Population fluctuation and vertical distribution of meiofauna in the Red Sea interstitial environment.

The composition and distribution of the benthic meiofauna assemblages of the Egyptian coasts along the Red Sea are described in relation to abiotic variables. Sediment samples were collected seasonally from three stations chosen along the Red Sea to observe the meiofaunal community structure, its temporal distribution and vertical fluctuation in relation to environmental conditions of the Red Sea marine ecosystem. The temperature, salinity, pH, dissolved oxygen, and redox potential were measured at the time of collection. The water content of the sediments, total organic matters and chlorophyll a values were determined, and sediment samples were subjected to granulometric analysis. A total of 10 meiofauna taxa were identified, with the meiofauna being primarily represented by nematodes (on annual average from 42% to 84%), harpacticoids, polycheates and ostracodes; and the meiofauna abundances ranging from 41 to 167 ind./10 cm(2). The meiofaunal population density fluctuated seasonally with a peak of 192.52 ind./10 cm(2) during summer at station II. The vertical zonation in the distribution of meiofaunal community was significantly correlated with interstitial water, chlorophyll a and total organic matter values. The present study indicates the existence of the well diversified meiofaunal group which can serve as food for higher trophic levels in the Red Sea interstitial environment.

Introduction

The increased interest of the biologists in studying benthic meiofauna started in the early 1980s. Its small size, together with difficulties in isolating the meiofauna from the sediments and the identification of species belonging to different taxa are probably the main obstacles of studying the benthic meiofauna (Austen et al., 1994; Harguinteguy et al., 2012). Meiofaunal organisms play an important ecological role in the aquatic ecosystem and are well suited for environmental impact assessment studies. They have short generation times, continuous reproduction, and in situ direct development, and therefore, their potential for rapid response to environmental changes is high (Fraschetti et al., 2006; Giere, 1993; Gyedu-Ababio and Baird, 2006; Harguinteguy et al., 2012). The marine meiofauna is often a very useful tool for biological monitoring since the community structure may be sensitive to both natural and anthropogenic environmental disturbances (Gyedu-Ababio and Baird, 2006; Mirto and Danovaro, 2004; Moreno et al., 2008; Harguinteguy et al., 2012). Moreover, the beeches may function as natural filters responsible for the remineralization of substances, which then return to the sea as nutrients (Coull and Chandler, 2001). The interstitial system of the beaches, in particular the system protected by muddy sediments, is formed by long and intricate food chains of bacteria, unicellular algae and meiofauna at the first levels. Therefore, biological systems are dependent on the productivity of coastal areas (Higgins and Thiel, 1988; Leguerrier et al., 2003).

The growth and diversity of meiofauna may be stimulated by feeding on bacteria, which could increase the recycling of nutrients into the ecosystem and thereby be expected to have a greater productivity (De Wit et al., 2001; De Troch et al., 2006). Moreover, the meiofauna can provide food for higher trophic levels, such as fish and marine invertebrates (Leduc and Probert, 2009). The spatial patterns of the structure of the meiofaunal community in sandy beaches of marine ecosystems may be associated with different environmental variables. Related to this, the sediment granulometry (Gómez Noguera and Hendrickx, 1997; Barnes et al., 2008), the organic matter source in coastal sediments (Danovaro et al., 2002; Flach et al., 2002; Moreno et al., 2008; Ingels et al., 2009; Pusceddu et al., 2009), and oxic and anoxic conditions in the interstitial pore space (Mirto et al., 2000; Sutherland et al., 2007) have a fundamental role in the richness and abundance of the benthic meiofauna.

The criteria in the study of benthic meiofauna were established by Giere (1993) and these concepts have been recently applied for the Egyptian fauna of the Red Sea (Hanafy et al., 2011; Ahmed et al., 2011). However, none of the two studies took place on the vertical distribution of the meiofauna. This somewhat meager data suggest that there is a need for more information on meiofaunal community of the Egyptian coasts along the Red Sea and their temporal changes, weather stochastic, seasonal or long term to understand their trophic relation in the benthic ecosystem. This pioneer study was undertaken to provide answers to the basic question on what are different types of meiofaunal metazoans and their spatio-temporal variation in the Egyptian coasts of the Red Sea.

Materials and methods

Sediment samples for environmental parameters and meiofauna were collected from three stations of Gabal El-Zeit (site I), Safaga (site II) and Al-Qulaan (site III) (Fig. 1); with the help of a hand core of 4.5 cm inner diameter and 10 cm length situated approximately 350 m apart in the sea. The three stations were selected based on their proximity to mangrove. Safaga (lat 26° 36′ 56″N, long 34° 00′ 43″E) and Al-Qulaan (lat 24° 21′ 28″N, long 35° 18′ 23″E) were closer to mangrove vegetation than Gabal El-Zeit (27° 48′ 10″N, long 33° 33′ 59″E). Samples for horizontal and vertical distribution were collected seasonally during 2012. Sampling was carried out where three replicate cores were collected at low tide by inserting the 10 cm length core into the sediment from each station. The core sediments were sub-sectioned at 2 cm interval for the study of vertical distribution of meiofauna, grain size analysis, and total organic matters. The percentage of silt/clay in the sediment was obtained by wet sieving using a 62 μm sieve to separate the fine and sand fractions, which were then dried at 80 °C and weighed (Harguinteguy et al., 2012).

