A taxonomic revision of the small mangrove genus Camptostemon ( Malvaceae )

. The true mangrove genus Camptostemon ( Malvaceae ) is becoming increasingly rare. This genus can be found in the Philippines, Borneo, Sulawesi, Maluku, Papua New Guinea, and Australia. Confusion remains over the taxonomic status of Camptostemon aruensis , endemic to Aru Islands, Indonesia. Therefore, a taxonomic revision is presented. Morphological characteristics, distribution maps, an identification key, and photographs of the species are provided. Based on type and type-locality specimens from the Aru Islands, C. aruensis is found to morphologically match C. schultzii . Camptostemon aruensis is a syn-onym of C. schultzii . Therefore, Camptostemon consists of two species, C. philippinensis (from the Philippines, Borneo, and Sulawesi), and C. schultzii (from Maluku, Indonesian Papua, Papua New Guinea, and northern Australia). Camptostemon philippinensis and C. schultzii are found in different geographic areas and do not share the same island.


Introduction
The genus Camptostemon Mast. (Malvaceae) belongs to true mangrove species that are becoming increasingly rare. Camptostemon is distributed in the Philippines, Borneo, Sulawesi, Maluku, Papua New Guinea, and Australia. Camptostemon is easily recognized from its trees-or shrubs-like habit, roots spreading horizontally along the surface of the soil, and it may bear knobbly pneumatophores, elliptic to obovate leaves, flowers with cup-shaped epicalyx, a bell-shaped or campanulate calyx, petals imbricate with white color, 5-20 stamens, fused into a tube at the base, a sessile ovary, a fruit capsule with densely woolly seeds, and leaves, flowers and fruits usually covered by densely spread scales.
Subsequently, in 1885, Sebastian Vidal published Cumingia S.Vidal, in 'Phanerogamae Cumingianae Philippinarum' with the only species being Cumingia philippinensis S.Vidal and claimed that Cumingia is very similar to Camptostemon (Troll 1933). Based on the close relationship between Camptostemon and Cumingia, Beccari (1886Beccari ( -1890, then concluded that Cumingia should be abandoned and Cumingia philippinensis was transferred to Camptostemon philippinensis (S.Vidal) Becc. Additionally, Beccari (1886Beccari ( -1890 published the third Camptostemon species collected from the Aru Islands, Maluku, Indonesia as C. aruensis Becc. Therefore, there were three species of Camptostemon sensu Beccari, namely C. aruensis which is endemic to the Aru Islands, Indonesia, C. philippinensis from the Philippines, Sulawesi, and Borneo, and C. schultzii from Australia and Papua New Guinea (Beccari 1886(Beccari -1890. Reinier Cornelis Bakhuizen van den Brink stated that C. aruensis was a synonym of C. schultzii without leaving any notes on his publication (Bakhuizen v. d. Brink 1924). Therefore, only C. philippinensis and C. schultzii were accepted as Camptostemon sensu Reinier Cornelis Bakhuizen van den Brink (Woodroffe & Grindrod 1991;Giesen et al. 2007). According to POWO (2022), there are three accepted species of Camptostemon, namely C. aruensis, C. philippinensis, and C. schultzii Based on BO specimens, C. philippinensis and C. schultzii are obviously distinguished. Camptostemon philippinensis has an obovate leaf shape and five stamens, while C. schultzii has an elliptic leaf shape and 20 stamens. However, C. aruensis is very similar to C. schultzii and it is hard to distinguish them from one another. During the flora exploration in several Camptostemon's distribution areas in Indonesia, such as in Talaud and the Banggai Islands in Sulawesi, the Aru and Tual Islands in Maluku, including the type-locality of C. aruensis on the Maikor Island, the Aru Islands, better herbarium specimens were collected. A taxonomic revision, therefore, was made. Morphological characteristics, distribution maps, an identification key, and photographs of the species were provided.

Materials and methods
The distribution of Camptostemon in Indonesia was investigated by carrying out flora explorations in different regions, including in the Talaud Islands of North Sulawesi in 2016, the Banggai Islands of Central Sulawesi in 2019, the Kei Islands of Maluku in 2021, and the Aru Islands of Maluku in 2022 (Fig. 1). The method of Camptostemon collection prescribed by Rugayah et al. (2004) and the processing of herbarium specimens by Djarwaningsih et al. (2002) was followed. Supporting data were recorded and photographs of the fresh specimens were taken. All specimens were stored in BO.
