Key Biodiversity Areas : Rapid assessment of phytoplankton in the Mesopotamian Marshlands of southern Iraq

Between the summers of 2005 and 2007, studies have been conducted for fi ve seasons in several marsh locations in southern Iraq. During fi ve surveys, 317 taxa of phytoplankton belonging to six major groups were identifi ed. Th ese included: 204 taxa of Bacillariophyceae (represented by 13 Centrales and 191 Pennales, thus 14% and 27% respectively of all taxa recorded), 59 Chlorophyta (28%), one Cryptophyta (4%), 39 Cyanophyta (21%), 10 Euglenophyta (2%) and four Pyrrophyta (4% of all the taxa recorded). Th e Central Marsh, Hammar Marsh and the Hawizeh Marsh had higher phytoplankton populations compared to all other studied sites. Th e dominant phytoplankton groups throughout the study area were the Bacillariophyceae, Chlorophyta and Cyanophyta. Th e dominant species were Cyclotella meneghiniana, Kirchneriella irregularis and Nitzschia palea. A progression in the richness and biodiversity of species occurred during winter. Th ese three phytoplankton groups were dominant in waters of southern Iraq and were responsible for most of the species richness and diversity observed. Generally, sites changed from summer to winter according to the changing conditions associated with nutrients, salinity, temperature, and light intensity. Th ese controlling factors infl uenced phytoplankton biomass from season to season.


Introduction
Aquatic ecosystems are dynamic with several biotic and abiotic variables changing in space and time.From 2005 to 2007, after refl ooding of the southern marshes, the Key Biodiversity Areas (KBA) project led by Nature Iraq undertook ecological surveys of fl ora and fauna across southern Iraq (Rubec and Bachmann 2008).Th e KBA Project was involved a rapid assessment in several marshes to understand changes that took place in the physicochemical characteristics of the marshes and consequently changes in phytoplankton composition.Most of the surveys occurred in the Central Marsh, Hammar Marsh, Hawizeh Marsh, Middle Euphrates, the Khor al-Zobayr, the Seasonal Marshes and the Shatt al-Arab.Although, the phytoplankton fl ora in some of these marshes has been studied previously, the present study contributes new information on the current status of phytoplankton populations and their diversity in these ecosystems.Th is is in relation to physicochemical characteristics of these waters after several decades of major environmental degradation caused by confl ict, dam building in the Tigris-Euphrates Basin and directed drainage by the previous regime.
Wetlands are ecosystems in which the soil, despite periodic fl uctuations in water level, is more or less continuously waterlogged.Non-marine wetlands generally have a water depth less than 2 m and, by this defi nition comprise as much as 6% of the land area of the earth's surface (Mitsch and Gosselink 1993).Studies have shown that marshes are suitable areas for the growth of several types of algae and higher aquatic plants.Th e marshes of southern Iraq seem especially suitable for growth of algae so that they diversify widely due to the shallow waters, the slow fl ow of the water attributable to low gradients and suitable nutrient concentrations and temperatures (Yaaqub 1992).Th erefore, these algae have been widely used for water quality monitoring, and as they are primary producers, they are easily aff ected by physical and chemical variations in their environment (Bartram and Balance 1996).
Temporal and spatial distributions of phytoplankton are determined by a variety of environmental factors, including sunlight, the availability of essential nutrients and water temperature.Hinton andMaulood (1980, 1982) showed that at least 77 diatom taxa and 101 non-diatom taxa are known from the brackish waters of southern Iraq, the Shatt al-Arab and the Hammar Marsh.A total of 129 algal species and 63 genera were in the marshes near Qurna (Pankow et al. 1979, Al-Saboonchi et al. 1982).Some 72 Bacillariophyta, 28 Chlorophyta, 26 Cyanophyta, two Euglenophyta, and one Cryptophyta have been recorded in Hammar Marsh (Nurul-Islam 1982).Dinofl agellates have also been recorded in the marshes (Evans 2001).

Materials and methods
For qualitative studies of phytoplankton, samples were taken by a phytoplankton net manufactured by Hydro-Bios (23 μm in pore diameter), which was placed into the water 10 to 15 cm below the water surface and pulled at an appropriate speed for 10 to15 min.Th e phytoplankton collected was transferred to a polyethylene container and preserved by adding Lugol's solution at a ratio of 1:100 with 40% formaldehyde until analyzed in the laboratory.Th e non-diatoms were identifi ed by taking a drop of the sample on a slide with a slide cover, and then examined using a compound microscope (x10, x40 and x100).For diatom identifi cation, a water sample was mixed with an equal volume of nitric acid in a 15 ml test tube to dissolve the organic matter surrounding the diatoms.Th e diatoms were precipitated by centrifuge and permanent slides were made using Canada balsam or Naphrax and a hot plate (Patrick and Riemer 1975).
For the quantitative study of phytoplankton, one-liter water samples were collected in polyethylene containers and preserved with a Lugol/formaldehyde solution (as described above).Following sedimentation the total number of phytoplankton organisms was counted (Furet and Benson-Evans 1982).Permanent slides were prepared and diatoms were identifi ed using a compound microscope.Smith (1950), Prescott (1944, 1982) and Th ompson (1959) were references used in phytoplankton identifi cation.Th e Shannon-Wiener Diversity Index (H) was used to determine the diversity and compare among stations.Th is was done using the statistical software CANOCO 4.5 package (Ter Braak and Šmilauer 2002); the equation is:

Study area
Most of the fi eld sites in southern Iraq had not been surveyed since at least 1979 or earlier.An initial February and March 2005 survey was restricted to seven sites in southern Iraq.It was limited by practical and security issues in that period and seen as a start-up, experience-building exercise.All other southern KBA sites were included in the subsequent 2005 through 2007 surveys.In order to facilitate fi eld survey logistics, seven major wetland areas as shown in Fig. 1 and Table 1 were defi ned.
During summer 2005 survey, Cyanophyta had the highest total count (90,207.1 × 10 3 cells L -1 ).Th e dominant Cyanophyta species were Anabaena sp., Microcystis aeruginosa, Merismopedia convolute, Oscillatoria geitleri, Oscillatoria limnetica, and Lyngbya limnetica.Th ese genera of Cyanophyta are known for their ability to produce potential toxic substances especially Anabaena, Lyngbya and Microcystis (Sivonen andJones 1999, Carmichael 2001).Th ese species are also among the most abundant Cyanophyta in fresh and brackish waters (Huisman et al. 2005).Microcystis possesses gas vesicles that make them buoyant.Th is characteristic may have aided in the dominance of this species because it allows it to receive more light than species lacking gas vesicles (Seckbach 2007).Most of these dominant Cyanophyta prefer relatively alkaline, warmer, saline and nutrient-rich waters (Wehr andSheath 2003, Al-Saadi andSulaiman 2006).Th e Cyanophyta were followed in abundance by the diatoms, Chlorophyta and Pyrrophyta, as shown in Appendix 1.
During both the winter and summer 2006 surveys, Chlorophyta had the highest total counts (37,308.9 × 10 3 cells L -1 and 23,180.8× 10 3 cells L -1 respectively).Th e Chlorophyta is known to occur primarily in freshwater.It was mainly dominated by Kirchneriella irregularis, Scenedesmus quadricauda, Monoraphidium contortum and Coelastrum astroideum.Non-motile chlorophytes were a component of the plankton community (e.g.Monoraphidium, Coelastrum and Scenedesmus).Under moderate conditions, these species are most abundant in freshwater ecosystems especially during the summer, when light and temperature are near their seasonal maximum and nutrients become a limiting factor.Th e diatoms followed the chlorophytes during both seasons in terms of abundance (41,804.5 × 10 3 cells L -1 ) and were dominated by Cyclotella atomus, Cyclotella meneghiniana, Achnanthes minutissima, Fragilaria ulna, Fragilaria vaucheriae, Nitzschia gracilis, Nitzschia longissima and Nitzschia palea.Cyclotella meneghiniana is known to prefer relatively slow fl owing, saline and alkaline waters (Stoermer and Smol 2004).
Achnanthes minutissima was one of the dominant pennate diatoms probably because this species is physiologically more active than larger diatom cells.Th is would partly be due to its large surface to volume ratios (Allen 1977).Usually, dominant algal groups of nutrient-rich, temperate freshwater wetlands include pennate diatoms, typically genera such as Achnanthes, Fragilaria, Navicula and Nitzschia (Stevenson et al. 1996).In the winter 2007 survey, Bacillariophyceae/Pennales had the highest total count (29,674.2× 10 3 cells L -1 ).Th e dominant species was Nitzschia palea, one of the most common species in this genus, which is often found in organically polluted waters (Palmer 1969).In addition, Oscillatoria limnetica was the main cyanophyte, Peridinium cinctum the main dinofl agellate and Kirchneriella irregularis the main chlorophyte observed.In the summer of 2007 survey, the chlorophytes that had the highest total counts (54,473.4 × 10 3 cells L -1 ) were Kirchneriella irregularis, Scenedesmus quadricauda and Monoraphidium convolutum.
Generally, in all of these surveys, the highest cell concentrations were in the Central Marsh, Hammar Marsh and Hawizeh Marsh (Table 2).Among the 24 sites in the Central Marsh, those with the highest diversity were Al Kinziryi, the Al Hammar Area and Al Fhood.From the 20 sites in the Hammar Marsh, the most diverse site was Al Sallal.Ojayradah was the most diverse site among the seven sites in the Hawizeh Marsh.
Th erefore, algal assemblages may diff er between restored and extant wetlands and could be valuable indicators of restoration success because algal species composition and diversity would diff er in low-and high-nutrient wetlands (John 1993, Mayer andGalatowitsch 1999 as cited in Stevenson et al. 2006).Sites obviously also revealed changes from summer to winter, associated with changes in nutrients, temperature and light intensity.Th erefore, changes in seasonality as shown by varying environmental variables could strongly aff ect phytoplankton variability (Abdul-Hussein and Mason 1988).Variations in the annual temperature regime appear to be the major cause of temporal variability of phytoplankton in the area, as observed by Gayoso (1998).According to richness and diversity indicators, the authors observed that there is an improvement in water quality in the southern Iraqi marshes especially in winter.Th is may be attributed to the fact that in winter nutrient levels are higher due to seasonally higher rainfall and thus higher runoff from the surrounding lands.Oxygen concentrations are also higher at lower temperatures.Canonical Correspondence Analysis (CCA) was used to elucidate the relationships between biological assemblages of the phytoplankton samples and their environment to determine the phytoplankton richness and diversity in the marshes.As a result, there was an increase in the phytoplankton richness and diversity of these marshes, as illustrated in Figs 2 and 3.
Each object shape in Fig. 2 demonstrates a phytoplankton sample obtained during the surveys, indicating the diversity and richness during the fi ve surveys.Diversity and richness values of the fi rst two surveys during the summer of 2005 and the winter of 2006 were scattered compared with the values recorded during the 2007 winter and summer, where they started to develop and increase in numbers.
Fig. 3 demonstrates that the phytoplankton diversity ranged between 1.6-2.1 during summer 2005 and winter 2006, while diversity values became higher during the following surveys ranging between 2.1 and 2.4, meaning that the diversity increased.It is clear that the diversity during the fi rst two surveys was lower compared to the following surveys where the diversity began to even out and fl uctuate to a lesser degree.Th e increase in the phytoplankton diversity and richness were most likely related to the environmental conditions that also started getting more stable.
An important reason for the success of certain algal species in wetland habitats is their ability to tolerate variations in water level and desiccation.Water levels may fl uctuate several times in a few months or persist for several years.Algae that are subjected to a variable moisture regime must have the capacity to adapt to tolerate the extremes of these environmental conditions (Wehr and Sheath 2003).Th us, many factors may contribute to phytoplankton diversity and production in wetlands, including nutrients, temperature, light, macrophytes, etc. (Stevenson et al. 1996).As in other water bodies, nutrient conditions, climate, and geology infl uence species composition but in wetlands, water level, plant composition and degree of mixing with other water bodies are also important for the phytoplankton community (Goldsborough and Robinson 1996).
In the southern Iraqi marshes, the authors observed that diatoms, Chlorophyta and Cyanophyta were the dominant phytoplankton groups, which agrees with the fi ndings of Goldsborough and Robinson (1996).