Figure 1

Location of sampling sites (with red colours) chosen for collecting meiofauna at the northern part of the Red Sea during the present study.

Sediment samples containing meiofauna were preserved in 4% formalin and stained with Rose Bengal (Ansari et al., 2001). In the laboratory, these samples were elutriated of larger sand particles using a shake and decant procedure (Cross and Curran, 2000) and meiofauna were sorted by sieving through 0.50 and 0.062 mm mesh sizes sieves. The content of the 0.062 mm sieve was recovered and preserved in the fixative (Ditlevsen, 1911). Then, the fauna were identified to higher taxa and counted under a stereomicroscope (Higgins and Thiel, 1988), and dry weight biomass was obtained by multiplying a factor of 0.00045 with total number of taxa recorded on each sampling date and station (Ansari, 1989). The meiofaunal density was standardized to individuals per 10 cm2. Identification of meiobenthic organisms were performed using the keys of Riedl (1969), Tarjan (1980), Norenburg (1988), Platt and Warwick (1988) and Huys et al. (1996).

Temperature was recorded with the help of a centigrade thermometer. Interstitial water was collected for the estimation of salinity and dissolved oxygen. For the estimation of salinity, method of Strickland and Parsons (1972) was followed. Oxygen concentration was estimated using an oxygen meter. The percentage of interstitial water of the sediment was measured regularly. Wet sediment from the fraction of core was weighed on a watch glass, dried at 100 °C to constant weight and re-weighed. Wet weight minus dry wet was interpreted as a rough estimate of the weight of the interstitial water from which the percent interstitial water was calculated (Tietjen, 1969). Total organic matters of each sediment sample were determined according to Holme and McIntyre (1984). Sedimentary pigment determination was made according to Tietjen (1968) to obtain estimates of chlorophyll a in the sediment.

Simple correlation coefficient (r) was used to find the relation between different environmental parameters and meiofaunal density. Data on meiofauna density obtained in the present study was subjected to the ANOVA analysis to understand whether there exist any significant correlations in the meiofaunal densities with depth.

Results

Physico-chemical conditions

Physico-chemical parameters and sediment characteristics of the three stations are shown in the (Table 1). The seawater temperature was observed to vary from a low of 17.5 °C during winter to 23.7 °C during summer. The variation in water salinity was from 40.6 psu in winter to 44.2 psu during summer. The dissolved oxygen content varied from 4.1 to 5.3 mg/l. The oxygen content showed an inverse relation with temperature and salinity during the present study. Fluctuations in pH around slightly alkaline values were generally limited and varied between7.6 and 8.3. The sediment was predominantly loose mud and had silt as the most dominant constitute with sand and clay in different proportions at station II and III, however the sediment collected from the station I differed completely and dominated by high values of sand. The average values of sand, silt and clay at station I were 79.64%, 11.84% and 8.51%, respectively. While at station II the values for the same constituents are 14.63%, 71.17%, and 9.69%, respectively and in station III these values were 35.16%, 52.09% and 12.74%, respectively.

Table 1

Physico-chemical and sedimentary properties at the three stations chosen along the northern part of the Red Sea during the present study.

Site and parameter	Season
	Spring	Summer	Autumn	Winter
Gabal El-Zeit
Water
Temperature (°C)	20.0	21.7	19.6	17.5
Salinity (psu)	41.5	43.3	42.0	41.8
pH	8.2	8.3	8.1	8.0
Dissolved oxygen (mg/l)	5.2	5.0	5.1	5.3
Sediment
Sand (%)	87.42	70.74	77.5	82.9
Silt (%)	11.28	12.28	14.2	9.62
Clay (%)	1.30	16.98	8.3	7.48
Redox (mv)	49.7	46.6	45.8	48.5
Total organic matters (mg/g)	3.94	8.5	5.06	5.63
Safaga
Water
Temperature (°C)	21.8	23.7	22.2	20.0
Salinity (psu)	42.4	44.2	41.8	40.6
pH	7.7	7.9	7.7	7.6
Dissolved oxygen (mg/l)	4.6	4.1	4.3	4.8
Sediment
Sand (%)	13.28	17.64	11.40	16.20
Silt (%)	77.62	66.93	82.44	57.7
Clay (%)	9.1	15.43	6.16	8.1
Redox (mv)	110.8	120.5	130.2	120.6
Total organic matters (mg/g)	5.27	9.87	3.4	5.13
Al-Qulaan
Water
Temperature (°C)	22.3	23.6	21.8	21.3
Salinity (psu)	43.6	44.0	42.8	41.6
pH	7.9	8.1	7.7	7.8
Dissolved oxygen (mg/l)	4.9	4.5	4.7	5.1
Sediment
Sand (%)	33.25	37.75	33.40	36.26
Silt (%)	55.45	46.55	56.44	49.94
Clay (%)	11.30	15.70	10.16	13.8
Redox (mv)	273	284	258	247
Total organic matters (mg/g)	7.87	9.4	7.37	5.0

