Research Article |
Corresponding author: Chrysoula Ntislidou ( ntislidou@bio.auth.gr ) Academic editor: Maurizio Pinna
© 2018 Chrysoula Ntislidou, Canella Radea, Sinos Giokas, Martin T. Pusch, Maria Lazaridou, Dimitra C. Bobori.
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:
Ntislidou C, Radea C, Giokas S, Pusch MT, Lazaridou M, Bobori DC (2018) Rediscovery of the endemic gastropod Dianella schlickumi (Gastropoda, Hydrobiidae) and its discrimination from Dianella thiesseana: environmental correlates and implications for their conservation. Nature Conservation 27: 35-58. https://doi.org/10.3897/natureconservation.27.23289
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The aquatic snail genus Dianella (Gastropoda: Hydrobiidae) has only two representatives in Greece: Dianella schlickumi Schütt, 1962 and Dianella thiesseana (Kobelt, 1878). D. schlickumi, a narrow endemic species to Lake Amvrakia (in Aitoloakarnania, western-central Greece), is considered as Critically Endangered (Possibly Extinct, sensu IUCN 2017). Our study confirmed its presence in Lake Amvrakia, where it had not been detected for more than 30 years. We document the unknown anatomical characters based on the D. schlickumi specimens. Moreover, the presence of D. thiesseana in the nearby lakes Trichonis and Lysimachia was also confirmed, while morphometric analyses enabled the discrimination between the two species. Redundancy Analysis revealed conductivity, dissolved oxygen and pH as the main environmental variables related to the above species’ distribution, shaping their community structure. Both Dianella species require urgent conservation measures to be enforced, due to their habitat degradation from human activities, which are limiting and fragmenting their range. For that purpose, effective management plans have to be elaborated and implemented at the mentioned lakes, focusing on the reduction of human pressures and on the improvement of their habitats.
Pyrgulinid, Greek lakes, anatomy, morphometrics, environmental correlates, conservation
Freshwater habitats cover less than 1% of the earth’s surface, but they support almost 10% of the known species on the planet (
The Balkan region is rich in freshwater fauna due to high endemism (
The distribution of gastropod species is often associated with biotic and abiotic habitat parameters (e.g.
The species of the subfamily Pyrgulinae (Caenogastropoda: Truncatelloidea: Hydrobiidae) are widely distributed in western Asia as well as in central and south-eastern Europe (
Out of those, two pyrgulinid species, belonging to the genus Dianella Gude, 1913, are known to be present in lentic systems of Greece: Dianella schlickumi Schütt, 1962 and Dianella thiesseana (Kobelt, 1878). The first species is known from Lake Amvrakia and the latter from lakes Trichonis and Lysimachia (Aitoloakarnania, western-central Greece) (
The external morphology, the anatomy and the phylogenetic position of the majority of Pyrgulinae have been extensively studied and discussed (
Hence, the aims of the present study were to: (a) report the rediscovery of the seemingly extinct pyrgulinid D. schlickumi, (b) describe its unknown anatomical characters, (c) examine its morphometric discrimination from D. thiesseana and (d) reveal the environmental parameters that probably drive the distribution of both species.
We studied three natural lakes located in the western-central part of Greece (Figure
Geographical position, morphological and limnological features of the studied lakes. Alt: altitude; Zmean: mean depth; Zmax: max depth; La: lake surface area; TL: trophic level, ET: eutrophic, MT: mesotrophic, OL: oligotrophic; WMM: warm monomictic.
