Introduction
Sea urchins form a large group of benthic marine invertebrates belonging to the phylum Echinodermata, which comprises 1013 extant accepted species belonging to 115 genera (Kroh and Mooi, Reference Kroh and Mooi2024), distributed at all latitudes in various marine environments and ranging from the intertidal to the deep sea (Iken et al., Reference Iken, Brey, Wand, Voigt and Junghans2001; Lebrato et al., Reference Lebrato, Iglesias-Rodríguez, Feely, Greeley, Jones, Suarez-Bosche, Lampitt, Cartes, Green and Alker2010). The order Arbacioida Gregory, 1900 includes 26 known extant species and seven recognized genera belonging to a single family, the Arbaciidae Gray, 1855. Within the family, the genus Arbacia Gray, 1835 is distributed from tropical to temperate and sub-Antarctic regions of the Pacific, Atlantic oceans and Mediterranean Sea and comprises six valid species: Arbacia dufresnii (Blainville, Reference Blainville1825), Arbacia lixula (Linné, Reference Linné1758), Arbacia nigra (Molina, 1782) (Gianguzza and Bonaviri, Reference Gianguzza, Bonaviri and Lawrence2013; Courville et al., Reference Courville, Poulin, Saucede, Mooi, Lessios, Martinez Salinas and Diaz2023). Arbacia punctulata (Lamarck, Reference Lamarck1816), Arbacia spatuligera (Valenciennes, Reference Valenciennes1846) and Arbacia stellata (Blainville, Reference Blainville1825; Gianguzza and Bonaviri, Reference Gianguzza, Bonaviri and Lawrence2013).
The species A. spatuligera is located in the Southeastern Pacific Ocean from northern Peru to Puerto Montt, in south-central Chile (Larraín, Reference Larraín1975; Lessios et al., Reference Lessios, Lockhart, Collin, Sotil, Sanchez-Jerez, Zigler, Perez, Garrido, Geyer, Bernardi, Vacquier, Haroun and Kessing2012; Millán et al., Reference Millán, Díaz, Poulin, Merino-Yunnissi and Martínez2019). Valenciennes first described the species in 1846 with reliable and detailed drawings and descriptions for that time. More recent descriptions and figures were published by Koehler (Reference Koehler1914). In 1935, Mortensen mentioned that the species easily distinguished from the other southern species A. dufresnii by its colour, with ‘no green (patches of) nor red colour in the interambulacral – as also by its club-shaped aboral spines’. Larraín (Reference Larraín1975) defined neotypes for A. spatuligera in an extensive monography focused on extant and fossil echinoid species from Chile. He proposed a new detailed description of the species and an extended diagnosis.
Bathymetric records of A. spatuligera indicate that the species occurs in shallow waters above 30 m depth (Larraín, Reference Larraín1975; Lessios et al., Reference Lessios, Lockhart, Collin, Sotil, Sanchez-Jerez, Zigler, Perez, Garrido, Geyer, Bernardi, Vacquier, Haroun and Kessing2012; Gianguzza and Bonaviri, Reference Gianguzza, Bonaviri and Lawrence2013; Millán et al., Reference Millán, Díaz, Poulin, Merino-Yunnissi and Martínez2019). However, due to logistical limitations to recreational scuba diving (Kramer et al., Reference Kramer, Eyal, Tamir and Loya2019), most of the knowledge about the distribution and ecology of A. spatuligera was based on information obtained from shallow areas (<30 m depth).
