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Corresponding author: Sanda Iepure ( sanda.iepure@academia-cj.ro ) Academic editor: Giuseppe Messana
© 2021 Sanda Iepure, Carmen-Andreea Bădăluţă, Oana Teodora Moldovan.
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:
Iepure S, Bădăluţă C-A, Moldovan OT (2021) An annotated checklist of groundwater Cyclopoida and Harpacticoida (Crustacea, Copepoda) from Romania with notes on their distribution and ecology. Subterranean Biology 41: 87-108. https://doi.org/10.3897/subtbiol.41.72542
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Romania, by its position in East-Central Europe has a complex geological history, high landscape heterogeneity and variable climatic conditions, ranging from temperate-continental in the northeast to sub-Mediterranean in the southwest. These conditions have created repeated waves of colonisation of groundwater by copepods, which raise particular interest in this group from a biogeographical perspective. The earliest investigations on groundwater copepods, dating back to the beginning of the 19th century, have resulted in a wealth of information on the richness of this group, making Romania one of the best studied regions from this perspective in Europe. Groundwater copepods in Romania are currently represented by 107 species and subspecies, of which 60 are harpacticoids (56%) and 47 are cyclopoids (43.9%). Of these, 50.5% are strict stygobites (32.7% harpacticoids and 17.7% cyclopoids). Among stygobite copepods 29 species (35 harpacticoids and 19 cyclopoids) are endemic to the country. Almost 86% of the species are single-site endemics (single cave, or single hyporheic or phreatic site) and the rest are restricted in distribution to a single aquifer or hydrographic basin. The aim of the present checklist represents a significant contribution to the knowledge of groundwater copepods in Romania and provides a sound baseline for future comparative faunal studies focused on the affinities and origins of copepods and the analysis of their biogeographical distribution patterns at regional and continental scales.
Biodiversity, endemics, Romania, Subterranean habitats
Crustaceans are the most diversified group of aquatic invertebrates in groundwater, representing more than 65% of the total groundwater species currently known from Europe (
Copepods are highly diversified in groundwaters and commonly subjected to isolation and allopatric speciation and discontinuous distributions because of vicariance in isolated areas or following ancient drainage patterns (
In the last decades, several works have been oriented towards explaining copepods high diversity at a continental level and especially in the western and central part of Europe (
Eastern Europe has a great diversity of groundwater fauna in karst and non-karst regions distributed from the Black Sea to the highest peaks of the Carpathians and Balkan Mountains. This heterogeneous landscape has been shaped by paleogeographic and paleoclimatic events (
Groundwater
crustaceans in Romania are represented by more than 300 taxa (
Studies of groundwater copepods in Romania have long history dating back to the 1900s when Pierre-Alfred Chappuis started his work on the taxonomy at the Speleological Institute Emil Racovita in Cluj until 1956. Among copepods, the harpacticoids were the subject of his studies in this country; he published more than 160 articles and described more than 70% of the currently known species (
Harpacticoids have been studied mainly by Eugen Şerban (1956) and Doina Zincenco (1967–1970).
The past decade was marked by a renewed interest on the taxonomy of copepods from Romania, resulting in new descriptions of species and new records of species previously known from single or a few sites of this country (
As part of an ongoing project aimed to revise the systematics of groundwater copepods from Romania, we here assembled an updated checklist of copepods known to date along with some notes on their geographical distribution, habitat preferences and ecology. Our goal is to complement the previous works by including a comprehensive bibliography of copepods in Romanian groundwater and unpublished data.
The study area is Romania (centered on 45°N, 25°E) and cover 238,391 km2. The country is located in the south-eastern part of central Europe and is bounded by the Carpathian Mountains, the lower course of the Danube (for a length of 1,075 km), and the Black Sea. The country has a great diversity in topography (altitudinal range from sea level to 2544 m a.s.l.), geological substrates and climate (Fig.
A total of 1.9% (~ 4400 km2) of the exposed land surface of Romania is represented by isolated karstified rocks of Mesozoic ages, strongly influenced by the Neozoic uplift of the Carpathian Mountains which broke the unity of most limestone outcrops (
The Apuseni Mountains (10,750 km2) include the most important karst area of Romania (
The Banat karst hosts the largest compact limestone area in Romania (Fig.
Dobrogea karst comprises a group of low elevation mountains and tablelands between the Danube and the Black Sea (< 500 m a.s.l.) (Fig.
