Splitting the Pisonia birdcatcher trees: re-establishment of Ceodes and Rockia (Nyctaginaceae, Pisonieae)

Abstract Several genera of Nyctaginaceae, currently merged under Pisonia, have been described for the Indo-Pacific region. Results from a recent molecular phylogenetic study of tribe Pisonieae showed that Pisonia is non-monophyletic and comprises three well-supported lineages: one including typical Pisonia and allies (Pisonia s.str.), a clade of species which corresponds to the original description of Ceodes and a third lineage whose single representative was formerly treated under the monotypic genus Rockia. Thus, as part of an effort to achieve a natural classification for tribe Pisonieae, this work proposes to re-establish Ceodes and Rockia to accommodate taxa with inconspicuous glands on anthocarps, recognising 21 species (20 for the former and one for the latter), of which 16 are new combinations: Ceodes amplifoliacomb. nov., Ceodes artensiscomb. nov., Ceodes austro-orientaliscomb. nov., Ceodes browniicomb. nov., Ceodes caulifloracomb. nov., Ceodes coronatacomb. nov., Ceodes diandracomb. nov., Ceodes gigantocarpacomb. nov., Ceodes gracilescenscomb. nov., Ceodes lanceolatacomb. nov., Ceodes merytifoliacomb. nov., Ceodes muellerianacomb. nov., Ceodes rapaensiscomb. nov., Ceodes sechellarumcomb. nov., Ceodes taitensiscomb. nov. and Ceodes wagnerianacomb. nov. A general distribution of each species recognised in this work is also included, along with line drawings and colour pictures of representative species of Ceodes, Pisonia and Rockia and an updated dichotomous key based on reproductive characters for the nine genera (Ceodes, Cephalotomandra, Grajalesia, Guapira, Neea, Neeopsis, Pisonia, Pisoniella and Rockia) comprising the tribe Pisonieae. Résumé Plusieurs genres de Nyctaginaceae actuellement fusionnés sous Pisonia ont été décrits pour la région Indo-Pacifique. Les résultats d’une récente étude phylogénétique moléculaire de la tribu Pisonieae ont montré que Pisonia est non monophylétique et comprend trois lignées bien supportées: une comprenant Pisonia typique et ses alliés (Pisonia s.str.), un clade d’espèces qui correspond à la description originale de Ceodes et une troisième lignée dont l’unique représentant était auparavant traité sous le genre monotypique Rockia. Ainsi, dans le cadre d’un effort pour parvenir à une classification naturelle de la tribu Pisonieae, ce travail proposons de rétablir les Ceodes et Rockia pour accueillir des taxons avec des glandes discrètes sur les anthocarpes, reconnaissant 21 espèces (20 pour les premières et une pour les dernières), dont 16 sont de nouvelles combinaisons: Ceodes amplifoliacomb. nov., Ceodes artensiscomb. nov., Ceodes austro-orientaliscomb. nov., Ceodes browniicomb. nov., Ceodes caulifloracomb. nov., Ceodes coronatacomb. nov., Ceodes diandracomb. nov., Ceodes gigantocarpacomb. nov., Ceodes gracilescenscomb. nov., Ceodes lanceolatacomb. nov., Ceodes merytifoliacomb. nov., Ceodes muellerianacomb. nov., Ceodes rapaensiscomb. nov., Ceodes sechellarumcomb. nov., Ceodes taitensiscomb. nov. et Ceodes wagnerianacomb. nov. Une distribution générale de chaque espèce reconnue dans ce travail est également incluse, ainsi que des dessins au trait et des images en couleur des espèces représentatives de Ceodes, Pisonia et Rockia, et préparé une clé dichotomique mise à jour basée sur les caractères reproductifs des neuf genres (Ceodes, Cephalotomandra, Grajalesia, Guapira, Neea, Neeopsis, Pisonia, Pisoniella et Rockia) comprenant la tribu Pisonieae.