Original descriptions (Hooker 1876;Beccari 1886Beccari -1890Troll 1933) from holotypes of related species were consulted and compared. A comprehensive study was conducted by examining all specimens of related species directly in BO, scanned images of herbarium specimens from K and L, as well as online portals including Australasian Virtual Herbarium or AVH, e-ReColNat, Global Biodiversity Information Facility or GBIF, Integrated Digitized Biocollections or iDigBio, JSTOR, and MNHN Vascular Plant (P) (Damayanto & Irsyam 2022). Furthermore, an identification key and descriptions of the species including the photographs were provided. Distribution maps were produced by the Quantum GIS software. Herbaria abbreviations followed the guidelines by Thiers (2023).
Scales of leaves were observed with a scanning electron microscope (SEM) in the Zoology Characterization Laboratory, National Research and Innovation Agency through E-Layanan Sains for SEM. A sample of abaxial leaves (1 × 1 cm) was mounted on a stub using carbon tape and coated with gold using a coater model IB-2 (Giko Engineering, Japan). The samples were observed in Jeol JSM-IT200 SEM at ×300 magnifications. Description. Trees or shrubs. Roots spread horizontally along the surface of the soil and may bear knobbly pneumatophores. Leaves obovate to elliptic. Part of leaves, flowers, and fruits usually covered by densely spread scales. Flowers cluster up to 7 (or 8)-flowered, umbel; cup-shaped epicalyx; calyx campanulate; petals 5 lobes, imbricate, white; stamens 5-20, fused into a tube at the base; ovary sessile. Fruits capsule, dehiscent, contains densely woolly seeds.
Habitat and ecology. Camptostemon is only found in mangrove habitats (a true mangrove) (Giesen et al. 2007;Azizah 2021) in open rocky shores, on sandy beaches within the tidal range, inner edges of the mangrove forest, often reaching the margins and bordering the tidal streams (Giesen et al. 2007), tidal-stream edge (Djamaluddin 2018a), low intertidal region along tidal creeks (Middeljans 2014), and rarely in estuarine mangroves. Loranthaceae species, Amyema mackayensis (Blakely) Danser was reported to become a parasite on Camptostemon (Giesen et al. 2007).
Habitat and ecology. Camptostemon philippinensis occurs in mangrove habitats only and frequently encountered in the inner edges of the mangrove forest, often reaching the margins, and bordering the tidal streams (Giesen et al. 2007) and in the low intertidal region along tidal creeks (Primavera 2009). In Sulawesi, C. philippinensis was found in the habitat tidal-stream edge (Djamaluddin 2018a). On the Talaud Islands, Sulawesi, C. philippinensis grows facing directly to the open sea, in tidal edge areas covered by the dead coral formation and it was associated with Sonneratia alba Sm. (Lythraceae). In Borneo, C. philippinensis was found near the estuary. Camptostemon philippinensis was reportedly one of the mangrove species that had the lowest relative dominance, relative density, relative frequency, and importance values (Middeljans 2014).  In Indonesia, C. philippinensis is found in Sulawesi and Borneo (Troll 1933;Saenger 1998;Fernando & Pancho 1980;Giesen et al. 2007;Duke et al. 2010a;Herison & Romdania 2020). In Borneo, C. philippinensis can be found in the province of East Kalimantan [Berau (Mukhlisi & Sidiyasa 2014) and Teluk Balikpapan], the province of South Kalimantan (Laut Island), and Malaysia (Sandakan). In Sulawesi, particularly, C. philippinensis can be found in the province of North Sulawesi [the Mantehage Island (Djamaluddin 2018a) and the Talaud islands], the province of Gorontalo (Moluo), the province of Central Sulawesi (Donggala) (Wahyuningsih et al. 2012), the province of South Sulawesi (Malili, Lampia), and the province of Southeast Sulawesi (Kabaena Island). The exploration did not find C. philippinensis on the Banggai Islands even though intensive mangrove exploration had been carried out in the area (Fig 5).
