AMZ vol 19 (2021) pp 99-111

Arxius de Miscel·lània Zoològica, 19 (2021): 99–111

Khirani–Betrouche Moulaï ISSN: and 1698–0476

Does salinity have an influence on the diversity and structure of the wintering waterbirds of the Saharan wetlands in Algeria?

F. Khirani–Betrouche, R. Moulaï

Khirani–Betrouche, F., Moulaï, R., 2021. Does salinity have an influence on the diversity and structure of the wintering waterbirds of the Saharan wetlands in Algeria? Arxius de Miscel·lània Zoològica, 19: 99–111, Doi: https://doi.org/10.32800/amz.2021.19.0099 Abstract Does salinity have an influence on the diversity and structure of the wintering waterbirds of the Saharan wetlands in Algeria? Between 2017 and 2019, 42 species of wintering waterbirds were recorded in the wetland complex of the Oued Righ valley in the Algerian Sahara. The intersite amplitudes of salinity explained the variations in species richness and distribution of waterbirds in the various wetlands studied. Oligohaline (0.5–5 ‰) and mesohaline (5–18 ‰) environments, represented by Lake Ayata, Lake Sidi Khelil and Oued Kherouf, were the most favorable to Anatidae with the exception of the Tadornes where their presence was noted in the euhaline (30–40 ‰) and hyperhaline stations (> 40 ‰). The presence of the greater flamingo Phoenicopterus roseus and the slender–billed gull Chroicocephalus genei stood out in the most holomorphic areas of the complex, such as Chott Merouane.

Dataset published through GBIF (Doi: 10.15470/6fqd0h) Key words: Waterbirds, Sahara, Wetlands, Salinity, Algeria Resumen ¿Influye la salinidad en la diversidad y estructura de las aves acuáticas invernantes en los humedales del Sahara, en Argelia? Durante el período 2017–2019 se registraron 42 especies de aves acuáticas invernantes en el complejo de humedales del valle de Oued Righ, en el Sahara argelino. Las diferencias de salinidad explican las variaciones en la riqueza de especies y en la distribución de las aves acuáticas en los diferentes humedales estudiados.

Los ambientes oligohalinos (0,5–5 ‰) y mesohalinos (5–18 ‰), representados por el lago Ayata, el lago Sidi Khelil y el Oued Kherouf, son los más favorables para los anátidos con la excepción del género Tadorna, que está presente en los puntos de estudio euhalinos (30–40 ‰) e hiperhalinos (> 40 ‰). El flamenco común Phoenicopterus roseus y la gaviota picofina Chroicocephalus genei se distinguen por su presencia en las zonas más holomorfas del complejo como Chott Merouane.

Datos publicados en GBIF (Doi: 10.15470/6fqd0h) Palabras clave: Aves acuáticas, Sahara, Humedales, Salinidad, Argelia © [2021] Copyright belongs to the authors, who license the journal Arxius de Miscel·lània Zoològica to publish the paper under a Creative Commons Attribution 4.0 License, which permits its distribution, and reproduction in any medium, provided the original authors and source, the journal Arxius de Miscel·lània Zoològica, are cited.

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Resum Influeix la salinitat en la diversitat i l’estructura dels ocells aquàtics hivernants als aiguamolls del Sàhara, a Algèria? Durant el període 2017–2019 es van registrar 42 espècies d’ocells aquàtics hivernants al complex d’aiguamolls de la vall d’Oued Righ, al Sàhara algerià. Les diferències de salinitat expliquen les variacions en la riquesa d’espècies i en la distribució dels ocells aquàtics als diversos aiguamolls estudiats. Els ambients oligohalins (0,5–5 ‰) i mesohalins (5–18 ‰), representats pel llac Aiata, el llac Sidi Khelil i l’Oued Kherouf, són els més favorables per als anàtids, excepte el gènere Tadorna, que és present als punts d’estudi euhalins (30–40 ‰) i hiperhalins (> 40 ‰). El flamenc rosat Phoenicopterus roseus i la gavina de bec prim Chroicocephalus genei es distingeixen per ser presents a les zones més holomorfes del complex com ara Chott Merouane.

Dades publicades a GBIF (Doi: 10.15470/6fqd0h) Paraules clau: Ocells aquàtics, Sàhara, Aiguamolls, Salinitat, Algèria Received: 11 /02/2021; Conditional acceptance: 29/03/2021; Final acceptance: 19/04/2021 Fatima Khirani–Betrouche, Riadh Moulaï, Laboratoire de Zoologie Appliquée et d’Ecophysiologie Animale, Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, 06000 Algérie.

