Five new species and one new genus of recent miliolid foraminifera from Raja Ampat (West Papua, Indonesia)

Raja Ampat is an archipelago of about 1,500 small islands located northwest off the Bird’s Head Peninsula of Indonesia’s West Papua province. It is part of the Coral Triangle, a region recognized as the “epicenter” of tropical marine biodiversity. In the course of a large-scale survey on shallow benthic foraminifera we have discovered one new genus and five new species of recent miliolid benthic foraminifera from the highly diverse reefal and nearshore environments. The new fischerinid genus Dentoplanispirinella is characterized by its planispiral coiling and by the presence of a simple tooth, that differentiate it from Planispirinella Wiesner. It is represented in our sample material by the new species Dentoplanispirinella occulta. The other four species described herein are Miliolinella moia, Miliolinella undina, Triloculina kawea and Siphonaperta hallocki. All new species are comparatively rare and occur sporadically in the sample material. Detailed morphological descriptions, scanning electron microscopy pictures of complete and dissected specimens as well as micro-computed tomography images are provided.


INTRODUCTION
The Raja Ampat Archipelago (West Papua, Indonesia) off the northwestern coast of New Guineas Bird's Head Peninsula (Fig. 1B) is one of the most species rich marine environments (Erdmann & Pet, 2002;McKenna, Allen & Suryadi, 2002), situated in the Indo-Pacific's ''epicenter'' of biodiversity, commonly referred to as the Coral Triangle (Hoeksema, 2007). The Coral Triangle encompasses a large part of the tropical marine waters of Indonesia, the Philippines, Malaysia, the Solomon Islands, Papua New Guinea and Timor-Leste (Fig. 1A). It includes ecoregions that are each home to at least 500 species of hermatypic corals and also show extraordinary diversity among coral associated species (Veron, 1995;Veron et al., 2009;Roberts et al., 2002;Bellwood & Hughes, 2001;Tittensor et al., 2010). The region is recognized as a ''species factory'' and functions as the most significant net exporter of biodiversity for adjacent reef regions (Briggs & Bowen, 2013;Ekman, 1953).
To date, however, large-scale systematic studies on benthic foraminifera from Raja Ampat are lacking. The archipelago consists of the four main islands Waigeo, Batana, Salawati, and Misool, and hundreds of small satellite islets, which are largely uninhabited. Due to its remote location and difficult access conditions the coral reefs of the region remained relatively unexplored and pristine. However, increasing exposure to exploitation have required the establishment of several marine protected areas (Agostini et al., 2012). The first and to date only report on benthic foraminifera from Raja Ampat is that of Hofker (1927) andHofker (1930), who examined the material taken by the Siboga Expedition (1899-1900) that included five samples from Raja Ampat. He documented nine species of benthic foraminifera including eight rotalid taxa and the miliolid symbiont bearing species Peneroplis pertusus (Forskål).