Mesophotic reef ecosystems (MREs) are considered a continuation of shallow reefs (Hinderstein et al., Reference Hinderstein, Marr, Martinez, Dowgiallo, Puglise, Pyle, Zawada and Appeldoorn2010) with depths up to 150 m in tropical and subtropical latitudes (Rocha et al., Reference Rocha, Pinheiro, Shepherd, Papastamatiou, Luiz, Pyle and Bongaerts2018). They are characterized by the presence of light-dependent organisms and their associated biological communities (Eyal and Pinheiro, Reference Eyal and Pinheiro2020). Along the central coast of Chile, temperate MREs have been poorly studied due to the logistic implications of taking samples in zones that exceed the no-decompression limits for recreational scuba diving (Shreeves and Richardson, Reference Shreeves and Richardson2006). These logistic limitations are reflected by the scarce information available about species' bathymetric ranges, habitat preferences and communities' structures (Kahng et al., Reference Kahng, Garcia-Sais, Spalding, Brokovich, Wagner, Weil and Toonen2010). In order to explore and generate new knowledge about these deep ecosystems, technical dives with closed-circuit rebreathers (CCRs) were performed for the first time over Chilean temperate reefs. As a result, the present work presents novel ecological information about the presence and distribution of the sea urchin A. spatuligera in four temperate MREs of the continental shelf off Chile, in addition to data from two shallow rocky reefs.
Material and methods
In February 2019, April, May, August and September 2022, photographic and video records of the sea urchin A. spatuligera were obtained from four mesophotic rocky reefs: Pichidangui in the Coquimbo Region, two artificial reefs (shipwrecks) and one sandy slope at Valparaíso Bay, between 36 and 63 m depth, nearby the central coast off Chile (Figure 1). Thirty minutes bottom time dives were performed to search for the target species. Photos and videos were taken using a GoPro 9 and a Sony RX100V camera with underwater housing and a light system. A Shearwater Petrel dive computer recorded the depth at which organisms were observed. All dives were made during the day using the JJ-CCR rebreather with different gas mixtures as diluents (air and trimix) according to the maximum depth for each dive (Table 1).
Map of distribution and records of the sea urchin Arbacia spatuligera in shallow (<30 m depth) and mesophotic reefs (36–63 m depth) in the Southeastern Pacific Ocean: the black asterisk represents all previous records in the literature and OBIS.org; (2) the green points represents two locations of the shallow rocky reefs with Macrocystis pyrifera; (3) the orange point is a single location of a mesophotic rocky reef covered by turf algae; (4) the yellow point represents a mesophotic sandy slope; and finally (5) the black-flagged points represent two shipwrecks within the mesophotic reef ecosystem.
Localities surveyed with the sampling year, geographical coordinates, country, reef type, habitat (RRWM, rocky reef with Macrocystis pyrifera; SWCK, shipwreck; RRWCA, rocky reef with calcareous algae; SSWD, sandy slope with debris), depth range, number of organisms, survey technique (VC, visual census; C, collected) diving system and references
We recorded 128 individuals of A. spatuligera in four mesophotic reefs on the central coast of Chile at depths ranging between 36 and 63 m (Table 1). The four reefs presented differences in habitat and light conditions. Large rocks with filamentous algae (turf), sponges, crustose algae (order Corallinales) and channels with sand characterized the rocky reef of Pichidangui. The two shipwrecks in the Bay of Valparaíso lie on a bottom of fine sand and silt with filamentous algae and the striped anemone Anthothoe chilensis (Lesson, 1830) attached to the deck and hull. Light penetration at both sites is limited compared to the Pichidangui rocky reef. The sandy slope presented much plastic debris and abandoned fishing gear, which was used as a substrate for individuals of A. spatuligera. On this site, three individuals of A. spatuligera were observed next to three specimens of the lobed anemone Antholoba achates (Drayton, 1846). The highest abundance of this species was recorded in the rocky reef of Pichidangui at depth ranges between 40 and 58 m. On this site, we found variable numbers ranging from a single individual to an aggregation of 11 sea urchins on the rocky substrate (Figure 2). The artificial reef with the lowest abundance (10 individuals) was the deepest ship at 63 m. The organisms with the smallest recorded size were found on the sandy slope with debris, while the organisms with the largest sizes were observed on the rocky reef of Pichidangui.
