Research Article |
Corresponding author: Charles L. Griffiths ( charles.griffiths@uct.ac.za ) Academic editor: Yves Samyn
© 2015 Robyn P. Payne, Charles L. Griffiths, Sophie von der Heyden, Erich Koch.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Payne RP, Griffiths CL, von der Heyden S, Koch E (2015) The cushion–star Parvulastra exigua in South Africa: one species or more? ZooKeys 524: 1-16. https://doi.org/10.3897/zookeys.524.6145
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The cushion–star Parvulastra exigua (Lamarck, 1816) is a widely distributed member of the temperate intertidal fauna in the southern hemisphere. In South Africa, it occurs in sympatry with the endemic Parvulastra dyscrita (Clark, 1923), the two species being differentiated predominantly by gonopore placement. Several recent studies have suggested that there may be additional cryptic species within the P. exigua complex in South Africa, based variously on color morphology, genetic evidence and the differential placement of the gonopores. This paper attempts to resolve whether one or more species are represented within P. exigua. A total of 346 P. exigua and 8 P. dyscrita were collected from sites on the west and south–west coasts of South Africa; morphological, anatomical and genetic analyses were performed to determine whether cryptic species and/or P. exigua specimens with aboral gonopores were present. Results show that neither cryptic species nor P. exigua specimens with aboral gonopores occur at these sites. This study thus refutes previous claims of the existence of aboral gonopores in South African P. exigua, and suggests that a single species is represented. The distinction between P. exigua and P. dyscrita is also confirmed, and features separating these two species are clarified and documented.
Cryptic species, gonopore, Parvulastra dyscrita , Parvulastra exigua , Patiriella , starfish
The dwarf cushion–star Parvulastra exigua (Lamarck, 1816) is a prominent and widespread member of the temperate intertidal fauna in the southern hemisphere (
Step in taxonomic history | Performed by |
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P. exigua first described as Asterias exigua. |
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Asterina exigua Lamarck found to be conspecific with Asterina kraussii Gray and Asteriscus pentagonus Müller & Troschel. |
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Oral gonopore placement of Asterina exigua first noted. Oral gonopore placement of Asterina exigua confirmed. |
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Asterina exigua moved into the new genus Patiriella (often ignored by later authors). |
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A new species with aboral gonopores, Asterina dyscrita described; suggestion made that it may only be a variety of Asterina exigua. |
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Asterina dyscrita placed into synonymy with A. exigua. |
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Asterina (Patiriella) exigua reviewed; it was proposed that there was a second species within exigua with aboral gonopores. |
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It was suggested that the species with aboral gonopores was Asterina dyscrita and moved to the genus Patiriella due to morphological similarity with Patiriella exigua. |
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Patiriella exigua and Patiriella dyscrita moved to the new genus Parvulastra which is distinguished from Patiriella based on ray width, ray plate alignment and is supported by previous molecular studies conducted by |
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Parvulastra exigua and Parvulastra dyscrita were confirmed to be two separate species based on morphological (external gonopore position) and molecular evidence (mtDNA COI). Another species that only occurs in Kommetjie was recognized within P. exigua, but no species description was recorded. |
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While the larger P. dyscrita has a fairly consistent mottled coloration (Fig.
Abactinal (A) and actinal (B) view of Parvulastra exigua, with equivalent views of Parvulastra dyscrita (E, F), with the P. exigua mottled color morph found on the east coast of South Africa (C) and an adult P. exigua laying sticky eggs via oral gonopores onto the underside of a rock (D). All photos by C.L. Griffiths; individuals not to scale, with approximate sizes given in Table
Contrary to her expectations,
The major differentiating features between P. exigua and P. dyscrita are the position of the gonopore and reproductive mode. Parvulastra exigua is an ovipositor that spawns predominantly from August to October (
However, in
The studies of both
Where possible, 90 starfish were collected during low spring tide from intertidal rocky shores at each of four main collecting sites (Fig.
Number of starfish collected per sampling location. Brackets indicate the number of Parvulastra dyscrita collected.
