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Research Article Early Development of Monoplex Pilearis

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Research Article Early Development of Monoplex Pilearis 1 Research Article 2 Early Development of Monoplex pilearis and Monoplex parthenopeus (Gastropoda: 3 Cymatiidae) - Biology and Morphology 4 5 Ashlin H. Turner*, Quentin Kaas, David J. Craik, and Christina I. Schroeder* 6 7 Institute for Molecular Bioscience, The University of Queensland, Brisbane, 4072, Qld, Australia 8 9 *Corresponding authors: 10 Email: [email protected], phone: +61-7-3346-2023 11 Email: [email protected], phone: +61-7-3346-2021 1 12 Abstract 13 Members of family Cymatiidae have an unusually long planktonic larval life stage (veligers) which 14 allows them to be carried within ocean currents and become distributed worldwide. However, little 15 is known about these planktonic veligers and identification of the larval state of many Cymatiidae 16 is challenging at best. Here we describe the first high-quality scanning electron microscopy images 17 of the developing veliger larvae of Monoplex pilearis and Monoplex parthenopeus (Gastropoda: 18 Cymatiidae). The developing shell of Monoplex veligers was captured by SEM, showing plates 19 secreted to form the completed shell. The incubation time of the two species was recorded and 20 found to be different; M. parthenopeus took 24 days to develop fully and hatch out of the egg 21 capsules, whereas M. pilearis took over a month to leave the egg capsule. Using scanning electron 22 microscopy and geometric morphometrics, the morphology of veliger larvae was compared. No 23 significant differences were found between the shapes of the developing shell between the two 24 species; however, it was found that M. pilearis was significantly larger than M. parthenopeus upon 25 hatching. Although statistical analysis did not find morphological differences, this study concludes 26 biological differences do exist between these two closely related species of Monoplex. 27 28 29 Keywords: Cymatiidae, veligers, scanning electron microscopy, geometric morphometrics 30 Abbreviations: Scanning electron microscopy (SEM), Principal Component Analysis (PCA), 31 Monoplex spp. abbreviated as M. where applicable. 2 32 Introduction 33 The features of the protoconch are widely used to identify gastropods, especially Caenogastropoda 34 (Solsona 1999). The protoconch is the first stage of shell growth in gastropods, which begins in 35 embryo and can be retained into adulthood (Muthiah 2000a; Muthiah 2000b). The protoconch is 36 generally classified into two phases, protoconch I and protoconch II (Sang et al. 2019). Protoconch 37 I is the first stage of the protoconch formed in embryo and is generally smooth and unornamented. 38 (Robertson 1971; Jablonski and Lutz 1983; Sang et al. 2019) Protoconch II can be ornate and 39 useful for identifying species differences and is formed before metamorphosis to mature shell 40 (teleochonch) (Robertson 1971; Jablonski and Lutz 1983; Sang et al. 2019). The differences in 41 the protoconch are used to distinguish cryptic species in Naticidae (Littorinimorpha) and 42 Neritiliidae (Neritimorpha), among others (Solsona 1999). The protoconch is so distinctive, 43 beyond species identification, its structure allows for differentiation between life cycle types 44 within Gastropoda (Solsona 1999) and this determination of the larval development type of a 45 fossilized or extinct specimen, solely based on protoconch features, can be invaluable for 46 paleontologists and evolutionary biologists (Solsona 1999; Kano 2008). 47 The primary biological function of the protoconch may be to provide protection for planktonic 48 larva (hereafter veligers) (Hickman 1999; Hickman 2001). Although this statement at first appears 49 self-evident, many planktonic veligers are eaten whole by zooplankton predators and the shell is 50 of limited protection (Pennington and Chia 1985; Hickman 1999; Hickman 2001). Nonetheless, 51 studies using scanning electron microscopy (SEM) have identified shell features that may result in 52 a protective advantage for larval gastropods (Hickman 1999; Hickman 2001). These features 53 include spiral ridging to reduce fracturing, ‘beaks’ or protrusions that protect the veliger’s aperture, 54 and strategically reinforced notches around the apertural opening (Hickman 1999; Hickman 2001). 3 55 Although these adaptations have been observed in several veliger species, shell structure and a 56 description of protoconch features are lacking in Monoplex veligers. 