Photographic records of Arbacia spatuligera and their habitats in three of four mesophotic temperate reefs off central coast of Chile: (A–C) individuals recorded on deck and hull of a shipwreck between 36 and 46 m deep with the presence of filamentous algae and the striped anemone Anthothoe chilensis; (D–H) individuals recorded on a sandy slope with plastic debris, abandoned fishing gear and a car wheel between 40 and 56 m deep with the presence of filamentous algae and the lobed anemone Antholoba achates; (G) aggregation of 10 individuals; (I–O) individuals from the rocky reef between 40 and 58 m deep with filamentous algae, sponges, crustose algae (order Corallinales) and channels with sand.
Twelve individuals were collected at 53 m depth off Pichidangui (Figure 1) for specimen identification in May 2023. The collected specimens exhibit striking similarities in all aspects to those photographed during the initial fieldwork in 2022 (Figure 2I–O). Samples were preserved in 95% ethanol and prepared for morphological observations and DNA sequencing. To perform morphological observations, tests were cleaned off using a brush and a diluted bleach solution, allowing removal of all spines and soft tissues to reveal the plate patterns. Systematic nomenclature and terminology for morphological description follow Kroh (2020). Plates are numbered according to Lovén's system (Lovén, Reference Lovén1874).
The isolation of DNA, PCR and preparation for Sanger sequencing were performed in the Molecular Ecology Laboratory of the Millennium Institute of Biodiversity of Antarctic and Subantarctic Ecosystems at Universidad de Chile, Chile. DNA was extracted from the spines and gonads preserved in 95% ethanol using the DNeasy Blood & Tissue Kit by QIAGEN. The mitochondrial genome's cytochrome oxidase subunit I (COI) was amplified for seven individuals. COI primers specific to the genus Arbacia were used, ArbaF and ArbaR (Haye et al., Reference Haye, Segovia, Muñoz-Herrera, Gálvez, Martínez, Meynard, Pardo-Gandarillas, Poulin and Faugeron2014). PCRs were performed using Accustart II PCR ToughMix (ref. 95142-800) following notice volumes (for a 50 μl PCR reaction, 5 μl of total genomic DNA, 1 μl of each primer and 25 μl of Taq polymerase). Cycling conditions consisted of an initial denaturation at 94°C for 3 min followed by 40 cycles of 1 min denaturing at 94°C, 45 s annealing at 45°C and a 1 min extension at 72°C, with a final 3 min extension at 72°C. Sequencing was performed in one direction because COI amplification has been successful before for Arbacia (Courville et al., Reference Courville, Poulin, Saucede, Mooi, Lessios, Martinez Salinas and Diaz2023), using automatic sequencers from MACROGEN Chile.
Results
Genetic data
All seven specimens sequenced from Pichidangui correspond to one unique COI haplotype of A. spatuligera, already recorded by Millán et al. (Reference Millán, Díaz, Poulin, Merino-Yunnissi and Martínez2019). The haplotype sequence was deposited in the GenBank database (GenBank accession number: PP733318). It corresponds to the COI haplotype ‘AspaCN1’ (GenBank accession number: MK382495.1), and this haplotype corresponds to the Hap1 on the haplotype network presented by Millán et al. (Reference Millán, Díaz, Poulin, Merino-Yunnissi and Martínez2019) and aligns with the most prevalent haplotype (114 out of 140 individuals; Millán et al., Reference Millán, Díaz, Poulin, Merino-Yunnissi and Martínez2019) within A. spatuligera, found from Concepción (Chile) to Lima (Peru) in shallow water (0–30 m).
Morphological data
The specimens observed along the coasts of Valparaiso (Figure 2A–H) exhibit the typical morphology of A. spatuligera as described by Mortensen (Reference Mortensen1935) and Larraín (Reference Larraín1975): they are characterized by white, short and club-shaped spines on the aboral side and long, and slender spines at the ambitus. The test colouration is light brown, and the interambulacrum is marked by a vestigial bare interambulacral area in larger specimens. In contrast, samples from Pichidangui (Figure 2I–O) were distinguished by long and slender dark brown spines extending adapically along the interambulacrum up to the apical system. The test colouration in these specimens is dark green, which deviates from the typical light brown to light green colouration observed in other studied specimens.
