2005). These two tribes, as recognized in our study, are strongly supported by bootstrap values higher than 95% (Wurdack et al., 2005). However, certain representatives of the two tribes are morphologically similar, exemplified by the lectotype of Bernardia which was initially described as Adelia bernardia L. For a recent example, Adelia cinera (Wiggins and Rollins) A. Cerv., V. W. Steinm. and Flores Olvera was moved from Bernardia (Cervantes et al., 2003).
As part of an ongoing project on the systematics of the West Indian genera Lasiocroton and Leucocroton, we investigate the taxonomic placement of Lasiocroton trelawniensis based on morphological, palynological, and DNA evidence. Our study shows that this Jamaican endemic does not belong to the Adelieae, but to the Bernardieae where we have placed it in Bernardia, a neotropical genus with approximately 70 species (Radcliffe-Smith, 2001) and seven sections (Muller Argoviensis, 1866; Pax and Hoffman, 1912). Pax and Hoffman (1912) provided the most recent published taxonomic treatment for this genus. Hereafter, we will refer to this species as B. trelawniensis (see taxonomic treatment below).
The lectotype of this genus is Bernardia carpinifolia Griseb. (= B. dichotoma (Willd.) Mull. Arg.) (Webster, 1994), and it was published by Grisebach in the 19th century (Grisebach, 1859). Later Muller Argoviensis (1866) published B. dichotoma, based on the earlier name Croton dichotomus Willd. (Willdenow, 1805). Bernardia dichotoma is the name currently used in the West Indian Floras and B. carpinifolia is considered a synonym (e.g., Adams, 1972; Correll & Correll, 1982; Howard, 1989; Liogier, 1953, 1986; Liogier & Martorell, 2000). The type species is endemic to the Caribbean Islands, and it belongs to the section Tyria (Klotzsch) Mull. Arg., a taxon with 26 species as described by Cervantes (2006). Because this section includes the type of the Bernardia, according to the rules of botanical nomenclature, we will refer to this taxon as section Bernardia. Pax and Hoffman (1912) morphologically differentiated this group as shrubs having an indumentum with stellate or fasciculate trichomes, glandulous receptacles, and lacinulate-lacerate styles.
Materials and Methods
Pollen Study. Pollen from Bernardia trelawniensis and Lasiocroton macrophyllus (Sw.) Griseb. was removed from herbarium specimens collected in the wild in Jamaica (B. trelawniensis: Jestrow 1004 (FTG); L. macrophyllus: Jestrow 1003 (FTG)) and studied with Scanning Electron Microscopy (SEM) in the Florida Center for Analytical Electron Microscopy (FCAEM) of Florida International University (FIU) using the instrument JEOL JSM 5900LV. Untreated pollen was coated with gold-palladium using a SPI-Module Sputter Coater at 367 [Angstrom] for 4 min. Although pollen for other species of Bernardia were not examined in our study, we made comparisons with SEM images previously published by Nowicke et al. (1999) and Takahasi et al. (2000).
DNA Study. Our study is based on phylogenetic analyses of nucleotide sequences of the chloroplast regions rbcL and trnL-F, and uses both data available in GenBank and published by Wurdack et al. (2005), as well as new nucleotide sequences generated for this study. The ingroup included all the sequences available from GenBank for those taxa placed in Clades A6, A7, and A8 of the "core acalyphoid" group as defined by Wurdack et al. (2005) (24 species in 20 genera for trnL-F, and 19 species in 18 genera for rbcL). The sequence of Bernardia available for the trnL-F in GenBank is for B. scabra Mull. Arg., but it only had the half of the 3' end. The Bernardia GenBank (GB) sequence for rbcL is for B. myricifolia (Scheele) Watson. The ingroup had the following sequences obtained by us. For rbcL: Bernardia dichotoma (GB: EF470580; Jestrow 1001 (FYG)) and B. trelawniensis (GB: EF470579; Jestrow 1004 (FTG)). For trnL-F: Bernardia dichotoma (GB: EF470582 and EF470584; Jestrow 1001 (FTG)), B. myricifolia (GB: EF470581 and EF470583; Barron S. Rector 335 (FTG)), and B. trelawniensis (GB: EF107750 and EF107751; Jestrow 1004 (FTG)).
