Research Article |
Corresponding author: Paulo Henrique Costa Corgosinho ( pcorgo@gmail.com ) Academic editor: Kai Horst George
© 2020 Paulo Henrique Costa Corgosinho, Terue Cristina Kihara, Pedro Martínez Arbizu.
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, Kihara TC, Arbizu PM (2020) A new species of Psammonitocrella Huys, 2009 (Copepoda, Harpacticoida, Ameiridae) from California (USA), with a discussion of the relationship between Psammonitocrella and Parastenocarididae. ZooKeys 996: 19-35. https://doi.org/10.3897/zookeys.996.55034
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The freshwater harpacticoid Psammonitocrella kumeyaayi sp. nov. from the Nearctic Region (California; USA) is proposed. The position of the genus within Harpacticoida and its relationship with the Parastenocarididae is discussed. The new species can be included within Psammonitocrella on account of a) the cylindrical furca, longer than the telson, b) the unmodified inner spine on the basis of the male first leg, c) loss of the outer spine on the second exopodal segment of the first leg, d) loss of the outer spine of the third exopodal segment of the second, third, and fourth legs, e) loss of the inner apical seta on the third exopodal segment of the second and third legs, f) transformation of the inner apical seta of the third exopodal segment of the fourth leg into a spine, and g) loss of the endopodite of the fourth leg. The new species differs remarkably from P. boultoni, and P. longifurcata in the loss of the outer spine of the second exopodal segment of the fourth leg, in the presence of a one-segmented fifth leg exopodite, and in the presence of an outer seta on the basis of the first and second legs. Both Psammonitocrella and the known species of Parastenocarididae have a one-segmented endopod on the fourth leg, and the endopods of the second and third legs are reduced to one or two segments. Psammonitocrella is currently allocated into the Ameiridae, and evidence suggesting a sister-group relationship with Parastenocarididae—both share the loss of the inner seta on the first endopodal segment of the first leg—indicates that the Parastenocarididae should be included into the Ameiridae. In an evolutionary context, Parastenocarididae could have evolved from a lineage of freshwater ameirids that became interstitial in continental waters and colonized aquifers and groundwaters.
fresh water, groundwater diversity, meiofauna, phylogeny, Psammonitocrella kumeyaayi sp. nov., San Clemente Canyon, systematics
The family Ameiridae Boeck, 1865 is composed of about 300 species accommodated in 47 marine and freshwater genera (
Psammonitocrella Huys, 2009 is known only from the USA, and is represented by P. boultoni Rouch, 1992 and P. longifurcata Rouch, 1992. The taxonomic position of this genus was debated in the last decades. In their analysis of a wide range of ameirid-like taxa,
In this work we describe Psammonitocrella kumeyaayi sp. nov from the historical collection of late Professor W. Noodt, collected by himself in the state of California, USA, in 1974. An amended diagnosis is offered for the genus, and the position of the new species within the genus Psammonitocrella is briefly addressed. Here we discuss an alternative hypothesis for the position of Parastenocarididae within Harpacticoida.
A single male specimen of the new species was sorted from a sample collected by Prof. Wolfram Noodt on 29/03/1974 at a locality identified as San Clemente Canyon (California, USA). The sampling locality is described in Noodt’s field notebook and in the sample identification as “wenig fließendes stehendes Wasser”, an almost lotic or a standing water environment or with very low current. After an extensive toponymic search we concluded that Prof. Noodt was referring to the San Clemente Canyon in San Diego County. The San Clemente Canyon is nowadays included in the Marian Bear Memorial Park in the city of San Diego, a linear open space park along a canyon rich in temporary water bodies.
The habitus was drawn from the whole specimen temporarily mounted onto one slide with glycerin as mounting medium; adhesive plastic discs were used to support the cover slip and prevent destruction of the specimen (
The terms ‘furca’ and ‘telson’ are used according to
The diagnosis represents the reconstructed ground pattern of Psammonitocrella. It is amended from
Abbreviations used in the text and figures: A1= antennule, A2 = antenna, aes = aesthetasc, ap= apomorphy, benp(s)= basendopod(s), cph = cephalothorax, DAS= distal apical seta; DOS= distal outer seta; enp= endopod, exp(s)= exopod(s), enp1–3 = endopodal segments 1–3, exp1–3 = exopodal segments 1–3, Fu= furca, GF = genital field, IAS= inner apical seta/spine; ms= modified spine, md = mandible, mx1 = maxillule, mx2 = maxilla, mxp = maxilliped, P1–P6= legs 1 to 6, pl= plesiomorphy, Ur1 to 5= first to fifth urosomites.
