Corresponding author: Paulo H.C. Corgosinho ( email@example.com )
Academic editor: Michael Ohl
© 2017 Paulo H.C. Corgosinho, Nikolaos V. Schizas, Daniel Previattelli, Carlos E. Falavigna da Rocha, Edinaldo Nelson dos Santos-Silva.
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: Corgosinho PHC, Schizas NV, Previattelli D, Falavigna da Rocha CE, Santos-Silva EN (2017) A new genus of Parastenocarididae (Copepoda, Harpacticoida) from the Tocantins River basin (Goiás, Brazil), and a phylogenetic analysis of the Parastenocaridinae. Zoosystematics and Evolution 93(1): 167-187. https://doi.org/10.3897/zse.93.11602
Eirinicaris antonioi gen. et sp. n. (Parastenocaridinae) is described from the Brazilian rocky savannas, an ecosystem under heavy anthropogenic pressure. The subfamily is distributed worldwide, with representatives in Africa, Asia, Australia, Europe, and North America. This is the first time a non-Remaneicaris Parastenocaridinae is described from a Neotropical region indicating that Parastenocaridinae species were already present in a vast geographical area, before the split of the Gondwana. The new taxon is included within the subfamily Parastenocaridinae based on the following characters: 1) segments 5, 6, and 7 of the male antennules forming a functional unit for clasping the female; 2) segment 7 with small process at the inner margin, forming an incipient “pocket-knife” structure with segment 6; 3) last segment pointing medially when closed; 4) the endopod of female leg 3 one-segmented and spiniform, without distal seta; 5) the apophysis and terminal seta of the exopod of male leg 3 are fused; 6) the genital field is rectangular and much broader than the height in the female; 7) the group of three lateral setae I, II, and III of the furca and the dorsal seta are situated at the same level in the female; and 8) the basis of leg 1 has an inner seta. The new taxon can be distinguished from all other Parastenocaridinae genera by the unique sexually dimorphic telson and furca. In the male, the dorsal seta is inserted at the midlength of the furca and setae I, II, and III are displaced anteroventrally. A phylogenetic analysis of the subfamily Parastenocaridinae is given based on the description of the type species of each genus and available descriptions of all Parastenocaridinae species. Eirinicaris gen. n. is the sister taxon of a clade formed by Kinnecaris and Monodicaris, sharing with them the long male and female leg 5 with a long spiniform process, and with Kinnecaris, a distal pore on the spiniform process.
biodiversity, Brazilian rocky savannas, Crustacea, neotropics, new species, phylogeny
Copepods of the family Parastenocarididae Chappuis, 1940, are typical representatives of fresh groundwater meiofauna (
The taxonomy and phylogenetic relationships among the species of Parastenocarididae are far from resolved with many genera being potentially paraphyletic or polyphyletic. Most of the confusion can be attributed to
Many genera were revised or proposed recently (viz.
The Neotropical fauna of Parastenocarididae is represented by the genera Remaneicaris, Murunducaris Reid, 1994, Brasilibathynellocaris, Siolicaris, Iticocaris, Forficatocaris Jakobi, 1972, and Potamocaris Dussart, 1979. With the exception of Remaneicaris, all the remaining genera belong to the subfamily Fontinalicaridinae.
In order to improve our knowledge on the biodiversity of Brazil, the National Council of Scientific Research (CNPq) launched in 2010 a call for proposals, to assess the biodiversity of neglected taxonomic groups in understudied Brazilian ecosystems. Our project focused on the microcrustaceans from the Brazilian rocky savannas. These environments fall into the category of azonal biomes (
This contribution describes one of the several new species and genera discovered during an intensive sampling effort conducted in 12 rocky fields in the Brazilian inland. A non-Remaneicaris Parastenocaridinae is described from a Neotropical region for the first time and its phylogenetic position within the Parastenocaridinae is discussed.
Specimens of an undescribed taxon were found associated with moss in the littoral zone of the Água Fria River, tributary of the São Bartolomeu River, Tocantins hydrographic basin, 1230 m MSL. The sampling station, characterized by a rocky riverbed, is located at Chapada dos Veadeiros, Alto Paraíso de Goiás, Goiás State, Brazil: 14°5’30.89”S, 47°29’34.47”W (Fig.
