Short Communication |
Corresponding author: Xavier Turon ( xturon@ceab.csic.es ) Academic editor: Tito Lotufo
© 2023 Betzabé Moreno-Dávila, Leonardo Huato-Soberanis, Jaime Gómez-Gutiérrez, Carolina Galván-Tirado, Carlos Sánchez, Teresa Alcoverro, Eduardo F. Balart, Xavier Turon.
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Citation:
Moreno-Dávila B, Huato-Soberanis L, Gómez-Gutiérrez J, Galván-Tirado C, Sánchez C, Alcoverro T, Balart EF, Turon X (2023) Taxonomic identity of Distaplia stylifera (Tunicata, Ascidiacea), a new arrival to the eastern Pacific displaying invasive behavior in the Gulf of California, Mexico. ZooKeys 1157: 109-125. https://doi.org/10.3897/zookeys.1157.95986
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A colonial ascidian of the genus Distaplia caused a mass mortality of the pen shell Atrina maura (Sowerby, 1835) during June 2016 in the southwest of the Gulf of California (Mexico), with a significant socio-economic cost. Tentatively identified in previous works as Distaplia cf. stylifera, a precise taxonomic determination was still lacking. In the present work, based on a detailed morphological study, it is confirmed that this aggressive species is Distaplia stylifera (Kowalevsky, 1874). Originally described from the Red Sea, the species currently has a wide circumtropical distribution (with the exception of the Eastern Pacific to date) and is reported as introduced in parts of its range. The present account thus represents an important range extension of this species. However, when revising the original description and later observations, the reported variability of several characters makes it likely that the binomen is in fact a complex of species, as is common in other ascidians with wide distributions. A complete morphological and genetic study including populations from the entire range of distribution would be necessary to settle the status of D. stylifera. Taxonomic uncertainties hinder a correct interpretation of biogeographical patterns and inference on the origin of the studied population. Nevertheless, the known introduction potential of the species, coupled with an explosive growth in an anthropized environment, and the lack of any previous reports in the Eastern Pacific, strongly suggest that the investigated population represents yet another instance of ascidian introduction. From the point of view of management, its invasive behavior is cause for great concern and warrants mitigation measures.
Ascidian, Gulf of California, introduced species, mass mortality, taxonomy, tunicate
Taxonomic identification of introduced species is a pre-requisite of any meaningful study of their biology and ecology, including correct ecosystem management (
Several species of ascidians, known as sea squirts, are highly successful invaders and cause significant damage, modification, or impact to their new habitats, displacing native species or causing harm in aquaculture farms in several regions of the world (
Eleven introduced species of ascidians have been detected in Mexico and five of them in the Gulf of California (
A rapid population growth of an ascidian, preliminarily identified as Distaplia cf. stylifera, was detected in Ensenada de La Paz starting in June 2015 and causing one year later (June 2016) a mass mortality event on Atrina maura (Sowerby, 1835), a bivalve whose natural populations are harvested and represents an economically relevant income for regional fishermen (
The goal of the present study is to describe the morphology of the ascidian (allegedly D. stylifera) collected in Ensenada de La Paz, BCS, Mexico, and discuss its taxonomic status as compared with previous descriptions of D. stylifera in other regions of the world.
The study area (Bahía de La Paz) is located southeast of Baja California Sur (24°07'05"N, 110°17'08"W and 24°80'85"N, 110°70'18"W) (Fig.
A area of study in Ensenada de La Paz located in the southern part of Bahía La Paz, Baja California Sur, Mexico B both bodies of water are located on the southwest coast of the Gulf of California, Mexico C sampling sites and potential sources of dispersal of tunicates (circles) [FONATUR (Fidepaz) (24°07'3"N, 110°20'47"W), del Palmar (24°09'09"N, 110°19'39"W), Abaroa (24°09'11"N, 110°19'36"W), La Paz (24°09'17"N, 110°19'31"W), Cortéz (24°09'19"N, 110°19'26"W), Palmira (24°10'58"N, 110°18'09"W) and Costa Baja (24°13'07"N, 110°18'12"W)].
Colonies of the three different color morphs (white, orange, and purple) of Distaplia cf. stylifera were collected with autonomous diving, using a spatula to extract the colonies from the substrate in four sampling sites of Ensenada de La Paz BCS (24°8'01"N, 110°23'26"W; 24°7'29"N, 110°22'25"W; 24°8'41"N, 110°21'52"W; 24°9'31"N, 110°20'16"W) during December 2017, June 2021, and October 2021, to investigate the identity of the species that caused the mass mortality event of pen shells Atrina maura (
Morphological observations were carried out on relaxed and preserved material using a stereomicroscope with mounted digital camera. Staining was performed when necessary, using Masson’s Hemalum. These morphological observations were compared with relevant descriptions from the literature (see Discussion).
For molecular analyses, zooids from 12 ascidian colonies with white, orange, and purple coloration were dissected and their digestive tracts removed to minimize contamination. Their genomic DNA was extracted using the Qiagen DNeasy Blood & Tissue kit (Qiagen, Valencia, CA), following the manufacturer’s protocol. To amplify a fragment of the mitochondrial Cytochrome Oxidase I (COI) gene, different primer sets were used, either universal (
Didemnium styliferum Kowalevsky, 1874: 443, pl. 30, figs 1–16.
Holozoa bursata Van Name, 1921: 366–368, figs 44–47.
