A new genus of Australian orb-weaving spider with extreme sexual size dimorphism (Araneae, Araneidae)

The new Australian orb-weaving spider genus Mangrovia in the family Araneidae Clerck, 1757 is described. It is characterised by extreme sexual size-dimorphism (eSSD) with females (total length 8–10 mm) ca. 3 to 5 times larger than males (2.5–3 mm). Whilst Mangrovia shares with the informal Australian ‘backobourkiine’ clade a single seta on the male pedipalp patella, the genus is probably more closely related to the ‘zealaraneines’ or associated genera. In addition to eSSD and the single patellar spine, the genus is characterised by a distinct subterminal embolus branch in males. The new genus includes two species: the type species Mangrovia albida (L. Koch, 1871) comb. nov. (= Epeira fastidiosa Keyserling, 1887, new syn.) from Queensland and Mangrovia occidentalis sp. nov. from Western Australia. Both species are apparently coastal and occur in mangroves, but also in riparian woodland. Spiders were found resting in rolled-up leaves adjacent to their orb-web.


Introduction
Extreme sexual size dimorphism (eSSD), a phenomenon where one sex -generally the female -is at least twice as big as the other, is not a common phenomenon in spiders and mostly expressed in orb-weaving taxa (family Araneidae Clerck, 1757, incl. Nephilinae Simon, 1894 and Phonognathinae Simon, 1894) and combfooted spiders (family Theridiidae) (Hormiga et al. 2000;Kuntner and Coddington 2020;Yu et al. 2022). There are several hypotheses explaining eSSD, for example an increase of female size due to fecundity advantage (Head 1995;Coddington et al. 1998), male dwarfism due to selection for early maturation (Gunnarson and Johnsson 1990;Vollrath and Parker 1992), or gravity advantages (Moya-Laraño et al. 2002). However, a recent review of eSSD in spiders suggests that the phenomenon is most likely the expression of a complex of evolutionary forces, originating both in natural and sexual selection (Kuntner and Coddington 2020).
The incidence of eSSD is low within the traditional Araneinae Clerck, 1757 (sensu Scharff and Coddington 1997); at the genus level, only Kaira O. Pickard-Cambridge, 1889 has significantly smaller males than females (Levi 1993b;Hormiga et al. 2000), although eSSD is known to occur in other traditional 'araneine' genera at the species level (e.g. Piel 1996;Framenau et al. 2010). A recent multi-gene molecular phylogenetic analysis of the Araneidae did not confirm a monophyletic 'Araneinae'; however, this study also found multiple origins (and reversals) of eSSD at the genus level in the Araneidae (Scharff et al. 2020) (see also Yu et al. (2022) for a re-analysis of the dataset with focus on Poltys Simon, 1881 and Cephalonotus Simon, 1895). Scharff et al.'s (2020) comprehensive analysis of world-wide Araneidae has transformed our understanding of araneid relationships, in particular with respect to the traditional subfamily Araneinae. The Australian species formed several well supported clades at the subfamily level, although Scharff et al. (2020) did not establish formal subfamilies for them due to their poor taxonomic knowledge and morphological circumscription. Of these groups, the 'backobourkiines' are now best known due to some recent taxonomic studies (e.g. Framenau et al. 2010Framenau et al. , 2021aFramenau et al. , b, 2022Framenau 2011;Joseph and Framenau 2012). A uniting character appears to be the presence of a single macroseta on the male pedipalp patella and the median apophysis of the male pedipalp forming an arch over the radix (Scharff et al. 2020). The backobourkiines include Australian genera, such as Acroaspis Karsch, 1878, Backobourkia Framenau, Dupérré, Blackledge & Vink, 2010, Carepalxis L. Koch, 1872 (also known from the Nearctic), Hortophora Framenau & Castanheira, 2021, Novakiella Court & Forster, 1993, Plebs Joseph & Framenau, 2012 (also known in the Oriental region) and Socca Framenau, Castanheira & Vink, 2022. There are two currently known cases of eSSD in the backobourkiines (Scharff et al. 2020). In Backobourkia eSSD is expressed at the species level, as only one of three species in the genus, B. collina (Keysering, 1886), is highly dimorphic (Framenau et al. 2010). In contrast, in a species-group represented by Parawixia dehaani (Doleschall, 1859) in Scharff et al.'s (2020) analysis -referred to as 'Araneus dehaani-group' in Yin et al. (1997) -eSSD appears to be expressed at the genus-level as a second species in this group, Araneus albomaculatus Yin, Wang, Xie & Peng, 1990, is also extremely sizedimorphic (Yin et al. 1997). The male of the third species in the group, A. shunguangensis Yin, Wang, Xie & Peng, 1990, is currently unknown. The dehaani-group apparently represents a new genus in the backobourkiines with P. dehaani clearly not belonging to Parawixia based on molecular data (Scharff et al. 2020).