Corresponding author: F. Khirani–Betrouche. E–mail: fbetrouche@hotmail.fr ORCID ID: F. Khirani–Betrouche: 0000-0003-4891-9166; R. Moulaï: 0000-0001-7935-4415

Introduction Wetlands are reservoirs for biodiversity, providing habitats for large numbers of waterbirds (Sebastián–González and Green 2014; Cherkaoui et al., 2015, 2017). However, data on wetlands at the southern border of the Mediterranean in North Africa, especially those in inland areas (Hamza and Selmi, 2018) have received little attention and data are lacking.

Many North African wetlands, nevertheless, are recognized as Important Bird Areas and appear to play a crucial role as wintering and breeding sites for a wide range of waterbirds (Bensaci et al., 2013; Cherkaoui et al., 2015; Hamza and Selmi 2015; Cherkaoui et al., 2017).

The distribution of birds throughout the wetland area is related to the biological and ecological criteria characteristic of both the species and the site (Houhamdi, 1998; Houhamdi and Samraoui, 2002). Understanding the relationships between species richness and environmental factors is fundamental for better management and conservation (Donald et al., 2002; Kosicki and Chylarecki, 2012). The physico–chemical parameters of wetlands (salinity, PH, temperature, oxygen levels, mineralization and conductivity) influence the choice of feeding, resting and breeding sites for many species of waterfowl.

Our present study focuses on the possible influence of water salinity on the distribution and structure of the aquatic avifauna of Saharan wetlands. Salinity is a structuring parameter in the biology of aquatic organisms (Green and Figuerola, 2003; Kushlan, 1993).

Various waterbird communities have been observed along the salinity gradient (Ysebaert et al., 2000), particularly in arid conditions, thus influencing the choice of feeding, resting and breeding sites for many species of aquatic birds. Salinity could therefore be an indicator of these characteristics of the environment. Waterbirds are sensitive to changes in salinity. The ability of large numbers of waterbirds to profitably use saline lakes basically depends on concentrations of invertebrate fauna (Senner et al., 2018). Waterbird use of these arid–land wetlands throughout the annual cycle depends on physiological adaptations that take advantage of abundant saline wetland–derived prey. These adaptations are linked

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to metabolism, digestion, and osmosis. Newly–hatched waterbirds, for example, must be raised near fresh water as they do not yet have a well–developed salt gland to cope with heavy salt loads (Haig et al., 2019).

To our knowledge, this is the first study in this area to relate salinity, a distinctive physicochemical parameter in these wetlands, with the distribution of wintering waterbirds. It should be noted that the Oued Righ Valley was the subject of a single sampling study in which 53 waterbird species of all statuses were recorded by Bensaci et al. (2013).

Material and methods Study area The eco–complex of the Oued Righ Valley wetlands in the Algerian Sahara is one of the most important wetland complexes in Algeria (fig. 1). This Saharan depression constitutes a wintering area that is favorable for the aquatic avifauna of the western Palearctic and a migratory stopover during the great crossing of the Sahara to reach the sub–Sahelian wetlands (Isenmann and Moali, 2000).

The Oued Righ Valley includes several wetlands, three of which are classified as RAMSAR sites: Chott Merouane, Oued Kherouf and Chott Sidi Slimane. This valley in south–eastern Algeria occupies an area of 11,738 km 2 (Khechana et al., 2010). As part of the whole of the lower Sahara basin, it is a vast depression elongated between 32° 54' N and 34° 9' N. Like all Saharan regions, this depression is characterized by an arid continental climate.

The average annual rainfall is low and irregular, about 80 mm, so it does not have a role in the direct recharge of aquifers and wetlands (Habes et al., 2016). The water comes from runoff, and surplus irrigation water arises not only from the drainage of palm groves but also from groundwater (Khechana and Derradji, 2014). Our study focused on six wetlands: Chott Merouane (sometimes designated on maps as Chott Felrhir) and Oued Kherouf (fig.

2) both of which have been classified as Ramsar sites since 2 February 2001), Lake of Sidi khelil, Chott Tendla, Lake of Ayata (fig. 3) and Lake of Merdjadja (table 1).