The sedimentary organic matter, chlorophyll a and interstitial water are illustrated in (Table 2). A well defined vertical profile was recorded for the interstitial water, total organic matter and chlorophyll a concentration. The interstitial water content showed a decreasing trend from surface to a depth of 10 cm in the sediment. A difference of over 50% in the total organic matter values was observed in the top (0–4 cm) and bottom (4–10 cm) layer. The same trend of decreasing values with increasing depth was followed by chlorophyll a and the interstitial water.

Table 2

Vertical distribution of meiofauna, organic matter, chlorophyll a, interstitial water in the sediment collected from the northern part of the Red Sea during the present study.

Parameter	Core depth (m)
	0–2 cm	2–4 cm	4–6 cm	6–8 cm	8–10 cm
Density (ind./10 cm2)	109	59	27	11	6
Total organic matter (mg/g)	6.36	5.64	4.31	2.41	1.92
Chlorophyll a (μg/g sed.)	0.87	0.43	0.34	0.21	0.11
Interstitial water (%)	34	32	27	21	19

Total number of meiofauna varied from 17.87 to 56.10 ind./10 cm at station I and from 97.43 to 192.52 ind./10 cm2 at station II. In the station III the meiofaunal population density varied between 106.82 and 139.6 ind./10 cm2. The total biomass fluctuated between 0.008 and 0.0866 mg/10 cm2 at stations I and II, respectively. The faunal density was lowest during winter and increased during summer at the three stations (Table 3). Four major meiofaunal groups were represented in the present study. Nematodes were the most dominant group with percentage contribution of 67%. Harpacticoid copepods were the second most abundant group; they contributed 12% of the total meifaunal density. Polycheates remained the third major group and contributed 10%, while ostracodes occupied the fourth level with percentage contribution of 4%. Oligocheates and gnathostomulids occupied the fifth level with a percentage of 3% for each. Other taxa (Amphipoda, Cumacea, Isopoda and Nemertina) occurred in limited number and collectively averaged 1% of the total meiofauna.

Table 3

Total population density (ind./10 cm2 sed.) and biomass (mgC/10 cm2 sed.) of meiofauna at the three stations during the present study.

Season	Gabal El-Zeit		Safaga		Al-Qulaan
	Density	Biomass	Density	Biomass	Density	Biomass
Spring	56.10	0.0252	184.62	0.0831	138.82	0.0625
Summer	44.08	0.0198	192.52	0.0866	139.6	0.0628
Autumn	34.77	0.008	189.6	0.0853	106.82	0.0480
Winter	17.87	0.0156	97.43	0.0438	109.37	0.0492

On an average about 79% of the total fauna was restricted to the top 0–4 cm layers and there was a consistent decrease in the number with increasing depth in the sediment. Out of the total number of meiofaunal population density in the 10 cm depth sediment core, only about 3% were present at the 8–10 cm layer and the remaining 97% in the top layers. There was a significant difference (p < 0.01) in the total number observed between 0–2 and 8–10 cm depth. Table 4 describes the values of total meiofaunal biomass, evenness, Shannon–Weaver index and species richness at the three locations.

Table 4

Average values of diversity indices of meiofauna in the Red Sea at the three different sites chosen for the present study.

Diversity index	Site
	Gabal El-Zeit	Safaga	Al-Qulaan
Number of species	13	17	31
Population density (ind./10 cm2)	41	167	141
Biomass (mgC/10 cm2)	0.018	0.075	0.063
Eveness (E)	0.91	0.84	0.92
Shannon–weaver index (H)	2.53	2.63	2.86
Species richness (D)	3.6	3.6	4.0

