Biodiversity Data Journal :
Taxonomic Paper
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Corresponding author: Hanane Rassam (hananerassam@gmail.com)
Academic editor: Dimitris Poursanidis
Received: 22 Aug 2021 | Accepted: 14 Oct 2021 | Published: 02 Dec 2021
© 2021 Hanane Rassam, Mohamed Ghamizi, Hassan Benaissa, Catharina Clewing, Christian Albrecht
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:
Rassam H, Ghamizi M, Benaissa H, Clewing C, Albrecht C (2021) The fingernail clams (Bivalvia: Veneroida: Sphaeriidae) of Morocco: Diversity, distribution and conservation status. Biodiversity Data Journal 9: e73346. https://doi.org/10.3897/BDJ.9.e73346
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In Morocco, many uncertainties surround the current diversity and distribution of the bivalve family Sphaeriidae. Such information, including taxonomy and conservation status, are vital for further studies to improve the knowledge of this family in Morocco and represents the first step towards the development of a national conservation plan for all freshwater bivalves.
Between 2016 and 2019, several investigations were carried out to assess the diversity and distribution of Sphaeriidae in the different basins of Morocco, covering different types of habitat (lakes, springs, rivers and small ponds). The identification of specimens and their morpho-ecological features was based on morphological and morphometric analyses. The data on the general distribution of the collected species allowed the evaluation of their conservation status as well.
The shell morphology and morphometric analyses revealed the existence of five species belonging to the genus Pisidium [P. casertanum (Poli, 1791), P. (cf.) personatum Malm, 1855, P. subtruncatum Malm, 1855, P. amnicum (O. F. Müller, 1774) and Pisidium sp.] and one species to the genus of Musculium [M. lacustre (O. F. Müller, 1774)]. Sphaeriidae were found in all Moroccan basins, except Bouregreg and Sakia El Hamra-Oued Eddahab Basins. The results showed that Sebou Basin was the species richest with the occurrence of the five species, while Loukkos and Sous-Massa Basins had the lowest-species richness with one species only. The conservation status of sphaeriids in Morocco was evaluated for the first time and resulted in P. (cf.) personatum and P. subtruncatum being proposed as Least Concern and Vulnerable, respectively, while the status of Regionally Extinct is suggested for both species P. amnicum and M. lacustre.
First evaluation of the diversity and species richness of the family Sphaeriidae in Morocco with an assignment of an updated conservation status of the recorded species.
Pisidium, Musculium, Moroccan basins, mountain biodiversity, morphometry, conservation, freshwater ecosystems
The North African region is globally identified as containing ecosystems with an important biodiversity (
One of the freshwater taxa present in these rivers is the family Sphaeriidae, commonly referred to as fingernail and pea clams, including the tiniest freshwater bivalves in the world with lengths from 2 to 25 mm (
The North African Region represents a biogeographic transition between the Palearctic and Afrotropical realms. The molluscan biogeography of the North African Region is well-defined. On the basis of the composition of mollusc communities since the beginning of the Holocene,
Given the importance and the lack of information on the basic bio-ecological features of Sphaeriidae in Morocco, this study aims to: i) present a first evaluation of the diversity of Sphaeriidae in Morocco, including species richness and composition, using morphometric and geometric analysis, ii) assess the distribution pattern of Sphaeriidae in Moroccan freshwater basins and iii) assign a conservation status to the Moroccan species of Sphaeriidae.
Between 2016 and 2019, a total of 164 sampling sites were investigated covering the nine hydrological basins of Morocco (Fig.
Location of the study area with sampling sites. A Geographic position of Morocco. B Map of Morocco with different basins assigned with numbers following the national division of the basins; 1: Loukkos Basin, 2: Moulouya Basin; 3: Sebou Basin, 4: Bouregreg Basin, 5: Oum Er Rabia Basin, 6: Tensift Basin, 7: Drâa-Ziz-Rhériss Basin, 8: Souss-Massa Basin, 9: Sakia El Hamra- Oued Eddahab. C -F Distribution maps of all five species (M. lacustre and P. amnicum occur in the same locality) across the country with their respective bibliographic records (marked with rhombi) (coordinates are given in Suppl. material
Results of the morphometric analysis of three species of Sphaeriidae from Morocco. A Principal Component Analysis (PCA) with variables that contributed most to the PCA analysis, based on the measured ratios. Length L (maximum distance on the anterior – posterior axis), length of anterior part LA, length of posterior part LP, height H (maximum distance on the dorsal-ventral axis), length of umbo LU, length of the ligament of the left valve LL, length of the hinge LH, height of the hinge of the left valve HH; B Mean outline of semi-landmarks of the three species (species symbols as in A).