Family Ameiridae Boeck, 1865
Ameiridae. Body small, slender, and cylindrical, without distinct demarcation between prosome and urosome. Integument weakly chitinized, with or without lateral cuticular windows on P2–P3-bearing somites (presence of these cuticular windows is uncertain for P. longifurcata and P. boultoni); hyaline posterior fringe of all somites smooth. First pedigerous somite incorporated into cephalosome. Prosome ornamented only with sensilla; Ur ornamented with rows of small spinules. Genital (Ur2) and Ur3 separated in female; GF with single large copulatory pore, wide copulatory duct, and two small semicircular seminal receptacles; single small genital aperture covered by fused reduced P6, without armature or ornamentation. Telson unornamented or ornamented with small spinules and tube pores. Anal operculum unornamented or ornamented with small spinules, wide and convex, not reaching or reaching posterior end of anal somite. Fu slender, tapering distally or cylindrical, slightly divergent, longer than anal somite, with long tube pores in P. kumeyaayi sp. nov.; seta VII inserted subdistally, close to inner margin, less than half the ramus length; outer setae I and II inserted on the proximal half of Fu; seta III on the same plane as seta VII; seta VI minute; seta V without breaking plane; seta IV longer, as long as or shorter than ramus. A1 long and slender, eight-segmented in female, 10-segmented, haplocer, and geniculate in male; without seta on short first segment in female, with a seta on the first segment in male. A2 composed of coxa, basis, two-segmented enp and one-segmented exp; exp armed with three setae. Md with narrow cutting edge and two-segmented uniramous palp; basis unarmed; enp with three to five apical setae. Mx1 with praecoxal arthrite armed with three distal claws, one or two minute oral setae, and one or two accessory aboral setae; coxa with two or three apical setae; basis with two to four apical setae; enp present or absent. Mx2 with syncoxal endite armed with a single element, or endite absent; basal endite armed with three elements; enp1 drawn out into a claw, with an accessory seta; remaining endopodal segment represented by one or two setae. Basis of P1 with unmodified inner spine in male, and with or without outer seta; without any other sexual dimorphism in swimming legs; basis of P2 with or without outer seta. Enp of P1 three-segmented; enp of P2 and P3 one- or two-segmented, of P4 reduced to small knob or completely absent; P1 enp1 unarmed, long, reaching distal margin of exp2 or nearly as long as exp1; P1 enp2 unarmed, longer than enp3; P1 enp3 with outer seta, with or without geniculation, inner seta probably geniculated in all species; if enp of P2 and P3 two-segmented, then first segment unarmed, second segment with one apical seta. All swimming legs with three-segmented exps; exopodal segments of P2–P4 subequal in length; P1–P4 exp1 without inner seta; exp2 of P1 without outer spine and with inner seta; exp2 of P2 and P3 with inner seta and outer spine; exp2 of P4 with or without outer spine and with inner seta; exp3 of P1 with two outer spines, two geniculate distal setae, and without inner armature; P2–P4 exp3 without outer spine; P2–P3 exp3 with or without inner apical seta; inner apical seta of P4 exp3 may be transformed into a spine. P5 similar in both sexes; fused to somite or free; with or without recognizable endopodal lobe, and with recognizable exopodal lobe, or exp one-segmented; endopodal lobe (if present) armed with one or two elements; exopodal lobe or exp with four, three, two or only one seta.
Psammonitocrella boultoni Rouch, 1992.
Psammonitocrella longifurcata Rouch, 1992; P. kumeyaayi sp. nov.
Setal formulae of the swimming legs as hypothesized to occur in the ground pattern of the genus. Roman numerals represent spines; Arabic numerals represent setae.
Legs | Basis | Exopod | Endopod |
---|---|---|---|
P1 | 1-I | I-0, 0-1, II-2-0 | 0-0, 0-0, 0-I+1*-0 |
P2 | 1-0 | I-0, I-1, 0-I+2**-0 | 0-0, 0-1-0+ |
P3 | 1-0 | I-0, I-1, 0-I+1-0 | 0-0, 0-1-0+ |
P4 | 1-0 | I-0, I-1++, 0-I+1-I# | Knob## |
Holotype : One male dissected and mounted onto 7 slides (reg. no. SMF 37256/1-7; 1-7 refers to the number of slides).
Type locality : San Clemente Canyon, San Diego, California, USA (32.8446°N, 117.1949°W).
Total length 302 µm, measured from rostrum to end of furca. Rostrum not fused to cph, with two sensilla on tip (Fig.
A1 haplocer (Fig.
A2 (Fig.
Md (Fig.
Mx1 (Fig.
Mx2 (Fig.
Mxp (Fig.
P1 (Fig.
P2 (Fig.
