Research Article |
Corresponding author: Oscar Lisi ( olisi@unict.it ) Academic editor: Sandra McInnes
© 2017 Oscar Lisi, Anisbeth Daza, Rosana Londoño, Sigmer Quiroga.
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:
Lisi O, Daza A, Londoño R, Quiroga S (2017) Echiniscidae from the Sierra Nevada de Santa Marta, Colombia, new records and a new species of Bryodelphax Thulin, 1928 (Tardigrada). ZooKeys 703: 1-14. https://doi.org/10.3897/zookeys.703.12537
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Three species of Echiniscus are recorded for the first time from Colombia: Echiniscus dariae, Echiniscus kofordi, and Echiniscus perarmatus. In addition, the description of the new species Bryodelphax kristenseni sp. n., is mainly based on the presence of ten paired plus two unpaired granularly sculptured ventral plates, the dorsal plate ornamentation with superficial irregular pores, no spine on the anterior legs, and the hind legs without papillae or dentate collar.
Biodiversity, Bryodelphax kristenseni sp. n., Echiniscus , Heterotardigrada , water bear
To date, only ten species of Echiniscidae Thulin, 1928, have been reported from Colombia: Echiniscus bigranulatus Richters, 1908a, Echiniscus blumi Richters, 1903 sensu lato, Echiniscus madonnae Michalczyk & Kaczmarek, 2006, Echiniscus quadrispinosus Richters, 1902 sensu lato, Echiniscus spiniger Richters, 1904, Echiniscus testudo (Doyère, 1840), Echiniscus virginicus Riggin, 1962, Echiniscus wendti Richters, 1903, Pseudechiniscus novaezeelandiae (Richters, 1908b) sensu lato, and Pseudechiniscus suillus (Ehrenberg, 1853) (
This survey was based on tardigrade specimens deposited in the Centro de Colecciones Biológicas de la Universidad del Magdalena under the catalogue acronym CBUMAG:TAR. The material was collected between 2011 and 2012, from different localities (San Lorenzo, Bella Vista, and Medium basin of Garupal River) in the Sierra Nevada de Santa Marta, Colombia, from 543 and 2,200 m a.s.l. All specimens were preserved on slides in Hoyer’s medium.
Tardigrades were examined using a Phase Contrast Microscope (PCM) Zeiss Axiolab A1 with an adapted digital camera Zeiss AxioCam ERc 5s used for the photographic records, and a Differential Interference Contrast Microscope (DIC) Zeiss Axio Scope A1. The measurements were acquired with the software Zeiss AxioVision SE64. The sc ratio is the ratio of the length of a given structure to the length of the scapular plate (
For evaluations at genus level regarding Bryodelphax, the following material was examined from the Pilato and Binda collection: Bryodelphax brevidentatus Kaczmarek, Michalczyk & Degma, 2005 (paratype, slide No. 5386), Bryodelphax meronensis Pilato, Lisi & Binda, 2010 (holotype, slide No. 5350 and a paratype, slide No. 5347), Bryodelphax parvulus Thulin, 1928 (from Israel, slide No. 5348; from northern Italy, slide Nos. 1288, 1290–91; from Morocco, slide No. 1280; from central Sicily, slide No. 1880, and from Ustica island, about 60 km north of Sicily, slide No. 1296), Bryodelphax mateusi (Fontoura, 1982) (holotype, slide No. 5062).
21 specimens, CBUMAG:TAR:00068 (1 specimen), 00085 (11 specimens), 00098 (2 specimens), 00099 (2 specimens), 00101 (1 specimen), 00102 (2 specimens), 00103 (2 specimens). Microhabitat: mixture of a moss from the family Meesiaceae and lichens of the genera Hypotrachyna, Usnea, Parmotrema, Parmelinopsis, growing on tree trunks. Localities: San Lorenzo, Sierra Nevada de Santa Marta, 11°06'20.0"N, 74°03'54.4"W, 1930 m a.s.l, and Bella Vista Sierra Nevada de Santa Marta, 11°05'47.8"N, 74°05'04.4"W, 2200 m a.s.l.