MATERIAL AND METHODS
This study was conducted with 30 sediment samples from the Raja Ampat Archipelago (New Guinea, Indonesia) from around the islands of Waigeo, Batana, Kawe, Fam and adjacent small islets in an area that covers about 2,500 km 2 (Fig. 1C). The archipelago is located in the central Indo-Pacific warm pool with an average annual sea surface temperature of 29 • C . Raja Ampat is further situated in the passage way of the Indonesian Throughflow, a major ocean current that leads water masses from the western Pacific to the eastern Indian Ocean. Previous studies have shown that the reef fauna of Raja Ampat is strongly current dependent (Devantier, Turak & Allen, 2009;Turak & Souhoka, 2003). The samples were collected by snorkeling and SCUBA diving in September 2011 by M Langer. Sediment surface samples from the top 2 cm were collected from the fore-reef slope of fringing reefs, with two samples from a patch reef, and two samples from a sandy channel with sparse coral cover ( Table 1). The sediment was predominantly carbonaceous (∼ 90%) and included fine-grained sediments as well as coarse reef rubble. All samples were washed through a 63 µm sieve and dried at 50 • C in an oven overnight. Foraminifera were picked from each sample and the best preserved specimens were imaged using a Tescan VEGA MV2300 Scanning Electron Microscope (SEM) at the Steinmann Institute of the University of Bonn. Digital plates were assembled using Adobe Photoshop CS6. Micro-computer tomography (CT) scan imaging was conducted using a phoenix v|tome|x s computed tomography system at the Steinmann Institute and visualization was carried out with Avizo 7.1.0. The new species and the new genus are described in detail using the supra-generic classification of Loeblich & Tappan (1987).
Repository of the Material: the holotypes and topotypic paratypes of the new species are deposited in the micropaleontology collection of the Steinmann Institute of Paleontology at the University of Bonn, Germany (MaLaPNG 2011-10, MaLaPNG 2011-11, MaLaPNG 2011-12, MaLaPNG 2011-13, MaLaPNG 2011. The electronic version of this article in Portable Document Format (PDF) will represent a published work according to the International Commission on Zoological Nomenclature (ICZN), and hence the new names contained in the electronic version are effectively published under that Code from the electronic edition alone. This published work and the nomenclatural acts it contains have been registered in ZooBank, the online registration system for the ICZN. The ZooBank LSIDs (Life Science Identifiers) can be resolved and the associated information viewed through any standard web browser by appending the LSID to the prefix http://zoobank.org/. The LSID for this publication is: urn:lsid:zoobank.org: pub:FB001C3C-AEA9-45D5-9224-EDD084378897. The online version of this work is archived and available from the following digital repositories: PeerJ, PubMed Central and CLOCKSS.

RESULTS
Smaller miliolid benthic foraminifera are typical dwellers in surface sediments of shallow water reefal and lagoonal habitats. By studying the highly diverse assemblages of benthic foraminifera from Raja Ampat, taken from different locations around the islands (Fig. 1C), we recorded a total of 455 species among them 249 miliolid species, of which five are described here as new. Four species belong to the widely distributed miliolid genera of Miliolinella Wiesner, Triloculina d'Orbigny and Siphonaperta Vella. As the morphological properties of the fifth species differentiate it from any previously known genera, we designate and describe it as the new genus Dentoplanispirinella. Description. Test small, broadly circular in outline, discoidal to slightly biconvex. Periphery with a weakly developed subrounded keel that encircles the entire test margin. Wall thick, calcareous, porcelaneous, imperforate. Coiling involute, throughout planispirally enrolled with 2.5 to 3.5 tubular chambers per whorl, each whorl slightly offset to the proceeding coil with a tendency to become sigmoiline (axial section as seen in CT scan, Fig. 2H). Lateral wall extensions of the adult chambers entirely cover the earliest chambers and tend to overlap the umbilical region in each whorl. Sutures oblique, thin and irregular. Aperture arch-shaped, triangular in juvenile specimens, high and subtriangular in adult specimens, tapering apically, on the base connected with the peripheral margin of the proceeding chamber and provided with a very small and thin tooth. In juvenile specimens the tooth appears just like a little knob or slightly raised spine.
Remarks. Dentoplanispirinella gen. nov. resembles Planispirinella Wiesner, 1931 in having a discoidal shape, a high aperture and a planispiral chamber arrangement, but differs from Planispirinella by the presence of a tooth and the more biconvex test shape in apical view (Fig. 2B). The apertural features and the coiling mode of Dentoplanispirinella further distinguish it from Nummoloculina Steinmann 1881, which has an apertural flap and an early quinqueloculine coiling. Type locality. The holotype and the paratype are from sample station MS03 (16m), a sand channel between Arborek Island and Pulau Mansuar; Raja Ampat, New Guinea (Indonesia).