We were unable to sample broadly within Bernardia. However we included Bernardia dichotoma. The lectotype of the genus (B. carpinifolia) is a synonym of B. dichotoma. Our Bernardia sampling further included B. myricifolia, a species also belonging to section Bernardia with B. dichotoma. Bernardia scabra belongs to section Polyboea (Klotzsch) Mull. Arg. and was included in our analyses in order to have in our ingroup as many species as possible for this genus. The outgroup included two species (Seidelia triandra (E. Mey.) Pax and Leidesia procumbens (L.) Prain), belonging to Clade A5 (as defined by Wurdack et al. (2005)); based on previous phylogenetic studies this group is sister to all the genera of the ingroup (Wurdack et al., 2005). The nucleotide sequences of the outgroup were also retrieved from Wurdack et al. (2005) via GenBank.
DNA of plant samples were extracted from silica-dried material using a Qiagen DNeasy Plant Mini kit. PuReTaq Ready-To-Go PCR beads were used for the PCR amplification reaction mix. For both regions the cycle program is as follows: 80[degrees]C: 5 min, (94[degrees]C: 1 min, 50[degrees]C: 1 min, 72[degrees]C: 2 min) x35, 72[degrees]C: 5 min. The trnL-F amplification was obtained from four primers in two separate fragments due to difficulties in amplifying the region as a whole. The first fragment was amplified using primers "c" and "d" from Taberlet et al. (1991). Primers "e" and "f" were used to amplify the second fragment (Taberlet et al., 1991). The rbcL amplification was obtained using forward primer, rbcL RH1, and reverse primer, rbcL 3'ZC (Zurawski and Clegg, 1987). Cycle sequencing was performed in both directions with the ABI PRISM[TM] BigDye[TM] v.3.1 Terminator Cycle Sequencing Kit (Perkin Elmer) following the manufacturers instructions. The primers used for PCR amplification were also utilized for the cycle sequencing reactions. Nucleotide sequences were visualized on a PE Applied Biosystems 377 automated sequencer at the Florida International University (FIU) DNA Core Facility.
All sequences were assembled and visually aligned, using Sequencher 3.1.1 (Gene Codes, Michigan). Both regions, rbcL and trnL-F, were found to be alignable and no regions were omitted in the analysis. Maximum Parsimony analysis was performed using PAUP* 4.0b10 (Swofford, 2003) using the heuristic algorithm with equal weights and unordered characters, tree-bisection-reconnection (TBR) swapping, and MulTrees "on". Gaps were coded as uninformative. Phylogenetic support for each clade was evaluated through bootstrap analysis (Felsenstein, 1985) using 100 replicates in PAUP* with the same settings, except MulTrees was set to "off" in order to shorten calculation time for both the trnL-F and combined bootstrap analyses. Consistency index (CI; excluding uninformative characters) and retention index (RI) were also calculated (Kluge & Farris 1969; Farris 1989).
We conducted three different phylogenetic analyses, the first based on the rbcL data matrix (23 taxa), the second one on the trnL-F data set (29 taxa), and the third one on a combined matrix that included data from trnL-F and rbcL. The combined analyses only included those species for which data were available for both markers (22 taxa), with the only exception being for the genus Dysopsis Baill. As the genus Dysopsis included different species for the rbcL and the trnL-F analyses, the sequences from the two different species were combined as Dysopsis sp. for the combined analysis. This approach was also followed by Wurdack et al. (2005). We feel this is justified given the very close associations of the two taxa, both were historically considered varieties of the same species, and presently some authorities consider Dysopsis to be a monotypic genus (Radcliffe-Smith 2001). Also for the combined analysis, both the rbcL and trnL-F regions for each taxa were included with equal weighting according to individual base characters.
Results and Discussion
Pollen Data. Bernardia trelawniensis has a punctate tectum with a psilate surface and lacks an operculum (Fig. 1). These are characteristics of Bernardia pollen that do not occur in Lasiocroton (Nowicke et al., 1999; Takahasi et al., 2000). In contrast, the pollen of Lasiocroton is strikingly different with both a fusiform operculum and a crotonoid tectum (Fig. 1, Table 1). Additional distinctive micromorphological features previously recorded by Nowicke et al. (1999) and Takahasi (2000) (i.e., margo and costa ectocolpi) are also indicated in Table 1. The presence or absence of margo and costa ectocolpi of B. trelawniensis were not observed. Nowicke et al. (1999) included nine species of Bernardia and Takahasi et al. (2000) included three species of Lasiocroton, allowing for robust confidences in their conclusions about pollen structure. The palynological data clearly supports the placement of our target species in Bernardia and not in Lasiocroton.