Methods for collecting and analyzing data The field study was conducted during two wintering periods (2017–2018 and 2018–2019).

Thirty–three visits totaling approximately 230 hours were made. Counts were carried out by direct observation of different waterbird species using a telescope (KITE SP 82 ED) and binoculars. An exhaustive count of individuals was carried out when the distance was less than about 200 m and the number of individuals was less than 200. When the group was greater than 200 individuals or if it was at a remote distance, we proceeded by dividing the visual field into several bands, counting the number of birds in an average band and reported as many times as bands (Blondel, 1975; Tamisier and Dehorter, 1999). All wetlands except Chott Merouane were fully studied. In Chott Merouane, which is very large, we established three stations, covering a total area of about 1,500 hectares.

To calculate wetland salinity, we chose the direct method using a portable optical refractometer with a measuring range of 0–100 ‰. We analysed a total of eleven stations on the six wetlands and classified these according to the categorization of the salinity of Mediterranean wetlands proposed by Farinha et al. (1996): freshwater < 0.5 ‰, Oligohaline (0.5–5 ‰), Mesohaline (5–18 ‰), Polyhaline (18–30 ‰), Euhaline (30–40 ‰) and Hyperhaline > 40 ‰.

The salinity was determined during the wintering periods in 11 stations of the Oued Righ wetland complex (table 2). To measure the salinity of stations, we employed the direct method, using a portable optical refractometer with automatic temperature compensation (ATC) from AUTOUTLET with a measuring range from 0 to 100 ‰.

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To Biskra City

N Chott Melghir

Algeria El–Hamraia 1 Lake

Chott Merouane Oued Kherouf

El–Hamraia 2 Lake

Sidi khelil Lake To El–Oued City

Chott Tendla

Africa

Chott Tighdidine

Merara Lake

Ayata Lake Merdjadja Lake Temacine Lake To Ouargla City

Wetlands studied

10 km

Chott Lgoug Wetland Urban area

National road Oued Righ Canal

Fig. 1. Geographical location of the Oued Righ Valley eco–complex and location of the studied wetlands.

Fig. 1. Localización geográfica del ecocomplejo del valle de Oued Righ y situación de los humedales estudiados.

To determine the affinities and intersite variations according to the different degrees of salinity we carried out a factor analysis of correspondences (AFC). The significance level for statistical analysis is p–value < 0.001 (fig. 4).

To determine the affinities and inter–site variations according to the different salinity levels during the monitoring periods, a correspondence factorial analysis was carried out using XLstat version 2016 software. The significance level for statistical analysis was p–value < 0.001.

Results Forty–two species of wintering waterbirds were observed in the framework of this study, representing 42 % of the waterbird species recorded so far in Algeria. Fourteen species were breeding birds, representing nearly 34 % of the breeding waterbirds in Algeria (Samraoui et al., 2011). As regards breeding birds of high heritage value, we report the marbled teal Marmaronetta angustirostris, the ferruginous duck Aythya nyroca, the greater flamingo Phoenicopterus roseus and the slender–billed gull Chroicocephalus genei (IUCN, 2018).

Among the 42 species of wintering waterbirds in the six wetlands studied, 13 species of Anatidae were observed. The highest presence of Anatidae was found in winter, at Lake Ayata, Lake Merdjadja, and Oued Kherouf (table 3; dataset published in GBIF: Doi: 10.15470/6fqd0h).

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Fig. 2. Oued Kherouf, Photo by F. Khirani–Betrouche, 24/02/2019.

Fig. 2. Oued Kherouf. Foto de F. Khirani–Betrouche, 24/02/2019.

Fig. 3. Lake of Ayata, Photo by F. Khirani–Betrouche, 21/03/2019.

Fig. 3. Lago de Ayata. Foto de F. Khirani–Betrouche, 21/03/2019.

The wintering waders inventoried were represented by Recurvirostridae (Himantopus himantopus, Recurvirostra avosetta), Charadridae (Vanellus vanellus, Charadrius dubius, Charadrius alexandrinus) and Scolopacidae (Gallinago gallinago, Tringa ochropus, Tringa totanus, Tringa stagnatilis, Tringa erythropus). Their presence was most significant in the mudflats of Sidi Khelil Lake, Chott Tendla, Ayata Lake and Chott Merouane.

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Table 1. Characteristics of the Oued Righ Valley wetlands. The surface area of the Saharan wetlands is not stable because the water bodies are subject to great evaporation during the dry seasons. The geographical data thus remain approximate.

