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Echinodermata: Echinoidea) of Mexico Caballero-Ochoa, A.A., Buitrón-Sánchez, B.E., Conejeros- Vargas, C.A., Esteban-Vázquez, B.L., Ruiz-Nava, M.P., Jiménez-López, J.C., Solís-Marín, F.A., & Laguarda-Figueras, A. (2021). Morphological variability of recent species of the order Cassiduloida (Echinodermata: Echinoidea) of Mexico. Revista de Biología Tropical, 69(S1), 423-437. DOI 10.15517/ rbt.v69iSuppl.1.46382 DOI 10.15517/rbt.v69iSuppl.1.46382 Morphological variability of recent species of the order Cassiduloida (Echinodermata: Echinoidea) of Mexico Andrea Alejandra Caballero-Ochoa1,2* Blanca E. Buitrón-Sánchez3 Carlos A. Conejeros-Vargas4 Brenda L. Esteban-Vázquez1 Mariana P. Ruiz-Nava5 José Carlos Jiménez-López6 Francisco A. Solís-Marín7 Alfredo Laguarda-Figueras7 1. Facultad de Ciencias, Universidad Nacional Autónoma de México. Circuito Exterior, C.P. 04510, Ciudad de México, México; [email protected] (*Correspondence), [email protected] 2. Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, C.P. 04510, Ciudad de México, México. 3. Instituto de Geología, Departamento de Paleontología, Universidad Nacional Autónoma de México, Circuito Exterior, C.P. 04510, Ciudad de México, México; [email protected] 4. Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, C.P. 04510, Coyoacán, Ciudad de México, México; [email protected] 5. Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México. Av. de Los Barrios 1, Tlalnepantla de Baz, C.P. 54090, Estado de México, México; [email protected] 6. Posgrado en Ciencias de la Tierra, Instituto de Geología, Universidad Nacional Autónoma de México. Circuito Exterior, C.P. 04510, Ciudad de México, México; [email protected] 7. Colección Nacional de Equinodermos “Dra. Ma. Elena Caso Muñoz”, Laboratorio de Sistemática y Ecología de Equinodermos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, C.P. 04510, Ciudad de México, México; [email protected], [email protected] Received 15-VII-2020. Corrected 09-IX-2020. Accepted 15-XI-2020. ABSTRACT Introduction: In Mexico, there are two recorded living species of Cassiduloida: Cassidulus caribaearum and Rhyncholampas pacifica. Most of the taxonomic studies on cassiduloids have used external morphology, pedicellariae and morphometric characters; however, the intraspecific variation of quantitative and qualitative characters has been poorly evaluated. Objective: To compare the basic morphology of R. pacifica and C. carib- aearum. Methods: We examined a total of 2 158 specimens of R. pacifica and C. caribaearum, selecting 50 to evaluate shape and size with linear regression and Principal Component analysis. We selected an additional 62 specimens per species to identify significant character correlations and morphological groups within species. Results: There is a direct relationship between Test length and Test width. Test height/Test width, and Total length (oral view)/Distance from the ambitus to the peristome apex, are the two main ratios to distinguish both species. C. caribaearum is more dorsoventrally compressed and has a round peristome base; versus R. pacifica has a tall and triangular one. There are four morphological groups of C. caribaearum and two groups for R. pacifica. Conclusions: These two species can be distinguished with reliable morphological characters, in which peristome shape suggests that R. pacifica is more adapted to burrowing deeper into certain types of substratum. Key words: Neognathostomata; Cassiduloida; morphometry; Mexico. Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 423-437, March 2021 (Published Mar. 30, 2021) 423 The order Cassiduloida (sensu Souto, since then (Kier, 1962; Kier, 1974; Suter, Mooi, Martins, Menegola, & Marshall, 2019) 1988; McNamara, Pawson, Miskelly, & Byrne, includes the families Cassidulidae, Eurhodi- 2017). Kier (1962) noticed several morpho- idae, Faujasiidae, Neolampadidae, and Pliol- logical changes within the cassiduloids: abrupt ampadidae (Souto et al., 2019), is represented reduction from two pores to one pore in each by 800 species, most of them fossils and a ambulacral plate beyond the petal and the intro- few living ones (Kier, 1962). One of the most duction of buccal pores (Cenomanian), due to characteristic aspects of these families is that a radical change in the living habits (began to their fossil record, and not the living represen- borrow shallowly into the substratum); and a tatives, contains most of their morphological change in the structure of the apical system diversity. Their variable morphology has made from tetrabasal to monobasal (Maastrichtian), their taxonomic study complicated and pos- probably produced by parallel mutations and sibly denotes that the group is in the process