The Romanian copepods checklist has been assembled by gathering copepod species records available from current literature, species records mentioned in projects reports and unpublished data collected by the author (Sanda Iepure) referred to as present data. Data from 485 geo-referenced subterranean localities corresponding to 248 sites were assembled. Copepod species distribution maps were generated using ArcGIS software, version 10.2.2 (
Subterranean localities included in the dataset account for 107 species and subspecies and records of undescribed and new to science taxa are not included. Sampling in the selected habitats has been constrained by suitable accessibility to the aquifers: caves, wells and hyporheic zone. The methods used for sampling vary from direct water filtering in caves, springs, and wells. The hyporheic zone is sampled by using the Bou-Rouch (
The taxonomy and the recent changes in species names were updated using the
In the Suppl. material
The elevation of sampling sites ranges from 0 to 1250 m a.s.l., about 81% of sites occurs below 800 m a.s.l. Cyclopoids have been recorded from more than 61% of sites (300 out of a total of 485 records), the remaining ones being harpacticoids (185 records). Ecologically, stygobite copepods are the best represented (54 species representing 51.42% from the total), followed by stygophiles (29 species, 27.2% from the total) and stygoxenes (22 species, representing 20.95% from the total).
Copepods are mostly recorded from caves (113 harpacticoid species and 120 cyclopoid species) and the hyporheic zone (with 27 harpacticoid species and 110 cyclopoid species). The second most diverse habitat for harpacticoids is the tap water (24 species), wells (12 species) and springs (six species); and for cyclopoids, wells (48 species), springs (11) and tap water (10), respectively.
The harpacticoids are the most diverse group in groundwater of Romania, with 60 species (56%) from 184 sites, which belong to three families: Canthocamptidae (with two subfamilies, Canthocamptinae and Morariinae and ten genera), Ameiridae (one subfamily, Ameirinae and two genera) and Parastenocarididae (with five genera). The most frequent species are two stygophiles (Bryocamptus unisaetosus and B. echinatus) and one stygobite (Spelaeocamptus spelaeus) (Fig.
The distribution of the four most abundat stygobite species of copepods in the dataset. a Distribution of Spelaeocamptus spelaeus (Harpacticoida) in Romania based on 16 occurences (15 caves and one tap water) b Distribution of Acanthocyclops milotai (Cyclopoida) in Romania based based on 13 occurences (caves) c Distribution of Diacyclops clandestinus in Romania based on 13 occurences (caves, hyporheic, wells, springs, tap water) d Distribution of Acanthocyclops kieferi in Romania based on 12 occurences (caves, hyporheic, wells, tap water).
The main representatives harpacticoid copepods were species of the genera Bryocamptus (16 species), Elaphoidella (10) and Parastenocaris (9) (Table
Summary of groundwater copepods inventory: number of taxa, ecology, groundwater habitats and endemics.
Harpacticoida | Cyclopoida | |
---|---|---|
Families | 4 | 2 |
Subfamilies | 4 | 2 |
Genera | 19 | 14 |
Species | 59 | 47 |
Ecology | ||
Stygoxenes | 8 | 22 |
Stygophyles | 17 | 6 |
Stygobites | 35 | 19 |
Groundwater habitats | ||
Caves | 113 | 120 |
Wells | 12 | 48 |
Aquifers | 24 | 9 |
Hyporheic zone | 27 | 110 |
Springs | 6 | 10 |
Endemics | 18 | 11 |
Elaphoidella
is the second more species-rich harpacticoid genus in Romanian groundwater, the majority of species being known from the southern part (Suppl. material
Parastenocaris
species are mainly known from caves and tap waters (of Cluj Napoca and Bucuresti towns) and only one species is recorded from the interstitial marine sediments close to the Black Sea (Suppl. material
Cyclopoids with 47 species and subspecies (43.9%) belong to two families, Halicyclopidae (with one genus) and Cyclopidae (with two subfamilies, Eucyclopinae and Cyclopinae and 13 genera). Halicyclopinae, usually found in brackish waters is represented by one species Halicyclops rotundipes reported from interstitial sediments of the Black Sea coast (Fig.