Tabla 1. Características de los humedales del valle de Oued Righ. La superficie de los humedales del Sahara no es estable porque las masas de agua están sometidas a una gran evaporación en las estaciones secas, por lo que los datos geográficos son aproximados.

Wetland

Geographical coordinates

Bounding Box

Class and subclass (Ramsar criteria)

Surface (in ha)

Depth Vegetation (in m) (reedbed, in ha)

Chott Merouane

34° 01' 48.2" N

5° 58' 35.7" E,

II, III

337,700

0.4–3

20

1,200

0.8–3

70

33° 55' 03.5" N,

(M, Q, Sp, Ss, Y, 3, 5, 9):

6° 23' 01.0" E,

[5, 6, 7, 8]

34° 07' 21.3" N

Oued Kherouf

6° 05' 52.9" E

33° 52' 45.0" N

6° 00' 56.6" E,

II, III

6° 01' 12.2" E

33° 43' 27.3" N,

(M, 3, 5, Y, Sp, Q, 9):

6° 04' 06.8" E,

[5, 6, 7, 8]

33° 56' 05.0" N

Sidi Khelil Lake

33° 51' 08.4" N

5° 58' 13.3" E,

5° 58' 18.7" E

33° 51' 02.1" N,

5° 58' 19.9" E,

33° 51' 23.9" N

ChottTendla

33° 39' 35.5" N

6° 02' 26.5" E,

6° 03' 23.0" E

33° 37' 48.0" N,

6° 03' 27.1" E,

33° 40' 27.1" N

Ayata Lake

33° 29' 32.4" N

5° 59' 11.2" E,

5° 59' 26.8" E

33° 29' 20.6" N,

5° 59' 38.3" E,

33° 29' 44.1" N

Merdjadja Lake

33° 03' 13.3" N 6° 03' 57.3" E

6° 03' 06.3" E,

II (Q, R)

20

2.5

80

II, III (Y, 3, 6)

600

0.2–0.4

5

II (Q)

155

0.2–1.3

70

II (Q)

16

3

5

33° 03' 06.3" N,

6° 04' 00.4" E,

33° 03' 20.6" N

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Table 2. Salinity of the stations studied in Oued Righ wetlands.

Tabla 2. Salinidad de las estaciones estudiadas en los humedales de Oued Righ.

Station 1

Salinity

coordinates

sampling

Wetland

4

33° 29' 34.5" N

21/01/2019

Ayata Lake

21/01/2019

Ayata Lake

24/01/2019

Chott Tendla

24/01/2019

Chott Tendla

26/01/2019

Chott Merouane

27/01/2019

Sidi Khelil Lake

02/02/2019

Merdjadja Lake

03/02/2019

Sidi Khelil Lake

05/02/2019

Oued Kherouf

05/02/2019

Oued Kherouf

12/02/2019

Chott Merouane

6

3

25

4

31

5

98

6

12

7

15

8

23

9

15

10

23

11

Date of

(in ‰)

2

Geographical

61

5° 59' 25.6" E 33° 29' 37.7" N 5° 59' 26.2" E 33° 40' 03.7" N 6° 03' 21.9" E 33° 39' 41.5" N 6° 03' 25.2" E 34° 02' 12.0" N 5° 59' 20.3" E 33° 51' 04.9" N 5° 58' 19.0" E 33° 03' 09.9" N 6° 03' 57.4" E 33° 51' 17.1" N 5° 58' 18.7" E 33° 52' 47.0" N 6° 01' 12.3" E 33° 53' 16.2" N 6° 01' 56.6" E 34° 00' 33.6" N 6° 00' 11.7" E

The presence of the wintering populations of greater flamingo Phoenicopterus roseus, slender–billed gulls Chroicocephalus genei and shelduck Tadorna tadorna which are added to the nesting populations was particularly high at Chott Merouane. Correspondence analysis (fig. 4) showed that the first two factor axes explained more than 92 % of the total observations.

The F1 axis opposes low salinity environments, Oligohaline, Mesohaline and Polyhaline, and high salinity environments, Euhaline and Hyperhaline. This axis thus represents the general salinity level, 80, accounting for 41 % of the total inertia. This suggests a priori a significant relationship between the level of salinity and the distribution of species.