of parallel selections. Recent studies have shown extinction (Suter, 1988). that their evolutionary history has been domi- The cassiduloids first appeared and nated by high levels of homoplasy and a dearth changed from infaunal to epifaunal habits of unique, novel traits (Souto et al., 2019). during the Lower Jurassic (Boivin, Saucède, In Mexico, there exist two living species Laffont, Steimetz, & Neige, 2018; Souto et of cassiduloids: Cassidulus caribaearum and al., 2019). They diversified in the Early Creta- Rhyncholampas pacifica (Buitrón-Sánchez, ceous and survived the K-Pg mass extinction, Solís-Marín, Conejeros-Vargas, & Caballero- were common in the Late Cretaceous and Ochoa, 2019). Cassidulus caribaearum inhab- Early Cenozoic, being more successful in the its warm, shallow waters (26-28 °C), from Eocene (> 40 % of the echinoid diversity), and less than 1 to 18 m in depth, buried up to 20 finally have dramatically declined in number cm in calcareous sand (± 2 000-44 μm) or Fig 1. Distribution map of Cassidulus caribaearum and Rhyncholampas pacifica in Mexico. 424 Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 423-437, March 2021 (Published Mar. 30, 2021) carbonate substratum of the tropical Atlantic being the first study focused on this computa- West coast, and it is probably endemic to the tional approach for cassiduloids. Caribbean Sea (Fig. 1) (Kier, 1975; Gladfel- The test shape is the most important char- ter, 1978; Borrero-Pérez, Benavides-Serrato, acteristic to distinguish between species of & Diaz-Sanchez, 2012; Solís-Marín et al., cassiduloids (Souto et al., 2019). In most of 2013; Solís-Marín, Caballero-Ochoa, Laguar- the studies, the morphological diversity of the da-Figueras, & Durán-González, 2017; Souto order Cassiduloida has been described (Souto et & Martins, 2018). Rhyncholampas pacifica al., 2019); however, the intraspecific variation lives in warm, shallow waters (26-30 °C) of the of the morphological characters of the recent Tropical Eastern Pacific Ocean (Fig. 1). This cassiduloids in Mexico has not been evalu- species lives gregariously and partially buried ated. The objective of this work is to compare to the level of the petaloids on sandy beaches the basic morphological and morphometric at a depth of 2 to 130 m (Agassiz, 1872; Clark, aspects, as well as to evaluate the intraspecific 1925; Mooi, 1990; Solís-Marín et al., 2013; variation of the morphometric characters of R. Caballero-Ochoa, Martínez-Melo, Conejeros- pacifica and C. caribaearum. Vargas, Solís-Marín, & Laguarda-Figueras, 2017; Schultz, 2017). MATERIALS AND METHODS Morphometrics evaluates the size and shape variation of biological forms through sta- Data collection: A total of 2 158 speci- tistical analysis (Ocakoglu & Ercan, 2013). The mens of recent cassiduloids were examined: C. traditional approach involves two-dimensional caribaearum and R. pacifica; these are housed linear measurements such as lengths, widths at Colección Nacional de Equinodermos “Dra. and distances, and angles or ratios; it has been Ma. Elena Caso Muñoz” (ICML-UNAM) in used in taxonomy since it is useful for mak- Mexico (Appendix 1). ing morphological comparisons and establish- ing specific boundaries, as well as assessing Morphometric analyses: We selected 50 growth changes (Ocakoglu & Ercan, 2013; specimens of different sizes of C. caribaearum Remagnino, Mayo, Wilkin, Cope, & Kirkup, and R. pacifica, from 3.3 to 51 mm in length; 2016; MacLeod, 2017). The application of these were randomly selected and were pho- morphometrics on cassiduloid taxonomy dates tographed from the aboral, oral and lateral back to McKinney (1986), who discussed the views. ImageJ software was used to obtain nine heterochronic-ecological relationships between measurements for each specimen: TLa, TW, fossil irregular echinoids, including Rhynchol- Da-ppa, TLo, Da-pta, THl, TWl, PpL, and PpW ampas species. Although Carter and Beisel (Fig. 2, Table 1). A linear regression analysis (1987) did not perform any statistical analysis, was performed to test the relationship between they also considered width/length ratios of the the length and width of the test in GraphPad test for separating Eurhodia, Rhyncholampas Prism. A Principal Component analysis using and Cassidulus species. In addition, Ciampa- Primer-6 software was performed; five ratios glio and D’Orazio (2007) and Martínez-Melo were considered: 1) test length (aboral view)/ (2008) provided insights into the growth tra- test width (at the level of the apical system), jectories and heterochronic processes between 2) test length (aboral view)/distance from the Eurhodia appendiculata, Rhyncholampas caro- ambitus to the periproct apex, 3) test
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