The morphological features of the specimens correspond with the description of E. dariae (Kaczmarek & Michalczyk, 2010), a species that has only been reported for the Neotropical region; with the type locality of Costa Rica, and Peru (
This is the first record of this species for Colombia.
11 specimens, CBUMAG:TAR:00143 (5 specimens), 00144 (6 specimens). Microhabitat: lichen from the genus Parmotrema growing on a tree trunk. Locality: Medium basin of Garupal River, Sierra Nevada de Santa Marta, 10°13'48.4"N, 073°48'01.5"W, 543 m a.s.l.
These specimens were compared with the holotypes of E. walteri Pilato & Lisi, 2003 and E. kofordi Schuster & Grigarick, 1966 deposited in the Binda and Pilato collection (Catania, Italy), concluding that the specimens corresponded perfectly with E. kofordi. This species has a wide distribution; with the type locality Santa Cruz Island (Galápagos Islands, Ecuador), it has been recorded from India (Andaman Islands), United States, Mexico, Costa Rica, and Venezuela (
This identification provides the first record for Colombia.
21 specimens, CBUMAG:TAR:00098 (7 specimens), 00099 (10 specimens), 00101 (4 specimens). Microhabitat: lichen from the genus Parmotrema, growing on a tree trunk. Localities: Bella Vista, Sierra Nevada de Santa Marta, 11°05'47.8"N, 74°05'04.4"W, 1930 m a.s.l.
The morphological characters of the Colombian specimens agree with the original description of E. perarmatus (Murray, 1907). This species, according to the literature, has a tropical and subtropical distribution; with the type locality, Cape Colony (South Africa), it has also been recorded in Indonesia, Hawaii, United States, and Venezuela (
This is the first record (sensu lato) for Colombia.
Holotype and 10 paratypes extracted from a sample composed of lichen (Parmotrema), liverworts (Frullania, Plagiochila), and mosses (Calymperaceae, Amblystegiaceae). The sample was collected in 2011 at the medium basin of Garupal River, Sierra Nevada de Santa Marta, 10°13'48.4"N, 073°48'01.5"W, 543 m a.s.l.
Four additional specimens, CBUMAG:TAR:00198 (1 specimen), 00100 (3 specimens), collected in 2012 from Bella Vista, Sierra Nevada de Santa Marta, 11°05'47.8"N, 74°05'04.4"W, 1,930 m a.s.l. The microhabitat was a lichen from the genus Usnea.
Type repository: The holotype and paratypes are deposited in the Centro de Colecciones Biológicas de la Universidad del Magdalena (CBUMAG), Santa Marta, Colombia. Slide numbers: Holotype (mature female) CBUMAG:TAR:00143-8; Paratypes: CBUMAG:TAR:00137 (3 specimens: 1 juvenile and 2 mature females), 00138 (5 specimens: 1 larva and 4 mature females), 00143 (1 specimen: mature female), 00144 (1 specimen: juvenile).
Small Bryodelphax with ten paired plus two or three unpaired ventral plates (IX/X:2-(1)-4-4-2-4-2-1-2-1 according to
Body colourless, eyespots absent or not visible after mounting. Total body length, 126.5 µm. Scapular and terminal plate not distinctly divided but unsculptured folds indicate the different portions of the plates (Fig.
Bryodelphax kristenseni sp. n. A habitus and dorsal cuticular plates (paratype CBUMAG:TAR: 00137-2; the arrow indicates the caudal portion of the third median plate) B scapular plate of the holotype, the ornamentation is visible (the specimen is oriented with the head pointing left) C ventral surface of the holotype, with several ventral plates visible (arrows indicate those that are better visible) D internal claw spurs (arrow a), and granular sculpture of the ventral plates (arrows b) (paratype CBUMAG:TAR:00144-7). Scale bars: 10 µm (A–C); 5 µm (D).
All plates show apparent double sculpture: big pores more or less irregular in size and distribution, often fused to one another (Fig.