The F2 axis, whose factorial weight is 11,80 %, opposes the Hyperhaline environment on the one hand and Oligohaline, Mesohaline and Polyhaline environments on the other.

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Table 3. Wintering waterbirds recorded in the wetlands of the Oued Righ Valley from 2017 to 2019: UICN, UICN conservation status. Phenological status: W, wintering; T, transient; RB, resident breeder; MB, migratory breeder. Biogeographical origin: OW, Old World; C, cosmopolitan; E, European; ET, European–Turkestanian; ETH, Ethiopian; H, Holarctic; IA, Indo–African; M, Mediterranean; P, Palearctic; PX, Paleo–Xeric; SAR, Sarmatic; SIB, Siberian; TM, Turkestan–Mediterranean; UB, Abuiquist; NEARC, Nearctic; ARC, Arctic.

Tabla 3. Aves acuáticas hibernantes registradas en los humedales del valle de Oued Righ entre 2017 y 2019: IUCN, estado de conservación de la UICN. (Para las abreviaturas del estado fenológico y del origen biogeográfico, véase arriba).

Maximum records from 2017 to 2019 Family Species

Biogeographical Phenological origin status IUCN

Chott Merouane

Date

Oued Kherouf

Date

Sidi Khelil Date

Chott Tendla Date

Ayata Lake Date

Merdjadja Lake

Date

Anatidae Tadorna tadorna S W, MB LC 237 22/12/2017 90 16/03/2018 26 18/02/2018 160 11/03/2018 42 12/11/2018 18 07/01/2018 Tadorna ferruginea H W, RB LC 21 15/01/2019 5 24/02/2019 2 06/01/2018 26 24/03/2019 12 04/01/2018 7 13/01/2019 Spatula querquedula P MB, T LC 0 / 13 16/03/2018 21 22/03/2019 0 / 12 21/03/2019 3 14/02/2018 Spatula clypeata H W, T LC 0 / 20 13/04/2018 445 12/03/2018 18 09/04/2018 617 08/04/2018 58 21/04/2018 Mareca strepera H W LC 0 / 3 30/01/2019 8 06/01/2018 0 / 6 04/01/2018 0 / Mareca penelope P W, T LC 0 / 4 25/03/2019 5 18/02/2018 0 / 3 21/03/2019 0 / Anas platyrhynchos H W, RB LC 8 10/03/2018 18 16/01/2019 23 18/12/2017 0 / 45 17/01/2019 26 13/01/2019 Anas acuta P W, T LC 0 / 8 16/03/2018 7 12/03/2018 0 / 7 05/11/2018 0 / Anas crecca H W LC 22 15/01/2019 180 14/01/2019 50 06/01/2018 0 / 63 03/01/2018 7 13/01/2019 Marmaronetta angustirostris SAR W, RB, T VU 2 10/03/2018 134 16/03/2018 186 12/03/2018 0 / 274 21/03/2019 38 07/01/2018 Aythya ferina P W VU 0 / 12 24/02/2019 6 18/12/2017 0 / 8 03/01/2018 2 17/12/2017 Aythya nyroca TM W, RB NT 0 / 41 19/12/2017 59 06/01/2018 0 / 67 17/01/2019 42 14/02/2018 Aythya fuligula P W, T LC 0 / 18 23/03/2019 23 22/03/2019 0 / 12 08/04/2018 18 21/04/2018 Oxyura leucocephala NEARC W EN 6 12/02/2018 0 / 2 06/01/2018 0 / 0 / 0 / Rallidae Rallus aquaticus Gallinula chloropus Fulica atra Porphyrio porphyrio

C T LC 0 / 0 / 0 / 0 / 2 05/11/2018 0 / C W, RB LC 46 15/01/2019 60 16/01/2019 27 12/03/2018 20 02/01/2018 41 20/12/2017 45 04/02/2018 P W, RB, T LC 18 10/03/2018 12 16/03/2018 31 12/03/2018 5 11/03/2018 39 08/04/2018 23 21/04/2018 OW W, T LC 0 / 8 16/03/2018 0 / 0 / 4 21/03/2019 0 /

Podicipedidae Tachybaptus ruficollis Podiceps cristatus Podiceps nigricollis

OW W, MB LC 0 / 32 13/04/2018 28 18/02/2018 0 / 20 05/11/2018 21 21/04/2018 OW W LC 0 / 0 / 0 / 0 / 2 04/01/2018 2 04/02/2018 OW W LC 0 / 5 14/01/2019 6 06/01/2018 0 / 6 03/01/2018 3 13/01/2019