Samples of damp moss living next to the waterline were collected on August 12, 2012. The material was concentrated using a 50 μm mesh size net and preserved in 4% formalin. Animals were stained with rose Bengal and sorted with a stereomicroscope. Whole specimens and dissected material were mounted on slides in lactic acid for morphological inspection.
The terms ‘furca’ and ‘telson’ are used according to
In order to determine the position of the new genus within Parastenocarididae, the method of phylogenetic systematics of Hennig (1966) was followed. The cladogram (Fig.
Study area. Type locality indicated with triangle. Insert shows the type locality (Água Fria River, National Park of the Chapada dos Veadeiros, Brazil) of Eirinicaris antonioi sp. n.
Character matrix for phylogenetic reconstruction of the valid genera included by
The phylogenetic analysis is based on data from published literature. All the original descriptions and the descriptions of the species included in
When necessary in the text is used of the Newick (parenthetical) phylogenetic notation to discuss the species relationships within and between closely related clades.
A1 eight-segmented in male, seven-segmented in female. Male A1 haplocer, eight-segmented, haplocer, with small process in segment seven; segments 5, 6, and 7 forming a functional unit for clasping the female, in grasping position, segment 7 bent inwards against segment 6, segment 8 points in opposite direction. Allobasis of Mx with two endites; proximal endite with one seta; distal endite with two elements, one of them transformed into serrated spine; proximal endopodal segment drawn out into claw, distal endopodal segment with two setae. Basis of P1 without remarkable sexual dimorphism; with inner and outer seta, the former longer in male; enp not sexually dimorphic. P2 enp without marked sexual dimorphism. Male P3 with quadratic smooth coxa; basis short, quadratic, with row of spinules close to outer seta, without inner ornamentation; enp modified, aesthetasc-like; exp unisegmented, rectangular, longer than wide, with irregular inner margin and with medial hump, outer margin straight, with unevenly distributed spinules, distal margin flat, inner apophysis shorter than supporting segment, blade-shaped, without distal seta or spine, thumb slightly longer than apophysis, with broad base, proximal expansion on both sides and leaf-shaped distal blade. Female P3 with spiniform enp ⅔ as long as exp-1. Male P4 enp cylindrical, approximately half as long as exp-1, with three distal spinules and one medial outer spinule. Enp of female P4 spiniform, almost as long as exp-1, distally bipinnate. Male and female P5 well developed, a simple triangular plate reaching middle of genital somite in male, inner margin drawn into long and pointed, outwardly curved, spinous process with distal pore, without inner ornamentation, reaching beyond the genital field in female; armature consisting of very long outer basal seta and two additional setae, of which proximal most shorter. Male P6 large, tetra-lobbed fused plate covering genital area. Female P6 represented by naked opercular plate much broader than the height covering genital opening. Male telson with proximal lateral pore, transverse row of small spinules along entire dorsal surface, anterior to sensilla, and rows of spinules covering most of preopercular lateral margin. Female telson smooth, with proximal ventral pore and ventral tube pore near insertion of furca. Male furca irregular, with distal outer pore, longer than width, inner and dorsal margins convex, outer and ventral margins concave; dorsal, inner and outer margins covered by spinules; lateral setae I, II and III, and dorsal setae VII separated by wide gap, setae I, II, and III displaced to antero-ventral position, seta I modified into short spine, with broad base and acuminate tip, seta III 1/3 as long as furca, with one long peduncle and one distal aesthetasc-like structure, 1/2 size of seta II, seta II with broad base, a long peduncle and one distal aesthetasc-like structure; setae IV to VII smooth, dorsal seta (VII) medially inserted in a depression; seta IV inserted subdistally on outer margin, approximately as long as telson without furca, seta V distal, twice as long as seta IV, seta VI distal, 1/2 as long as seta IV; proximal bulges on inner and outer margins. Female furca rectangular with distal ventral pore, longer than wide, smooth, slightly tapering distally, with inner flat lobe; setae smooth, lateral setae I, II, and III, and dorsal seta VII inserted medially and more or less opposite to each other; lateral setae reduced to one small (seta III) and two tiny setae (setae I and II); two uncinate processes anterior to insertion of dorsal seta VII, setae IV, V and VI inserted distally, length and ornamentation of setae IV, V, and VI as for the male; seta VI inserted beneath flat lobe, small spinules close to its insertion.