Distaplia bursata
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Distaplia mikropnoa
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Distaplia stylifera
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Polyclinum mikropnous
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CEAB.ASC.DIST–001: Ensenada de La Paz, Mexico; two purple colonies, one as epibiont on sea pen A. maura and one attached to a PVC pipe, 1–3 m depth, 03/Dec/2017. CEAB.ASC.DIST–002: Ensenada de La Paz, Mexico; two white colonies, one epibiont on A. maura and one attached to a buoy, 1–3 m depth, 03/Dec/2017. CEAB.ASC.DIST–003: Ensenada de La Paz, Mexico; three orange colonies epibiont on A. maura, on a rope and on a buoy, 1–3 m depth, 03/Dec/2017. CEAB.ASC.DIST–004: Ensenada de La Paz, Mexico; three orange colonies attached to wooden yacht docks, 0.5 m depth, 19/Jun/2021. CEAB.ASC.DIST–005: Ensenada de La Paz, Mexico; three purple colonies attached to wooden yacht docks, 0.5 m depth, 19/Jun/2021. CEAB.ASC.DIST–006: Ensenada de La Paz, Mexico; three white colonies on wooden yacht docks, 0.5 m depth, 19/Jun/2021. CEAB.ASC.DIST–007: Ensenada de La Paz, Mexico; eight orange colonies on wooden yacht docks, 0.5 m depth, 9/Jul/2021. All the colonies examined in the present study have been deposited in the Biological Collection of the Center of Advanced Studies of Blanes (CEAB) with voucher codes CEAB.ASC.DIST–001 to 007.
Colonies can be mushroom-like with orange color and white mottles marking the common cloacal apertures (Fig.
The zooids are up to 5 mm in length (excluding the gonadal sacs) (Fig.
The thorax has a smooth-rimmed oral siphon (or with six slight lobulations), with a large atrial aperture exposing most of the branchial sac. An atrial languet, often consisting of a wide flap-like lid with smooth or lobed margins, is placed at the top of the atrial aperture (Figs
Distaplia stylifera A zooid (thorax and abdomen) B abdomen C larva. Abbreviatures: a. anus; am. ampullae; ap. adhesive papillae; oc. ocellus; o. oocyte; pv. parastigmatic vessels; pg. pyloric gland vesicle; sc. statocyte, sg. stigmata; st. stomach; t. testes. Scales bars: 1 cm (A); 0.5 mm (B, C).
The abdomen has an elongated and curved stomach. Its wall is marked by fine plications (> 20 per side) that, in section, are visible in both the outer and the inner surface of the wall (Figs
The gonads lie in a pedunculated sac, with one well-formed oocyte (sometimes a smaller second one) at the bottom and a cluster of five or six elongated or wedge-shaped testes placed vertically. The common sperm duct arises posteriorly from the cluster of testes, but turns anteriorly at its very beginning, without overlapping the oocytes (Figs
All Distaplia colonies examined had larvae incubating in long sacs that reach posteriorly deeper than the zooids themselves in the colonies. Usually, several larvae can be seen in the brooding sacs, containing up to two well-formed larvae plus three embryos. Larvae are ~ 1.3 mm length, and when fully developed their body become elongated, reaching up to 1.5 mm in trunk length. Larvae possess three adhesive papillae, two dorsal and one ventral, with a globular ampulla each in the stalks. The oozooid is well-formed, with four rows of stigmata already present and an incipient abdomen folded under the branchial sac (Figs
Distaplia stylifera was described in the Red Sea (
Sites of previous records of Distaplia stylifera: 1) Red Sea,
Despite obtaining positive amplifications with all the primer pairs assayed, no sequence could be obtained that blasted with ascidian mitochondrial COI. Our sequences were closer to algae, mycoparasites or bacteria with an 80–83% similarity. These results may be due to the presence of mutations in the binding sites or contamination. However, we consider contamination unlikely given the care taken during the extraction of the samples.
The taxonomy of the genus Distaplia is mainly based on characters such as colony shape, arrangement of zooids in systems, presence or not of gonadal sac, stigmata per row, stomach shape and external surface, and muscle arrangement (
However, the descriptions of D. stylifera reported in the literature are not entirely consistent in several morphological characteristics. As is common in widespread colonial ascidians, it is possible that worldwide reports of D. stylifera encompass a group of closely related species. One critical diagnostic morphological characteristic is the presence or absence of parastigmatic vessels. All the colonies collected at Ensenada de La Paz had parastigmatic vessels.
Several authors reported D. stylifera testis with as many as 15 oval follicles (
We consider that these variable morphological characters (presence or absence of parastigmatic vessels, number and shape of testes and sperm duct, gonadal pouch stalked or not stalked) indicate that several species have been mixed under the taxonomic name D. stylifera, as suggested also by
Unfortunately, we could not obtain sequences of our colonies. There are no sequences of Distaplia stylifera available in GenBank and BOLD public databases, either. COI data for the single well-represented species of Distaplia in these databases, D. bermudensis Van Name, 1902, revealed divergences ~ 14–20% for different morphotypes and distribution areas. This indicates either high intraspecific variability or the existence of multiple species under D. bermudensis binomen, as suggested by some authors (
Interestingly, the species (or some members of the species complex if it proves to be so) has been likely introduced in some parts of its distribution. In western Atlantic it is found from North Carolina to Brazil.
Albeit taxonomic uncertainty impedes sound interpretation of biogeographical patterns, given the mass mortality event of pen shells in Ensenada de La Paz caused by D. stylifera, it can behave as a typical impactful invasive species. This fact, coupled with a likely previous introduction history in the Western Atlantic and the lack of reports in the Eastern Pacific, strongly suggests that it is a new arrival to the Gulf of California. The species was first noticed by
We gratefully acknowledge to CONACyT 421011/263861 PhD scholarship to BBMD. J.G.-G. is a COFAA-IPN fellow, EDI-IPN, and J.G.-G, C.G.T., C.S. and E.F.B. are SNI fellows. Partial funding was provided by project MARGECH (PID2020-118550RB, MCIN/AEI/10.13039/501100011033) from the Spanish Government.