The species of Paracyclops have been recorded from different types of groundwater habitats in Romania, but mainly from the hyporheic habitat, e.g., P. imminutus Kiefer, 1929 and P. fimbriatus (Fischer 1853) (
The subfamily Cyclopinae is the main contributor to species diversity among the Cyclopidae and has few genera that successfully colonized groundwaters i.e., Acanthocyclops (15 species), Diacyclops (nine) and Speocyclops (two). All three genera include an important fraction of stygobionts reported from karst and detrital aquifers.
Acanthocyclops
has 13 stygobites, two stygoxenes and one stygophile. The stygobiont species of Acanthocyclops belong to two distinct lineages: (1) kieferi, a highly diversified group in the Mediterranean region including 10 species found in saturated karst (Apuseni and Banat Mountains), and hyporheic zone of rivers (
Diacyclops
appears highly diversified in the hyporheic zone of Romanian rivers, from which several species at present assigned to the species D. clandestinus and species belonging to the D. languidoides-group are still to be described. Speocyclops has only two species described from Romania, Speocyclops troglodites from caves in Apuseni Mountains and S. lindbergi from one cave in Banat. Graeteriella, a stygobite genus of Cyclopinae widely distributed in groundwater from western continental Europe (
The species of Cyclops, a predominantly Palearctic cold‐adapted genus and rare in groundwater (
The present checklist provides an updated taxonomy and distribution of copepods in Romanian groundwater. Overall, a total of 107 species and subspecies distributed among four families, five subfamilies and 33 genera of which 54 stygobites are included in this list (Tables
The copepod diversity is dominated by Canthocamptidae and Cyclopidae, showing high similarities with those of neighboring ECE regions (
Hotspots, referred to as areas of high groundwater biodiversity at the country level are the karst areas of Apuseni (in northwest) and Banat Mountains (in southwest) (Figs
Copepods seem to be unequally distributed throughout the country, with large cold spots especially in non-karst areas or the alpine region in the Carpathian Mountains, which are still poorly explored (Fig.
Groundwater
copepods of Romania are divided in two main groups regarding their origin: some families have a direct marine origin, with relatives still living in the primary environment while some others are of more ancient freshwater origin, for which the closest relatives are traceable in surface freshwater or semiterrestrial wet habitats (
The taxa of freshwater origin are more frequently recorded from Romanian groundwater. Among the Harpacticoida, the most successfully in the subterranean domain are the species of Elaphoidella, Bryocamptus, Moraria, and Parastenocaris and the Eucyclops, Acanthocyclops and Diacyclops genera among the Cyclopoida.
Species | Localities | Habitat |
---|---|---|
Copepoda Harpacticoida | ||
Chappuisius inopinus | Bucureşti | Tap water |
Clujensicaris clujensis | Cluj Napoca, Sura Mare cave | Tap water, cave |
Elaphoidella damianae | Bucureşti | Tap water |
Elaphoidella elaphoides | Bucureşti | Tap water |
Elaphoidella gracilis serrulata | Bucureşti | Tap water |
Elaphoidella juxtaputealis | Bucureşti | Tap water |
Elaphoidella romanica | Buhui Cave, Gaura Porcariului Cave | Cave |
Nitocrella hirta bucarestiensis | Bucureşti | Tap water |
Parastenocaris chappuisi | Mamaia | Interstitial |
Parastenocaris jeanneli | Bucureşti | Tap water |
Parastenocaris karamani brevicaudata | Bucureşti | Tap water |
Parastenocaris latisaetosus | Bucureşti | Tap water |
Parastenocaris minuta | Cluj Napoca | Tap water |
Parastenocaris nana | Cluj Napoca | Tap water |
Parastenocaris pannonica | Bucureşti | Tap water |
Parastenocaris phreatica | Cetatile Ponorului Cave | Cave |
Parastenocaris subterranea | Bucureşti | Tap water |
Parastenocaris uncinatus | Bucureşti | Tap water |
Copepoda Cyclopoida | ||
Eucyclops graeteri scythicus | Movile Cave | Cave |
Acanthocyclops balcanicus bisaetosus | Alun Cave, din Dealul Humpleului Cave, Pepii Cave, Poarta Alunului Cave | Cave |
Acanthocyclops milotai | Oase Cave, Buhui Cave, Pauleasa Pothole, Socolovat Cave, Ponor Plopa Cave, Ponor Uscata Cave, Boilor Cave, de sub Carsa Cave, Gaurile lui Miloi II Cave, Padina Matei Cave, Padina Popii Cave, Gaura Haiduceasca Cave, de sub Cetate Cave II, de sub Rol Cave | Cave |
Acanthocyclops plesai | Din Fata Rachitii Cave | Cave |
Acanthocyclops propinquus | Corbasca Cave, Magura Cave | Cave |
Acanthocyclops radevi | Limanu | Well |
Acanthocyclops cf. reductus | De dupa Carsa Cave | Cave |
Acanthocyclops stygius | Cluj Napoca, Dracoaia Cave, Sighistel Valley | Tap water, cave, hyporheic zone |
Acanthocyclops transylvanicus | Cotețul Dobreștilor Cave, Poarta Alunului Cave, Întorsuri Cave Ciur Izbuc Cave, Ungurului Cave, Dobos Cave | Cave |
Speocyclops lindbergi | Hotilor de la Baile Herculane Cave | Cave |
Taxonomic summary of cave copepods biodiversity hotspots (with * stygobite species).