[FIGURE 1 OMITTED]
Molecular Phylogenetic Data
rbcL. The final aligned matrix for the rbcL parsimony analysis was 1,446 nucleotide characters in length. There were 137 variable characters, with 54% (74) of these parsimony-informative. This phylogenetic analysis yielded 64 most-parsimonious trees of 230 steps each (CI=0.5409; RI=0.7137). The strict consensus of the 64 most parsimonious trees is shown in Fig. 2. Bernardia trelawniensis forms a polytomy with the other two species of Bernardia included in the analyses, with 100% bootstrap support.
trnL-F. The final aligned matrix for the trnL-F parsimony analysis had 1,419 nucleotide characters. There were 319 variable characters, with 42% (135) of these being parsimony-informative. The parsimony analysis yielded 18 most-parsimonious trees of 433 steps each (CI=0.7031; RI=0.8455). The strict consensus of all 18 most parsimonious trees is shown in Fig. 2. The strict consensus shows Bernardia trelawniensis as sister to B. dichotoma with bootstrap support of 83%, and this clade is sister to B. myricifolia (bootstrap support of 90%).
The trnL-F study also has some additional phylogenetic implications for the family. Wurdack et al. (2005) showed that the tribe Bernardieae s.s. (Clade A7) to form a strongly supported monophyletic group after the phylogenetic analyses of the rbcL data alone and of the combined rbcL and trnL-F data set. However, the trnL-F phylogeny obtained by Wurdack et al. (2005) weakly supported the recognition of the tribe Bernardieae s.s. (Clade A7 after Wurdack et al. (2005)) with a bootstrap value of 59%. However, our phylogeny with the inclusion of three complete Bernardia sequences increased the support for this clade (to 96%). Therefore our molecular analysis provides additional strong support for the recognition of this tribe.
[FIGURE 2 OMITTED]
Combined. The parsimony analysis yielded a tree of 582 steps (CI=0.6347; RI= 0.7794). This tree is shown in Fig. 3. The three Bernardia species in the analysis form a monophyletic clade with a bootstrap of 100%. The combined analysis nests Bernardia trelawniensis into Bernardia sect. Bernardia with a bootstrap of 73%. The molecular data support the palynological results of placing Bernardia trelawniensis within Bernardia and also provide additional support for the phylogenetic conclusions of Wurdack et al. (2005).
Morphological evidence. During our initial field studies in Jamaica (May 2005), we noticed morphological features that were in conflict with the placement of this taxon in the Antillean genus Lasiocroton (Radcliffe-Smith, 2001; Webster, 1994). Bernardia trelawniensis has leaves with denticulate margins, whereas, all other species in Lasiocroton have leaves with entire to sinuate margins (Radcliffe-Smith, 2001; Webster, 1994). In addition, a single pistillate flower was found on a primarily staminate plant of B. trelawniensis, and it is known that monoecy occurs in Bernardia but not in Lasiocroton (Radcliffe-Smith, 2001; Webster, 1994).
[FIGURE 3 OMITTED]
Our initial morphological observations for Bernardia were supplemented by those provided by Radcliffe-Smith (2001) and Cervantes et al. (2003). We also found additional morphological characters that show that this taxon belongs to Bernardia (Table 1). All species of Bernardia have glands near the base of the leaf whereas no species in the Adelieae s.s. have glands on their leaves. Bernardia trelawniensis has glands numbering from one to three, though these glands are not obvious, particularly on immature leaves. Furthermore, the glands exhibited by B. trelawniensis, are abaxial on the lamina and quite flat which is typical for Bernardia sect. Bernardia. This situation is quite different from B. corensis (Jacq.) Mull. Arg. of sect. Polyboea which has a pair of tuberculate glands at the joining of the lamina and petiole. In addition, Bernardia species have stipules, while Lasiocroton species are exstipulate. Bernardia trelawniensis has small, 1-2 mm long subulate stipules, similar to other members of Bernardia sect. Bernardia.