Altitudinal distribution range of species of Sphaeriidae: P. amnicum (
Extensive sampling of sphaeriids covered all types of freshwater habitats (river systems, streams, lakes, reservoirs, ponds and marshes) using a sieve of 200 µm pore diameter. The sampling was conducted to the possible extent in reachable areas with the highest probability of occurrence. Localities mentioned in bibliographic records of the presence of some species of Sphaeriidae were also visited and checked according to
Species were identified on the basis of the main morphological characters (e.g. hinge plate, shell shape, ligament pit) using, for example, the identification keys of Sphaeriidae presented by
For morphometric analysis, the specimens of different habitats and localities were photographed using a digital microscope system (Keyence VHX-2000). Seven variables were selected and measured on the three shell axes using the tpsDig v.2.17 programme (
From these measurements extracted from the photographs, a series of ratios was derived: hinge length/shell length (LH/L), shell width/shell length (W/L), shell height/shell length (H/L), hinge height/shell height (HH/H), ligament length/shell length (LL/L) and anterior length/posterior length (LA/LP). The statistical package PAST v.4.06 (
For outline analysis, 60 semi-landmarks were marked on the 30 right valves in order to draw a 2-dimensional mean shape for each of the three species using tpsrelw v.1.70 (
To identify the spatial distribution of Sphaeriidae in the Moroccan basins, the georeferenced records were projected on the map using QGIS software v. 3.4.1 (2018). “Between basins” comparison of the species composition was implemented using Jaccard’s Similarity Index, working with presence-absence data using the following expression:
Cj= a/(a+b+c),
where a is the number of species shared between the two compared sites, b and c are the number of species exclusive to site 1 and site 2, respectively. The index value goes from 0 (no similarity) to 1 (identical). A dendrogram was plotted using PAST v.4.06 (
The geographic range (criteria B) was used to evaluate the IUCN Red List category of Sphaeriidae in Morocco, based on the regional IUCN Red List guidelines. The extent of occurrence (EOO) and area of occupancy (AOO), respectively were defined according to the IUCN Red List (
Autochtonous
Cosmopolitan. More widely present in the Northern Hemisphere than the Southern one where it is more limited to high altitudes localities (
Shell dimensions: Mean length = 4.09 ± 0.7 mm; Mean height = 3.42 ± 0.59 mm; Mean width = 2.52 ± 0.76 mm.
Key features: Extremely variable, but can be separated from other species by its flattened umbo and shell (Fig.
Remarks: The species is known to be highly variable morphologically (
Autochtonous
Holarctic. Found in Europe, North Africa, Siberia to Baikal Lake and North America (
Shell dimensions: Mean length = 2.92 ± 1.23 mm; Mean height = 2.45 ± 1.08 mm; Mean width = 1.74 ± 1.37 mm.
Key features: Subtriangular shape with a striated shell, opisthogyrous umbo (Fig.
Europe, Asia and North Africa (
Shell dimensions: Mean length = 2.92 ± 0.7 mm; Mean height = 2.45 ± 0.6 mm; Mean width = 1.74 ± 0.88 mm.
Key features: Rounded shape, centrally located umbo, but not prominent. The presence of a raised callus in the hinge is a specific feature of the species (Fig.
Remarks: Pisidium personatum may be confused with P. casertanum as both species share similar morphological features, but P. personatum can be easily identified from other species of Pisidium by the presence of a callus in the hinge plate between the ligament pit and the lateral teeth on both valves, although it is less marked on the left valve.
Palearctic. More common in the north of Europe than in the south. In Morocco, it was reported in the present study only from a reservoir outlet.
Shell dimensions: Mean length = 8.5 ± 1.5 mm; Mean height = 6.96 ± 1.24 mm.
Key features: Large size (up to 10 mm) and clearly marked striations on the shell, irregularly spaced and denser near the umbo. The umbo is not prominent, placed posteriorly (Fig.
Two species of Sphaeriidae from Hachlaf lake. A Musculium lacustre, B- Pisidium amnicum. a,b- Internal view of right valve of M. lacustre and P. amnicum, respectively, c,d- Hinge plate of right valve of M. lacustre and P. amnicum, respectively, e,f- External view of the right valve of M. lacustre and P. amnicum, respectively.
Remarks: Pisidium amnicum remains the largest representative of Pisidium and, thus, it is always easy to distinguish.
Overall, no external distinguishing morphological features. However, the shell outline and hinge plate are closer to P. casertanum (Fig.
Shell dimensions: Length = 5.91-5.41 mm; Height = 4.71-4.45 mm
Key features: Quadrangular shell formed with a cap-like umbo centrally placed (Fig.
The morphological diagnosis and morphometric analysis of the sampled specimens were of great usefulness as they permitted the identification and discrimination of species, based on the different morphometric ratios calculated as shown in Fig.
More than 164 sites were sampled during the working period, out of which 56 were inhabited by species of Sphaeriidae (see Suppl. material
In terms of species richness, the Sebou Basin ranked first with the occurrence of all six species, whereas Souss-Massa and Moulouya had the lowest species number with only one species found. The Bouregreg and Sakia El Hamra-Oued Eddahab Basins were exceptional since no sphaeriids were found.
Pisidium casertanum was found in all the basins except Bouregreg and Sakia El Hamra-Oued Eddahab. Pisidium (cf.) personatum occurred in five basins: Loukkos, Tensift, Sebou, Souss-Massa and Oum Er Rabia. Pisidium subtruncatum was recorded in four basins: Tensift, Sebou, Moulouya and Oum Er Rabia. Pisidium sp. was present in both Oum Er Rabia and Sebou Basins, whereas P. amnicum and M. lacustre were only reported from Sebou Basin (Fig.