The morphological study of specimens from Pichidangui enabled the identification of diagnostic characters of the species A. spatuligera (Figure 3A–C). It includes a narrow naked interambulacral area reduced to the interradius in larger specimens (Figure 3C), poorly developed aboral ambulacral tubercles that do not reach the ocular plates (Figure 3A), periproctal plates forming a pyramid shape with small and narrow extensions at the tips (Figure 3A) and larger ambulacral pores compared to other species of the genus (Figure 3C). However, specimens from Pichidangui also show unique morphological characters that had been not reported in A. spatuligera so far (Valenciennes, Reference Valenciennes1846; Koehler, Reference Koehler1914; Lovén, Reference Lovén1887; Mortensen, Reference Mortensen1910, Reference Mortensen1935; Agassiz and Desor, Reference Agassiz and Desor1846; Agassiz, Reference Agassiz1872; Agassiz and Clark, Reference Agassiz and Clark1908). Interambulacral tubercles are large, with usually three tubercles per plate of a subequal size above the ambitus and the same size throughout the aboral surface (Figure 3A–C). The adoral area is characterized by shorter phyllodes and a pentagonal peristome (Figure 3B). This population's tags are much smaller, only reaching the second interambulacral plate (Figure 3B). The aboral spines are brown, long and slender, even close to the apical system, and the test shows an overall dark green colouration (Figure 2I–O). These morphological variations have prompted the need for an amended diagnosis to describe and characterize A. spatuligera accurately.
Morphology of Arbacia spatuligera from Chile: (A–G), A. spatuligera from Pichidangui; (A–C), specimen AS_PI1; (A), aboral view; (B), oral view; (C), lateral view; (D), phyllodes and sphaeridial pit; (E), apical system of AS_PI5; (F–G), lateral views of AS_PI6; (H–J), A. spatuligera from Las Cruces, specimen AS_30CL (H), aboral view; (I), oral view; (J), lateral view. Scale bars equal 10 mm.
Systematic part
Phylum Echinodermata Klein, Reference Klein1778
Class Echinoidea Schumacher, Reference Schumacher1817
Order Arbacioida Gregory, Reference Gregory and Lankester1900
Family Arbaciidae Gray, Reference Gray1855
Genus Arbacia Gray, Reference Gray1835
Arbacia spatuligera (Valenciennes, Reference Valenciennes1846)
1846 Echinus spatuliger Valenciennes: pl. 6; fig. 2.
1846 Echinus (Agarites) spatuligera Agassiz & Desor: p. 353.
1872 Arbacia spatuligera A. Agassiz: p. 93; p. 403, pl. 35, fig. 7.
Reference Jackson1912 Arbacia spatuligera Jackson: p. 115; p. 158.
1914 Arbacia spatuligera Koehler: p. 240; pl. 12, figs. 14, 19–20.
1935 Arbacia spatuligera Mortensen: p. 577–579; pl. 70, figs 1–5; pl. 71, fig 6; pl. 87, figs. 1–6.
1975 Arbacia spatuligera Larraín: p. 53 61; figs. 39–53
Emended diagnosis
Arbacia with ambulacral tubercles not reaching the apical system; tip of supra-anal plates with a small and narrow extension; extended phyllodes; naked interambulacral area vestigial even in largest specimens (D > 65 mm); colour brown to green; spines white to light brown.
