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Distribution and Numbers of Three Globally Threatened Waterbird Species Wintering in Morocco: The Common Pochard, Marbled Teal, and White-Headed Duck

Distribution and Numbers of Three Globally Threatened Waterbird Species Wintering in Morocco: The... Hindawi International Journal of Zoology Volume 2021, Article ID 8846203, 17 pages https://doi.org/10.1155/2021/8846203 Research Article Distribution and Numbers of Three Globally Threatened Waterbird Species Wintering in Morocco: The Common Pochard, Marbled Teal, and White-Headed Duck 1 1 1 Asmaaˆ Ouassou , Mohamed Dakki , Mohammed-Aziz El Agbani, 1 2,3 Abdeljebbar Qninba , and R’himou El Hamoumi Study Centre of Bird Migration, Geo-Biodiversity and Natural Patrimony Laboratory, Department of Zoology and Animal Ecology, Scientific Institute, Mohammed V University in Rabat, Rabat 10106, Morocco Laboratory of Ecology and Environment, Ben M’sik Faculty of Sciences, Hassan II University, Casablanca, Morocco GREPOM/BirdLife Morocco, Sale´, Morocco Correspondence should be addressed to Asmaaˆ Ouassou; asmaa.ouassou@gmail.com Received 3 August 2020; Revised 25 December 2020; Accepted 31 December 2020; Published 21 January 2021 Academic Editor: Marco Cucco Copyright © 2021 Asmaaˆ Ouassou et al. &is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Morocco plays a key role in the life of many migratory birds and their survival, thanks to the diversity and richness of its ecosystems. &e International Waterbird Census (IWC) has been regularly implemented in Morocco since 1983. &anks to this program, a large database on wintering waterbirds’ populations has been collected. In this article, we summarize the wintering data of three globally threatened waterbirds: Aythya ferina, Marmaronetta angustirostris, and Oxyura leucocephala. &e pop- ulation of Aythya ferina, which is declining, is largely distributed in the country, in over a hundred wetlands, 26 of which verify the national importance criteria. Marmaronetta angustirostris has a stable trend over the years even though its population can know high annual fluctuations; it winters in more or less 50 wetlands, among which 18 host more than 1% of its regional population and 16 verify the criteria for national importance. On the contrary, Oxyura leucocephala, a globally endangered bird only encountered in a dozen wetlands, shows a moderate increase in its numbers; only two wetlands verify the Ramsar criterion 6, while a total of six can be considered of national importance. Furthermore, given the conservation statuses of these waterbirds and according to the Ramsar criterion 2, all their hosting sites are of international importance. &e results presented in this paper are a crucial step for the adoption and implementation of adequate conservation measures for the species and their key sites. Nevertheless, com- prehensive research and coordinated efforts on the factors (ecological and anthropogenic) influencing the species, at the national and international levels, are required for a better understanding of their populations’ dynamics. Waterbird Agreement, the country undertakes regular water- 1. Introduction bird censuses that provide an appropriate basis for effective Morocco is a North African country, with highly diversified decision-making in their conservation. In fact, Morocco has ecosystems and coastlines along both Atlantic Ocean and been regularly participating, since 1983, in the International Mediterranean Sea [1, 2]. It is located at the crossroads of many Waterbird Census (IWC), one of the largest biodiversity bird migration routes between Europe and Tropical Africa, and monitoring programs in the world, thanks to the coordination its wetlands play a crucial role for thousands of birds as of the Study Centre of Bird Migration (in the Scientific Institute) stopover, wintering, and breeding areas [3, 4]. &e country has and the collaboration of GREPOM/BirdLife Morocco, which ratified almost all international and regional agreements for the provides the majority of field volunteers. conservation of these birds and their habitats. In the context of &is article provides new syntheses on three globally the Ramsar Convention and the African-Eurasian Migratory threatened species of Anseriformes [5]: the White-headed 2 International Journal of Zoology Duck Oxyura leucocephala (Scopoli, 1769), an endangered Nevertheless, given the large number of wetlands to be bird [6], and two vulnerable species the Marbled Teal censused, some missions can start in late December (es- ´ ´ ´ Marmaronetta angustirostris (Menetries, 1832) [7] and the pecially in the Saharan region). Moreover, in some rare st Common Pochard Aythya ferina (Linnaeus, 1758) [8]. cases, data from censuses during the 1 week of February &e Common Pochard is a Eurasian duck found in a were accepted; they were conducted in some sites (Atlas wide variety of wetlands (marshes, lagoons, lakes, artificial lakes) that were not accessible, during January, because of reservoirs, and rivers), with eutrophic to pH neutral waters, heavy snow. &e number of wetlands censused, at least once, but it mostly prefers large open bodies of water with in the context of this program is 272 (IWC