Discussion

The meiofauna composition was quite similar among the three sites chosen for the present study, however, its densities varied significantly among them. During the present study, the meiofauna showed considerable fluctuation in the total population density, which coincided with parallel changes in specific environmental parameters. The total density of meiofauna attained its highest values of 192.52 ind./10 cm2 at Safaga (site II) during summer and its lowest values of 17.78 ind./10 cm2 at Gabel El Zeit (site I) during winter. The sedimentary environment in station II was different compared to station I (i.e. higher organic content, higher chlorophyll a values and smaller grain size. The highest densities of meiofauna coincided with the highest percent of silt (82.44%) & clay (15.43%); highest total organic matters (9.89 mg/g); and highest chlorophyll a (1.1 μg/g sed.) recorded at station II. Similar observations were recorded in the NW Shelf of Cuba (Armenteros et al., 2009), Mediterranean marine system (Moreno et al., 2008), coasts of South Africa (McLachlan et al., 1981, sandy beaches of Spain (Rodríguez et al., 2003). Besides physico-chemical sediment differences, another important factor that may influence the meiofaunal density is the fluctuation in the density of the most dominant group. During the present study, Nematoda was the most dominant group which constituted more than 60% of the total meiofauna. Similar results on the temporal variation with nematode’s dominancy in meiofaunal communities have been reported from different geographical regions (Rodríguez et al., 2003; Moreno et al., 2008; Landers et al., 2012; Harguinteguy et al., 2012; Meleno et al., 2013).

The total density observed in the present study was similar to those reported from other shallow regions of the northern Red Sea and ranged between 100 and 130 ind./10 cm2 (Hanafy et al., 2011), and also was very close to that of recorded by Hulings (1975) in sandy beaches along the coasts of Jordan with a higher population density of 223 ind./10 cm2 and lower values of 44 ind./10 cm2. However, estimates of meiofaunal densities in other coastal regions (for example: sandy beaches of the Nuevo Gulf, Argentina; Harguinteguy et al., 2012) were extremely very higher (1500–6500 ind./10 cm2) than the present study. These differences could be related to the oligotrophic conditions prevailing in the Red Sea.

In the current study, site III (Al Qulaan) was found to be the most diversified site among the three sites chosen for this study as it contains higher number of nematode and copepod taxa. This is mainly due to the location of this site within Wadi El Gemal protectorate area which contains the most productive habitats of mangroves and seagrass meadows. Increased diversity in seagrass meadows has been reported for meiofaunal nematodes (Ndaro and Olafsson, 1999) and copepods (Nicholls, 1944; Noodt, 1964; Hicks, 1986). Possible explanations are more food availability, sediment stability, protection from predators, and habitat complexity in the mangal and seagrass meadows (Orth and Heck, 1984).

On the other hand, over 50% of the population density of all meiofaunal taxa occurred in the upper layer of 0–4 cm depth and then these densities were sharply progressively decreased with increasing depth in the sediment (Table 2). Significant vertical decrease in meiofaunal densities as being recorded in the present study have also been reported in many other studies (Ansari et al., 1980; Cantelmo, 1978; Ndaro and Olafsson, 1999). In the present study, nematodes were the only group present in the entire core and dominated the fauna. A number of nematode species are known to withstand near anaerobic condition in the sediment (Wieser, 1975) and this may explain the regular occurrence of this group in the deeper layer of the sediments of the present study. Generally, those parameters which control macrofauna are also responsible for the distribution and abundance of meiofauna. Food availability and oxygen are considered important factors responsible for the vertical distribution of meiofauna. Moreover, sediment chlorophyll provides information on the primary conductivity in the sediment and considered to be an important parameter for the distribution of meiofauna in the marine benthic habitat (Lee et al., 1977; Coull and Bell, 1979). Significant vertical decrease in the meiofaunal density was positively correlated with sediment chlorophyll a (r = 0.81; p ⩽ 0.01), interstitial water (r = 0.74; p ⩽ 0.01) and organic matter (r = 72; p ⩽ 0.01).These factors proved limiting in shallow coastal areas as they form important sources of food and energy supply (Coull and Bell, 1979; McIntyre, 1969).

There has been much debate on the ultimate fate of meiobenthos in the ecosystem. The pathways from meiofauna could be linked to macrofauna, nektons and nutrient regeneration (Coull, 1973). It is because majority of meiofauna in the interstitial environment of the Red Sea occur in the top few centimeters of sediment where they are easily accessible to predators including fishes. This hypothesis was supported by many other investigators (Sudarshan and Neelakantan, 1986). The nematodes seem to play the role of conveyer belt and therefore the meiofauna of Red Sea could be considered important as food for higher trophic levels.

In conclusion, a total of 10 meiofaunal taxa were identified at the interstitial habitat of the Red Sea, with meiofauna community being primarily dominated by nematodes, harpacticoid copepods, polycheates and ostracodes. The meiofaunal density is influenced by a set of physico-chemical factors of the sediment as well as by the presence of the biogenic structures. The more food availability of mangroves and seagrass meadows, their sediment stability, protection from predators, and their habitat complexity increase the density of meiofaunal community in the Red Sea sediment. Over 50% of the density of all meiofaunal taxa occurred in the upper layer of 0–4 cm depth and progressively decreased with increasing depth in the Red Sea sediment.