Type material
The syntype illustrated by Valenciennes in 1846 is supposed to be in the collections of the MNHN – Paris. Vadon et al. (Reference Vadon, Ridder and Jangoux1984) mention A. spatuliger in the list of Echinoid species, whose type or types should be in the collections of the Museum of Paris but have not been found there. A thorough search in the MNHN's zoological collection (2022) did not locate this syntype. Larraín (Reference Larraín1975) defined a neotype, housed in the Museum of the Zoological Department of the Universidad de Concepción, Chile under reference number 7966.
Occurrence
Arbacia spatuligera is found within the Warm Temperate Southeastern Pacific Province (Spalding et al., Reference Spalding, Fox, Allen, Davidson, Ferdaña, Finlayson, Halpern, Jorge, Lombana, Lourie, Martin, McManus, Molnar, Recchia and Robertson2007), spanning a latitude range from 42° to 6°S between Puerto Montt (south-central Chile) and Chiclayo (northern Peru). Mortensen (Reference Mortensen1935) mention the presence of A. spatuligera in Guayaquil, Ecuador, near 2°S latitude, in the Tropical Eastern Pacific Province. However, none of the specimen preserved in the large, extensive collection of the natural history museum comes from Ecuador and this occurrence remains doubtful.
It was initially reported from the subtidal zone, as documented by Mortensen (Reference Mortensen1935), Larraín (Reference Larraín1975) and Millán et al. (Reference Millán, Díaz, Poulin, Merino-Yunnissi and Martínez2019). Our study reveals its presence in deeper mesophotic environments as well.
Emended description
Test circular to subpentgonal in outline at ambitus. Test large, reaching 70–80 mm in diameter. Living specimens dark brown to dark green, with lighter, usually white, spines. Denuded test light green, sometimes deep brown. Allometric relationship between test height and test diameter (Supplementary Material 1) described by linear regression model ln (y) = 1.0543 ln (x)–ln (0.8703); R 2 = 0.9149.
Apical system Small, dicyclic to hemicyclic, with no tubercles (Figure 4A, B). Ocular plates usually exsert (53%) in large specimens (TD > 40 mm), plate V often insert (47%) and plates I rarely insert (5%). Plates I and IV closer to periproct margin. Juveniles always with dicyclic apical system, ocular plates becoming insert with growth. Ocular and genitals free of tubercles in adults. Periproct oval with maximum diameter in direction 1-IV, as it is usually the case in species of the genus Arbacia. Gonopores small, slightly elongated. Ocular plates with numerous ophicephalous pedicellariae, connected to the plate by a small, circular granule.
Arbacia spatuligera, details of test plating. (A–B) apical system: A, small specimen AS_32LC (TD = 30 mm); B, larger specimen AS_6CO (TD = 45 mm); (C) aboral plate of ambulacrum; (D–E) aboral plates of interambulacrum: D, small specimen AS_23CL (TD = 30 mm); E, larger specimen MNHN_6097 (TD = 70 mm). Scale bars equal 10 mm.
Peristome Relative peristome diameter large, usually close to 50% of the test diameter. Buccal notches deep, tags usually long and narrow (spanning up to 3 tubercles), shorter in specimens from Pichidangui (spanning < 2 tubercles). Peristome shape usually characterized by extended phyllodes, resulting in a highly intricate contour of the peristome. Perignathic girdle thin and long, auricles usually not in contact, forming an arch over the perradius. Peristome relative size decreasing with growth. Allometric relationship between peristome diameter and test diameter described by linear regression model ln (y) = 0.70993 ln (x)–ln (0.4006); R 2 = 0.9016.
Ambulacra Narrow (half of the interambulacra), each plate with one imperforate and non-crenulate primary tubercle of the same size as interambulacral ones at the ambitus and quickly decreasing in size adapically. Tubercles spaced aborally, not reaching apical system. Tubercles separated by fine granules at the perradial suture (Figure 4C). Ambulacral plates trigeminate from ambitus to apical system, of arbaciid type aborally, forming more complex compound plating adorally and leading to narrow phyllodes adorally. Aborally, pores of a pair deeply conjugate, and pore-pairs separated by marked ridges. Neural canal poorly developed. Close to peristome, single perradial pit for sphaeridium along perradius of each ambulacrum.