Lake | Latitude | Longititude | Alt (m.a.s.l) | Zmean (m) | Zmax (m) | La (km2) | TL | Lake type |
---|---|---|---|---|---|---|---|---|
Trichonis | 38.573333 | 21.552222 | 18† | 30† | 57‡ | 96.5 | OL/MT§ | WMM† |
Lysimachia | 38.558597 | 21.376873 | 16† | 3| | 9| | 13.1 | ET | | WMM| |
Amvrakia | 38.652150 | 21.219867 | 16† | 23 | 53¶ | 11.8 | MT# | WMM# |
Macroinvertebrate samplings were conducted in spring and autumn 2014 by boat, at the sublittoral and profundal zones of each lake, using an Ekman-Birge grab (three replicates per station, 225 cm2 sampling area). A total of 66 samples were collected in the studied lakes [Amvrakia: 14 stations (7 stations at each zone), Trichonis: 13 (5 and 7 stations at the sublittoral and profundal zones, respectively) and Lysimachia: 6 (3 stations at each zone); Figure
Genitalia of male and female specimens and other soft body characteristics of D. schlickumi from Lake Amvrakia were studied and compared with those of D. thiesseana collected from Lake Trichonis during the present study and with some additional individuals collected in 2016 (Figure
Shell morphometry was recorded in both D. thiesseana (Trichonis: 33 individuals and Lysimachia: 5 individuals) and D. schlickumi (Amvrakia: 44 individuals) in well preserved shells of adult specimens, using the software ImageFocus v3.0.0.1. Seven linear measurements were taken, specifically: shell height (H), shell width (W), shell aperture height (Ha), shell aperture width (Wa), spire height (SH), body whorl height (BWH) and penultimate whorl height (PWH) (Figure
External morphological measurements taken in specimens of Dianella schlickumi and Dianella thiesseana.
The studied populations were also tested for morphological diversification using a landmark-based method of acquiring geometrical data of shape and size. Shell variation has been traditionally quantified through linear measurements and ratios to distinguish between individuals and populations, amongst and within snail species. Recently, geometric morphometrics (GMs) have been employed for examining shells, both to provide direct size-free analyses of shell shape (
For that purpose, we used sub-samples of the undamaged and well preserved shells of adult specimens (i.e. 15 D. schlickumi and 9 D. thiesseana specimens), using the aperture features. Specimens were set down on the same plane, with the aperture facing up and we took digital photographs of them. Geometric morphometric variables of the shells were obtained with 18 landmarks (LM) representing the outline of the shell and of the aperture as shown in Figure
Dianella schlickumi and Dianella thiesseana specimens positioned with the axis of the shell on the y-axis and the aperture in the same plane as the objective, showing the location of the 18 landmarks (LM1-LM18) used. A D. schlickumi B D. thiesseana.
All geometric morphometric analyses were performed with MorphoJ (
Detrended Correspondence Analysis (DCA) (indirect gradient analysis) (programme CANOCO version 4.5.1;
Dianella schlickumi was found at the south-east part of Lake Amvrakia, in 5 (S7, S11, S12, S13, S14; Figure
Dianella schlickumi and Dianella thiesseana abundances (number of individuals sampled by Ekman-Birge grab, 225 cm2 sampling area) per sampling station and environmental parameters measured in lakes Trichonis, Lysimachia and Amvrakia.
Lake | Station | Abundance (ind./m2) | Environmental parameters | ||||||
---|---|---|---|---|---|---|---|---|---|
Dianella schlickumi | Dianella thiesseana | Depth (m) | Secchi (m) | DO (mg/l) | pH | Cond (μS/cm) | WT (oC) | ||
Trichonis | S6 | 59 | 18.0 | 6.4 | 9.05 | 10.04 | 319 | 18.8 | |
S13 | 44 | 13.0 | 5.6 | 8.92 | 10.73 | 320 | 15.0 | ||
Lysimachia | LYS | 15 | 3.8 | 1.7 | 9.77 | 8.13 | 363 | 11.9 | |
Amvrakia | S7 | 15 | 13.0 | 5.2 | 8.87 | 9.74 | 982 | 21.2 | |
S11 | 15 | 8.0 | 4.7 | 8.38 | 10.10 | 921 | 20.5 | ||
S12 | 44 | 11.5 | 4.8 | 8.48 | 10.48 | 922 | 20.5 | ||
S13 | 44 | 9.0 | 5.1 | 8.66 | 10.42 | 916 | 21.6 | ||
S14 | 607 | 5.0 | 3.2 | 8.47 | 10.62 | 898 | 20.9 |
Ctenidium-Osphradium: Ctenidial filaments broader than high; osphradium elongate, approximately opposite to the middle of ctenidium.