Male dissected holotype mounted onto three slides (sample VEA17/B/R/ROF/musgo; 20 Jan 2012; MZUSP 35273). One dissected female paratype mounted onto one slide (sample VEA17/B/R/ROF/musgo; 20 Jan 2012; MZUSP 35274), one undissected female paratype (sample VEA15/C/CP/50; 20 Dec 2012; MZUSP 35274), and two undissected male paratypes mounted onto a single slide (sample VEA17/B/R/ROF/musgo; 20 January 2012; MZUSP 35274).
National Park of the Chapada dos Veadeiros (North of Goiás, Brazil); Água Fria River; 1230 m MSL; speed of water current from low to medium; temperature 20 ±5°C; pH 5 ±1. Coordinates: 14°5’30.89”S, 47°29’34.47”W.
The generic name is in honour of the first author’s wife, Eirini Grapsa, combining her first name with the ancient Greek substantive for shrimp, καρίς (caris). The specific epithet “antonioi” is posthumous homage to Antonio Alves Corgosinho Filho, father of the first author.
Length 320μm (variability of the type series 314-328μm), measured from rostrum to end of telson excluding furca. Rostrum not fused to cephalothorax, with wide base and two sensilla on tip (Fig.
Labrum (not shown) triangular in lateral view.
Md as in Fig.
Mx1 as in Fig.
Mx as in Fig.
P3 as in Figs
P4 as in Figs
Eirinicaris antonioi sp. n. Male: A habitus, lateral view; B anal somite with caudal furca, lateral view; C anal somite with caudal furca, dorsal view; D anal somite with caudal furca, ventral view; E mouthparts; e1 antennule; e2 mandible; e3 maxillulae; e4 maxillae; e5 maxilliped. Scale bars: 1 = 50 µm (A); 2 (B, C, D) = 50 µm; 3 (E) = 20 µm.
Eirinicaris antonioi sp. n. Male: A antennule, with process arrowed on segment seven, segment six laterally detached; B P1, anterior; C P2, anterior; D P3, anterior; d1 distal part of exopod of P3 showing the apophysis, anterior; d2 distal part of exopod of P3 showing the apophysis, posterior; E P4, anterior; F P5, with distal pore arrowed. Scale bar = 25µm.
Eirinicaris antonioi sp. n. Female: A antennule; B P1, depicted with coxa, basis enp-1 and exp-1; C P2 enp; D P3, anterior; E P4 anterior; F P5, with distal pore arrowed; G genital field; H anal somite with caudal furca; I furca, lateral view. Scale bar 1 (A, F) and 2 (C, D, E, G, H, I) = 25µm.
SEM image of Eirinicaris antonioi sp. n. A male habitus, lateral view; B female habitus, ventral view. Scale bar A = 10µm; B = 20µm.
SEM image of Eirinicaris antonioi sp. n. Male: A antennule in lateral view; B antennule segments 6 (yellow) and 7 (coral); C antennule, segment 8 showing modified seta; D telson and furca, lateral; E furca, dorsal view; F furca, ventral view, showing modified setae I, II and III and distal pore arrowed. Scale bars A = 10µm; B = 1µm; C = 200µm; D = 2µm; E = 2µm; F = 2µm.
SEM image of Eirinicaris antonioi sp. n. Male: A P1 showing inner seta of basis; B P3 with endopod and thumb in colour, P4; C claviform aesthetasc representing the endopod of P3; D P5, lateral view, with distal pore arrowed; E P5 and P6. Female: F pro- and urosomites, ventral view showing endopods of P3 and P4, and P5 and P6. Scale bars A = 10µm; B = 10µm; C = 1µm; D = 2µm; E = 2µm; F = 102µm.
Length 310μm (variability of the type series 310-326μm), measured from tip of rostrum to end of telson, excluding furca. Sexual dimorphism expressed in A1, P1, P3, P4, genital-double somite, number of integumental windows, telson and furca. Cephalothorax and Urs-2-4 with dorsal integumental windows; window on Urs-4 extending into ventral area (Figs
A1 seven-segmented (Figs
P2 enp (Fig.