Introduction
The tribe Pisonieae Meisn. in Nyctaginaceae (Caryophyllales) contains the most diverse woody assemblage of the family, represented by over 200 species distributed mainly in the tropical and subtropical regions of the New World (Douglas and Spellenberg 2010). Although members of Pisonieae are present -and often common -in all types of Neotropical habitats and are important components for many ecosystems, taxonomic delimitations at the generic and species levels are still obscure and in urgent need of updated treatments. The tribe currently comprises seven accepted genera (Cephalotomandra H.Karst & Triana, Grajalesia Miranda, Guapira Aubl., Neea Ruiz & Pav., Neeopsis Lundell, Pisonia L. and Pisoniella (Heimerl) Standl.), all of them restricted to the New World except Pisonia, which has a pantropical distribution (Douglas and Spellenberg 2010). However, other genera have been erected in the last three centuries to include some of the Indo-Pacific taxa with dried anthocarps and inconspicuous glands along anthocarp ribs, which have been either recognised as accepted or treated as synonyms of Pisonia by different authors, resulting in a convoluted taxonomic history that we aim to clarify below and that is also summarised in Figure 1.
Ceodes J.R. Forst. & G.Forst., which was described by Forster and Forster (1776), is the oldest of the Indo-Pacific genera with its type species Ce. umbellifera J.R.Forst. & G.Forst. collected in Tanna Island at Vanuatu, characterised by the absence of stalked glands along the ribs of anthocarps (Seemann 1863). Later, Du Petit-Thouars (1804) established the genus Calpidia Thouars, whose detailed description is based on material collected in Mauritius and which, just as Ceodes, differed from Pisonia, mainly by the absence of glandular emergences on the surface of its anthocarps (Du Petit-Thouars 1806; see Figs 2, 3). The protologues of Ceodes and Calpidia describe essentially the same diagnostic characters and it is possible that Du Petit-Thouars was unaware that Ceodes had been described 28 years earlier, as he did not mention this genus in either of his two publications on Calpidia.
In a global treatment of Nyctaginaceae, prepared by Choisy (1849), he merged Calpidia under Pisonia and, as with Du Petit-Thouars, he did not include Ceodes in this treatment. Over 30 years later, Bentham and Hooker (1880) maintained both Calpidia and Ceodes as synonyms of Pisonia. However, they recognised the monotypic genus Timeroyea Montrouz. (using the orthographic variant "Timeroya") from New Caledonia, which besides Ceodes and Calpidia, represents a third genus with inconspicuous glands on its anthocarps, but was characterised by having many (25-30) stamens (Montrouzier 1860;Beauvisage 1901).
Nine years after Bentham and Hooker's publication, Heimerl (1889) presented his first tribal treatment for Nyctaginaceae, in which he split Pisonia into six sections, resulting in an expanded delimitation of this genus. Timeroyea was reduced to a section of Pisonia (as P. sect. Timeroya), while P. sect. Prismatocarpae was established to accommodate taxa with up to 15 stamens, resulting in two sections of Pisonia with inconspicuously-glanded taxa. In this treatment, Calpidia was listed as a synonym of Pisonia, while Ceodes was not mentioned at all. Subsequent work by Heimerl (1913a), based on the examination of additional material, led him to propose the split of Pisonia sensu lato with the reinstatement of Calpidia to embrace all taxa placed under P. sect. Prismatocarpae and P. sect. Timeroya. Here, Calpidia differed from other Pisonia sections by the absence of bracteoles, having a reduced perisperm that forms gelatinous traces and starch accumulation in the embryo and by its geographic distribution. In the following publication which included palynological analysis, Heimerl (1913b) proposed new combinations to Calpidia, including some of the newly described species by Warburg (1891) and Bargagli-Petrucci (1901) and described the monotypic genus Rockia Heimerl to accommodate the Hawaiian endemic P. sandwicensis Hillebr. Although the anthocarps of Rockia have inconspicuous glands located along the ribs, Heimerl (1913b) distinguished it from Calpidia by the presence of bracteoles and the number of pores in pollen grains, where Rockia has sessile flowers with one bract and two bracteoles at its base and tricolpate pollen, while Calpidia has pedicellate flowers lacking any bracts or bracteoles at the upper portion of the pedicels and pollen with four or more colpi, resulting in many apertures.
