The Impact of Some Environmental Factors on the Distribution of the Benthic Ostracod Species from of Safaga Island, Red Sea, Egypt ()
1. Introduction
The Ostracoda is a class of Crustacea characterized by a bivalved carapace, which encloses the body and appendages. Ostracods occur in almost all types of water bodies, and they are one of the most abundant groups of benthic microfauna. In addition, they distribute almost everywhere from shallow marine to deep-sea environments, and they are useful as indicators of the environmental parameters variation [1].
Generally, the controlling factors on marine ostracods are water temperature, depth, salinity, dissolved oxygen, pH, alkalinity, food supply and sediment organic matter content [2]. To testify this, Mesquita-Joanes et al. [3] maintained that temperature is the most important factor affecting ostracod growth and survival. Furthermore, Ruiz et al. [4] stated that salinity was the most important factor in species distribution. Also, Ruiz et al. [4] stated that ostracods may be affected by pH and electrical conductivity.
Though ostracod species are numerous and abundant in the Egyptian Red Sea region, benthic ostracods have received little attention in ecological studies. What we have are only some studies on the recent benthic marine ostracods of the Red Sea, such as [5] which dealt only with Cypridinidae, [6] characterized the ostracod community of Al Gardaqa, and [7] investigated the ostracod assemblages of the Abu Dhabi lagoon. In addition, [8] and [9] investigated ostracods from the Gulf of Aqaba, [10] and [11] gave information on foraminifers and ostracods from the Jordanian Gulf of Aqaba. Also, [12] gathered data on benthic ostracods from El Hameira (Gulf of Aqaba) and [13] collected data on ostracods from Safaga Bay.
The goals of this study were to identify and determine the ostracod assemblages that live between 0.5 m to 30 m depths on the east side of Safaga Island, to determine the ecological parameters of the environment in which these species live and to figure out the impact of these ecological factors on the distribution and abundance of ostracod species according to the seasons.
2. Materials and Methods
In the current study, 32 samples are collected by using the nylon net (150 μm mesh size) and Van Veen grab from eight stations of the east side of Safaga Island (Figure 1 and Table 1). The period of the collection extends through four seasons between 2018 and 2019 (June 2018, September 2018, January 2019, and March 2019). The nylon net was used in collecting of samples at depths from 0.5 - 1 m while, samples at depths from 5 to 30 m were collected by the Van Veen grab. At each one of 8 collection sites, about 500 ml of sediment samples were collected for studying species of ostracods. The sediment samples containing ostracod species were fixed in 4% formaldehyde solution.
The ostracod species studied in this work were not listed in the IUCN Red List of Threatened Species (http://www.iucnredlist.org/) [14]. No permits were required for the labeled study, which conformed to all applicable guidelines.
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Figure 1. (a) Map showing location of Gazirat safaga. (b) Map showing the eight collecting sites. (c) Map showing enlargement of the eight collecting sites at different depths (from google earth).
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Table 1. Depths and coordinates of the stations in the east side of Safaga Island.
At each collection site, some ecological factors such as pH, dissolved oxygen (DO), water temperature, electrical conductivity and salinity were measured seasonally using an environmental Multi Probe System. Also, total dissolved solids (TDS) were calculated by multiplying the electrical conductivity value by 0.65. Additionally, organic matter, and calcium carbonate percentage were determined.
Ostracod species were picked in the laboratory using a tiny pipette from a petri dish containing some of the collected samples under a binocular microscope. Then ostracod species were counted, preserved in 70% alcohol and examined in detail under a stereomicroscope.
For scanning electron microscope studies, the collected ostracod species were fixed in a mixture of one volume of 1% of osmium tetraoxide and three volumes of 4% glutraldehyde. Then they were dehydrated in series of ethanol and sputter-coated with gold, and viewed under a JSM 5400 LV SEM, at an accelerating voltage of 15 kV at Assiut University.