Interambulacra Wide, with up to five imperforate and non-crenulate primary tubercles per plate at the ambitus, all similar in size in large specimens (TD > 70 mm). Smaller specimens (TD < 50 mm) bear three to four tubercles at ambitus (Figure 4D). Tubercles decrease in size above the ambitus. Inner tubercles abutting the oral suture of the plate and usually decreasing in size towards interradius, except for specimens from Pichidangui with subequal tubercles aborally (Figure 3). Adradial column of large primary tubercles reaches the apical system. The second column of tubercles almost reaches the apical system. Tubercles with large mamelons, narrow platforms, and broad areoles, occupying most of plate width at ambitus. Except for naked interradial area, plates coarsely granulated between tubercles. Bare area usually restricted to interradius and vestigial in large specimens (TD > 70 mm). Number of interambulacral plates high, usually between 15 and 16 plates (TD = 40 mm) and 17 plates (TD = 50 mm). Large specimens, reaching 70 mm TD, bears up to 21 interambulacral plates. Height of plates not varying along aboral surface adapically (Figure 4E).
Pedicellariae of three types, ophicephalous, tridentate and triphyllous, abundant over the test. All pedicellariae are white in adult specimens.
Ophicephalous pedicellariae (Figure 5A, B) differentiated between the oral and aboral sides. Aboral surface covered with numerous ophicephalous pedicellariae, including area surrounding the apical system. Valves of ophicephalous pedicellariae circular, narrow and constricted in upper part, with indented and sharply serrated blade edges (Figure 5A). Buccal membrane covered by second type of ophicephalous pedicellariae (Figure 5B) with higher, elongated valves, indented blade edges and slight serration. Upper part of the valve slightly constricted.
(A–D) SEM photographs of valves of pedicellariae of Arbacia spatuligera; A, valve of apical ophicephalous pedicellaria; B, valve of oral ophicephalous pedicellaria; C, valve of apical tridentate pedicellaria; D, valve of apical tridentate pedicellaria. Scale bars equal 300 μm.
Tridentate pedicellariae (Figure 5C–D) small, being only twice as long as ophicephalous pedicellariae. Abundant on both oral and aboral surface, including on ocular plates but absent on buccal membrane. Valves of tridentate pedicellariae slender, elongated and not constricted in the middle. Blade edges finely serrated. Width-to-length ratio varies between 0.51 and 0.63 (Figure 5C–D).
Triphyllous pedicellariae scarce and resemble those found in other Arbacia species, as noted by Agassiz and Clark (Reference Agassiz and Clark1908) and Larraín (Reference Larraín1975). Valves of triphyllous pedicellariae elongated and constricted in middle part. Blade edges finely serrated.
Spines Two morphologies of A. spatuligera spines are known. Typical form with aboral spines short and robust, exhibiting a distinctive ‘club-shaped’ morphology (Mortensen, Reference Mortensen1935); long, and slender at ambitus. Spines length usually equal to test diameter, up to 50 mm. Specimens from Pichidangui with long and slender spines over the entire aboral side, up to apical system. Presence of long and sturdy aboral spines, consistently sized across the aboral surface, linked to the presence of large, equally sized interambulacral tubercles. Ambital and subambital spines with large ‘enameled’ tips. Spines white in typical form, but appear darker, approaching a brown hue in long-spine form.