Coast | Location | High | Medium | Low | Sand | Total |
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West | Britannia Bay (B) | 33 | 31 | 2 | – | 66 |
Langebaan Lagoon (L) | – | – | – | 9 | 9 | |
Kommetjie (Ko) | 33 | 30 | 33 | – | 96 | |
South–west | Kalk Bay (Ka) | 30 | 30 | 34(6) | – | 94 |
Strandfontein (S) | – | – | 2 (1) | – | 2 | |
Macassar (M) | – | – | (1) | – | 1 | |
Hermanus (H) | 33 | 32 | 30 | – | 95 | |
Total | 363 |
The oral and aboral surface of each specimen was photographed after collection to document the color pattern of each starfish. After preservation in 70% ethanol, several qualitative and quantitative characteristics, based predominantly on previous taxonomic descriptions from both known species, were recorded, using a dissecting microscope and digital caliper respectively (Table
Starfish characteristics examined per specimen and used in multivariate analyses.
Characteristic | Technique | |
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Quantitative | R/r | Expression of body proportion. R = greater radius measured along the ambulacral groove. r = smaller, interambulacral radius. Both measured along three non–deformed arms per specimen and averaged. |
Peristomial membrane diameter | Used as an expression of body size. Measured twice per specimen and averaged. | |
Madreporite diameter | Measured twice per specimen and averaged. | |
Papulae diameter | Five diameters measured per specimen and averaged. | |
Oral plate spines | Number of oral plate spines. | |
Oral plate erect spinulation | Number of erect spines per oral plate. | |
Oral marginal plate spinulation | Number of oral marginal spines. | |
Qualitative | Color morph | Green or mottled. |
Abactinal surface spinulation | Described as having either fine, short columnar or coarse, granuliform globose spinelets. | |
Abactinal surface texture | Either clusters of spinelets, or evenly granular surface texture. | |
Adradial actinal spinulation | Absent or present. Where present, noted whether these spines occurred in more, or less than, three arms. | |
Furrow/Ambulacral spinulation | Classified according to relative number of plates with one spine, as well as the presence or abundance of three spines per plate. | |
Actinal intermediate plate spinulation | Classified according to the relative number of plates with one or two spines, starting position of the plates with two spines and the presence of plates with three spines. | |
External visible gonopore position | Having either oral gonopores or none (aboral gonopores are difficult to observe). | |
Gonopore position by dissection | Dissected to determine gonad placement and definitively document gonopore position. |
Overall, 354 specimens were included in the multivariate analyses, which were performed on unstandardised and untransformed characteristic data using PRIMER v.6.1.5 (Plymouth Routines in Multivariate Ecological Research;
Shape and color pattern of four specimens from each of the seven groups of seven specimens as defined in Table
Specimen groups selected for genetic analyses. Each group comprises seven individuals identified on an MDS.
Group | Description |
1. Mottled | Individuals from south–west coast with variegated coloration. |
2. Green | Individuals from west coast with green coloration. |
3. Orange | Individuals from west coast with orange coloration. |
4. Two oral plate spines | Individuals with two oral plate spines, as opposed to the four observed in most specimens collected. |
5. Langebaan | Individuals from a sandflat habitat with deep aboral ‘dents’ and peculiar abactinal surface spinulation. Some also appear non–pentagonal. |
6. Peculiar | Individuals with atypical coloration, shape, size etc. |
7. Parvulastra dyscrita | Outgroup included for comparison. |
The one–way ANOSIM (analysis of similarity) routine was performed to determine whether possible specimen groupings are associated with any of the documented characteristics, with the significance of the statistical tests assigned at the 5% level. Thereafter, SIMPER (similarity percentage analysis) was used to determine the characteristics that contribute to at least 90% of the difference between divergent cluster groups.
Overall, 49 specimens were selected for genetic analyses (Fig.
A partial section of the mtDNA cytochrome oxidase I gene was amplified by PCR, using a combination of primers; the invertebrate primers LC01490 and HCO2198 (
Geneious v.6.1.6 was used to build an unrooted neighbor–joining tree with bootstrap support from consensus sequences that had a final length of 345 bp. Sequences were also analyzed using TCS v.1.21. (
Of the 354 specimens included in the analysis, eight were identified as Parvulastra dyscrita and the remainder as Parvulastra exigua. The two species are morphologically distinct (Fig.
Characteristics that distinguish P. exigua from P. dyscrita, based on published literature and measurements taken during the present study.