Conclusions and recommendations
Th e main conclusions from these studies are: Th e phytoplankton groups that dominate the southern marshes are diatoms, Chlorophyta and Cyanophyta, with other groups having a low number of species; In all sites of the southern marshes of Iraq studied, especially in the Central Marsh, Hammar Marsh and Hawizeh Marsh, phytoplankton richness and diversity increased from 2005 to 2007.
Based on these studies, several recommendations relevant to the management of the marshes of southern Iraq are made by the authors: Phytoplankton should be used for ongoing biological monitoring and as indicators for organic pollution in the marshes; Th e controlling factors infl uencing phytoplankton biomass may vary from season to season and phytoplankton biomass may be more sensitive and responsive to environmental variables in winter and summer as compared to autumn and spring.Monitoring programs should be fl exible to allow for adjustment to these changing environmental conditions; Monitoring studies should focus on the main parameters that have the greatest eff ects on the phytoplankton community.Th ese are: light penetration, temperature, pH, water fl ow, nutrient levels and land use, in particular for water buff alo and cattle grazing.
H = -∑ (Ni/N)* Ln *(Ni/N) N = the hall summation of species density in the single station Ni = density of single species

Figure 1 .
Figure 1.Major wetlands of southern Iraq indicating specifi c locations of marshes surveyed for phytoplankton assessment.

Figure 2 .
Figure 2. Seasonal phytoplankton diversity and richness in all sites.

Figure 3 .
Figure 3. Seasonal phytoplankton diversity contour in all sites.

Table 1 .
Th e seven major wetland areas of southern Iraq.