In his last comprehensive synthesis of Nyctaginaceae, Heimerl (1934) maintained Rockia as an accepted genus and additionally recognised three sections in Calpidia, based on the presence of a rostrum -a beaked or filamentous extension at the apex of the anthocarps -and the number of stamens: Ca. sect. Excelsae (= P. sect. Prismatocarpae), Ca. sect. Paucistaminatae and Ca. sect. Timeroyea. Calpidia sect. Timeroyea, represented by the New Caledonian endemic Ca. artensis (Montrouz.) Heimerl, is characterised by flowers with a high number of stamens (≥ 30), while the Indo-Pacific widespread Ca. sect. Excelsae, which includes Ca. excelsa (Blume) Heimerl and Ca. brunoniana (Endl.) Heimerl, has flowers with 6-30 stamens. On the other hand, species with less than five stamens and a rostrum were placed into Ca. sect. Paucistaminatae, most of whose representatives occur in Papua New Guinea (e.g. Ca. longirostris (Teijsm. & Binn.) Heimerl).
Unlike with his former treatment, Heimerl (1934) mentioned Ceodes, but did not evaluate its status under the argument that he lacked enough information about this genus to reach a taxonomic decision, even when Skottsberg (1926), years before, had acknowledged the priority of Ceodes over Calpidia. Skottsberg re-established Ceodes under the argument that there were extant original specimens and that the scant description of the genus was similar to other names published during the late 18 th century. However, Skottsberg's treatment was restricted to the plants from Hawai'i and included only two species in Ceodes (Ce. brunoniana (Endl.) Skottsb. and Ce. forsteriana (Endl. ex Walp.) Skottsb.) and listed a third one (Ce. excelsa (Blume) Skottsb.) as a questionable species. As Heimerl (1934) still did not accept Ceodes and retained Calpidia in his new treatment of Nyctaginaceae, Skottsberg (1936) published a work focused on the nyctaginaceous trees from Hawai'i where he reinstated his views on the priority of Ceodes, this time recognising only one species (Ce. umbellifera, including Ce. excelsa and Ce. forsteriana as synonyms). In this same work, he also described the genus Heimerlia Skottsb. to accommodate Ce. brunoniana, a species characterised by having hermaphroditic flowers. Following Skottsberg's views, Heimerl (1937) finally accepted the priority of Ceodes over Calpidia and described a new form for Ce. umbellifera (Ce. umbellifera f. amplifolia Heimerl), but did not effectuate any transfers from the sections of Calpidia he previously published. Two years later, in their first paper on a series of publications on the plants from Papua New Guinea, Merrill and Perry (1939) proposed two new combinations for species of Ceodes. Finally, Skottsberg (1941) corrected the name Heimerlia to Heimerliodendron Skottsb. after noticing that the former had been already described for a fungus.
In a new and drastically different treatment for the group, Stemmerik (1964a) proposed a broad definition for Pisonia which re-incorporated all taxa with inconspicuous glands along anthocarps. In his revision, which was restricted to the Indo-Pacific taxa, he merged Calpidia, Ceodes, Heimerliodendron and Rockia within Pisonia. The three sections of Calpidia, recognised by Heimerl in 1934, were transferred to Pisonia, where P. sect. Prismatocarpae sensu Heimerl (1889) (same as Ca. sect. Excelsae sensu Heimerl 1934) was restored. Rockia was merged into P. sect. Paucistaminatae (sensu Heimerl 1934) along with the taxa with pedicellate flowers and having an anthocarp rostrum. Therefore, the delimitation of the three sections of Pisonia, proposed by Stemmerik (1964a), was based on characters used by Heimerl (1934) to define his sectional ranks, such as type of glands on anthocarps, presence of a rostrum and number of stamens. However, he did not consider the absence of bracts and bracteoles at the upper portion of the pedicels, presence of starch in the embryo and number of apertures in pollen grains, as he argued that at least the pollen structure was not a constant character and, therefore, had no utility separating genera (Stemmerik 1964b).