P3 as in Figs
After the revisionary work of
List of genera redefined after
|Genera redefined after
|New genera proposed after
||Potamocaris, Murunducaris, Simplicaris Galassi and De Laurentiis, 2004, Monodicaris, Asiacaris, Dussartstenocaris, Horstkurtcaris, Iticocaris, Cottarellicaris; Himalayacaris and Indocaris.|
Of the genera mentioned on Table
The genus Eirinicaris strongly differs from all the above Parastenocaridinae genera by its unique sexually dimorphic telson and furca. Eirinicaris does not exhibit all the diagnostic characters of Parastenocaridinae, as proposed by
List of characters and phylogenetic discussion. The characters are listed below and the state of each character is indicated within parentheses.
Inner spine on the basis of leg 1: sexually monomorphic (0); sexually dimorphic (1);
Seta on the distal endite of Mx: modified, brush-like (1); not modified (0);
Seta on the Md palp: modified, brush-like (1); unmodified (0);
No. of armature elements on praecoxal arthrite of Mxl: >5 (0); 5 (1);
No. of segments of male A1: 10 (0); 9 (1); 8 (2);
No. of segments of female A1: 8 (0); 7 (1);
No. of segments of the A2 enp: 2 (0); 1 (1);
No. of armature elements on triangular A2 exp: three spines/setae, at least 1 modified (0); 1 seta (1);
No. of segments on mandibular palp: 2 (0); 1 (1);
Accessory setae on the first enp/claw of Mx: present (0); absent (1);
Syncoxal seta of Mxp: present (0); absent (1);
P4: sexually dimorphic (1); monomorphic (0);
No. of endopodal segments of P1: 3 (0); 2 (1);
Inner seta on enp-1 of P1: present (0); absent (1);
No. of endopodal segments of P2: 2 (0); 1 (0);
Exp-2 of P2: with outer seta (0); without (1);
Exp-2 of P2: with inner seta (0); without (1);
No. of endopodal segments of P3: 2 (0); 1 (1);
Exp-2 of P4: with outer seta (0); without (1);
Exp-2 of P4: with inner seta (0); without (1);
No. of endopodal segments of P4: 2 (0); 1 (1);
Exp of male P3: not prehensile (0); prehensile (1);
Integumental windows: absent (0); present on Cphl and urosomites (1);
Armature of the first Mx endite: 2 (0); 1 (1);
P5 exp and benp: separate (0); fused (1);
Inner seta on the basis of P1: present (0); absent (1);
Ornamentation of basis of the male P4 between exp and enp: present (1); absent (0);
Shape of the genital operculum: broader than height (0); higher than width (1);
Exp of the male P3: with a proximal hump (1), without hump (0);
Length and shape of enp of female P3: short and rounded (0); long and spiniform (1);
Relative position of lateral setae I, II and III, and dorsal furcal setae VII: aligned (1); dorsal seta posterior to lateral setae (0);
Penultimate segment of the male A1: with apophysis (1); without apophysis (0);
Armature of the apophysis of male P3: with one distal spine (0); spine lost or reduced to a hyaline structure (1);
No. of armature elements on second endite of Mx: two setae and one spine (0); 3 (1); 2 (2);
P5 intercoxal sclerite: present (0); absent (1);
Enp of the male P4 fused to the basis: present (1); absent (0);
Flat strong spine on coxa of male P4: absent (0); present (1);
Medial ornamentation on the outer margin of P4 exp-3: absent (0); present (1);
Medial ornamentation on the outer margin of P4 exp-2: absent (0); present (1);
Medial ornamentation on the outer margin of P2 exp-3: absent (0); present (1);
Medial ornamentation on the outer margin of P2 exp-2: absent (0); present (1);
Enp of male P3: present (0); absent or reduced to a seta (1);
Position of outer setae of P4 exp-3: distal (0); subdistal (1);
Ornamentation of the basis of the male P4: simple row of spinules (0); with normal spinules of equal sizes (1); sclerotized, of different sizes (2); with strongly transformed spinules building a spinular complex or differently build into petaloid structures (3); lost but conserving the enp (4); loss of enp (5) loss of ornamentation and enp (6);
Length of the apophysis of the male P3: short (0); long (1);
Relative position of male setae I, II and III, and dorsal furcal setae VII: setae I, II, and III and seta VII inserted at distal third of the furca, or setae I, II and III anterior to the dorsal seta VII (0); at the same plane on furca’s midlength (1); setae I, II and III located proximally in the ventral margin of the furca, dorsal seta VII on the distal third (2);
Relative position of female lateral and dorsal furcal setae: lateral and dorsal seta inserted at the distal 1/3 of the furca or setae I, II, and III are anterior to the dorsal seta VII (0); at the same plane on furca’s midlength (1);
Shape of female furca: cylindrical (0); tapering distally (1);