A second well-supported group including Australian orb-weavers are the 'zealaraneines', which largely include New Zealand genera such as Colaranea Court & Forster, 1988, Cryptaranea Court & Forster, 1988and Zealaranea Court & Forster, 1988, but also the Australian species Araneus albotriangulus (Keyserling, 1887) and A. talipedatus (Keyserling, 1887), both misplaced at the genus level and representing new genera (Scharff et al. 2020). Most closely related to the zealaraneines appear to be true Araneus Clerck, 1757, but also species in the large genus Neoscona Simon, 1895 (Scharff et al. 2020). Zealaraneines have no known synapomorphies, but in contrast to backobourkiines, males have two pedipalp patellar spines and the median apophysis does not form an arch over the radix (see Court and Forster 1988;figs 354-358, 360-362). There is no known case of eSSD in the zealaraneines where females are generally only slightly larger than males (Court and Forster 1988).
Our current revision of Australian orb-weaving spiders recovered a novel case of eSSD. Females of Araneus albidus (L. Koch, 1871), a species originally described based on a female only, are approximately three to five times larger than males. As in the dehaani-group, eSSD appears to act at the genus level, as a second undescribed species very similar to A. albidus is also extremely size-dimorphic. The male pedipalps of A. albidus (and the undescribed species) have only one patellar spine suggesting close affinities with the backobourkiines. However, other genitalic characters, for example the shape of the median apophysis of the male pedipalp, do not match any of the genera currently recognised in this group and these species may therefore be a zealaraneine, or not belong to any of these two well-supported indigenous Australo-Oriental groups.
The aim of this study is to describe these two species in a new genus as a working hypothesis for future phylogenetic analyses of Australian Araneidae, specifically the species of the backobourkiines and zealaraneines sensu Scharff et al. (2020).

Materials and methods
Descriptions and terminology follow recent publications on Australian orb-weaving spiders (e.g. Framenau et al. 2010Framenau et al. , 2021aFramenau et al. , b, 2022. Fresh and well-preserved specimens were used instead of historic and often poorly preserved type specimens for redescriptions. Colour patterns were described based on specimens preserved in ca. 75% ethanol. The descriptions of the male pedipalp relate to their position as a limb, i.e. a full view of the bulb with the cymbium in the background of an image is a retrolateral view as in Araneidae the cymbium is situated mesally. Our standard views of the pedipalp therefore generally show the ventral view -to illustrate the generally diagnostic median apophysis -or the dorsal view -with the tegulum in full view -as the cymbium is situated to the side in the images.
Male pedipalps were expanded by alternately submerging them for ca. 20 min in warm 10%KOH and distilled water until maximum expansion was reached. Female genitalia were dissected and then cleared in warm 10%KOH for 20 mins and transferred into lactic acid on a microscopic slide under a coverglass to further clear internal features for imaging. Measurements are given in millimetres taken at an accuracy of one tenth of a millimetre, except for eye and labium sizes measured at a hundredth of a millimetre.
Images of preserved specimens were taken in different focal planes with a Nikon D300 digital SLR camera attached to a Leica M16A stereomicroscope and combined with Auto Montage (vers. 5.02) software from Syncroscopy to increase depth of field. We used 2 Nikon R1C1 wireless speedlights instead of fibre optics to illuminate the exposures. The latter were used as guide-light for focusing. Microscopic images of cleared epigynes and expanded pedipalps were taken in different focal planes (ca. 20-30 images) on a Leica DMC4500 digital camera mounted to a Leica M205C stereomicroscope and combined using the Leica Application Suite X, v. 3.6.0.20104. All photos were edited and mounted in the software Photoshop CC 2020.

AM
Australian Type-species. Epeira albida L. Koch, 1871, designated here. Etymology. The genus-group name is derived from the general habitat preferences of the two species, which are often found in coastal mangroves and woodlands. The gender is feminine.
Diagnosis. Within an Australian context, Mangrovia gen. nov. males have only a single patellar spine on the pedipalp, a character considered a putative synapomorphy of the backobourkiines. However, Mangrovia gen nov. differ considerably from members of the backobourkiines by somatic and genital morphology. Both species in the genus display eSSD with females about 3-5 times larger than males, but eSSD is absent in the backobourkiines (with the exception of B. collina and species in the dehaani-group (sensu Yin et al. 1997)). The median apophysis in backobourkiines is elongate transverse with the base forming an arch over the radix, but it is short with an apical, spine-like projection in Mangrovia gen. nov. The female epigyne in Mangrovia gen. nov. has a terminal pocket, absent in all backobourkiines.