A recent phylogenetic study of tribe Pisonieae, based on molecular data (Rossetto et al. 2019), indicated that Pisonia, as delimitated by Stemmerik (1964a, b), is non-monophyletic. The current definition of Pisonia places taxa with inconspicuous glands along anthocarp ribs ( Fig. 3A-C, F) into two distinct, well-supported lineages (i.e. clades A and C sensu Rossetto et al. 2019; Fig. 4), while typical Pisonia and its allies with glandular emergences (Fig. 3D-E) are restricted to clade B (Pisonia s.str.; Fig. 4). In clade A, formed by taxa carrying pedicellate flowers without bracteoles, members of the P. sect. Prismatocarpae and P. sect. Timeroyea (sensu Stemmerik 1964a) are included in the clade Ceodes, although these sections were not clustered in natural groups. Concurrently, P. sandwicensis from the P. sect. Paucistaminatae is placed in clade C as sister to the Neotropical genera Guapira and Neea (Rossetto et al. 2019;Fig. 4). Therefore, in order to simplify the classification of the tribe by designating monophyletic genera for the two independent lineages with inconspicuous glands within the tribe, it is necessary to resurrect Ceodes and Rockia. The objective of this work is to re-establish these two genera and to provide new combinations where necessary. To facilitate recognition in herbaria and in the field, we also provide colour pictures and line drawings of representative species of Ceodes, Pisonia and Rockia and a dichotomous key for the nine genera comprising the tribe Pisonieae.

Materials and methods
For the taxonomic treatment, we compiled accepted names following Stemmerik's revision (1964a), which is the most recent comprehensive treatment for Pisonieae in the Pacific region. We also consulted other more recent regional treatments and species descriptions and provided new generic combinations of the taxa that, according to our understanding, are currently considered as accepted (Friedmann 1986;Fosberg 1987;Philcox and Coode 1994;Florence 2004;Whistler 2004). Additional information on geographic distributions was obtained from Heimerl (1913b) and Stemmerik (1964b). Generic descriptions were based on Heimerl (1913b;1934), while Skottsberg (1936) was used specifically for the description of pollen structure of Ceodes.

Results and conclusions
Here we re-established the genera Ceodes and Rockia, recognising 20 species for the former and one for the latter. Sixteen out of the 20 species, recognised for Ceodes, represent new combinations (see Taxonomic treatment section). The re-establishment of Ceodes and Rockia provides an important step to refine our knowledge of the taxonomy and evolution of Pisonieae from the Indo-Pacific region. This work also has considerable implications for estimates of regional biodiversity, as many species of Ceodes are island endemics, while Rockia would be a genus restricted to the Hawaiian Archipelago (Wagner et al. 2005).
Some species of Pisonieae have been reported as dominant components of the vegetation from remote islands, in part because their sticky anthocarps can travel long distances attached to the feathers of seabirds (St. John 1951;Airy-Shaw 1952). Therefore, future studies on the taxonomy, ecology and biogeography of Pisonieae will help us understand how interactions with pollinators, seed dispersers (Walker et al. 1991;Murphy and Legge 2003;Burger 2005) and mycorrhiza (Hayward and Hynson 2014) have contributed to promote endemism in trees with a high dispersal capability. Inflorescence. Axillary, terminal or occasionally cauliflorous, arranged in compound cymes.

Key to genera from tribe Pisonieae
The following dichotomous key is compiled to separate the nine currently accepted genera within Pisonieae, based on reproductive features because vegetative (i.e. leaves and twigs) characters do not seem to provide enough resolution to help set apart these genera. Unfortunately, members of Pisonieae tend to have fugacious reproductive seasons and many collections in herbaria lack flowers and/or fruits. Thus, we support the recommendation made by Caraballo-Ortiz and Trejo-Torres (2017) on preparing multiple vouchers from a plant or population across seasons to document the full phenology of species and their range of morphological variation.