New marine heterotardigrade lineages (Echiniscoididae) from the tropics

Figures & data

Table I. Collecting site locations, characteristics and collecting dates for new species. Abbreviations: j – juvenile, l – larva, u – sex unidentified. The geographic reference system: WGS84.

Species	Coordinates	Locality	Sample type	Water temperature and salinity	Collection date	Analyses
						PCM	DNA	SEM
E. basalticus sp. nov.	20°00ʹ30”S 57°40ʹ47”E	Indian Ocean, Mauritius, Grand Gaube	barnacles from basaltic rocks	33.5°C	27.02.2019	4♀♀ + 1♂ + 1 j	1 u	–
E. bufocephalus sp. nov.	25°59ʹ17”N 51°01ʹ25”E	Indian Ocean, Qatar, Al-Zubarah	mussels Brachidontes variabilis (Mytilidae)	17°C 50‰	07.03.2012	20♀♀ + 4 j + 1 l + 4 u	–	4
E. lichenophilus sp. nov.	18°20ʹ54”N 68°49ʹ54”W	Atlantic Ocean, Antilles, Bayahíbe, La Roca	lichens Ephebe lanata (Lichinaceae) from basaltic rocks	32°C 35.5‰	24.12.2018	36♀♀ + 36♂♂ + 28 j	8 u	10
E. musa sp. nov.	25°25ʹ19”S 48°24ʹ26”W	Atlantic Ocean, Baía de Paranaguá, Ilha das Bananas	barnacles from granite rocks	26.5°C	22.01.2019	2♀♀ + 1♂	3 u	–
E. trichosus sp. nov.	27°04ʹ23”S 109°19ʹ25”W	Pacific Ocean, Rapa Nui, Anakena Beach	barnacles from basaltic rocks	25°C 36.5‰	11.01.2009	14♀♀ + 3♂♂	9 u	8

Table II. GenBank accession numbers for the Echiniscoides spp. sequenced in this work.

Species	18S rRNA	28S rRNA			ITS-1	COI
		28S-Eutar-F + 28SR0990	28Sa + 28Srd5b	28Srd4-8a + 28Srd7b1
E. basalticus sp. nov.	ON180697	ON180891	ON180694	ON180700	ON180894	ON178666
E. lichenophilus sp. nov.	ON180698	ON180892	ON180695	ON180701	ON180895	ON178667–9
E. musa sp. nov.	ON180699	ON180893	ON180696	ON180702	ON180896	ON178670
E. trichosus sp. nov.	–	–	–	–	–	JQ689580–1

Figure 1. Bayesian phylogeny of Echiniscoididae based on COI. Values at the nodes signify posterior probabilities. Echiniscus testudo was used as an outgroup. The scale bar represents 0.5 substitutions per nucleotide position.

Table III. Measurements [in µm] of selected morphological structures of individuals of Echiniscoides basalticus sp. nov. (type series) mounted in Hoyer’s medium. Abbreviations: N – number of females/structures measured, Range refers to the smallest and the largest structure among all measured specimens; SD – standard deviation.