The cuticular pillars (Fig.
Ventral plates present, but faint and difficult to observe, consist of ten paired plus two unpaired (IX/X:2-(1)-4-4-2-4-2-1-2-1 according to
Apart from the cephalic cirri, only the lateral filament A is present (26.5 µm long = 21.0% of body length and 150.7% of the scapular plate length). Internal cephalic cirrus 8.0 µm long; external cephalic cirrus 11.5 µm long; cephalic papilla 4.0 µm long; clava c. 4.7 µm long (Table
Spines on the first pair of legs absent or not visible under PCM. The dentate collar on the fourth pair of legs absent (but the sculptured platelet of the dentate collar present). No papilla visible on the hind legs under PCM. External claws smooth. Internal claws with spur oriented towards the base (Fig.
Measurements (µm) and %bo %sc values of selected morphological structures of the hotolotype and paratypes of Bryodelphax kristenseni sp. n.
CHARACTER | N | MIN – MAX | MEAN | SD | HOLOTYPE | ||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
µm | %bo | %sc | µm | %bo | %sc | µm | %bo | %sc | µm | %bo | %sc | ||||||||
Body length | 10 | 106 | – | 131 | 121.1 | 9.1 | 126.5 | ||||||||||||
Scapular plate length | 10 | 16.2 | – | 21.7 | 13.9 | – | 19.4 | 20.4 | 16.4 | 1.9 | 1.5 | 17.6 | 13.9 | ||||||
Lateral appendage A | 8 | 24.8 | – | 27.2 | 18.8 | – | 24.0 | 115.9 | – | 163.5 | 26.5 | 21.4 | 129.0 | 0.8 | 1.8 | 15.9 | 26.5 | 21.0 | 150.7 |
Clava | 5 | 3.8 | – | 4.8 | 3.4 | – | 4.3 | 15.7 | – | 26.3 | 4.7 | 3.7 | 19.0 | 0.4 | 0.3 | 4.0 | 4.7 | 3.7 | 21.0 |
Int. cephalic cirrus | 9 | 6.6 | – | 8.3 | 5.2 | – | 7.0 | 31.9 | – | 45.5 | 8.0 | 6.3 | 39.0 | 0.7 | 0.5 | 4.0 | 8.0 | 6.3 | 45.5 |
Ext. cephalic cirrus | 10 | 9.5 | – | 13.1 | 8.5 | – | 10.6 | 51.7 | – | 65.4 | 11.4 | 9.2 | 56.3 | 1.0 | 0.7 | 4.7 | 11.5 | 9.1 | 65.4 |
Cephalic papilla | 7 | 3.5 | – | 4.5 | 3.1 | – | 3.8 | 19.3 | – | 25.6 | 4.1 | 3.4 | 21.2 | 0.4 | 0.2 | 2.2 | 4.0 | 3.2 | 22.8 |
Ext. claw I | 9 | 5.3 | – | 6.4 | 4.7 | – | 5.6 | 28.6 | – | 34.2 | 6.2 | 4.9 | 29.9 | 0.4 | 0.3 | 2.1 | 6.0 | 4.7 | 33.8 |
Int. claw I | 8 | 5.6 | – | 7.0 | 5.0 | – | 5.9 | 30.4 | – | 36.2 | 6.6 | 5.3 | 32.2 | 0.5 | 0.3 | 2.2 | 6.4 | 5.0 | 36.2 |
Spur | 8 | 1.0 | – | 1.3 | 1.2 | 0.1 | 1.1 | ||||||||||||
Spur/Claw | 0.2 | – | 0.2 | 0.2 | 0.0 | 0.2 | |||||||||||||
Ext. claw II | 7 | 5.1 | – | 6.3 | 4.5 | – | 5.6 | 27.3 | – | 32.9 | 5.8 | 4.7 | 28.7 | 0.4 | 0.4 | 1.9 | 5.8 | 4.6 | 32.9 |
Int. claw II | 6 | 5.5 | – | 6.6 | 4.7 | – | 5.1 | 23.7 | – | 31.7 | 6.0 | 5.0 | 26.2 | 0.5 | 0.1 | 3.0 | 6.0 | 4.7 | 26.9 |
Spur | 7 | 0.9 | – | 1.1 | 1.1 | 0.1 | 1.0 | ||||||||||||
Spur/Claw | 0.1 | – | 0.2 | 0.2 | 0.0 | 0.2 | |||||||||||||
Ext. claw III | 7 | 4.4 | – | 6.3 | 4.2 | – | 5.5 | 25.0 | – | 31.7 | 6.0 | 4.7 | 28.5 | 0.7 | 0.4 | 2.2 | 5.6 | 4.4 | 31.7 |
Int. claw III | 4 | 5.2 | – | 6.4 | 4.7 | – | 5.7 | 29.1 | – | 33.6 | 6.1 | 4.8 | 29.7 | 0.6 | 0.5 | 2.1 | 5.9 | 4.7 | 33.6 |
Spur | 4 | 1.0 | – | 1.2 | 1.1 | 0.1 | 1.1 | ||||||||||||
Spur/Claw | 0.2 | – | 0.2 | 0.2 | 0.0 | 0.2 | |||||||||||||
Ext. claw IV | 6 | 5.2 | – | 7.2 | 4.9 | – | 6.0 | 29.1 | – | 35.2 | 6.5 | 5.3 | 31.5 | 0.7 | 0.4 | 2.1 | |||
Int. claw IV | 3 | 6.0 | – | 6.5 | 5.0 | – | 5.5 | 30.6 | – | 37.3 | 6.3 | 5.3 | 32.3 | 0.3 | 0.3 | 3.5 | |||