Extent of Occurrence and Area of Occupancy differed significantly amongst the regional populations of the species. EOO ranged from 15,219 km2 to 50,915 km2, while AOO ranged between 40 km2 and 104 km2. Table
Results of the regional conservation status assessment for three species of Sphaeriidae in Morocco. EOO: Extent of Occurrence, AOO: Area of Occupancy; no. unique occ.: number of unique occurrences; no. subPop.: number of subpopulations; no. loc: number of locations; LC: Least Concern; VU: Vulnerable; NA: Not applicable.
P. casertanum |
P. (cf.) personatum |
P. subtruncatum |
P. amnicum |
M. lacustre |
|
EOO (km2) |
50,915 |
45,741 |
15,219 |
NA |
NA |
AOO (km2) |
104 |
52 |
40 |
4 |
4 |
no. unique occ. |
27 |
13 |
11 |
1 |
1 |
no. subPop. |
16 |
13 |
8 |
1 |
1 |
no. loc |
20 |
13 |
8 |
1 |
1 |
category criteria B |
LC |
LC |
VU |
CR |
CR |
category code |
LC B1a+B2a |
LC B1a+B2a |
VU B1a+B2a |
CR B2a |
CR B2a |
The results of the present study confirmed the existence of at least six sphaeriid species occurring in different basins in Morocco. These findings have cleared up doubts about the existence of other species mentioned in literature as synonyms or living species in Morocco.
All the seven species recorded by
The difference in the number of species mentioned for Morocco may have several possible explanations: the identification on which the authors relied at the time was based on morphological and anatomical features; however, the genus Pisidium is cryptic and its species show pronounced intra-specific variations, influenced by environmental conditions (
Sphaeriids were collected in different habitat types, including lakes and reservoirs, springs, channels, marshes and rivers (streams, dam outlets and larger tributaries). River systems were the habitat with the greatest abundance of Sphaeriidae.
Pisidium casertanum was the most abundant species of sphaeriid in all habitat types. This species is euryeceous and is, therefore, considered the most common member of the family. It can be found in almost all habitat types ranging from temporal and ephemeral ponds to large rivers and lake bottoms (
The distribution of species of Sphaeriidae in Morocco is uneven across the nine basins and across the different altitudes. The highest diversity is recorded in the Middle Atlas which links the Sebou and Oum Er Rabia Basins with the presence of all the five species in the 50 x 50 km square around the city of Ifrane. The Middle Atlas is known for its richness in aquatic resources mainly from snowmelt and heavy rainfall, resulting in a variety of ecological habitats (springs, lakes, tributaries, marshes and large rivers), which may explain the specific diversity that occurs in this region.
With respect to elevation, the highest diversity of sphaeriids species in Morocco was found between 1,000 and 2,000 m a.s.l. in the Sebou Basin. No species were recorded below 462 m. Pisidium casertanum is the species that showed a wide altitudinal spectrum ranging from 462 to 3,137 m a.s.l. Despite being a lowland species (
The conservation status following the IUCN Red List guidelines was elaborated for the first time at the national level for all the species of Sphaeriidae recorded in Morocco. Out of the five species, P. casertanum and P. personatum have been assessed as “Least Concern” species in Morocco. Pisidium personatum was previously assessed by the IUCN Red List at the North African scale as Vulnerable (
In the present work, we present a first conclusive overview of the diversity and distribution of the species of Sphaeriidae in Morocco. The country very likely contains a western Palearctic relict fauna of sphaeriids, which, due to their small size, seem to be easily transported over long distances. Many European species have been found in North Africa and these findings are being tested in a phylogeographic context elsewhere. The faunistic and taxonomic data on Sphaeriidae and, particularly, on the genus Pisidium are scarce in Africa and even more so in North Africa. This is probably due to their small size, hidden mode of life and lack of clear diagnostic characters; therefore, listing the biodiversity of such a cryptic group may be impaired. Given this situation, more extensive future work is needed to study the ecology, life cycle patterns and the phylogeny of the species of Sphaeriidae.
The authors would like to address a special thanks to Ulrich Böβneck who passed away before the writing of this paper, for his contribution in the field work and helping the first author with valuable ideas and advice. The authors also thank the High Commission for Water and Forests (HCEFLCD) for granting permits for collecting in the Moroccan basins.
Coordinates of occurrence sites of Sphaeriidae in Morocco with cross-marked presence of species per basin. DRA: Drâa-Ziz-Rhéris Basin, OER: Oum Er Rabia Basin, SEB: Sebou Basin, TEN: Tensift Basin, SM: Souss-Massa Basin, ML: Moulouya Basin, LK: Loukkos Basin, Pca: P. casertanum, Ppe: P. (cf.) personatum, Psu: P. subtruncatum, Pam: P. amnicum, Mla: M. lacustre. The cross is marked in bold at locations where P. (cf.) personatum occurred.