Mangrovia gen. nov. differs from the members of the zealaraneines as currently known (see Introduction section) by its eSSD, absent in any known zealaraneines, and the presence of only one patellar spine on the male pedipalp, whereas there are always two in zealaraneines (Court and Forster 1988). The median apophysis of zealaraneines is elongate transverse, with a variable number of spine-like protrusions, but much shorter and only with a single spine-like protrusion in Mangrovia gen. nov.
Outside the backobourkiines and zealaraneines, Mangrovia gen. nov. appears most similar to species of Neoscona (Berman and Levi 1971;Grasshoff 1986;Levi 1993a), in particular with respect to the male genitalia. However, eSSD is absent in any known Neoscona species and males of Neoscona have distinctly enlarged tibiae on the second leg with numerous and strong spines, often in diagnostic arrangement. Mangrovia gen. nov. males do not have enlarged tibiae II. In contrast to Mangrovia gen. nov., males in Neoscona have two patellar spines on the pedipalp, not one, and the embolus of Mangrovia gen. nov. has a subterminal side branch (e.g. Fig. 2B, C), not present in Neoscona. An embolus lamella is absent in Mangrovia gen. nov. males, but present in Neoscona (e.g. Levi 1993a; fig. 6).
Diagnosis. Males M. albida comb. nov. can be separated from M. occidentalis sp. nov. by subtle differences in key pedipalp sclerites, specifically the conductor is less elongate (Figs 2B, 7B), and the terminal apophysis is less bent apically (Figs 1C, 6C). In addition, the subterminal branch of the embolus appears larger in M. albida comb. nov. than in M. occidentalis sp. nov. (Figs 2B, 7A). Females of M. albida comb. nov. are distinguished from those of M. occidentalis sp. nov. by the shorter scape and its wider tip (scape longer and thinner with thinner tip in M. occidentalis sp. nov.) (Figs 3C, 8C).
Variation. Total length males 2.7-3.0 (n = 3), females 8.3-9.7 (n = 5). There is very little colour variation in both males and females, although the folium pattern in males can be very distinct.
Remarks. Rack (1961) listed the holotype of Epeira albida L. Koch, 1871 as her catalog number 218 in the collection of the ZMH; however, this cannot be the holotype as this specimen is an immature female and the original description and illustrations by L. Koch (1871) clearly show a mature female with fully developed epigyne. We here consider a female in the collection of the NHMUK London the holotype of E. albida. This specimen has the typical label handwritten by L. Koch and matches well the description in L. Koch (1871).
Keyserling (1887) described Epeira fastidiosa Keyserling, 1887 based on a mature male. The holotype of this species matches in all diagnostic characters the males that are here recognised as conspecific with the female M. albida comb. nov. We therefore consider E. fastidiosa a junior synonym of M. albida comb. nov. Similarly to M. albida comb. nov., the designation of the holotype of E. fastidiosa remains ambiguous. Rack (1961) considered a male in the ZMH (Rack (1961)-catalog no. 237) as holotype of the species, but there is also a male in the NHMUK (1890.7.1.4150) from the type locality Rockingham that could be the holotype, as part of the Keyserling-collection was sold to the NHMUK (J. Beccaloni, pers. comm.). Both specimens are very similar and match Keyserling's (1887) original description. We here follow Rack's (1961) initial designation of the holotype of E. fastidiosa to maintain consistency with previous literature.
Habitat preferences and life history. Habitat descriptions found on labels with museum specimens include 'mangroves' and 'riparian', where spiders were found in rolled leaves near the orb-web. Mature spiders were found between December and April.
Distribution. This species is only known from coastal Queensland (Fig. 5). Etymology. The specific epithet is a Latin adjective in apposition -occidentalis -meaning western, and it refers to its distribution that is limited to coastal Western Australia.
Variation. Male only known from holotype; the spine on the median apophysis of the left pedipalp was broken off, therefore the right pedipalp is illustrated here. Female total length 8.7-10.6 (n = 8); there was little colour variation in females although the abdomen venter showed distinct white guanine spots in most specimens.
Habitat preferences and life history. Collection data on labels with museum specimens of M. occidentalis sp. nov. exclusively lists 'mangroves' as habitat, where, similar to M. albida comb. nov., spiders were collected mainly from rolled leaves near the orb-web. Mature spiders were mainly collected in May, July and September with a single record in February.
Distribution. This species is only known from coastal Western Australia (Fig. 9).

Discussion
Mangrovia gen. nov. males have a single patellar spine on the male pedipalp, a character that was noted by Scharff et al. (2020) to occur in all backobourkiines, an Australasian clade in the analysis. This character was earlier recognised as taxonomically informative when employed in a study of Chinese araneids to key out two groups combined, species previous listed in Zilla C.L. Koch, 1834 (now all recognised as belonging to Plebs Joseph and Framenau. 2012) and the dehaani-group (Yin et al. 1997). Both Plebs and the dehaani-group have been confirmed as backobourkiines by molecular data (Scharff et al. 2020) showing that the single patellar spines can possibly serve as good diagnostic character beyond the Australian continent.