P3 (Fig.
P4 (Fig.
P5 (Fig.
P6 (not shown) represented by unarmed cuticular flap.
Setal formulae of the swimming legs. Roman numerals represent spines; Arabic numerals represent setae and spiniform setae.
Legs | Basis | Exopod | Endopod |
---|---|---|---|
P1 | 1-I | I-0, 0-1, II-2-0 | 0-0, 0-0, 0-2-0 |
P2 | 1-0 | I-0, I-1, 0-I+1-0 | 0-0, 0-1-0+ |
P3 | 1-0 | I-0, I-1, 0-I+1-0 | 0-0, 0-1-0+ |
P4 | 1-0 | I-0, 0-1, 0-I+1-I | absent |
The specific epithet “kumeyaayi” refers to the Kumeyaay native American people, who inhabited the area of San Diego County for 10,000 years. Evidence of their presence still remains in San Clemente Canyon.
Female unknown. The presence of integumental windows on the third and fourth pedigerous somites was reported by
According to
In fact, the 250+ species of the Parastenocarididae would code in the cladistic analysis of
One important achievement of
The simple removal of a genus from one family to another without proper discussion is naive, and it does not solve the real problem. The phylogenetic position of Psammonitocrella cannot be solved without discussing the position of its sister group, Parastenocarididae, nor without including in the discussion the Ameiridae as a whole. Note that also
The sister-group relationship between the Parastenocarididae and Psammonitocrella allows for only two systematic scenarios.
1) Parastenocarididae + Psammonitocrella are the sister group of the Ameiridae (or any other family). In this case, a new family should be proposed for Psammonitocrella, and the Parastenocarididae would be composed only by those species with the synapomorphic characters proposed by
or
2) Parastenocarididae + Psammonitocrella is a monophyletic group within the Ameiridae. In this case the family rank of the Parastenocarididae would be compromised. “Parastenocarididae” would be a junior subjective synonym of “Ameiridae”, and the Parastenocarididae + Psammonitocrella would be a derived group within the Ameiridae.
In an evolutionary context, it would make sense that the Parastenocarididae evolved from a lineage of freshwater ameirids that became interstitial in continental waters and colonized aquifers and groundwaters. The analysis offered by
We advocate for the consideration of alternative 2 as the most realistic evolutionary working scenario.
If we accept that Psammonitocrella is an Ameiridae, the evidence suggesting its sister-group relationship with the Parastenocarididae—both sharing the loss of the inner seta on the enp1 of the P1—indicates that the Parastenocarididae should be included into the Ameiridae. But the relationships to marine taxa as discussed by
According to
The family Parastenocarididae can be easily accommodated within the Ameiridae as the sister group of Psammonitocrella. Within the Parastenocarididae the P1 enp is reduced to a two-segmented enp [three-segmented P1 enp in Psammonitocrella], and the inner seta of P1 exp2 is lost [present in Psammonitocrella]; the enp of P2 and P3 is one-segmented [probably two-segmented in the ground pattern of Psammonitocrella], and the exp2 of P2 and P4 lost the inner and outer elements [present in Psammonitocrella]. The outer spine of the P4 exp2 is absent in the Parastenocarididae and in P. kumeyaayi sp. nov. For the mouthparts, the md has a uniramous palp in both Psammonitocrella and the Parastenocarididae (two-segmented in the former, without armature on the proximal segment, and one-segmented in the latter), and the mx1 has a reduced distal armature of three spines on the praecoxal arthrite of both taxa. Except for E. mexicana, the distal rim of the anal operculum of the species studied by
Taking this into account, future studies are necessary to unfold the relationship between the Ameiridae and Parastenocarididae. We believe that only a phylogenetic analysis of the Ameiridae and Parastenocarididae, with a large taxonomic coverage based on both traditional morphological and multi-gene datasets is suitable to undisputedly determine which one of the two hypotheses mentioned above is better supported by the data. Unfortunately, within the Harpacticoida the taxon sampling for molecular work is still in its infancy.