Conservation status. The population trend of C. philippinensis was reported to be decreasing with only 1,200 mature individuals in 2008 (Duke et al. 2010a). In some areas of the research station, C. philippinensis no more than 10 mature plants were found. On the Talaud Islands, Sulawesi, especially, C. philippinensis was only found in one spot, namely Makatara Utara, which formed even-aged stands where seedlings were rare. Pollution, habitat shifting and alteration due to climate change, habitat destruction, removal of mangrove areas for aquaculture and settlements, industrial, and tourism areas, were reported to be a threat to C. philippinensis (Duke et al. 2010a). Camptostemon philippinensis, therefore, is reported as an endangered species according to the IUCN red list of threatened species (Duke et al. 2010a).
In Indonesia, C. philippinensis is included in the list of protected plants according to the Regulation of the Minister of Environment and Forestry of the Republic of Indonesia number P.106/MENLHK/SETJEN/KUM.1/12/2018 (KLHKRI 2018). Recently, Pratiwi and Juerges (2020) reported C. philippinensis to be threatened due to renewable energy development on hydropower and wind power in Southeast Asia. The population of this mangrove species is generally decreasing due to anthropogenic threats mainly due to mangrove forest conversion for aquaculture  and cutting for charcoal and wood (Pototan et al. 2021). Furthermore, slow propagation rates of C. philippinensis threaten their long-term survival (Spalding & Leal 2021).
Description. Evergreen tree or shrub up to 33 m high, diameter 35 cm. Soft-wooded, a grey to brown bark with circular lenticels, inner bark pinkish or pale straw-colored, heartwood white. Roots spread along the soil surface and bear knobbly pneumatophores, lenticellate. Leaves simple, verticillate, exstipulate, elliptic (broadly elliptic in Maluku and Indonesian Papua specimens and narrowly elliptic in most specimens of Australia and Papua New Guinea), 4.5-14 × 2-6.4 cm, thick; apex obtuse, retuse to acute (obtuse to retuse in Maluku and Indonesian Papua specimens and acute in most specimens of Australia and Papua New Guinea), base cuneate to rounded, entire margin; adaxial surfaces shiny green and glabrous or sometimes with scattered scale but easily fall, abaxial surfaces pale green with densely spread scales, scales peltate up to 200 μm diameter; petiole 1-4.5 cm long, semi-terete to slightly canaliculate, covered by scales. Inflorescences borne in upper axils; peduncle 0.4-1.5 cm, unbranched, covered by densely spread scales; umbel up to 6 flowers; in all about 1.5-1.8 cm long at anthesis. Flowers up to 10 mm long; pedicle up to 5 mm long, covered by scales; cup-shaped epicalyx, 2-5 lobes, up to 5 mm long, covered by scales; calyx campanulate, 3-4 mm long, outer surface covered by scales; petal 5 lobes, 4-5.5 × 3-4 mm, white, apex rounded, outer surface covered by scales; stamens 20, fused into a tube with scattered hairs, positioned higher than corolla mouth, anthers bilobed; stigma bilobed; ovary conical-shaped. Fruit capsule with persistent calyx and epicalyx, pear-shaped, 1-2 cm long, bilocular, dehiscent with a septum in the middle, outer surface covered by scales, seeds densely woolly.
Habitat and ecology. Camptostemon schultzii appear in mangrove habitats only (Giesen et al. 2007;Herison & Romdania 2020) and can be found in mid to low intertidal areas and along seashores (Duke et al. 2010b), sandy beaches within the tidal range, open rocky shores (Giesen et al. 2007), intermediate to downstream estuarine zone in the low to the mid-intertidal region (Duke et al. 2010b), as well as in beachfront communities and lowland forest at an altitude of 0-30 m. On the Aru Islands, C. schultzii was found in sandy soil area, sandy-rocky area, near the rivers with water salinity of 0-10 ppm, with total dissolved solids (TDS) 575-3610 ppm, water temperature 28-30°C and air temperature about 31-33°C. It was associated with some other true mangrove species i.e., Distribution. Camptostemon schultzii is locally common in northern Australia (Mueller 1889) (from Cape Bossut to Gove in the northern territory, Joseph Bonaparte Gulf region, and the north coast of Melville Island) and southern Papua New Guinea (Duke et al. 2010b), such as in the Gulf Province and the Western Province. Camptostemon schultzii also appears in Indonesia (Giesen et al. 2007;Duke et al. 2010b), such as in Papua [Waigeo (Prawiroatmodjo & Kartawinata 2014), Yapen, Japakopa, Bomberai Peninsula, and Manokwari], and Maluku (Giesen et al. 2007;Herison & Romdania 2020) (Ambon, Aru Islands, and Tual) (Fig 11). Giesen et al. (2007) mentioned that the geographic range of C. schultzii does not overlap with C. philippinensis. Saenger (1998) mentioned that C. schultzii possibly appear as far north as Borneo, however, whether there is any overlap between these species in Borneo is not known. So far, C. schultzii were never found in Borneo. Camptostemon schultzii also never found on the Banggai Islands even though intensive mangrove exploration had been carried out in the area. Therefore, based on this study, the geographic range of C. schultzii does not overlap with C. philippinensis in Borneo. Both of these species are found in different geographic areas and do not share the same island.