Nervous system
(Figure
Non-genital anatomy of Dianella schlickumi. A Nervous system B Rectum full of faecal pellets. Abbreviations: cm -commissure; fp -faecal pellets; lc -left cerebral ganglion; lp -left pleural ganglion; sb - suboesophageal ganglion; sp -supraoesophageal ganglion; r -rectum.
Gastric caecum : Large and elongate gastric caecum on the posterior stomach chamber.
Rectum
: The U-shaped intestine loop in the pallial cavity roof was wide and the faecal pellets were packed sideways (Figure
Female reproductive system
(Figure
Penis
(Figure
Egg capsule
(Figure
Genital anatomy and egg capsules of Dianella schlickumi. A Female genitalia B Penis C Shell bearing egg capsules covered by fine-grained material D Egg capsule with embryo. Abbreviations: ag–albumen gland; b–beak-shape dilatation of the oviduct; bc–bursa copulatrix; fp–faecal pellets; fg–fine-grained material; e–eye; ec–egg capsules; em–embryo; ov: renal oviduct; pd–penial duct.
Seven out of the 12 morphometric measurements taken, differed statistically (p < 0.001) between the two species. Generally, individuals of D. thiesseana exhibited higher mean values compared to D. schlickumi, except for SH/BWH ratio, which was higher in D. schlickumi (Table
Average (±standard error) and range (minimum and maximum values) of the morphometric measurements (in mm) taken in Dianella thiesseana and Dianella schlickumi specimens. The results of t-test are also provided (* indicates the significant differences). n = number of individuals used: H: shell height; W: shell width; Ha: shell aperture height; Wa: shell aperture width; SH: spire height; BWH: body whorl height; PWH: penultimate whorl height.
Variables |
Dianella thiesseana (n=38) |
Dianella schlickumi (n=44) |
t-test | |
---|---|---|---|---|
F | p | |||
H | 6.79 ± 0.25 (4.16–9.78) | 6.17 ± 0.21 (4.34–10.89) | 3.95 | 0.063 |
W* | 3.01 ± 0.07 (2.20–3.86) | 2.65 ± 0.06 (1.93–3.75) | 0.40 | <0.001 |
Ha* | 2.45 ± 0.06 (1.58–3.16) | 2.07 ± 0.04 (1.61–2.92) | 1.45 | <0.001 |
Wa* | 1.67 ± 0.04 (1.18–2.22) | 1.45 ± 0.03 (1.05–1.91) | 0.04 | <0.001 |
SH | 4.10 ± 0.19 (2.05–6.38) | 3.97 ± 0.17 (2.50–7.70) | 8.87 | 0.797 |
BWH* | 2.69 ± 0.07 (2.00–3.77) | 2.20 ± 0.05 (1.64–3.25) | 0.86 | <0.001 |
PWH* | 0.67 ± 0.02 (0.34–0.92) | 0.54 ± 0.01 (0.34–0.78) | 5.23 | <0.001 |
H/W | 2.24 ± 0.06 (1.69–3.14) | 2.31 ± 0.04 (1.99–3.29) | 3.09 | 0.250 |
Ha/Wa | 1.47 ± 0.02 (1.19–1.82) | 1.44 ± 0.02 (1.16–1.93) | 0.85 | 0.255 |
SH/BWH* | 1.52 ± 0.06 (0.87–2.37) | 1.80 ± 0.04 (1.36–2.89) | 12.14 | <0.001 |
PWH/BWH | 0.25 ± 0.01 (0.16–0.38) | 0.25 ± 0.00 (0.17–0.32) | 0.62 | 0.731 |
BWH/W* | 0.89 ± 0.01 (0.77–1.09) | 0.83 ± 0.01 (0.73–0.98) | 0.15 | <0.001 |
Geometric morphometric analysis revealed a clear size and shape distinction between the two Dianella species. Shells of D. thiesseana were significantly larger (Centroid Size) than those of D. schlickumi (F1, 22 = 38.01, p < 0.0001, Figure
RDA ordination diagram of Dianella thiesseana and Dianella schlickumi abundances at sampling sites (circles) in relation to environmental parameters in lakes Trichonis (TRI), Lysimachia (LYS) and Amvrakia (AMV) in spring 2014 and 2015.