Trichomes also provide important diagnostic characters. Bernardia trelawniensis has strikingly stellate trichomes, densely arranged with long, erect and narrow radii of a glass-like appearance. Lasiocroton, which literally translates to "wooly croton", has stellate trichomes with thick and rugose radii that are typically brown in color. No species of Lasiocroton has trichomes similar to those of B. trelawniensis. While not all species of Bernardia have such trichomes, stellate trichomes are typical of Bernardia sect. Bernardia. Plants of B. trelawniensis have staminate flowers born on a short (5-10 mm) spicate inflorescence. In contrast, the staminate inflorescence of Lasiocroton is racemose to subpaniculate with a rachis ranging from 5 to 25 cm. Three additional floral structures (i.e., anthers, male disk glands, and pistillodes) also have consistent differences between the two genera. The main morphological features that distinguish Lasiocroton from Bernardia are listed in Table 1. These two genera are readily distinguishable, even from sterile specimens, on the basis of several morphological features.
One reason we believe Bernardia trelawniensis was assigned to Lasiocroton is because the original description only included pistillate specimens (Adams 1970). Male specimens provide the most obvious characters to distinguish the two genera. In addition, B. trelawniensis has some general features found in species of Lasiocroton. Traits shared by these two taxa include a pronounced abaxial leaf venation, a yellowish indumentum on recent growth, flowers with a single whorl of perianth, pistillate inflorescences of similar length and structure, a woody habit, and technically "stellate trichomes".
Our morphological observations suggest that Bernardia trelawniensis is closely related to the type of the genus. We are aware that our phylogenetic analyses had limited sampling within Bernardia, and that future studies might prove this genus not to be monophyletic. Two sections of Bernardia, Passaea (Baill.) Mull. Arg. and Traganthus (Klotzsch) Mull. Arg. were not included in our study, both have been suggested to possibly warrant generic status due to their unique morphologies (Webster, 1994; Radcliffe-Smith, 2001). As the morphology of the genus is not clearly understood, we cannot rule out the possibility of the paraphyly of Bernardia. However, even if future studies find Bernardia to be paraphyletic, B. trelawniensis will still remain part of Bernardia s.s. because of the species morphological similarities to the type of this genus.
Bernardia dichotoma is widely distributed on the Caribbean Islands (Correll & Correll, 1982; Liogier, 1953, 1986). After a preliminary study of specimens of B. dichotoma from Jamaica, the consistent traits that differentiate these two species are trichome density and color. The trichomes of B. dichotoma growing on Jamaica are dense and give a tomentose appearance with a whitish hue. In contrast, B. trelawniensis has significantly fewer trichomes of a yellowish hue. Cervantes (2006) included only one variety of B. dichotoma in her thesis and suggested that the species boundaries of B. dichotoma are not well established. However, on Jamaica, B. trelawniensis is readily identifiable from B. dichotoma based on our own observations in the field and of herbarium specimens.
We believe that Bernardia dichotoma represents a taxonomic complex with a poorly understood morphology, and we cannot rule out that B. trelawniensis could be a part of this complex. As Pax and Hoffman (1912) distinguished three varieties of B. dichotoma, clearly further research is needed to interpret morphological variation within B. dichotoma and its implications for the relationship between B. trelawniensis and B. dichotoma. This research is beyond the scope of this study, and we presently maintain the species status of B. trelawniensis until additional data are available.
Bernardia trelawniensis is Critically Endangered due to its precarious locality, thus placing the species at the forefront of conservation importance. A recent botanical expedition (2006) to the Cockpit Country, headed by Fairchild Tropical Botanic Garden, found the species growing on all elevations of Island View Hill but identified less than 50 individuals (Lauren Raz, pers. comm.). These additional field observations further support that B. trelawniensis is Critically Endangered.
The phylogenetic component of this paper has no impact on the assignment of Critically Endangered according to the guidelines of the IUCN. However, the phylogeny would have an impact on management strategies, if based on phylogenetic diversity. The conservation priority of a species closely related to a widespread species has a lower quantitative value of phylogenetic diversity when compared to a species with a highly differentiated morphology belonging to a restricted endemic genus (Rodrigues et al., 2005). This means, that while Bernardia trelawniensis was thought to have an unusual evolutionary history in Lasiocroton--with denticulate margins, glands, and stipules as autapomorphies--now the total amount of evolutionary change has been reduced by it placement in the morphologically similar Bernardia. Bernardia trelawniensis is Critically Endangered, but no longer has the prestige of being the only denticulate, glandular, and stipulate member of its genus.
Bernardia trelawniensis (C.D. Adams) Jestrow and G. R. Proctor, comb. nov. Lasiocroton trelawniensis C.D. Adams, Phytologia 20(5): 312. 1970. TYPE: JAMAICA, Trelawny Parish, 1.5 miles north of Warsop, Wilson Valley District, Island View Hill, collected on wooded limestone hilltop, 2000-2200 feet, 26 Mar 1960, G.R. Proctor 20746 (holotype IJ).