Phoenicopteridae Phoenicopterus roseus

H

W, RB

LC 9500 26/03/2019 25 16/03/2018

24 06/01/2018 10 24/03/2019 19 17/01/2019 0

/

Recurvirostridae Himantopus himantopus Recurvirostra avosetta

C TM

W, RB W, RB

LC 179 10/03/2018 82 16/01/2019 LC 54 15/01/2019 8 24/02/2019

0 0

/ /

NT 0 / 0 / LC 0 / 0 / LC 16 15/01/2019 8 14/01/2019 LC 48 26/03/2019 12 24/02/2019

0 / 0 / 2 17/01/2019 0 / 0 / 28 11/03/2018 25 08/04/2018 0 / 0 / 30 02/01/2018 16 20/12/2017 0 / 0 / 120 05/01/2018 21 12/11/2018 0 /

LC NT LC NT LC LC LC LC LC LC LC LC LC

0 / 5 24/03/2019 4 21/03/2019 0 / 9 24/03/2019 1 21/03/2019 12 12/03/2018 32 24/03/2019 18 08/04/2018 5 22/03/2019 6 11/03/2018 4 12/10/2018 0 / 25 11/03/2018 7 08/04/2018 0 / 17 11/03/2018 6 21/03/2019 0 / 9 05/01/2018 17 03/01/2018 11 06/01/2018 48 21/12/2017 15 04/01/2018 0 / 6 21/12/2017 7 20/12/2017 0 / 6 02/01/2018 4 17/01/2019 0 / 8 09/04/2018 6 08/04/2018 0 / 22 21/12/2017 19 04/01/2018 0 / 32 24/03/2019 16 12/10/2018

Charadridae Vanellus vanellus Charadrius hiaticula Charadrius dubius Charadrius alexandrinus Scolopacidae Numenius phaeopus Limosa limosa Calidris pugnax Calidris ferruginea Calidris alpina Calidris minuta Gallinago gallinago Tringa ochropus Tringa totanus Tringa stagnatilis Tringa glareola Tringa erythropus Tringa nebularia Hirundinidea Riparia riparia

P W P T P W C W, RB ARC P P ARC ARC ARC H P P P DP DP SIB

T T T T T T W W W W T W T

C T LC 0 / 0 /

Laridae Chroicocephalus genei SAR RB, W Chroicocephalus ridibundus P W, T Hydrocoloeus minutus P T Larus michahellis OW W Chlidonias hybrida OW T Chlidonias niger H T Ciconiidae Ciconia nigra Ciconia ciconia

0 / 6 13/04/2018 0 / 4 25/03/2019 51 26/03/2019 43 25/03/2019 12 26/03/2019 0 25/03/2019 29 10/03/2018 5 23/03/2019 57 26/03/2019 0 13/04/2018 10 22/12/2017 4 16/01/2019 48 22/12/2017 14 30/01/2019 0 / 0 30/01/2019 9 22/12/2017 2 19/12/2017 0 / 0 / 16 22/12/2017 5 14/01/2019 13 26/03/2019 11 23/03/2019

/ /

107 24/03/2019 35 20/12/2017 0 75 05/01/2018 17 17/01/2019 0

7 21/04/2018 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 /

51 12/03//2018 0 / 0 / 0 /

LC 351 12/02/2018 17 30/01/2019 8 06/01/2018 23 02/01/2018 14 17/01/2019 6 13/01/2019 LC 21 26/03/2019 0 25/03/2019 2 12/03/2018 7 11/03/2018 4 12/11/2018 0 / LC 4 13/11/2018 0 13/04/2018 0 / 0 11/03/2018 0 08/04/2018 0 / LC 2 15/01/2019 0 16/01/2019 2 18/12/2017 1 05/01/2018 1 20/12/2017 0 / LC 0 / 2 13/04/2018 1 12/03/2018 0 / 2 08/04/2018 0 / LC 0 / 0 / 1 12/03/2018 0 / 1 12/11/2018 0 /

P T LC 1 13/11/2018 0 / P W, T LC 8 10/03/2018 6 16/01/2019

Phalacrocoracidae Phalacrocorax carbo

OW

W, T

LC

Threskiornithidae Plegadis falcinellus Platalea leucorodia

OW OW

T W, T

LC 11 26/03/2019 0 / LC 13 26/03/2019 37 13/04/2018

Ardeidae Nycticorax nycticorax Ardeola ralloides Bubulcus ibis Ardea cinerea Ardea alba Egretta garzetta