The identification of ostracod species was conducted by using a variety of references such as: Bonaduce & Pugliese [8], Bonaduce et al. [9], Bonaduce et al. [6] [15] [16] [17] [18] and the help of Australian Museum. In the current study, the frequency of the ostracod species was calculated by using [19] frequency index. The results were evaluated as dominant (F ≥ 50%), common (50% > F ≥ 25%) and rare (F < 25%). To determine the similarity between the eight collection sites, Bray-Curtis Similarity Index was done. The Bray-Curtis dissimilarity was used to measure the variances in species populations between two different sites and can be calculated with the following formula:
. Multidimensional Scaling (MDS) was accomplished to investigate the regional distribution form [20]. SIMPER analyses were done to recognize the percentage of the influence of each species on the resemblances and variances within the clusters formed after mass analysis. Spearman’s rank correlation coefficient was done to determine the relationships between depth and other factors.
3. Results
3.1. Ecological Factors
Table 2 and Figures 2(a)-(h) summarized the values of the measured ecological parameters in Sea water of the collecting sites as temperature (˚C), pH, salinity (‰), dissolved oxygen (mg/L), conductivity (ms/cm), CaCO3 (%), TDS (g/l) and organic matter (%). The highest water temperature (35˚C) was measured at site1 in summer 2018, and the lowest water temperature (9˚C) was measured at site 8 in winter 2019 (Figure 2(a)). 504 individuals of ostracods belonging to 36 species were recorded on site 1 in summer (35˚C) and 31 individuals of ostracods representing eight species were recorded on site 8 (9˚C) in winter. 8.5 was the highest value of pH recorded in autumn and spring at sites 5 and 6, respectively. Besides, the lowest value of pH was 7.3 in spring at site 2.
The values of salinity varied from 38.2‰ to 42.2‰, where the lowest value was recorded in spring 2018 at site 6 and the highest value was noted in winter and spring at site 4 and site 8, respectively. Dissolved oxygen fluctuated between 4.11 to 9.6 mg/L and the conductivity values ranged from 60.1 to 64.6 ms/cm. As well as, total calcium carbonate ranged from 50% to 89%. Also, TDS ranged between 33.4 to 39.8 g/l and organic matter varied from 8.9% to 24.6%.
3.2. Ostracod Species and Seasonal Distributions
The collecting ostracods (39 species of Podocopida and four species of Myodocopida) identified in eight collecting sites on the east side of Safaga Island, as well as their Frequency Index values, were shown in Appendix, Table 3, and Figures 3-6. The frequency index (Fs) of the identified ostracod species (Figures 3-6) was calculated, yielding the following results; the ostracod species Cytherelloidea sp. gathered as rare and the sixteen species: Paranesidea sp., Neonesidea aff. Michaelseni, Aglaiocypris triebeli, Hiltermannicythere sp., Leptocythere rara, Rutiderma sp., Loxoconcha sp., Loxoconcha gisellae, Loxocorniculum
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Table 2. Values of ecological parameters in the eight sampling stations during the four seasons.
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Table 3. Frequency index values (Fs) for collected species.
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Figure 2. The seasonal differences of the studied ecological factors: (a) temperature, (b) pH, (c) salinity, (d) dissolved oxygen, (e) conductivity, (f) calcium carbonate, (g) TDS, (h) organic matter at the collecting sites.
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Figure 3. Scanning Electron Microscope showing images of the external view of: 1: Aglaiocypris triebeli; 2: Callistocythere arcane; 3: Callistocythere fluctuans; 4: Carinocythereis sp. 1; 5: Carinocythereis sp. 2; 6: Caudites levis; 8: Cyprideis littoralis (after [46]); 9: Cyprideis torosa; 10: Cytherella cf. punctata; 11; Ghardaglaia triebeli; 12: Hemicytherura videns aegyptica (after [46]) and 7: photograph of Cylindroleberis vix.
ghardaquensis, Loxoconchella dorsobullata, Cytherella cf. punctate, Carinocythereis sp. 1, Hiltermannicythere rubrimaris, Hemicytherura videns aegyptica, Cyprideis littoralis and Cyprideis torosa were grouped as common and the remaining species (26) were dominant.