Remarks
The presence of a well-developed epistroma, of sphaeridiae positioned in adoral pits in each perradius, of imperforate and non-crenulate tubercules, and of a periproct with four anal plates support the assignment of the species to the order Arbacioida. The compound, arbaciid-like plates of ambulacra, the occurrence of tubercles similar in size in both ambulacra and interambulacra at the ambitus, and of a clear difference in tuberculation between the oral and aboral side (aboral tubercles highly reduced in size and number), are diagnostic of the family Arbaciidae. The presence of a straight pore-zone with tube feet not arranged into arcs of three, of ambulacral tubercles forming a regular series throughout, of a large peristome (> 30% of test diameter), of interambulacra with numerous primary tubercles arranged in horizontal and vertical series, of a single sphaeridial pit near the peristomial edge in each interambulacrum, and of straight and finely striated spines with an enameled tip are all diagnostic characters of the genus Arbacia.
Discussion
Specimens of A. spatuligera from Pichidangui depart from the typical morphology of the species formerly described (Mortensen, Reference Mortensen1935; Larraín, Reference Larraín1975), which raises questions about the underlying processes at play. These morphological variations have prompted the need for an amended diagnosis to describe and characterize A. spatuligera accurately. The absence of genetic difference in COI gene between the two morphotypes suggests that morphological differences observed between the specimens from Pichidangui and the typical form are not the result of a species differentiation linked to either geographic isolation or ecological niche evolution in deeper environments. Millán et al. (Reference Millán, Díaz, Poulin, Merino-Yunnissi and Martínez2019) emphasized the absence of genetic structure and unexpectedly low genetic diversity in populations of A. spatuligera over its entire distribution range. Additionally, they found evidence of a recent demographic expansion of the species, estimated to have occurred 33,000–47,000 years ago. This is in line with the unique haplotype found in the studied specimens and the absence of genetic difference identified in COI sequences between the two morphologies.
The observed morphological variations may also result from phenotypic plasticity. The differences in spine length and colour are typical of ecophenotypic variations observed in echinoids. Phenotypic plasticity could be defined as the environmental sensitivity of a genotype to produce alternative phenotypes in response to environmental cues (Fusco and Minelli, Reference Fusco and Minelli2010). Environmental conditions, particularly water currents, frequently influence spine length (Mortensen, Reference Mortensen1943; Gallien, Reference Gallien1987). The occurrence of the studied specimens in a deep and calm environment with reduced tidal influence may have favoured the long spine morphology. The size and density of spines could also play a significant role in providing protection against predators (Smith, Reference Smith1980). The presence of long and sturdy aboral spines, with large, equally sized interambulacral tubercles, can be readily explained by the necessity of these spines to have a substantial, large muscle surface area for attachment (Smith, Reference Smith1980). The quantity of oral tube feet significantly impacts the ability to adhere to the substrate, and the observed reduction in the size of phyllodes in specimens from Pichidangui in a low-energy environment aligns with the ecophenotypic interpretation.
It is important to note that a population of A. spatuligera with a ‘typical morphology’ has also been observed in mesophotic environments along the coasts of Valparaiso (Figure 2A–H) at the same depth as those of Pichidangui. Moreover, another specimen, in all aspects similar to those from Pichidangui, was observed at 60 m depth in Algarrobo, Chile (Figure 6), 200 km away to the south (NUTME 2023 personal communication). Subsequent investigations focusing on the environmental conditions of these specimens, as well as their ecology, coupled with additional genetic studies, will offer further insights into which of these two hypotheses takes precedence.
Arbacia spatuligera new morphotype recorded off Algarrobo, Chile at 60 m deep. Photo credit: Millenium Nucleus for Ecology and Conservation of Temperate Mesophotic Reef Ecosystem (NUTME) 2023.
The bathymetric distribution and habitat preference of the genus Arbacia widely varies depending on the species. For instance, the Atlantic purple sea urchin (A. punctulata) is located at a maximum depth of 255 m (Hill and Lawrence, Reference Hill and Lawrence2003) while A. lixula is well adapted to shallow waters of the upper infralittoral in the Mediterranean Sea and Madeira Island (Roma et al., Reference Roma, Schertenleib, Ramalhosa, Gestoso, Canning-Clode and Lenz2021). On the other hand, the green sea urchin A. dufresnii located from the Pacific Ocean from Puerto Montt (locality where the distribution area of A. spatuligera ends) to the Falkland Islands (Bernasconi, Reference Bernasconi1966) has the deepest distribution of the genus reaching depths of 315 m (Bernasconi, Reference Bernasconi1953).