Character	N	Range (♀♀)			Mean	SD	Holotype	Allotype	Juvenile
		µm			µm	µm	µm	µm	µm
Body length	4	158 – 209			185	21	183	153	121
Body width	4	54 – 88			74	15	72	62	40
Anus-gonopore distance	4	6.5 – 12.3			10.1	2.7	9.7	153	–
Bucco-pharyngeal apparatus
Buccal canal length	4	35.2 – 45.4			40.2	4.2	40.9	31.1	27.8
Pharynx length	3	13.9 – 18.7			15.8	2.5	18.7	13.7	10.3
Placoid length	4	5.8 – 8.0			7.3	1.0	7.7	6.0	4.7
Head appendages
Cirrus internus length	4	2.8 – 4.0			3.4	0.5	3.2	2.2	2.7
Secondary clava height	4	6.4 – 8.5			7.2	0.9	6.8	6.3	?
Secondary clava width	1	6.9 – 6.9			6.9	?	?	?	?
Cirrus externus length	4	3.2 – 4.1			3.7	0.4	3.2	3.4	3.3
Primary clava length	4	3.5 – 3.9			3.7	0.2	3.8	3.0	2.3
Cirrus A length	4	8.1 – 9.6			8.8	0.7	9.1	?	?
Cirrus A/Body length ratio	4	4% – 5%			5%	1%	5%	2.2	?
Trunk appendage lengths
Cirrus E	4	6.7 – 9.3			7.9	1.1	7.6	7.2	5.5
Sensory organ on leg I	2	1.6 – 1.8			1.7	0.1	1.6	1.0	?
Sensory organ on leg II	2	1.5 – 2.3			1.9	0.6	2.3	1.4	?
Sensory organ on leg III	3	5.2 – 5.3			5.2	0.1	5.2	4.8	3.5
Sensory organ on leg IV	4	2.7 – 3.5			3.1	0.3	3.0	2.0	2.0
Claw heights
Claw I branch	4	7.4 – 9.4			8.6	1.0	9.4	?	?
Claw II branch	3	6.6 – 8.7			7.9	1.1	8.3	?	?
Claw III branch	4	7.0 – 9.0			8.2	1.0	9.0	7.7	5.3
Claw IV branch	4	8.4 – 11.2			9.8	1.2	10.1	8.4	5.9

Figure 2. Habitus of Echiniscoides basalticus sp. nov. (PCM): A. holotypic female, B. allotypic male. List of abbreviations (identical for all figures): cA – cirrus A, ce – cirrus externus, cE – cirrus E, ci – cirrus internus, p1–4 – sense organs on legs I–IV, pc – primary clava, sc – secondary clava (cephalic papilla). Scale bars in μm.

Figure 3. Drawing of Echiniscoides basalticus sp. nov. Scale bar in μm.

Figure 4. Buccal apparatus of Echiniscoides basalticus sp. nov. (PCM). Scale bar in μm.

Table IV. Measurements [in µm] of selected morphological structures of adult females of Echiniscoides bufocephalus sp. nov. (type series) mounted in Hoyer’s medium. Abbreviations: N – number of specimens/structures measured, Range refers to the smallest and the largest structure among all measured specimens; SD – standard deviation.

Character	N	Range			Mean	SD	Holotype
		µm			µm	µm	µm
Body length	16	147 – 192			163	16	153
Body width	16	64 – 90			74	8	70
Anus-gonopore distance	15	10.7 – 16.1			12.3	1.6	12.1
Bucco-pharyngeal apparatus
Buccal canal length	14	30.3 – 37.6			33.7	2.2	30.3
Pharynx length	12	11.4 – 16.0			14.4	1.2	11.4
Placoid length	14	3.7 – 5.2			4.7	0.4	3.7
Head appendages
Cirrus internus length	16	3.0 – 4.4			3.8	0.5	3.5
Secondary clava height	15	3.3 – 6.6			4.5	1.0	3.4
Secondary clava width	16	6.5 – 10.7			8.2	1.2	8.7
Cirrus externus length	16	5.6 – 8.2			7.1	0.8	6.6
Primary clava length	16	3.0 – 4.9			3.6	0.5	3.4
Cirrus A length	15	8.1 – 11.3			10.2	0.9	9.9
Cirrus A/Body length ratio	15	5% – 7%			6%	1%	6%
Trunk appendage lengths
Cirrus E	15	6.8 – 11.8			10.1	1.2	9.4
Sensory organ on leg I	14	1.4 – 2.0			1.8	0.2	1.7
Sensory organ on leg II	14	3.4 – 5.6			4.6	0.6	4.0
Sensory organ on leg III	11	4.2 – 6.5			5.3	0.7	?
Sensory organ on leg IV	15	2.8 – 4.3			3.4	0.4	3.3
Claw heights
Claw I branch	15	6.2 – 7.3			6.6	0.3	6.8
Claw II branch	16	5.9 – 7.1			6.4	0.4	5.9
Claw III branch	14	5.9 – 7.2			6.6	0.4	6.6
Claw IV branch	15	6.5 – 8.7			7.9	0.6	8.1

Figure 5. Habitus of the holotypic female of Echiniscoides bufocephalus sp. nov. (PCM). Scale bar in μm.