3.3. Species Abundance
According to the seasonal collecting samples, 43 of ostracods were collected and identified (Figures 3-6). Furthermore, the highest number of ostracod species (richness) (36) was recorded in summer (Figure 7) at the first site and the lowest number of species (8) was observed in winter at site 8 (Figure 7). Then, the maximum number of ostracod individuals (504) was detected at site1 in the
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Figure 4. Scanning electron microscope showing images of the external view of: 13: Hiltermannicythere rubrimaris; 14: Hiltermannicythere sp.; 15: Jonicythere sp.; 16: Leptocythere arinecola (after [46]); 17: Leptocythere rara; 18: Loxoconcha sp.; 19: Loxoconcha ghardaqensis; 20: Loxoconcha gisellae (after [46]); 21: Loxoconcha ornatovalve; 22: Loxoconchella dorsobullata; 23: Loxocorniculum ghardaquensis; and 24: photograph of Macrocypris minna.
summer and the lowest number of individuals was noted at site 8 in winter (Figure 7 and Appendix).
The distribution of ostracod species shows differently at each site. Seven ostracod species (Paranesidea fracticorallicola, Neonesidea schulzi, Tanella gracilis, Caudites levis, Loxoconcha ghardaqensis, Prionotoleberis lux, Ghardaglaia triebeli) were observed in every collecting site, so they have broader ranges of tolerances to diverse environmental factors. On the other hand, ostracod species Cytherelloidea sp. occurred in two collecting sites only and twelve species represented 44% of the total number of collecting ostracod species. A species of the genus Rutiderma Brady & Norman, 1896 (Figure 5 image 36) is reported in this paper for the first time but it is not described and therefore it is left in open nomenclature.
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Figure 5. Scanning electron microscope showing images of the external view of: 25:Miocyprideis cf spinolusa; 26:Moosella striata (after [46]); 26: Hiltermannicythere sp.; 27: Neonesidea aff. Michaelseni (after [46]); 28: Neonesidea schulzi; 29: Paradoxostoma altecaudatum (after [46]); 30: Paradoxostoma arcuatum; 31: Paranesidea sp.; 32: Paranesidea fracticorallicola; 34: Propontocypris sp.; 35: Quasdracythere borchersi (after [46]); 36: Rutiderma sp. and 33: photograph of Prionotoleberis lux.
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Figure 6. Scanning electron microscope showing images of the external view of: 37: Tanella gracilis (after [46]); 39: Xestoleberis ghardaqe; 40: Xestoleberis rhomboidea; 41: Xestoleberis rotunda (after [46]) and 38: photograph of Triebelina sp.
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Figure 7. Seasonal fluctuations in the individual numbers of ostracod species at the sampling sites during the period of collection.
According to Appendix and Table 4, site 1 had the highest number of ostracod individuals (1355) and site 8 had the lowest number (256). Furthermore, site 1 had the highest number of ostracod species (36) and site 8 had the lowest number (11). Also, Prionotoleberis lux was the dominant species in summer, Cylindroleberis vix in autumn, Caudites levis in winter and Cylindroleberis vix in spring according to the dominancy index values.
3.4. Bray-Curtis Similarity and Multidimentional Scaling (MDS) Ordination
The dendrogram of Bray-Curtis similarity and Multidimentional scaling (MDS) ordination of the collecting sites was formed of Bray–Curtis average clustering and the similarities between the stations were displayed in groups and shown in Figure 8 and Figure 9. The groups that exhibited the highest similarity and difference in each season were determined according to SIMPER analysis results. In summer, the similarity revealed three groups; the similarity within the first group was 42.3%, within the second group was 41% and was 59.5% within the third group. In autumn, the similarity displayed two groups; the similarity inside the first group was 42.1%, while that similarity was 34.2% within the second group. Furthermore, the similarity between the two groups was 38.5% and 40.3% of the first and second groups, respectively, during the winter season. In spring,
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Figure 8. Bray-Curtis similarity dendrograms of individual numbers of ostracod species at the collecting sites. (a) Summer; (b) Autumn; (c) Winter; (d) Spring.