Means ± 95% Confidence Intervals of centroid size for the two Dianella species and their ordinations based on landmark data.
Principal component analysis of Procrustes coordinates for Dianella schlickumi (black circles) and for Dianella thiesseana (open diamonds).
Canonical Variate Analysis: Dark-grey bins stand for Dianella schlickumi specimens and light-grey bins for Dianella thiesseana specimens.
Shape changes along the CV1: the shifts of landmark positions are indicated by straight lines. Each line starts with a dot at the location of the landmark in the starting shape (i.e. Dianella schlickumi). The length and direction of the line indicate the movement of the respective landmark towards the final shape (i.e. Dianella thiesseana).
The Monte Carlo test in RDA analysis revealed two out of the six environmental parameters examined as significantly different between the two species (p < 0.05): conductivity and Secchi depth. Depth and water temperature were excluded from the analysis due to their high inflation factor (> 20). The first and all canonical axes were statistically significant (p = 0.044 and p = 0.002 respectively). The first two ordination axes of RDA explained 99.5% of the total species variance (Monte Carlo test, p < 0.05). Axis I (eigenvalue 0.929, p < 0.05) was related to conductivity and DO (intra-set correlation values 0.952 and -0.788 respectively) and Axis II (eigenvalue 0.066) to pH (intra-set correlation value 0.428). D. schlickumi specimens from Lake Amvrakia were ordered at the positive side of Axis I, having the highest conductivity values while D. thiesseana specimens from the other lakes were ordered at the negative side of Axis I and correlated with lower values of conductivity and higher values of DO (Figure
Dianella schlickumi was recorded in the sublittoral zone of Lake Amvrakia in 1962 (
Under the IUCN Red List guidelines (IUCN 2017), D. schlickumi is considered as “Critically Endangered (Possibly Extinct)” [following the criteria B1ab (i, iii)] (
Both species thrive on soft substrate (
The anatomical characters of D. schlickumi known from literature (
D. schlickumi and D. thiesseana are discriminated due to their shell dimensions; the first one is smaller than the second (
In some cases, the environmental parameters set limits (
Both Dianella species require urgent conservation measures to be enforced and suitable management plans to be implemented in the whole studied area, focusing on the protection of these species and the improvement of their habitats. The studied lakes form an ecologically important complex as Special Conservation areas (Council Directive 92/43/EEC), listed in the NATURA 2000 network. However, the integrity of local mollusc populations in these ecosystems is threatened due to the presence of invasives; Ferrissia fragilis (Tryon, 1863) and Physa acuta Draparnaud, 1805 in lakes Trichonis and Lysimachia (
One of the main pressures identified in lakes Amvrakia, Trichonis and Lysimachia is eutrophication from agriculture run-off and wastewaters (
Our results confirm the rediscovery of the narrow endemic species Dianella schlickumi in Lake Amvrakia since past sampling efforts did not detect it for more than 30 years. Moreover, they provide basic knowledge on its anatomical, morphological and distributional patterns and its discrimination from Dianella thiesseana. The two species are discriminated by their shell size and shape. Moreover, the presence of Dianella thiesseana is confirmed in lakes Trichonis and Lysimachia. We conclude that further conservation measures have to be implemented for effective protection of both species.
We would like to thank Mrs Efi Mavromati from the Greek Biotope/Wetland Centre for providing us with data from the National Greek Monitoring Programme for the presence of Dianella thiesseana in Lake Lysimachia.