C W, T ETH T IA W, T P W C W, T OW W

0

/

16

23/03/2019

0 / 0 / 1 12/11/2018 0 / 5 18/12/2017 6 05/01/2018 8 17/01/2019 1 17/12/2017 10

12/03/2018

0 0

/ /

16

05/01/2018

9

17/01/2019

31

14/02/2018

8 24/03/2019 6 15/11/2018 4 21/04/2018 25 11/03/2018 8 21/03/2019 0 /

LC 0 / 12 16/03/2018 5 22/03/2019 3 24/04/2019 22 21/03/2019 34 21/04/2018 LC 0 / 4 13/04/2018 0 / 0 / 2 08/04/2018 0 / LC 43 26/03/2019 23 19/12/2017 0 / 41 11/03/2018 30 12/11/2018 0 / LC 25 15/01/2019 58 16/01/2019 18 06/01/2018 35 05/01/2018 20 17/01/2019 22 13/01/2019 LC 16 10/03/2018 46 23/03/2019 0 / 39 24/03/2019 4 15/11/2018 6 14/02/2018 LC 54 12/02/2018 28 25/03/2019 22 18/02/2018 58 02/01/2018 37 17/01/2019 17 17/12/2017

Accipitridae Circus aeruginosus P W, T LC 17 12/02/2018 6 14/01/2019

12 06/01/2018 3 05/01/2018 5 21/03/2019 2 14/02/2018

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F1 and F2 axes (92.21 %)

1.5

1

F2 (11.80 %)

Aythya nyroca

0.5

0

Aythya fuligula Anas crecca

Oligohaline

Fulica atra Spatula clypeata Tachybaptus ruficollis Anas platyrhynchos

Mesohaline

Chroicocephalus ridibundus Marmaronetta angustirostris Ardea alba

Polyhaline

Ardea cinerea

Charadrius alexandrinus Tadorna tadorna Gallinago gallinago Egretta garzetta Platalea leucorodia Tringa stagnatilisRecurvirostra avosetta Phalacrocorax carbo Tringa erythropus

–0.5

Himantopus himantopus Charadrius dubius

1 –2

Phoenicopterus roseus Chroicocephalus genei

Hyperhaline

–1.5

–1

–0.5 0 F1 (80.41 %)

Tadorna ferruginea

Euhaline

0.5

1

1.5

2

Fig. 4. Factorial correspondence analysis representing the distribution of wintering waterbirds as a function of the degree of salinity in the wetlands of the Oued Righ Valley.

Fig. 4. Análisis de correspondencia factorial que representa la distribución de aves acuáticas hibernantes en función del grado de salinidad de los humedales del valle de Oued Righ.

Thus the Oligohaline and Mesohaline environments below 18 ‰ were distinguished by the strong presence of Anatidae, with the exception of tadornes, which were distinguished by their presence in more holomorphic areas of the complex. The Northern shoveler Spatula clypeata, the tufted duck Aythya fuligula, and the Eurasian coot Fulica atra appeared to be inferred from the Oligohaline zones. The marbled teal Marmonetta angustirostris and common teal Anas crecca seemed more tolerant at slightly higher salinities.

Most species of Ardeidae, such as Egretta garzetta, Ardea Alba and Ardea cinerea, were present between Mesohaline and Polyhaline environments, with salinities below 30 ‰.

A strong presence of waders, such as the black–winged stilt Himantopus himantopus, the pied avocet Recurvirostra avosetta, the kentish plover Charadrius alexandrinus, the little ringed plover Charadrius dubius, the spotted redshank Tringa erythropus, and the common snipe Gallinago gallinago were observed in Polyhaline (18–30 ‰) and Euhaline environments (between 30 ‰ and 40 ‰).

The Hyperhaline environment represented in our case study by Chott Merouane was characterized by its original population, mainly flamingos Phoenicopterus roseus and slender–billed gulls Chroicocephalus genei (fig. 5).

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Fig. 5. Phoenicopterus roseus and Chroicocephalus genei at Chott Merouane, Photo

by F. Khirani–Betrouche, 15/01/2019.

Fig. 5. Phoenicopterus roseus y Chroicocephalus genei en Chott Merouane. Foto de F. Khirani–Betrouche, 15/01/2019.