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Table 4. The total seasonal number of ostracod individuals.
the similarity revealed two groups; those were 44% and 36.7% in the first and second groups, respectively.
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Figure 9. MDS ordination of the collecting sites produced with Bray–Curtis average clustering method.
The correlation among measured parameters such as water temperature, pH, salinity, dissolved oxygen, conductivity, total calcium carbonate, TDS, total organic matter, individual number, richness and depth were determined using Spearman’s rank correlation coefficient method and listed in Table 5. The results of correlation analysis displayed that the individual number and richness of ostracods were positively correlated with water temperature, dissolved oxygen, organic matter, salinity and total calcium carbonate, and the individual number of ostracods was negatively correlated with the depth of sea water.
4. Discussion
The results of this study confirmed the presence of distinct difference in the abundance of ostracod species between the eight collecting sites. The shallow sites (site 1 and 2) were characterized by higher densities than those of the benthic sites, this is chiefly related to the location of sites in an area contains seagrass, sea beds and macro-algae, thus the availability of food for ostracods. [21] recorded that some ostracod species living in close proximity to sea grasses, algae, and mangrove trees, which are abundant along the Red Sea’s coast. Moreover, [21] recorded that the ostracod species with higher percentages are associated with algae and seagrasses. The leaves promote the growth of macroalgae, which provide food and shelter for invertebrates, allowing them to reach significantly higher densities than in unvegetated benthic habitats [22]. According to Xie et al. [23] the benthic aquatic is not suitable for ostraod surviving because the decreasing of plants and reducing of water transparency.
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Table 5. The matrix of spearman’s rank correlation between ostracod assemblages and environmental factors in the sampling stations.
S: Correlation is significant. NS: Correlation is not significant. * Correlation is significant at the 0.05 level (2-tailed). ** Correlation is significant at the 0.01 level (2-tailed).
Distribution and abundance of ostracod species and specimens are related to numerous diverse ecological factors (Batmaz et al., [24]). The ecological parameters (temperature, dissolved oxygen, pH, salinity, CaCO3 (%) and TDS) and the physical characteristics (depths, aquatic plants and predation) control the occurrence and abundance of ostracod species [25] [26].
According to the results of Spearman’s rank correlation (Table 5), the individual number of ostracod species was correlated positively with temperature. Also, [27] noted that the species occurrence was positively related to both water temperature and electrical conductivity. In addition to this, Mesquita-Joanes et al. [3] discovered a high positive association between water temperature and ostracod population expansion, suggesting that temperature is important for species survival. Correspondingly, [28] and [22] noted that no direct relationship occurs between the distribution of ostracod species and temperature. [29] recorded that, water temperature and salinity are the major controlling factors governing ostracod distribution in estuarine environments. Moreover, a positive correlation was observed between individual numbers and richness and salinity, according to the correlation of Spearman’s rank (P < 0.01) (Table 3). [25] [26] suggested that salinity is an active factor in the diversity and the abundance of ostracod species. In the same way, [30] approved that salinity has a significant effect on the diversity of ostracod species.
In the current study, dissolved oxygen ranged from 4.11 to 9.6 mg/L and it correlated positively with individual and species numbers. According to Ahmed et al. [31] the higher values of dissolved oxygen during some months are owed to increase the activity of the photosynthesis process, while lower values might be because of using the organic substances and breathing of organisms. Moreover, [32] noted that dissolved oxygen is not an important factor within an aquatic ecosystem and it is the smallest effective analyst for the ostracod species, respectively. On the other hand, Külköylüoglu et al. [33] [34] noted a positive correlation between individual numbers of the species and dissolved oxygen. The pH of water of the current study does not fluctuate greatly at the different depths during the four seasons. Similarly, data noted by Sridhar et al. [35].
From this study, it is concluded that the relationship between abundance and richness of ostracod species were positive with total organic matter and total calcium carbonate. A similar observation was noted by [36]. [37] noted that the greater portion of the calcium carbonate content was made by the carbonate shells of some organisms like molluscs, foraminifera and algae.