Characteristic | P. exigua | P. dyscrita | Source | |
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Quantitative | Size; R/r | Small, up to 20 mm; 1.07–1.83 | Larger, up to 40 mm; 1.16–1.45 |
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Peristomial membrane diameter (mm) | 1.26–6.10 | 4.70–7.15 | – | |
Madreporite diameter (mm) | 0.19–2.92 | 2.27–4.62 | – | |
Papulae diameter (mm) | Large; 0.07–0.28 | Small, numerous; 0.13–0.26 |
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Oral plate spines | Two, four or variable. | Four or more, often variable. | – | |
Oral plate erect spinulation | Two tall oral spines per plate, often consisting of two spines in the place of one. | Two tall oral spines per plate, often consisting of ‘bunches’ of spines in the place of one. |
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Oral marginal plate spinulation | Three–five spines per plate, or a combination. | Five–seven spines per plate, or a combination. |
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Qualitative | Abactinal surface coloration | Dull khaki–green, orange, blue, brown and orange–shouldered on the west coast of South Africa. Variegated (often geometrical) patterns on the south and east coast, including most color combinations. | Mottled shades of pale pink, white, purple and maroon. |
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Actinal surface coloration | Variable; not consistently blue–green. | Not consistently blue–green; bluish yellow. |
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Abactinal surface spinulation | Fine, short columnar. | Coarse, granuliform globose. |
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Abactinal surface texture | Clusters of spines. | Evenly granular. |
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Adradial actinal spinulation | Absent. | Often present. |
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Furrow/ Ambulacral spinulation | Two (often three) slender, short spines. | Two (often three) slender, short spines. |
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Actinal intermediate plate spinulation | Each plate with only one or two spines, with the latter occurring more frequently distally. | Many plates with two spines each, some with three. |
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Subambulacral spines | Tall, thick, pointed spine on each adambulacral plate. | Large, blunt, truncate spine on each adambulacral plate. |
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External visible gonopore position | Oral or none. Often difficult to detect. |
None. Difficult to detect. |
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Gonopore position | Oral–two in each interradius, separated from oral plates by approximately three actinal plates. | Aboral. |
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All collected P. dyscrita specimens had muted shades of pink, white, brown and turquoise on the abactinal surface, with a bluish–yellow color orally (Fig.
Representative individuals of P. exigua collected from the various study sites are depicted in Fig.
As can be identified in Fig.
Non–metric MDS ordination of all specimens analyzed. Two clear clusters displayed which represent the species Parvulastra dyscrita on the left, and the species Parvulastra exigua on the right. Circles indicate 75% similarity. The specimen causing a cluster overlap is of the species P. exigua, but has many of the morphological characteristics associated with P. dyscrita due to its large size and possibly collection location.
Parsimony haplotype network for (A) 37 Parvulastra exigua and (B) 7 Parvulastra dyscrita specimens. Circle size relates to the frequency of each haplotype, with color indicating origin of the individuals. Smallest circles represent one individual and one haplotype. Extinct or not sampled haplotypes are marked by a blue dot and each line represents one mutational step.
Within the P. exigua cluster (Fig.
Parvulastra dyscrita and P. exigua show a clear separation, based on morphology, anatomy and genetics, unambiguously confirming them to be two distinct species. The differences in characteristics of the two species supports those defined in earlier taxonomic work (Table
The clear separation of these two species confirms
All P. exigua specimens collected exhibited oral gonopores, with only slight morphological differences in oral plate spines and abactinal surface spinulation, but no separation great enough to indicate the presence of a cryptic species. This was confirmed by molecular analyses; the haplotype network shows little genetic variation within P. exigua sampled at different localities, tidal height or specimen group.
After no P. exigua specimens from our original samples were found to have aboral gonopores, a further 200 P. exigua individuals were collected from Mouille Point, a location where a museum specimen with supposed aboral gonopores had been collected previously and examined by
Financial support was provided via a grant to C.L. Griffiths from the National Research Foundation SEAChange Programme. We are also grateful to Dr Rob Smith, Gilly Smith, Saachi Sadchatheeswaran and Michael Payne for assistance with specimen collection. Two anonymous reviewers are acknowledged for their constructive comments.