Figure 6. Drawing of Echiniscoides bufocephalus sp. nov. Scale bar in μm.

Figure 7. Detailed morphology of Echiniscoides bufocephalus sp. nov.: A. specimen in toto (SEM), B. head in close-up (dorsal view, SEM), C. head in close-up (ventral view, SEM), D. buccal apparatus (PCM). Scale bars in μm.

Figure 8. Cephalic and trunk appendages of Echiniscoides bufocephalus sp. nov.: A. peribuccal cirri and secondary clava (PCM), B. cirrus internus in close-up (SEM), C. cirrus A and primary clava (SEM), D. sensory organ on leg II (SEM), E. sensory organ on leg III (PCM), F. cirrus E (SEM). Scale bars in μm.

Figure 9. Detailed morphology of Echiniscoides bufocephalus sp. nov.: A. claws I (PCM), B. claws IV (SEM), C. anus and male gonopore (SEM), D. male gonopore in close-up (SEM). Scale bars in μm.

Table V. Measurements [in µm] of selected morphological structures of adult females of Echiniscoides lichenophilus sp. nov. (type series) mounted in Hoyer’s medium. Abbreviations: N – number of specimens/structures measured, Range refers to the smallest and the largest structure among all measured specimens; SD – standard deviation.

Character	N	Range			Mean	SD	Holotype
		µm			µm	µm	µm
Body length	15	189 – 267			242	24	267
Body width	15	72 – 112			98	11	107
Anus-gonopore distance	15	8.6 – 19.2			14.5	2.9	17.3
Bucco-pharyngeal apparatus
Buccal canal length	14	30.3 – 43.3			38.6	3.3	41.5
Pharynx length	6	13.4 – 21.1			18.3	2.6	18.4
Placoid length	15	6.6 – 8.7			7.4	0.6	7.5
Head appendages
Cirrus internus length	15	1.7 – 3.3			2.7	0.5	3.1
Secondary clava height	14	7.6 – 12.3			10.3	1.2	10.1
Secondary clava width	10	6.6 – 9.2			8.1	0.9	8.9
Cirrus externus length	14	2.5 – 3.8			3.2	0.4	3.1
Primary clava length	15	2.9 – 4.1			3.5	0.4	3.6
Cirrus A length	15	7.5 – 11.2			9.3	0.9	10.2
Cirrus A/Body length ratio	15	4% – 4%			4%	0%	4%
Trunk appendage lengths
Cirrus E	14	7.7 – 12.0			9.7	1.3	8.1
Sensory organ on leg I	9	1.2 – 2.5			2.0	0.5	1.4
Sensory organ on leg II	15	1.0 – 2.9			1.7	0.5	1.4
Sensory organ on leg III	15	2.7 – 4.0			3.3	0.4	3.2
Sensory organ on leg IV	15	2.3 – 4.5			3.5	0.6	3.9
Claw heights
Claw I branch	15	6.4 – 9.3			7.9	0.8	7.6
Claw II branch	15	6.2 – 9.0			7.8	0.8	8.5
Claw III branch	14	6.3 – 8.8			7.8	0.7	8.1
Claw IV branch	15	7.5 – 11.3			9.6	1.1	10.4

Table VI. Measurements [in µm] of selected morphological structures of adult males of Echiniscoides lichenophilus sp. nov. (type series) mounted in Hoyer’s medium. Abbreviations: N – number of specimens/structures measured, Range refers to the smallest and the largest structure among all measured specimens; SD – standard deviation.