Spur | 2 | 1.0 | – | 1.3 | 1.2 | 0.2 | |||||||||||||
Spur/Claw | 0.2 | – | 0.2 | 0.2 |
The paratypes exhibit the same morphology, but with a certain degree of variation with regard to appearance of the bands of the scapular and terminal plates, more visible in less relaxed specimens. The narrow posterior portions of the median plates (especially with regard to the third), are more visible in well-relaxed specimens but can be totally hidden in contracted specimens. In such specimens, the posterior elements of each couple of supplementary platelets, especially the third, could also be hidden. In addition, the orientation of the specimen on the slide meant the supplementary lateral platelets were not always clearly visible. With regard to the ventral plates, these were evident in some specimens, e.g. that chosen as holotype, but were not always easy to see. In general, the ventral plates varied from faint to almost invisible (without clear indication of a link with life stage); it took a very accurate, long observation under both PCM and DIC to identify all the plates and to be certain of the number and arrangement. Such plates show in PCM a faint granulation, which is actually what, in some cases, made them visible; their borders often being unclear. In some of the specimens not even one ventral plate was apparent at first sight, requiring very careful observation to detect at least some of them; thus this character can pass unnoticed. We therefore recommend great care in observing Bryodelphax before considering whether a specimen is without ventral plates, and also without supplementary lateral platelets.
Another character, for which considerable individual variability is noted, is the distribution of the cuticular pores, which may be arranged from a relatively regular distribution, as described in the holotype, to a quite random distribution. Additionally, the transversal bands of pores of the sub-portions of the paired and unpaired plates can be reduced to a single, more or less regular row.
Finally, the papilla of the hind legs in most specimens was not visible, but in a couple of individuals, there appeared to be an extremely small, faint papilla. However, the presence of particles in the slides preparation prevented us from being sure that what we observed was a papilla and not some out of focus particle. This character, therefore, needs to be confirmed.
The species is named in honour of Professor Reinhardt Møbjerg Kristensen, in particular for his valuable contribution to the taxonomy of Echiniscidae (
According to
Bryodelphax aaseae (Kristensen, Michalczyk & Kaczmarek, 2010) is the most similar species, sharing with the new species the same ventral plate configuration (if the median unpaired plate at the level of legs I is also present in the new species). These plates were described as smooth by the authors, but in
Bryodelphax kristenseni sp. n. differs from B. sinensis by having supplementary platelets, more numerous ventral plates (IX/X:2-(1)-4-4-2-4-2-1-2-1 vs VII:2-2-2-2-2-2-1 in B. sinensis), ventral cuticle smooth (dotted in B. sinensis), longer clava (3.4–4.3% of the body length vs. about 2.5% in B. sinensis).