Additional specimen examined. Jamaica. Trelawny Parish: 1.5 miles north of Warsop, Wilson Valley District, Cockpit Country, Island View Hill, limestone hilltop, 670 m, 18[degrees]17'13.8" N, 77[degrees]34'33.3" W, Jestrow 1004 (FTG).
Shrubs 1-4 m tall, dioecious with occasional deviations to monoecy, indumentum with stellate trichomes, latex absent. Leaves alternate, simple, elliptic to lanceolate, shortly rounded at base, glands numbering from 1-3 placed abaxially near base of lamina, lamina 3-10 cm long and 1-4 cm wide, denticulate margins, penninerved, prominent abaxial reticulate-pinnate venation, developing leaves yellowish abaxially, petiole 0.5-1 cm long. Subulate stipules 1-2 mm long. Staminate inflorescence spicate, axillary, 4-6 mm long. Staminate flowers with single whorl of poorly defined perianth, 5-merous perianth ~1 mm long. Pistillate inflorescence as terminal racemes, erect in fruit, 3-6 cm in length, 5-11 flowers, flowers sessile. Pistillate flowers with a persistent single whorl of 5-merous perianth ~2 mm long. Fruits 3-sectioned schizocarps, oblong-globose, 6-8 mm long, olive-green, tawny-tomentose.
Acknowledgments We dedicate this paper to the memory of Professor Grady Webster (1927-2005), the Euphorbiaceae authority who, during his graduate studies, worked alongside George Proctor in Jamaica over fifty years ago. We would like to thank the EPA GRO-STAR Fellowship (Number MA-91630201-3 to BJ) for financial support. Andreas Oberli and Devon Paddyfoot provided invaluable help during the field studies of BJ and GP in Jamaica. We would also like to thank Angelica Cervantes for sending us her doctoral thesis on the taxonomy of Bernardia. Our thanks go out to Barbara Maloney from FCAEM of FIU for technical support for this study. This study is part of the Ph.D. Dissertation of BJ, our gratitude also goes for his graduate study committee; Maureen Donnelly, Kelsey Downum, Grenville Draper, Carl Lewis, and Jennifer Richards who critically read an early draft of this paper. We also appreciate the three anonymous reviewers who provided useful comments. This is contribution number 141 from the Tropical Biology Program of FIU.
Published online: 16 April 2008
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Brett Jestrow (1,2,4) * George Proctor (3) * Javier Francisco-Ortega (1,2)
(1) Department of Biological Sciences, Florida International University, University Park, Miami, FL 33199, USA
(2) Center for Tropical Plant Conservation, Fairchild Tropical Botanical Garden, Coral Gables, Miami, FL 33156, USA
(3) Department of Life Sciences, Botany, University of the West Indies-Mona Campus, Kingston 7, Jamaica; e-mail: email@example.com
(4) Author for Correspondence; e-mail: firstname.lastname@example.org
Table 1 Morphological and Palynological Distinctions Between Bernardia and Lasiocroton, Adapted from Cervantes et al. (2003) and Jestrow (unpublished) Parameter Bernardia Lasiocroton Leaf Glands Present Absent Margin Dentate Entire to sinuate Stipules Present Absent Trichomes Simple, fasciculate, Rugose-stellate stellate Flower Anthers Basifixed Subdorsifixed Male disk glands Interstaminal or none Annular Pistillode Absent Filiform or absent Infloresence Pistillate infloresence Racemose to spicate Racemose to subpaniculate Pistillate rachis 1 mm to 20 cm 5 cm to 25 cm length Pollen Operculum Absent Fusiform Tectum Punctate to reticulate Crotonoid Costa ectocolpi Present Absent Margo Present Absent
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|Author:||Jestrow, Brett; Proctor, George; Francisco-Ortega, Javier|
|Publication:||The Botanical Review|
|Date:||May 1, 2008|
|Previous Article:||Molecular phylogenetics and biogeography of the Caribbean-centered Croton subgenus Moacroton (Euphorbiaceae s.s.).|
|Next Article:||The impact of ecology and biogeography on legume diversity, endemism, and phylogeny in the Caribbean region: a new direction in historical...|
|J. W. F. Slik, Macaranga and Mallotus (Euphorbiaceae) as Indicators for Disturbance in the Lowland Dipterocarp Forests of East Kalimantan.|