Character	N	Range			Mean	SD	Allotype
		µm			µm	µm	µm
Body length	15	137 – 218			171	24	180
Body width	15	54 – 85			63	9	72
Anus-gonopore distance	15	5.0 – 9.9			6.9	1.6	7.1
Bucco-pharyngeal apparatus
Buccal canal length	12	26.7 – 35.7			30.6	2.5	?
Pharynx length	7	12.0 – 14.4			13.2	0.9	?
Placoid length	13	4.4 – 6.4			5.3	0.6	?
Head appendages
Cirrus internus length	15	1.6 – 3.3			2.3	0.4	2.0
Secondary clava height	14	6.9 – 10.8			8.3	1.3	10.0
Secondary clava width	5	6.5 – 10.1			7.8	1.5	6.9
Cirrus externus length	15	2.1 – 3.3			2.6	0.4	2.1
Primary clava length	15	2.7 – 3.8			3.2	0.3	3.6
Cirrus A length	15	6.2 – 9.6			7.5	1.1	6.8
Cirrus A/Body length ratio	15	4% – 5%			4%	1%	4%
Trunk appendage lengths
Cirrus E	15	6.8 – 10.4			8.2	1.3	9.2
Sensory organ on leg I	7	1.1 – 2.1			1.5	0.3	1.7
Sensory organ on leg II	13	1.0 – 1.8			1.4	0.2	?
Sensory organ on leg III	15	2.3 – 3.4			2.9	0.4	3.2
Sensory organ on leg IV	15	2.1 – 3.9			3.0	0.5	3.1
Claw heights
Claw I branch	13	4.4 – 8.1			6.4	0.9	5.7
Claw II branch	15	5.0 – 8.0			6.1	1.0	5.5
Claw III branch	15	4.6 – 8.1			6.3	1.0	5.6
Claw IV branch	15	6.3 – 10.0			7.7	1.1	7.2

Figure 10. Habitus of the holotypic female of Echiniscoides lichenophilus sp. nov. (PCM). Scale bar in μm.

Figure 11. Drawing of Echiniscoides lichenophilus sp. nov. Scale bar in μm.

Figure 12. Detailed morphology of Echiniscoides lichenophilus sp. nov. (DIC): A. buccal apparatus, B. caudal body portion with cirri E, C. claws II and sense organ on leg II. Scale bars in μm.

Figure 13. Detailed morphology of Echiniscoides lichenophilus sp. nov. (SEM): A. specimen in toto, B. cephalic body portion with peribuccal cirri in frontal view, C. cephalic body portion with peribuccal cirri in lateral view, D. cirrus A and primary clava, E. cirrus E and sense organ on leg IV, F. claws II, G. claws III. Scale bars in μm.

Table VII. Measurements [in µm] of selected morphological structures of adults of Echiniscoides musa sp. nov. (type series) mounted in Hoyer’s medium. Abbreviations: SD – standard deviation.

Character	Holotype	Allotype	Paratype	Mean	SD
	µm	µm	µm	µm	µm
Body length	257	199	223	226	29
Body width	122	70	92	95	26
Anus-gonopore distance	15.8	9.8	11.1	12.2	3.2
Bucco-pharyngeal apparatus
Buccal canal length	?	36.5	?	36.5	?
Pharynx length	?	15.0	?	15.0	?
Placoid length	?	7.0	?	7.0	?
Head appendages
Cirrus internus length	4.0	2.8	3.7	3.5	0.6
Secondary clava height	11.4	8.0	8.6	9.3	1.8
Secondary clava width	8.7	6.9	6.2	7.3	1.3
Cirrus externus length	4.1	2.9	?	3.5	0.8
Primary clava length	3.7	3.7	4.0	3.8	0.2
Cirrus A length	11.7	10.9	?	11.3	0.6
Cirrus A/Body length ratio	5%	5%	?	5%	1%
Trunk appendage lengths
Cirrus E	10.2	9.4	11.0	10.2	0.8
Sensory organ on leg I	2.5	2.0	?	2.3	0.4
Sensory organ on leg II	2.3	1.4	?	1.9	0.6
Sensory organ on leg III	8.0	6.1	?	7.1	1.3
Sensory organ on leg IV	3.5	3.2	3.9	3.5	0.4
Claw heights
Claw I branch	11.5	9.9	11.0	10.8	0.8
Claw II branch	11.1	10.3	11.1	10.8	0.5
Claw III branch	10.8	10.4	11.5	10.9	0.6
Claw IV branch	12.7	13.4	14.1	13.4	0.7

Figure 14. Detailed morphology of Echiniscoides musa sp. nov. (PCM): A. holotypic female, B. anterolateral body portion of paratypic female, C. buccal apparatus, D. claws II. Scale bars in μm.