On the other hand, Hur et al. (2020) reported that C. schultzii was found in Arosbaya, Bangkalan Madura Regency, East Java, Indonesia, but there is no photograph or description provided. Therefore, this information is still doubtful. Morley et al. (2020) found a small amount of pollen Camptostemon in Perning, 12 km northeast of Mojokerto in East Java, Indonesia and then interpreted the extinction of the Camptostemon from Java as the disappearance of hypersaline mangroves following the development of wetter climates during the mid-Pleistocene. Meanwhile, Yoga et al. (2020) reported that the pollen fossils of C. schultzii were found in the Bojongmanik formation, Banten basin sediments, West Java, Indonesia.
The information on C. schultzii distribution in Java and its pollen fossils needs validation. There is uncertainty about the presence of C. schultzii in Java because the authors (KR and DN) have explored extensively in mangrove habitats in Java without recording C. schultzii.
Uses. In Australia, C. schultzii is used as poles of rafts (Baishya et al. 2020) and materials for pulp and paper production (Herison & Romdania 2020), such as sulfate-paper pulps with good strength properties (Giesen et al. 2007). Aboriginals in Australia used C. schultzii to treat skin infections (Duke et al. 2010b). In Aru Islands, C. schultzii is used as fuelwood and cork. Vernacular names. Based on Atlas of Living Australia (ALA 2021), C. schultzii is known as kapok mangrove. In Papua New Guinea, C. schultzii is known as tamagama, and on the Aru Islands as maum.
Conservation status. In 2008, the population trend of C. schultzii was reportedly stable, therefore, C. schultzii was categorized as the least concern based on the IUCN red list of threatened species (Duke et al. 2010b). On the Aru Islands, C. schultzii was found scattered throughout the area, and unfortunately, some of them were found to be decaying. Notes. According to Troll (1933) and Giesen et al. (2007), scales on the leaf surface of C. schultzii are only found in the abaxial. Based on this study, the scales were present on both sides of C. schultzii leaves in some specimens, but become glabrous when old on the adaxial surface. The young leaves of C. schultzii of some Papuan specimens bear scales on both sides of the leaves and the adaxial surface scales easily fall off when old, however, the scars of these scales are still visible on the upper surface of some mature leaves. On the other hand, Bakhuizen v. d. Brink (1924) stated that C. aruensis was a synonym of C. schultzii without leaving any notes on his publication. However, ALA (2022) (2022) reported that C. aruensis is an accepted species. Based on the type specimens (O. Beccari s.n., FI -holotype, code FI007729, JSTOR 2021) and better specimens collected from type-locality of C. aruensis in Maikor, Aru Islands, these specimens are morphologically very similar to C. schultzii, with elliptic leaves, flower with 20 anthers, and a hairy filament tube. Broadly elliptic leaves were found in Maluku and Indonesian Papua specimens and narrowly elliptic in most specimens of Australia and Papua New Guinea. Hence, C. aruensis is a synonym of C. schultzii, concurrent with the previous work of Bakhuizen v. d. Brink (1924).
Flowers appear from February to November. It is probably pollinated by wind and/or insects. In Australia, mature fruit appear between October and February (Giesen et al. 2007). Fruits are probably dispersed by water, while woolly seeds are dispersed by wind and/or water (Giesen et al. 2007;Herison & Romdania 2020). The generation length of C. schultzii is 35 years (Duke et al. 2010b).