57 Species within Monoplex have an unusually long planktonic larval state, allowing them to become 58 geographically widespread through major ocean currents (Scheltema 1966; Pechenik 1984; 59 Muthiah 2000a; Muthiah 2000b). However, few reports of the morphological features of the 60 protoconch development during this larval state are available. It is believed Monoplex planktonic 61 veligers develop or calcify their shell very little during this growth stage (Pechenik 1984). Due to 62 the planktonic development taking several years, it is difficult to study the growth of veligers in 63 the laboratory, and their wide distribution with ocean currents makes monitoring development in 64 field studies impractical. Muthiah and Sampath (Muthiah 2000a) offer the only account of larval 65 development of Monoplex pilearis in the laboratory, with images taken using low-resolution 66 brightfield microscopy. They described the reproductive behavior of 22 M. pilearis specimens in 67 laboratory conditions and the early development of eggs over 45 days (Muthiah 2000a; Muthiah 68 2000b). 69 Low-resolution SEM images of veligers believed to be Monoplex parthenopeus revealed that the 70 protoconch is not heavily calcified during the planktonic stage (Scheltema 1966; Pechenik 1984). 71 That report does not provide images nor a description of the protoconch features for aid in 72 identifying future specimens (Pechenik 1984). SEM is the gold standard in terms of resolution of 73 protoconch features (Solsona 1999; Kano 2008), although brightfield imaging has also been 74 reported in some instances (Muthiah 2000a). Early work used detailed ink sketches in publications 75 due to the lack of high-resolution microscopy imaging, leaving the scientific community a legacy 76 of protoconch features which were significantly better than the microscopy images of the time 77 (Beu 1987). Magnification of current brightfield microscopy is commonly on the scale of 1,000 – 4 78 2,000x, whereas SEM can reach greater than 50,000x magnification. For many species, this type 79 of high-resolution image of the protoconch is simply unavailable, limiting the ability of unknown 80 specimens to be properly identified and classified (Scheltema 1966; Pechenik 1984). In the study 81 of trans-Atlantic transport of veligers (Pechenik 1984), a definite identification would be of great 82 assistance, as well as of use in further studies examining the long-distance transport of various 83 planktonic veligers. The gastropod veligers collected by plankton tows in the mid-Atlantic were 84 tentatively identified as M. (Cymatium) parthenopeus (Scheltema 1966; Pechenik 1984). The proof 85 of live veligers being carried by the Gulf Stream provided an explanation for the world-wide 86 distribution of some members of Cymatiidae, yet a species level identification of these veligers 87 was challenging (Scheltema 1966; Pechenik 1984). 88 Geometric morphology is a suite of statistical methods to quantify the differences in shape between 89 a given set of specimens (Rohlf 1993). These methods quantify differences in morphology by 90 reducing shapes to a set of Cartesian coordinates based on consistent landmarks or by using outline 91 curves (Conde-Padin 2007; Avaca et al. 2013; Marquez 2017; Doyle 2018). This powerful method 92 enables quantitative distinction between shape and morphological landmarks (Avaca et al. 2013). 93 Quantitative comparison of shell shapes has been used to identify subtypes within and between 94 adult gastropod species and subspecies, including Buccinanops deformis, Littorina saxatilis, and 95 Littorina littorea (Conde-Padin 2007; Avaca et al. 2013; Marquez 2017; Doyle 2018). This 96 technique has not yet been applied to protoconch features, and here we investigated if geometric 97 morphometrics can be used to identify veliger gastropods. 98 Herein we report the first high-resolution SEM images of M. pilearis and M. parthenopeus 99 veligers, including images of the developing shell during the earliest life stages. In addition, further 100 information on the egg clutches and early development is described, adding to the works of 5 101 Pechenik and Muthiah (Pechenik 1984; Muthiah 2000a; Muthiah 2000b). Statistical analysis was 102 performed in an attempt to quantify morphological differences between the protoconch I of two 103 veliger species. To the best of our knowledge, this paper is the first attempt at using geometric 104 morphology metrics to describe the planktonic life stage of any species of Gastropoda. 105 Methods and Materials 106 Specimen Collection 107 Two specimens of M. pilearis were collected from Amity Point, North Stradbroke Island, 108 Queensland, Australia (Fig 1) and seven specimens of M. parthenopeus were collected from the 109 oyster lease of Greg Knight, North Stradbroke Island, Queensland, Australia. Specimens were kept 110 in aquaria and fed rock oysters at ad libitum. The female M. pilearis laid eggs on March 19, 2018, 111 whereas the female M. parthenopeus laid eggs on April 18, 2018. The water quality of the aquaria 112 over the course of the study is summarized in Table 1. The water flow through the
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