Figure 15. Drawing of Echiniscoides musa sp. nov. Scale bar in μm.

Table VIII. Measurements [in µm] of selected morphological structures of adult females of Echiniscoides trichosus sp. nov. (type series) mounted in Hoyer’s medium. Abbreviations: N – number of specimens/structures measured, Range refers to the smallest and the largest structure among all measured specimens; SD – standard deviation.

Character	N	Range			Mean	SD	Holotype
		µm			µm	µm	µm
Body length	13	139 – 229			173	25	186
Body width	7	64 – 102			82	13	?
Anus-gonopore distance	12	6.3 – 19.9			10.9	3.7	12.2
Bucco-pharyngeal apparatus
Buccal canal length	4	35.4 – 53.9			44.9	9.2	?
Pharynx length	4	18.5 – 25.4			22.0	3.1	23.6
Placoid length	6	7.1 – 11.8			9.2	1.9	8.6
Head appendages
Cirrus internus length	13	2.0 – 3.4			2.8	0.4	2.6
Secondary clava height	12	7.0 – 10.2			8.6	1.1	9.8
Secondary clava width	5	5.1 – 8.5			6.2	1.4	8.5
Cirrus externus length	10	2.2 – 3.9			3.0	0.5	2.7
Primary clava length	13	2.8 – 4.5			4.0	0.5	3.9
Cirrus A length	13	6.3 – 10.5			8.4	1.5	7.3
Cirrus A/Body length ratio	13	4% – 6%			5%	1%	4%
Trunk appendage lengths
Cirrus E	13	5.7 – 9.2			7.4	1.3	8.0
Sensory organ on leg I	5	1.1 – 3.4			2.0	0.9	?
Sensory organ on leg II	4	1.2 – 1.8			1.5	0.2	?
Sensory organ on leg III	13	4.0 – 7.4			5.4	0.9	5.9
Sensory organ on leg IV	13	2.7 – 4.6			3.5	0.5	3.8
Claw heights
Claw I branch	13	6.0 – 8.5			7.4	0.8	7.9
Claw II branch	13	5.8 – 8.6			7.4	1.0	7.5
Claw III branch	12	5.5 – 9.1			7.3	0.9	7.6
Claw IV branch	13	7.0 – 10.4			8.8	1.0	10.0

Figure 16. Habitus of the holotypic female of Echiniscoides trichosus sp. nov. (PCM). Scale bar in μm.

Figure 17. Drawing of Echiniscoides trichosus sp. nov. Scale bar in μm.

Figure 18. Detailed morphology of Echiniscoides trichosus sp. nov. (all but A in SEM): A. specimen in toto (DIC), B. dorsal sculpturing in the form of microtrichia, C. cephalic body portion with peribuccal cirri in frontal view, D. cephalic body portion with peribuccal cirri in lateral view, E. anterolateral body portion of paratypic female. Scale bars in μm.

Figure 19. Dorsal sculpturing of Echiniscoides trichosus sp. nov. in close-up (SEM). Scale bars in μm.

Figure 20. Detailed morphology of Echiniscoides trichosus sp. nov. (all but D in SEM): A. specimen in toto in dorsal view, B–C. specimens in toto in lateroventral view, D. claws III and sense organ on leg III (PCM), E. claws III, F. claws IV. Scale bars in μm.

Figure 21. Habitus of Echiniscoides hispaniensis Kristensen & Hallas, 1980 stat. nov. (SEM): A. female in lateral view, B. female in anterolateral view, C. male in ventral view, D. female in ventral view. Scale bars in μm.

Figure 22. Detailed morphology of Echiniscoides hispaniensis (SEM): A. cephalic body portion with peribuccal cirri in lateral view, B. cephalic body portion with peribuccal cirri in frontal view, C. peribuccal cirri and secondary clava in close-up, D. cirrus A and primary clava, E. caudal body portion, F. cirrus E and dorsal sculpturing in close-up. Scale bars in μm.

Figure 23. Detailed morphology of Echiniscoides hispaniensis (SEM): A. claws I, B. claws III, C. male gonopore. Scale bars in μm.