Discussion Anatidae were the most widely represented family with 13 species. The sensitivity of these waterbirds to hydrological regimes and environmental factors explains their abundance in relatively stable and less holomorphic wetlands rich in vegetation, such as Sidi Khelil, Ayata and Oued Kherouf lakes. The overall richness of Anatidae and Rallidae species increases with the increasing diversity of vegetation (Cherkaouiet al., 2015). Brochet et al. (2009), Duncan et al. (1999) and Bethke and Nudds (1995) found that mallards and other ducks reacted negatively to decreases in water levels and increased salinity.

Oligohaline and Mesohaline environments, such as Ayata Lake, Sidi Khelil Lake and Oued Kherouf, seem more favourable to aquatic birds. Most of the wintering Anatidae of this depression, such as Spatula clypeata, Anas crecca, Anas plathyrynchos, Aythya nyroca, Aythya fuligula, can be found in such areas. According to Ysebaer et al. (2000) the waterbird community in the Oligohaline and freshwater tidal areas was dominated by duck species.

This can be explained by a greater diversity of plant cover than that in Euhaline and Hyperhaline environments. Low salinity environments have higher plant productivity and diversity than environments with higher salinity (Broche et al., 2009; Veraart et al., 2004). This would also make them more interesting from a food perspective in terms of waterfowl (Brochet et al., 2009). Low salinity sites with a high floristic richness can be qualified as hypertrophic wetlands. In addition to serving as a direct food source for herbivorous birds and an indirect food source for invertebrate–feeding birds, vegetation cover plays a role in the protection of birds and the availability of nesting sites (Hargeby et al., 1994). On the other hand, in Euhaline and Hyperhaline environments, the disappearance of submerged macrophytes can lead to a significant decline in invertebrate biomass and could considerably limit the availability of food resources for waterfowl (Idestam–Almquist, 1998).

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Wintering waders in our study were represented by 10 species. These birds frequented most mudflats in the wetlands studied, being most abundant in Chott Tendla, Chott Merouane and Ayata Lake. The strong presence of waders in Polyhaline and Euhaline environments such as Charadridae and Scolopacidae can be explained on one hand by the relative tolerance of these birds to high salinity levels and on the other hand by the fact that these environments have water levels between five and 20 cm deep, which represents a favourable habitat for these small waders.

Ardeidea such as Ardea cinerea and Egretta garzetta, whose diet is based on tilapia Oreochromis niloticus (Pisces), are very abundant in these wetlands where the maximum salinity tolerance does not exceed 28 ‰ (Polyhaline and Mesohaline areas) according to Azaza and Kraiem (2007).

The remarkable presence of greater flamingo at Chott Merouane (where some stations have salinity levels above 60 ‰) is explained by the fact that its basic food, namely the crustacean Artemia salina, finds the ideal biotope for its development (Van Stappen, 2002).

The greater flamingo has become emblematic of Saharan Chott because it is observed throughout the entire year and nests there regularly (Saheb et al., 2006; Boulekhssaim et al., 2006, 2009; Samraoui et al., 2006, 2008; Bensaci et al., 2010).

Conclusion The results obtained have allowed us to confirm the hypothesis that the nature of the water exerts a certain influence on the distribution of wintering waterbirds in wetlands of hyper–arid regions such as the Sahara. The salinity reaches very high thresholds at sites such as Chott and Sebkhas, thus directly influencing the trophic resources available to aquatic avifauna.

In spite of their originality and importance, the Saharan wetlands of the Oued Righ Valley are subject to various threats. These especially include those of anthropic origin, such as the fragmentation of Chott Merouane due to road improvements, the pumping of water for domestic and agricultural purposes at Merdjadja Lake, effluent discharges of the sewage treatment system and chemical release of waste matter into Chott Sidi Slimane, and poaching at the majority of sites. Greater attention and protection is needed for these wetlands, particularly in the Ramsar sites such as Chott Merouane and Oued Kherouf where management and conservation plans should be developed and implemented.

Acknowledgements The authors would like to thank all those who contributed to this work, Messrs Boulazazen Abdelmoumen, Saber Benkeddour, and Zeghdi Ali. Our gratitude goes to the Directorate General of Scientific Research and Technological Development (D.G.R.S.D.T.) and the Algerian Ministry of Scientific Research for their support.

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