Hyaline margin of male P3: present (1); absent (0);
Sexual dimorphism on P5: strong, based on difference of length (1); absent or based on differences of ornamentation (0);
Width of the proximal part of the endopod of male P4: narrow base (0); broad base (1);
Length and ornamentation of the endopod of the female P4: longer than exp-1with ornamentation at distal 1/3; shorter than exp-1 or as long as exp-1 (0);
Shape of exp-1 of the male P4: strongly concave at the inner margin (1); not concave (0);
Shape of exp of the male P3: inflate, with proximal and medial hyaline cushions (1); without this character (0);
Length of male P5: spiniform process reaching far beyond its own urosomite (1); short (0);
Length of female P5: spiniform process reaching far beyond its own urosomite (1); short (0);
Furca: dimorphic (1); monomorphic;
Enp of male P3: transformed into an aesthetasc-like seta (1); without this character (0);
Cuticle ornamentation of body somites: smooth (0); pitted (1);
Position of integumental window in the last and penultimate Urs: dorsal (0); lateral (1);
Size and shape of the inner process on the penultimate segment of the male A1: strong and sickle-shaped (1); different shape (0);
Ventral ornamentation of male Urs 3: two groups of spinules (1); absent (0);
Size of enp of the male P2: normally developed (0); strongly reduced (1);
Shape of the enp of the male P4: “Y”-shaped, proximally bifurcate, with a distal flagellum or lamella (1); of a different shape;
Shape of the apophysis of the male P3: foliaceous and acuminate (1); different (0);
Length of the thumb of the exopod of the male P3: longer or as long as apophysis (0), shorter than apophysis (1);
Shape of the enp of the male P4: foliaceous or triangular lamella (0); y-shaped enp (1); long spiniform (2); short, claw-like, outwardly curved (3); lost (4);
Shape of the apophysis on the male P3 exp: smooth (0); proximally dilated, with a soft median attenuation and a thinner distal lamella at the outer margin (1); proximally dilated, with a subtle median depression and a thinner distal lamella (2);
Length of furca relative to the telson: longer than telson (1); as long or shorter than telson (0);
Shape of the enp of the male P4: spiniform, curved inwards, sigmoid (1); different shape (0);
Enp of the male P2: present (0); absent (1);
P5 in both sexes: present (0); reduced (1); absent (2);
Shape of thumb of the exp of the male P3: a pointed spine (0); digitiform, with rounded tip (1);
Outer seta of basis of P4: present (0); absent (1);
P5 dimorphism: with a single seta in both sexes, elongate in male (1); with 2 or more setae (0);
Distal pore on the spiniform inner process of P5: present (1); absent (0);
Shape of male furca: cylindrical (0); tapering distally (1); allometric in growth (2);
Ornamentation of the proximal outer margin of the male P3: more than two spinules (0); two spinules (1); less than two spinules (2); not ornamented (3);
The phylogenetic study of the family Parastenocarididae is a difficult task, which means working up
A phylogenetic hypothesis of the evolution of the subfamily Parastenocaridinae is herein proposed in order to discuss the phylogenetic position of the genus Eirinicaris. Recently,
Phylogeny of the Parastenocaridinae reconstructed by applying Hennigian principles and criterion of putative parsimony based on the data matrix of Table
The monophyletic status of the Parastenocarididae, Parastenocaridinae and Fontinalicaridinae were discussed in previous studies (Martínez Arbizu and Moura 1994;
Parastenocaridinae. Schmincke (2010) proposes the following diagnostic characters for the Parastenocaridinae, avoiding to make inferences about the polarization of the characters: 1) the segments 5 and 7 form a functional unit for clasping the female. The segment 7 is sickle-shaped in some species, with an apophysis developed at the distal inner corner, and can fold back onto the fifth segment during copula whereas the segment 8 points medially; 2) female P3 enp is long and spiniform; 3) the apophysis of male P3 is unarmed in most of the species; 4) the coxa of male P4 lacks an inner row of spinules, but a row of spinules may be present near the insertion of endopod or medially of the basis; 5) except for species of Kinnecaris, Monodicaris and Macacocaris, all Parastenocaridinae share a small P5 in both sexes, not reaching far beyond its own somite; 6) female genital field is rectangular and much broader than high, and 7) the lateral setae I, II, and III occur at the same level as, and almost opposite to, the dorsal seta VII.