wetlands net- abundant emergent vegetation [8–10]. In Morocco, it is a work). However, not all of them are visited every year, winter visitor, passage migrant, and occasional to regular depending on the availability of human, financial, and lo- breeder [4, 11, 12]. Evident nesting cases have been observed gistical resources. &e priority is always given to the wet- in five Northern marshlands: “Plan d’eau de Dwiyate” lands with the highest waterbirds’ numbers and specific [4, 13], “Merja Bargha” [4, 14], “Marais de Smir” [15], “Merja richness. de Sidi Bou Ghaba” (with the highest number of breeding During each visit, the observers (Table S4) counted all pairs, nationally: 25 in 2011) [16], “Merja de Fouwarate” waterbirds on the grounds, in the water, and even those [17], and in two Atlas lakes (“Aguelmam Afennourir” and flying inside the site, using binoculars and telescopes. “Dayet ‘Awa’” [4]). &e threats faced by the species and its Counting points and transects are determined for each limited breeding population have rendered it vulnerable in wetland, depending on its configuration and accessibility. Morocco [16]. When some wetlands are close to one another, in a way that &e Marbled Teal is commonly found in shallow allows frequent bird exchange between them, they are brackish wetlands [18], with rich emergent and submerging considered as complex sites and are covered during the same vegetation [9, 19, 20], avoiding open-water areas [20–22]. visit. Over the years (especially since the 1990s), most However, its distribution largely varies with seasons, espe- wetlands have been censused by the same group of ob- cially depending on its dietary needs [18]. In Morocco, it is a servers, using the same protocol; this makes the obtained resident breeder, winter visitor, and passage migrant [4, 11]. data more homogenous, comparable, and reliable. &e Its breeding population was estimated to 50–250 pairs [23], observers participating in the IWC program are ornithol- distributed in a dozen wetlands situated in the north and ogists, qualified and trained for bird identification. New south of the country [4, 16, 17, 23–25]. Nevertheless, it is the observers can join the program after going through training most regularly breeds in four wetlands [16, 17, 24]: “Merja de sessions on bird identification and counting methods, both Sidi Bou Ghaba,” “Merja de Fouwarate,” “Plan d’eau de theoretical and practical. During their learning phase, they Dwiyate,” and “Embouchure de Wad Massa.” &e species is can join the established observers’ teams during their census considered endangered in Morocco [16] mainly because of campaigns to strengthen their training. its habitat degradation and modification [16]. &e White-headed Duck is the only Palearctic species of the Oxyurini tribe [26]. Breeding birds are usually found in 2.2. Data Analysis. &e wintering waterbirds’ numbers are freshwater and brackish or eutrophic lakes with dense entered in an information system, which generates auto- matically tables per species and sites. emergent vegetation [22, 27], shallow and permanent or semipermanent [9], while wintering birds can be found in To calculate populations’ trends, we used the TRIM (TRends and Indices for Monitoring Data) freeware [36] deeper and larger wetlands, alkaline or saline, and with less vegetation [28]. In Morocco, it is a winter visitor, resident (version 3.54). TRIM generates estimations for missing counts and can analyze data for 4000 sites, over 100 years; breeder, and suspected passage migrant [11]. It is used to th breed in Morocco until the 20 century, before becoming this makes it very suitable for our large dataset, especially since not all sites are visited every year (Table 1). &e missing scarce and disappearing, due its habitats’ loss by agricultural development and droughts [25]. Since the 1990s, the species data imputations take into account a site effect and a time effect, assuming the counts in a year depend on those of the reappeared in “Plan d’eau de Dwiyate” [4, 29] and then expanded progressively to several other breeding sites year before (serial correlation). &e counts are assumed to be Poisson distributed and are converted into annual indices to [30, 31]: “Merja de Sidi Bou Ghaba,” “Merja de Fouwarate,” simulate the missing data and calculate trends, based on the “Barrage ‘Arabat’,” “Barrage El Mehraz,” “Merja Bargha,” completed dataset (with the first year as base year, to which cumulating about 60 couples. It is still vulnerable in Mo- the index 1 or 0 is attributed). &e overdispersion (when the rocco [12]. variance is larger than expected for a Poisson distribution) and the serial correlation can be estimated by TRIM, 2. Methodology through a generalized estimating equation (GEE) approach. &e recommended overall slope by TRIM is based on the 2.1. Counting Procedure. Our study is based on the dataset of the waterbirds’ winter census, between 1983 and 2019. &e imputed data and given with the results of the additive slope and the multiplicative slope, which reflects the magnitude of counting procedure was adopted according to standard bird monitoring techniques [32], and the protocol was refined annual change, as well as their standard errors. It is con- verted into