An association of Mangrovia gen. nov. with the backobourkiines is, however, poorly supported otherwise, as genital morphology of its two species is very unlike other representatives of this clade. The median apophysis of the male pedipalp does not form an arch over the radix as in all other backobourkiines and a basal extension of the conductor, referred to as paramedian apophysis or conductor lobe is absent (e.g. Framenau et al. 2010Framenau et al. , 2021bFramenau 2011). In addition, the epigyne scape has a terminal pocket, not found in any other backobourkiines, but otherwise common, for example, in members of the zealaraneines, a largely New Zealand clade (Court and Forster 1988;Scharff et al. 2020). An association of Mangrovia gen. nov. with zealaraneines is also more likely due to the similarities of its genitalia to Neoscona, a genus that was, albeit without statistical support, part of a sister group to zealaraines and true Araneus combined (Scharff et al. 2020). It is therefore possible that a potential loss of a patellar spine in comparison to other zealaraneines, Neoscona and Araneus is an artefact of males becoming smaller. Confidently placing Mangrovia gen. nov. in a phylogenetic context within the Araneidae will require, at a minimum, its inclusion into a phylogeny based on data from the molecular study by Scharff et al. (2020), although it has to be recognised that that study did not provide a fully resolved phylogenetic hypothesis of this spider family.
The pedipalp morphology of Mangrovia gen. nov. is very similar to that of Neoscona, although there are some differences, in particular in the apical section of the pedipalp, including terminal and subterminal apophyses and embolus. The Neoscona pedipalp also has three terminal sclerites, i.e. terminal apophysis, embolus lamella (Levi 1993a;"Terminal-Lamelle" in Grasshoff 1986) and the embolus. It is likely that the sclerite we termed subtermi-nal apophysis is homologous to Levi's (1993a) embolus lamella, but its shape is generally very different -and very variable -in Neoscona compared to the thin, needle-like structure in Mangrovia gen. nov. (Figs 2A, 7B). The embolus has a unique subterminal side-branch in Mangrovia gen. nov., the functional significance of which is unknown. 'Capped' emboli are not uncommon in the Araneidae (see Scharff and Coddington 1997) and are generally associated with the embolus breaking during copulation, possibly acting as mating plug in the epigyne to prevent the female from mating again. The function of the side branch of the Mangrovia gen. nov. embolus remains unknown.
As in Neoscona, the radix and stipes are either fused in Mangrovia gen. nov. or a stipes is absent. There seem to be a less sclerotised short section in the radix at least in M. albida comb. nov. (Fig. 2C, D), which may indicate a fusion point of radix and stipes, but a similar section is not necessarily visible in M. occidentalis sp. nov. (Fig. 7A). Other basal pedipalp sclerites are very similar to Neoscona, in particular the shape of the median apophysis. Similar to many Neoscona (Berman and Levi 1971;Grasshoff 1986;Levi 1993a), this sclerite cannot be used to differentiate between the two Mangrovia gen. nov. species due to its similarity in both species. Its apical spine has likely an important function during copulation interlocking with the terminal pocket of the epigyne. Few studies have investigated genitalia during copulation in the Araneidae to explore the functional roles of the different pedipalp sclerites. But the median apophysis interlocks with the terminal pocket of the scape in Larinia jeskovi Marusik, 1987(Mouginot et al. 2015. Both Mangrovia gen. nov. species appear to be specialists of coastal habitats, particularly inhabiting subtropical mangroves. Here, the apparently nocturnal spiders hide in a self-constructed rolled-leaf retreat adjacent to the web during the day. In Australia, constructing a retreat from a rolled leaf has been observed in other orb-weaving spiders. Apparently similar to Mangrovia gen. nov., Araneus praesignis (L. Koch, 1872) roll a leaf of the plant that harbours the spider's web (Whyte and Anderson 2017). In contrast, Araneus dimidiatus (L. Koch, 1871) incorporates a dead rolled leaf into the periphery of its web where the spider hides (Framenau et al. 2014). Both species are not true Araneus with phylogenetic relationships poorly resolved (Scharff et al. 2020). Australian species in the araneid subfamily Zygiellinae Wunderlich, 2004, i.e. in the genera Artifex Kallal & Hormiga, 2018, Deliochus Simon, 1894 and Phonognatha Simon, 1894, also suspend a dead rolled leaf in the web, but in contrast to A. dimidiatus it is suspended near the hub (Kallal and Hormiga 2018). It is clear that leaf-curling behaviour has evolved through different evolutionary pathways a number of times in the phylogenetic history of the Araneidae in Australia and resolving their origin requires testing with empirical data, specifically the compilation of a fully resolved phylogenetic hypothesis including all groups displaying this behaviour.