Eirinicaris can be included within the Parastenocaridinae because of the following synapomorphies (Characters 30–33):
a) Female P3 enp long, and spiniform, without distal seta (ap);
b) the group of three lateral setae of the furca (setae I, II and III), and the dorsal seta VII aligned (viz. female) (ap);
c) A1 is haplocer, with small process in segment 7 (this process is sickle-shaped in genera such as Kinnecaris and Monodicaris); segments 5, 6, and 7 forming a functional unit for clasping the female, in grasping position, segment 7 bends inwards against segment 6, segment 8 points in opposite direction (ap);
d) the apophysis and terminal seta of the exp of male P3 fused (ap);
In addition, Eirinicaris share the following symplesiomorphies with other Parastenocaridinae (Characters 26 and 28):
d) genital field rectangular, much broader than the height (pl);
e) basis of P1 with an inner seta (pl);
Length and shape of enp of female P3 (Character 30). Ranga Reddy et al. (2014) considered the female P3 with a terminal seta fused to the enp as a plesiomorphy for the Parastenocaridinae. However, we consider this character as an autapomorphy for the Parastenocaridinae, and the reduced, unarmed and linguiform enp as a plesiomorphy for the Fontinalicaridinae. Our decision is based on the observation of the copepodid development of the fontinalicaridin Proserpinicaris phyllura (Kiefer, 1938) described by
Relative position of lateral and dorsal furcal setae (Character 31). This character is the best documented for the family (
Penultimate segment of the male A1 (Character 32), and geniculation. Similarly to other Parastenocaridinae with penultimate segment of the male A1 sickle-shaped, and with a functional clasping unit formed by segments 5, 6 and 7 (pocket-knife type,
Armature of the apophysis of male P3 (Character 33). The apophysis is generally long and with a distal spine in Fontinalicaridinae, and the spine is usually missing in the Parastenocaridinae (see
The following two characters are considered symplesiomorphies for the Parastenocaridinae.
Inner seta on the basis of P1 (Character 26) The presence/absence of an inner seta on the basis of the P1 has been exhaustively discussed by Galassi and De Laurentiis (2004) and
Shape of the genital operculum (Character 28). A genital operculum which is broader than the height, appears consistently in the females of all the species of Parastenocaridinae studied so far. Interestingly, at least two types of genital operculum are evident within the Parastenocaridinae. In Eirinicaris, Simplicaris and Kinnecaris (see
Ranga Reddy et al. (2014) proposed a division of the Parastenocaridinae into two basic monophyletic groups: one composed by Himalayacaris, Remaneicaris and the Parastenocaris tirupatiensis-group (Indocaris), and a group composed of the remaining Parastenocaridinae, called here the crown-group. Our phylogenetic study confirms that Ranga Reddy’s et al. (2014: 813) characters 34 (position of outer setae on third exopodal segment of leg 4) and 35 (spinules near the insertion of the endopod of male leg 4) support the clade formed by Himalayacaris, Remaneicaris and Indocaris as proposed by Ranga Reddy et al. (2014). Characters 38 to 41 appear convergently in two monophyletic groups (Remaneicaris-Indocaris and Kinnecaris-Monodicaris). Character 37 is an autapomorphy for Himalayacaris. Character 50 is autapomorphic for Remaneicaris. Character 62 is autapomorphic for Kinnecaris. For a discussion on the relationships within this group see Ranga Reddy et al. (2014).
The crown-group is supported in the present study by character 44 (ornamentation of the basis of the male P4) and character 45 (length of the apophysis of the male P3). These are discussed below.