Diagnosis.
A species of Dentoplanispirinella gen. nov. with a discoidal to biconvex test shape, a slightly keeled periphery, a radial oriented, finely striate surface ornamentation and an arch-shaped, triangular aperture, provided with a small tooth.
Occurence. Dentoplanispirinella occulta is widely distributed in the Raja Ampat area in fine to coarse coral rubble samples from depths of 14 to 45 m.
Description. Test porcelaneous and imperforate. Almost circular in lateral view, lenticular and biconvex in apertural view with a slightly developed, subrounded keel and weakly inflated chambers. Coiling planispiral and involute. Two and a half to three and a half chambers visible from the exterior. Lateral wall extensions of the adult chambers entirely cover the earliest chambers and tend to overlap the umbilical region; the final chamber covers approximately half of the test surface. Sutures oblique, thin, irregular and recurved near the periphery. Test surface ornamented with radial oriented, fine, sub-parallel to anastomosing striae that are straight to slightly curved backwards, towards the outer margins of the chambers. Umbilical region and test periphery more weakly ornamented. Outer wall layer constructed of longitudinally aligned needle-shape crystals, oriented perpendicular to direction of ornamentation. The test appears matte white under the light microscope with a slightly translucent periphery. Apertural face not ornamented. Aperture arch-shaped and triangular in juvenile specimens, high and subtriangular in adult specimens, tapering apically, on the base connected with the peripheral margin to the preceding chamber and provided with a peristomal rim. Aperture provided with a very small and thin tooth, with the flat side oriented in lateral direction. Collins (1958, p. 374, pl. 4, Figs. 2A and 2B) by its more lenticular biconvex shape in horizontal section, the subtriangular shape of the aperture, the presence of a small tooth, and the striate surface ornamentation. Occurence. This species is widely distributed in the Raja Ampat area in fine to coarse coral rubble samples and occurs at depths between 12 and 45 m.

Remarks. Dentoplanispirinella occulta sp. nov. differs from Planispirinella involuta
Description. Test porcelaneous and imperforate, ovate in outline and slightly higher than broad. Test weakly compressed and flattened, subtriangular in apertural view. Chamber arrangement quinqueloculine with five chambers visible from the exterior. In some specimens only three to four chambers are visible. Periphery rounded to subrounded, chambers slightly inflated. Sutures curved, distinct and weakly depressed. Chambers tend to be off-centered, giving them a slanted appearance. Test wall smooth, translucent to opaque and glossy under the light microscope. Aboral end of the chambers slightly constricted. Aperture in basal position, a Miliolinella-type large subcircular opening with an everted peristomal rim and a semicircular, slightly excavated flap, that covers more than half of the opening. Remarks. Miliolinella moia sp. nov. differs from Miliolinella pilasensis McCulloch, 1977 (p. 566, pl. 238, Fig. 16 andLoeblich &Tappan, 1994, p. 57, pl. 99, Figs. 1-9) in its angular and more compressed outline, and the large subcircular opening. Millet (1898)

Diagnosis.
A small quinqueloculine species of Miliolinella Wiesner with inflated chambers, a rounded outline and an undulate to reticulate surface ornamentation.
Description. Test porcelaneous and imperforate, small, ratio of height and width variable but usually slightly higher than broad. Periphery rounded and chambers slightly inflated. Chamber arrangement quinqueloculine, with five chambers visible from the exterior. Aboral end rounded, flush with the surface in the holotype to slightly raised in paratypes. Wall smoothly finished, matte, translucent under the light microscope. Sutures curved and depressed. Test surface ornamented with numerous irregular, predominantly longitudinal, somehow honeycombed reticulate to undulate low anastomosing costae that are covering   (in well preserved specimens). Aboral end rounded and produced; oral end becoming more slender and leading into a short produced neck. Aperture terminal, a wide circular opening with a short T-shaped, bifid tooth, that reaches more than one third of the apertural diameter. Apertural opening surrounded by a slightly thickened and everted peristomal rim.
Occurence. Siphonaperta hallocki occurs sporadically in fine to coarse coral rubble samples from depths of 16 to 30 m.
• Martin R. Langer conceived and designed the experiments, performed the experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the paper, reviewed drafts of the paper.

New Species Registration
The following information was supplied regarding the registration of a newly described species: Dentoplanispirinella gen. nov. urn:lsid:zoobank.