Figure 24. Cuticular morphotypes within Echiniscoides (SEM): smooth cuticle – A–B. Echiniscoides sigismundi from Julebæk Strand (Sjælland, neotype locality), rugose cuticle – C. an undescribed Echiniscoides species from Los Angeles. Scale bars in μm.

Table IX. Main characteristics of described species of Echiniscoides.

Species	Cuticle	Adult claw formula*	Microhabitat	Distribution
E. andamanensis	smooth	8,8,8,7	barnacles Balanus variegatus	Thailand, Indian Ocean
E. basalticus sp. nov.	faint, irregular, polygonal sculpturing	9/10,9,9,8	barnacles	Mauritius, Indian Ocean
E. bruni	strong polygonal sculpturing	10,10,10,10	subtidal, coralligenous and sandy detritus	Sardinia, Atlantic Ocean
E. bufocephalus sp. nov.	irregular wrinkling	8,8,7,7	tidal, mussels Brachidontes variabilis	Qatar, Persian Gulf, Indian Ocean
E. costaricensis	strong polygonal-circular sculpturing	7,7,7,6	intertidal sand mixed with black magnetite	Costa Rica, Atlantic Ocean
E. galliensis	strong circular sculpturing, each circular tubercle with a line of discontinuous curves in the centre	10,9,10,9	tidal, barnacles Chthalamus stellatus	France, Atlantic Ocean
E. groenlandicus	mostly fine punctuations	8,8,8,8	barnacles Semibalanus balanoides	Northern Atlantic Ocean (Greenland, Norway)
E. hispaniensis	strong sculpturing, tubercles arranged like roofing tiles in PCM	7,7,7,6	barnacles Chthalamus stellatus and Eliminius modestus	Portugal and Spain, Atlantic Ocean
E. hoepneri	smooth	7/9,7/9,7/9,6/8	barnacles Semibalanus balanoides	Northern Atlantic Ocean (Greenland, Iceland, Faroe Islands)
E. lichenophilus sp. nov.	strong polygonal sculpturing	8/12,8/12,8/10,7/9	lichens Ephebe lanata	Hispaniola, Atlantic Ocean
E. mediterranicus	smooth	11,12,11,10	barnacles	Spain, Atlantic Ocean
E. musa sp. nov.	strong polygonal sculpturing	7,6/7,6/7,6	barnacles	Brazil, Atlantic Ocean
E. polynesiensis	strong circular sculpturing, each tubercle with a pointed elevation in the centre	9,9,9,8	algae	Australia and Polynesia, Pacific Ocean
E. porphyrae	fine punctuations	9,9,9,8	algae Porphyra	Marion Island, Indian Ocean
E. ritavargasae	faint, circular sculpturing mostly in the caudal body portion	9,9,9,9	barnacles Amphibalanus peruvianus, Balanus inexpectatus, Chthalamus panamensis	Costa Rica, Pacific Ocean
E. rugostellatus	strong polygonal sculpturing	9,9,9,8	barnacles Balanus glandula	Washington & California, Atlantic & Pacific Oceans
E. sigismundi	smooth	9,9,9,8	barnacles Semibalanus balanoides	Northern Atlantic Ocean (Greenland, Iceland, Faroe Islands, Scotland, Scandinavian Peninsula and Denmark, USA)
E. travei	smooth	8/11,8/11,8/11,8/11	algae Porphyra	Kerguelen Islands, Indian Ocean
E. trichosus sp. nov.	fine punctuations comprising microtrichia	11,11/13,11/13,10	barnacles	Rapa Nui, Pacific Ocean
E. verrucariae	fine punctuations	9,10,9,9	lichens Verrucaria	Marion Island, Indian Ocean
E. wyethi	smooth	8,8,8,7	barnacles Semibalanus balanoides	Maine, Atlantic Ocean

*Refers to the most frequent morphotype present within populations of a species, or is given collectively if no dominant pattern was observed/precise data are lacking in the original description.

Kristensen RM, Hallas TE. 1980. The tidal genus Echiniscoides and its variability, with erection of Echiniscoididae fam. n. (Tardigrada). Zoologica Scripta 9(1–4):113–127. DOI:10.1111/j.1463-6409.1980.tb00657.x.

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