Pestera de la Vadul Crisului |
HARPACTICOIDA |
Attheyella crassa |
Bryocamptus caucasicus |
Bryocamptus dacicus * |
Bryocamptus spinulosus |
Bryocamptus tatrensis |
Bryocamptus typhlops |
Bryocamptus vejdovskyi |
Maraenobiotus brucei carpathicus |
Maraenobiotus vejdovskyi vejdovskyi |
Moraria (Moraria) poppei |
Moraria brevipes |
Elaphoidella putealis * |
Pesceus schmeili |
Spelaeocamptus spelaeus * |
Cyclopoida |
Eucyclops serrulatus serrulatus |
Paracyclops fimbriatus |
Diacyclops bisetosus |
Megacyclops viridis |
Speocyclops troglodites * |
Pestera Moanei |
HARPACTICOIDA |
Attheyella wierzejskii |
Bryocamptus cfr. baikalensis |
Bryocamptus bispinosus |
Bryocamptus dacicus |
Bryocamptus echinatus |
Bryocamptus minutus |
Bryocamptus spinulosus |
Bryocamptus tatrensis |
Bryocampthus unisaetosus * |
Pesceus schmeili |
CYCLOPOIDA |
Paracyclops fimbriatus |
Pestera Ungurului |
HARPACTICOIDA |
Bryocamptus caucasicus |
Bryocamptus tatrensis |
Bryocamptus typhlops |
Bryocamptus zschokkei |
Maraenobiotus brucei carpathicus |
Pesceus schmeili |
Spelaeocamptus spelaeus * |
CYCLOPOIDA |
Acanthocyclops transylvanicus * |
Paracyclops fimbriatus |
The "insular" distribution of the listed endemic copepods is summarized in Table
The total number of endemic groundwater copepods is relatively low, 29 out of a total of 105 (representing 27.62%; Table
The hotspot localities of endemic species in Romania remain the tap water in București (12 endemics out of a total of 19 species) and Cluj Napoca (four out of a total of seven species) described by
Among harpacticoids, the genus with the highest number of endemics is Parastenocaris, Ecologically, Parastenocaris species have a preference for interstitial waters but the species in Romania, including the endemics, are all documented from caves (usually unsaturated epikarst) and tap water (phreatic habitat). The exception is P. chappuisi, which was found in interstitial waters close to the Black Sea coast.
The second most diverse endemic harpacticoid genus was Elaphoidella, with five endemic species out of a total of 10. Elaphoidella is cosmopolitan in distribution, usually inhabiting freshwaters and semi-terrestrial habitats. The other harpacticoid genera have usually two or three stygobites endemic species.
Among Cyclopoida the most diverse genera hosting endemics is Acanthocyclops with eight endemics out of a total of 15 (
This work was supported by a grant of the Ministry of Research, Innovation and Digitization, CNCS – UEFISCDI, project number PN-III-P4-ID-PCE-2020–2843 (EVO-DEVO-CAVE) within PNCDI III. SI and OTM were supported by a grant of the Ministry of Research, Innovation and Digitization, CNCS/CCCDI-UEFISCDI, project number 2/2019 (DARKFOOD), within PNCDI III. We thank both reviewers and the subject editor for the suggestions that improved the manuscript.
Checklist of groundwater Copepoda (Cyclopoida, Harpacticoida) from Romania
Data type: occurences, species ecology
Explanation note: Updated checklist of groundwater Copepoda (Cyclopoida, Harpacticoida) from Romania with their occurrence in the
sampling sites