Ornamentation of the basis of the male P4 (Character 44). A row of spinules on the basis of the male P4 close to the insertion site of the enp appears in derived groups within Remaneicaris (
Within the crown-group, this character evolves into a strong row of unequal spinules in Stammericaris, Cottarellicaris and Monodicaris. These spinules are strongly sclerotized and unequal in Parastenocaris, slender in Kinnecaris and are missing in Eirinicaris. Strong unequal spinules are present in Kinnecaris giselae Schminke, 2008. The condition observed in species of Cottarellicaris, Stammericaris, and in other species such as P. palmerae Reid, 1992, is not homologous to the condition observed for Parastenocaris brevipes and closely related species. In Parastenocaris, the spinular complex involves sclerotization, heteromorphy of the spinules, and the presence of anterior and posterior spinules on the basis. With exception of the enlargement and sclerotization of some spinules, nothing similar has been observed for Cottarellicaris, Stammericaris, and P. palmerae.
Length of the apophysis of the male P3 (Character 45). Remaneicaris, Indocaris and Himalayacaris have short apophyses which are, in general, as long as wide. Exceptions for this can be observed in Indocaris inopinata Ranga Reddy, Totakura & Shaik, 2016, and in Indocaris tirupatiensis (Ranga Reddy 2011). The shortest apophyses are found in Indocaris imbricata Ranga Reddy, Totakura & Shaik, 2016, and in Himalayacaris alaknanda Ranga Reddy, Totakura & Corgosinho, 2014, and in basal members of Remaneicaris, with some exceptions occurring in species belonging to more derived groups within Remaneicaris such as R. membranaceae (Noodt, 1965) and R. oncophora (Noodt, 1965) (Noodt 1965, Corgosinho 2007). The elongated apophysis seems to be also a derived character in Indocaris. Interestingly, I. inopinata displays an intermediate condition between I. imbricata and I. tirupatiensis. Hence, it seems more parsimonious to assume a shorter apophysis for the ground pattern of the Parastenocaridinae. A longer apophysis is a synapomorphy for the crown-group, and a convergent short apophysis appears both within the basal Parastenocaridinae as well as within the crown-group (viz. Cottarellicaris).
Following the above reasoning, the crown-group as defined here, can be divided into Michelicaris and two large monophyletic groups composed by the following genera:
a) Group-1: Stammericaris, Cottarellicaris, Italicocaris, Entzicaris, Horstkurtcaris, Macacocaris, Nanacaris, Asiacaris, Clujensicaris, Simplicaris, Lacustricaris, and Minutacaris;
b) Group-2: Parastenocaris, Kinnecaris, Monodicaris, and Eirinicaris.
Group-1. The monophyly of group-1 is supported on the ground of a complex series of transformations of the male P4 enp (Character 67).
Four main monophyletic subgroups were identified within group-1: (Stammericaris, Cottarellicaris); (Italicocaris, (Entzicaris, Horstkurtcaris)); Macacocaris; and ((Clujensicaris, (Asiacaris, Nanacaris)), (Minutacaris, (Simplicaris, Lacustricaris))).
Italicocaris, Entzicaris and Horstkurtcaris share a P3 apophysis with a “recorted” outer margin (Character 68, shape of the apophysis on the male P3 exp), proximally dilated, with a median depression and a thinner distal lamella. It is important to stress that
The third is composed solely by the genera Macacocaris; the fourth subgroup is composed by Clujensicaris, Asiacaris, Nanacaris, Simplicaris, Minutacaris; and Lacustricaris. In most of these species the male P3 exp is slender, slightly curved towards the inner margin, the apophysis is elongate, blade-shaped, with a rounded tip, without distal seta; the thumb ranges from smaller than the apophysis (Character 66; 0→1) as in Simplicaris, Minutacaris, Nanacaris, and Clujensicaris), to larger than the apophysis (Character 66; 1→0) as in Asiacaris. The monophyly of the group composed of Nanacaris, Asiacaris, Clujensicaris, Minutacaris, Simplicaris and Lacustricaris is supported by the presence of a short spiniform enp of the male P4 (Character 67), which is lost in Nannacaris, Asiacaris and Clujensicaris. This group also diplays a trend towards the reduction or loss of the armature of the basis of the male P4 as in Asiacaris and Clujensicaris (Character 44). This character appears convergently in Himalayacaris alaknanda. However, the male P4 enp is not completely lost in H. alaknanda, appearing as an inner uncinate bud on the basis.