The diagnosis of B. parvulus was revised by
Bryodelphax kristenseni sp. n. differs from B. asiaticus, which lacks the ventral plates, in having non-granulated ventral cuticle, anterior portions of median plates 1 and 2 markedly larger than the posterior portions (which are almost a stripe), while in B. asiaticus the posterior portions of those plates are only slightly smaller.
The new species differs from B. ortholineatus in having spurs on internal claws (absent in B. ortholineatus), in having supplementary platelets (not mentioned in the original description (Bartoš, 1963) and reported as absent by
As mentioned above, in B. kristenseni sp. n. the third median plate is divided into an anterior and a posterior portion; this character, until now, has been considered typical of the genus Bryochoerus, while in Bryodelphax the third median plate has been considered undivided.
At first, there were doubts on the identification due to the division of the third median plate, although hidden in some specimens, which led us to Bryochoerus; on the other hand, there was evident resemblance between these specimens and Bryodelphax aaseae, and with other species, e.g., Bryodelphax weglarskae (Pilato, 1972). This encouraged careful examination of that species as well as many others congeners, and it was noted that the divided third median plate was also present in B. aaseae (figs 7 and 8 in
The definition of the genus Bryodelphax is therefore suggested as follows:
Small Echiniscidae with non-flexible buccal tube with CaCO3 encrusted stylet supports. No lateral or dorsal appendages present except cirrus A. Median plates all divided, but the caudal portion of the third median plate may be hidden by the terminal plate. Without pseudosegmental plates. Ventral plates may be present.
With respect to
Authors from an earlier period (ca. 1900–1950s) traditionally considered many species to be cosmopolitan, which in tardigrade taxonomy created species-groups. These species-groups, along with past errors and misinterpretations, now require careful analysis in order to amend taxa descriptions and differentiate the sibling species. As taxonomic knowledge has progressed, key characters have been added that were not considered essential in older references. We are left with a legacy of early species descriptions that are often impossible to identify without type material, which in many cases is sadly unavailable. Taking into account the absent or poor state of older type material, and the difficulty in resampling a vaguely described locus typicus, the possibility of abolishing or classifying a suspect species as “species dubia” should be considered. This would help prevent further confusion created by non-taxonomists or beginners using an apparently simple diagnostic key (e.g.,
With our present contribution, based on material in a museum collection, three new records enrich the list of Echiniscidae recorded for Colombia. In addition, a species new to science was discovered, which provided the occasion to make evaluations at a higher taxonomic level. The fact that a relatively limited study provides new and interesting results, in spite of the great efforts from past decades, is evidence of how little is known about tardigrade fauna and biogeography for most regions of the world. It further highlights how much our taxonomic knowledge has grown and can still grow.
We are grateful to Prof. Giovanni Pilato for useful suggestions and making available his precious collection, to the Subject Editor Sandra McInnes and the reviewers for having improved the paper. This work was carried out in the framework of the research projects “Composición taxonómica de flora y fauna anhidrobiótica en micro-doseles de la Sierra Nevada de Santa Marta”, supported by Departamento Administrativo de Ciencia, Tecnología e Innovación “COLCIENCIAS” (#0091288) and the Universidad del Magdalena (BIO-659/2014), and “Diversidad de ositos de agua (Tardigrada) asociados a briófitos y líquenes epífitos en cultivos de café de la Sierra Nevada de Santa Marta, con un enfoque innovador para la apropiación social del conocimiento” supported by Fondo Patrimonial para la Investigación “FONCIENCIAS” 2015–2017 de la Universidad de Magdalena.
This is a scientific contribution number 8 from the Centro de Colecciones Biológicas de la Universidad del Magdalena.