The present study extends the known bathymetric range of A. spatuligera from 30 to 63 m depth, which is within the range of other species of the genus. No data on the species' density and preferred habitat were available so far. We report that the number of individuals present in each mesophotic reef is low compared to shallow sites in other locations on the Chilean coast (Table 1). For example, in the Biobio region, located ~556 km away from our study area, we have recorded up to 220 individuals in Penco and 188 in Laraquete (personal observation); both localities do not exceed 8 m depth. Habitat preference in shallow locations was consistent with the presence of a rocky bottom and holdfast and blades of giant kelp (Macrosystis pyrifera) and co-occurrence with the black sea urchin A. nigra and the red sea urchin Loxechinus albus (Figure 7).
Shallow records of Arbacia spatuligera in two rocky reefs in the Biobio Region, Chile: (A–B) Laraquete; (C–D) Penco.
The abundance of T. niger in Penco was lower (55 individuals) than A. spatuligera. In the locality of Laraquete, A. spatuligera co-occurred with two species of sea urchins, A. nigra (36 individuals) and L. albus with 12 individuals (Figure 7). In this last locality, individuals of A. spatuligera were also found in beds of the Magellan mussel, Aulacomya atra (Molina, 1782).
Conclusions
The population found off the coast of Pichidangui (Chile) shows a different morphology compared to all other specimens despite the lack of COI sequence divergence. This allows us to amend the diagnosis and description of the species and discuss these variations as potential ecophenotypic adaptation or recent geographical isolation. Arbacia spatuligera has a bathymetric distribution ranging from 5 to 63 m in depth. The species can be found on various bottom types, from rocky reefs with kelps Macrocystis pyrifera and Lessonia spp., filamentous algae, beds of the bivalve Aulacomya atra, to artificial reefs such as shipwrecks and sandy bottoms with hard substrate. It is necessary to continue with studies in this species to determine if there are differences between the feeding habits in shallow and mesophotic organisms. Finally, technical diving using CCRs is a fundamental tool in scientific diving for generating novel ecological knowledge in deep zones below 30 m depth, the recreational diving limit.
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S0025315424000389
Data availability
The data that support this study are available in Supplementary material.
Acknowledgements
We thank the two anonymous reviewers for carefully reading our manuscript and their many insightful comments and suggestions. We thank Alder Carrillo for the photos of Arbacia spatuligera of Penco and Laraquete and Moti from ODC Buceo for collecting specimens at Pichidangui.
Author contributions
Rigoberto Moreno-Mendoza: work conception, data acquisition, analyses, data interpretation, manuscript draft. Erwan Courville: taxonomic identification, molecular data acquisition, photography, manuscript draft. Luis Angeles Gonzalez: analyses, data interpretation, manuscript draft. Julio Duarte-Gutierrez: conception, analyses, data interpretation, manuscript draft. Marc Carulla: data acquisition, photography, manuscript draft. Daniel Malfanti-Bravo: conception, data acquisition, manuscript draft. Andrés Mena-Auladell: data acquisition, manuscript draft. Elie Poulin: molecular data acquisition, manuscript draft. Thomas Saucède: taxonomic identification, manuscript draft. Nuno Simões: data acquisition, analyses, data interpretation, manuscript draft.
Financial support
Thanks are due to BIOGEOSCIENCES, Millennium Institute BASE ICN2021_002 and ECOS-ANID ECOS220008. This research is also the product of a postdoctoral fellowship by CONACYT granted to Luis Enrique Ángeles González with CVU 475262 at Centro de Investigación Científica y de Educación Superior de Ensenada, Baja California (CICESE).
Competing interest
None.
Ethical standards
Not applicable.