The phylogenetic position of Macacocaris is difficult to decipher. Macacocaris shares many characters with other genera, such as the short enp of the male P4 (Character 63) as in Monodicaris, the pitted cuticle (Character 61) as in Kinnecaris and Monodicaris, strong and unequal ornamentation of the inner basis of the male P4 as in Monodicaris, Parastenocaris, Stammericaris and Cottarellicaris, and the dimorphic P5 (shorter in the male, with the elements arranged distally as in Parastenocaris). Additionally, the males of the genus Macacocaris males possess a strongly transformed A1, which
Group-2. This group is composed of the genera Parastenocaris, Kinnecaris, Monodicaris, and Eirinicaris.
“The Brevipes-group must be closely related to the Muscicola-group. The enp of P4 is built in the same way in both groups, however, the Brevipes-group, which is the most derived group of both, have kept the basal tooth or finger-like processes.” (free translation from
Parastenocaris, Kinnecaris and Monodicaris share the tapering furca in the male and female in which the lateral setae I, II and III, and the dorsal seta VII are situated in the middle of the rami, setae I, II and III opposite to seta VII (Characters 46 an 47, for the male and female, respectively). The tapering furca and the position of setae I, II, and III aligned opposite to seta VII is observed in the female of Eirinicaris (Character 48), changing position of setae I, II, and III, their relative position to seta VII (with a large gap between them), the shape and ornamentation of the furca in the male as the result of the extreme dimorphism.
Eirinicaris is closely related to Kinnecaris and Monodicaris. These three genera share the long spiniform process on the male and female P5, reaching beyond the middle of the second (genital) urosomite (Characters 55 and 56 for the male and female, respectively), and proximal insertion of the lateral setae on the female. An interesting character, which was previously described for Kinnecaris by
On the morphology of Eirinicaris gen. n. Eirinicaris gen. n. is an intriguing genus with some unique characters. The basis of the male P1 possesses a very long inner seta, a character never reported for this family before. The telson and furca are very ornate in the males of this species, and the furca exhibits an extreme level of dimorphism with setae I, II and III situated proximally on the ventral side of the furca. Spinular ornamentation on the telson and furca is not uncommon within the family. The presence of spinular ornamentation on the telson is present in species closely related to the parastenocaridin R. analuizae Corgosinho & Martínez Arbizu, 2005 and R. tridactyla Corgosinho, Martínez Arbizu and Santos-Silva, 2007. Other species within this subfamily such as P. spinicauda Wells, 1964, P. spinosa Wells, 1964, P. trisaetosa Chappuis, 1954, also possess spinular ornamentation on the telson. Within the Fontinalicaridinae, Parastenocaris nigerianus Chappuis, 1959 and some species of Forficatocaris exhibit spinular ornamentation of the telson. Concerning the furca, normally the modification occurs in females (
Equally impressive is the level of modification of the posterior seta of the last segment of the A1, the endopod of the P3 and the furcal setae I, II, and III in the males. The last segment of the male A1 possesses an additional modified aesthetasc-like seta ventrally. Additionally, the enp of the male P3, and the furcal setae II and III are transformed into aesthetasc-like structures. Within the Copepoda the aesthetascs are generally restricted to the A1. Aesthetascs are also present in the mouthparts of some Paranannopidae Por, 1986 (
Distribution and ecology. Prior to this study, Remaneicaris was the only representative of Parastenocaridinae in the Neotropical zone. The discovery of Eirinicaris in Brazil extends the geographical distribution of other monophyletic groups of Parastenocaridinae to South America, hence, indicating that all the main phylogenetic lineages of Parastenocarididae were already present in a vast geographical area, before the split of Pangea.
The authors would like to thank the National Council for Scientific and Technological Development (CNPq) and the São Paulo Research Foundation (FAPESP) for financing the project “Biodiversity of Microcrustaceans in Brazilian Rocky Fields” within the SCOPE of SISBIOTA (CNPq 563318/2010-4/ FAPESP 2010/52318-6). We also thank the Chico Mendes Institute for Biodiversity Conservation (ICMBio) and the Brazilian Institute of Environment and Renewable Natural Resources (IBAMA), the first for allowing our studies at the National Park of the Chapada dos Veadeiros (North of Goiás, Brazil) and the second for issuing permits to collect freshwater invertebrates in National Parks and other Brazilian territories. We are especially in debt to the director of the National Park of the Chapada dos Veadeiros and his staff for the field support and logistics.