The Bray-Curtis Similarity Index and MDS of the current result revealed that, the highest similarity in summer (59.5%) in the third group at sites 2 and 3. Furthermore, the highest similarity in autumn (42.1%) inside the first group was noted at sites 7 and 8. In other words, the highest similarity in winter (40.3%) was determined in the second group at stations 1 and 3. As well, the highest similarity in spring (44%) in the first group was recorded at sites 7 and 8. However, Bray-Curtis similarity index of some ostracod spcies from the Sea of Marmara showed five clustering groups and the level of similarity is very associated with habitat type and depth (Paçal et al., [38]).
The present collected ostracods categorized as follows: Cytherelloidea sp. was rare, sixteen species were common and the remaining species (26) were dominant. In the Adriatic Sea, Loxoconcha agilis was found to be the dominant species between 20 and 60 metres deep [28]. [21] recorded four rare species (Leptocythere arenicola, Cytherelloidea sp., Paranesidea n. sp., and Cytherois gracilis) in the intertidal zone of the mangrove ecosystem of the Red Sea Coast.
During four seasons, 32 samples were collected from 8 sites, where the individual numbers of ostracod species were biggest in summer and the lowest number were recorded in winter. Moreover, the richness of ostracods was close to each other in all seasons and all sites, except in the eighth site (30 m) where the richness was very low. The current study showed that the number of podocopid ostracods increase in low depths and decrease in high depths so, they favored the warm water. [39] discovered that the ostracods they collected were rare and only found in the warm waters of the E and NE shelves. Further, the individual number of Cylindroleberis vix and Prionotoleberis lux increases in deep water and decreases in shallow water, indicating that they prefer cold water. [19] discovered that Cylindroleberis vix at 15 to 20 m depth in the Mozambique Channel, Mayotte, and Prionotoleberis lux at 300 to 350 m depth near Mayotte, Indian Ocean.
The temperature is well known as the most important factor in increasing reproduction, and breeding periods influence the seasonal dominance of species. Orth et al. [40] noted that the low water temperatures from 15˚C to 20˚C resulted in the longest survival times, but high water temperatures between 20˚C to 24˚C provided the highest rates of moulting and shortest intermoult times. Also, in several crustacean species, higher temperatures determine an increase in the molt increment during the juvenile phase, while during the mature growth phase the reverse is true [40] [41]. [42] found that in small animals, the link between temperature and intermolt shortening is strong, but bigger animals are less responsive to temperature changes.
The data gained from the current study recommend that ostracod species have different tolerance values to many factors in variety of depths except Cytherelloidea sp. (Külköylüoglu et al., [33]; Külköylüoglu et al., [44]; Yavuzatmaca et al., [45]) support this datum.
5. Conclusions
In this study, 6733 ostracod individuals belonging to 43 species were collected seasonally from the east side of Safaga Island. The effects of some environmental factors on the collected ostracod species were determined in the eight collecting sites (see Table 2). The current results show that ostracod species have been affected by temperature, salinity, conductivity, pH, dissolved oxygen, TDS, and organic matter and CaCO3 at eight sampling stations. The highest number of ostracod individuals and richnesss were observed in summer, while the lower ones were recorded in winter. Furthermore, the statistical analyses were used to assess the influence of ecological factors on the present ostracod species at the various collecting sites.
The study of benthic ostracod environment relationships allows us to better understand the environmental characteristics, distribution and identification of the ostracod species found on the east side of Safaga Island at depths fluctuating from 0.5 to 30 m, providing variable information about biotic and abiotic ostracods patterns.
Acknowledgements
The author is deeply grateful for Editor in Chief of Open Journal of Marine Science and I would like to thank Zoology Department for providing the necessary technical support during the conduct of the current study.
Appendix
List of number of ostracod species collected during four seasons and corresponding abundances in the eight samples.
Abbreviations
Do: Dissolved oxygen; CO: Conductivity; T: Temperature; Ind. No: Individual numbers.