The monophyly of Psammonitocrella can be supported by some reductions of the armature of P1 to P4, and the length of the furca. Of remarkable importance is the cylindrical furca which is also longer than the telson (ap), the basis of P1 in male with unmodified inner spine (ap), loss of the outer spine on the P1 exp2 (ap), loss of the outer spine of the exp3 of P2 (ap), P3 (ap) and P4 (ap), loss of the inner apical seta (IAS) on the exp3 of P3 (ap) (
Nowadays the genus Psammonitocrella is composed of P. boultoni and P. longifurcata from Sycamore creek (Arizona, USA), and P. kumeyaayi sp. nov. from the San Clemente Canyon, San Diego (California, USA). The new species differs remarkably from P. boultoni, and P. longifurcata in the loss of the outer spine of the P4 exp2 (ap), in the presence of a one-segmented P5 exp (pl), and in the presence of an outer seta of the basis of P1 (pl) and P2 (pl). The one-segmented exp of the P5 of P. kumeyaayi sp. nov. closely resembles that of P. boultoni. In the former species it is armed with four elements —one very reduced spine on the left limb—, and three setae are present in the exopodal lobe of the P5 of P. boultoni. However, the benp of P. kumeyaayi sp. nov. is armed with two spines, but it is armed with only one spine in P. boultoni. The enp of the P2 and P3 is two-segmented in both P. boultoni and P. kumeyaayi sp. nov., whereas the P2 and P3 enp is one-segmented in P. longifurcata. The shape and length of the furca is similar in P. boultoni and P. kumeyaayi sp. nov., and it is much longer in P. longifurcata.
The two-segmented P2 and P3 enps of P. boultoni and P. kumeyaayi sp. nov. are definitely plesiomorphic within the genus. The one-segmented P5 exp and the presence of two spines on the benp of P5 of P. kumeyaayi sp. nov are also considered plesiomorphic. The long furca of P. longifurcata seems to be an apomorphic condition within the genus. The presence of the outer seta on the basis of the P1 and P2 are plesiomorphic for P. kumeyaayi sp. nov. Considering this, it seems possible that P. longifurcata and P. boultoni forms a monophyletic group within Psammonitocrella, sharing the absence of the outer basal seta of P1 and P2, what could be also supported by the fact that P. longifurcata and P. boultoni occur in sympatry. The absence of the outer seta on the basis of P1 and P2 is uncommon within Harpacticoida, whilst the reduction or loss of the enp may have occurred convergently many times. Appendage reductions, character losses, and miniaturization (i.e., the evolution of extremely small adults) are common denominators of the ‘darkness syndrome’ of many stygobionts (
1 | Enp2 of P4 with outer spine | 2 |
– | Exp2 of P4 without outer spine; enp two-segmented in the P2 and P3; enp of P4 absent; armature of the exp3 of P2–P3 (0-I+1-0); armature of the exp-3 of P4 (0-I+1-I); P5 with an outer seta, benp with two spines, exp one-segmented, with asymmetric armature; telson and furca with long tube pores; furcal ramus about 2.5 longer than wide | P. kumeyaayi sp. nov. |
2 | Two-segmented enp of P2 and P3; enp P4 reduced to a knob; armature P2 and P3 exp3 (0-I+1-0); armature P4 exp3 (0-I+1-I); P5 with an outer seta, benp with a single seta, expopodal lobe fused to benp and armed with 3 setae; furcal ramus about 4 times longer than wide | P. boultoni |
– | One-segmented enp of P2 and P3; enp P4 absent; armature of P2 exp3 (0-I+2-0); armature of P3–P4 exp3 (0-I+1-0); P5 with an outer seta, reduced into a small plate, with asymmetric armature; furcal ramus almost 7 times longer than wide | P. longifurcata |
1) A new species of the freshwater ameirid genus Psammonitocrella is proposed for California (USA). The new species can be clearly distinguished from its congeners by the absence of the outer spine on P4 exp2 and the presence of a one-segmented P5 exp.
2) P. kumeyaayi sp. nov. is probably the sister group of a monophylum formed by P. boultoni and P. longifurcata. However, without the study of the species described by
3) If Psammonitocrella is an Ameiridae, the evidence suggesting its sister-group relationship with the Parastenocarididae indicates that the Parastenocarididae should be included into the Ameiridae.
4) Future phylogenetic studies should include both freshwater and marine ameirids, to test the hypothesis that some freshwater taxa are more related to marine ones, and that the invasion of the fresh water by this family followed multiple waves. In addition, the position of the Parastenocarididae and Leptopontiidae within the ameirid-like harpacticoids should be tested.
We would like to thank the CeDAMar (Census of Diversity of Abyssal Marine Life), which have supported the first author, granting him with a postdoctoral scholarship from 2004 to 2008. We are also indebted to the DZMB (Senckenberg am Meer, Wilhelmshaven, Germany) for the logistic support during this work. This study would not have been possible without the study of Noodt´s collection. We express our special gratitude to Dr Ahmed Ahnert who curated Noodt´s material after he passed away and put it at our disposal for the present study at the DZMB. The work of the first author was supported by FAPEMIG (CRA–BPV-00393-16 and CRABPV-00547-17). We would like to thank Dr Thomas Glatzel, Professor Dr Samuel Gómez and an anonymous reviewer for their valuable comments and corrections of the manuscript.