one of six trend categories: (i) strong increase: an over the years [14, 33–35]. &e censuses are conducted increase significantly greater than 5% per year; (ii) moderate annually, usually during January, to avoid recounts. International Journal of Zoology 3 Table 1: Number and percentage of wetlands visited per year. Year Number of surveyed wetlands % of the IWC wetlands network (272) Average 73 27 1983 47 17 1984 82 30 1985 49 18 1986 35 13 1987 69 25 1988 69 25 1989 56 21 1990 71 26 1991 94 35 1992 86 32 1993 94 35 1994 77 28 1995 89 33 1996 46 17 1997 70 26 1998 65 24 1999 65 24 2000 62 23 2001 65 24 2002 56 21 2003 62 23 2004 65 24 2005 59 22 2006 66 24 2007 77 28 2008 85 31 2009 79 29 2010 62 23 2011 100 37 2012 43 16 2013 78 29 2014 115 42 2015 70 26 2016 88 32 2017 76 28 2018 99 36 2019 131 48 increase: a significant increase, but not significantly more To better understand the species evolution, we used than 5% per year; (iii) stable: no significant increase or different parameters, mainly as follows: decline, and it is certain that trends are less than 5% per year; (i) &e average number of a species in each site is (iv) uncertain: no significant increase or decline, but not calculated for the long term and short term and certain if trends are less than 5% per year; (v) moderate corresponds to the arithmetic mean. decline: significant decline, but not significantly more than (ii) &e national average corresponds to the sum of the 5% year; (vi) steep decline: decline significantly greater than average numbers in each site. 5% year. A significance threshold is also provided for the increasing and declining trends: (i) highly significant: (iii) &e total annual numbers correspond to the sum of p< 0.01 (i.e., confidence level of 99%); (ii) significant: the species numbers in each site for every year. p< 0.05 (i.e., confidence level of 95%). (iv) &e total number per site is the sum of all the For the Common Pochard and the Marbled Teal TRIM species numbers observed per year in said site. analyses, three periods were considered: long term (v) &e occurrence of a species in a site corresponds to (1983–2019), medium term (2000–2019), and short term the number of winters it has been observed in this (2010–2019). For the White-headed Duck, which has been site. regularly observed in Morocco only starting 2005, the trend (vi) &e census number of a site corresponds to the was calculated for the periods of 2005–2019 (long term) and number of years during which it has been visited. 2010–2019 (short term). 4 International Journal of Zoology (vii) &e occurrence percentage of a species in a site However, this number hides very high interannual fluc- corresponds to the ratio of its occurrence to the tuations (Figure 2), knowing that the total annual num- bers vary between 27 (in 1996) and 3.755 ducks (in 2013). site’s census number. Morocco hosts 47% of the regional population “West (viii) &e 1st census of a site corresponds to the first year Mediterranean/West Mediterranean and West Africa” during which it has been visited. [37]. &e species was present in 295 counts and absent in (ix) &e standard deviation was calculated for each site, 651 counts (no observed birds during visits), while 904 to determine the deviation of the numbers ob- data are missing (Table S2). Its population trend (Figure 2) served annually from the average. is stable in the long term (additive slope � −0.0050 ± 0.0092; multiplicative slope � 0.9950± 0.0092), whilst it 􏽳��������� is uncertain in the medium term (additive slope � - 􏽐 x − x􏼁 0.0208± 0.00169; multiplicative slope � 0.9794± 0.0166) (1) σ � , and short term (additive slope � 0.0097± 0.0447; multi- plicative slope � 1.0097± 0.0452). where x is the observed number in site i, x is the arithmetic i &e White-headed Duck’s national average is 445 between mean, and N is the number of observations. 2005 and 2019 and 542 individuals during the last decade To prioritize future conservation measures, we have (2010–2019). Morocco hosts 22% of the regional population identified for each species, categories of key sites, based on “Spain and Morocco” [37]. &e observed total annual numbers recent data (2010–2019): varied between 1 and 1.730 (Figure 3). &e species was ob- served, in the context of IWC, during the period 2005–2019 (i) Sites of international importance, priority 1 (SII1): and was present in 29 counts and absent in 58 counts (no wetlands verifying the 6th Ramsar criterion (the observed birds during visits), while 45 records are missing species’ numbers reach or exceed regularly (5 (Table S3). &e population’s trend (Figure 3), for the 2005–2019 winters or more) 1% of its regional population. period, is a moderate increase (additive slope � 0.2749± 0.1181; (ii) Sites of international importance, priority 2 (SII2), multiplicative slope � 1.3164± 0.1554; p< 0, 05). In the short verifying the 2nd Ramsar criterion (sites supporting term, it is uncertain (additive slope � 0.3899± 0.4609; multi- vulnerable, endangered, or critically endangered plicative slope � 1.4768± 0.6807), but with an increasing species). tendency. (iii) Sites of national importance (SNI): the species’ average number, in those sites, equals or exceeds the 1% of the national average. 3.2. Spatial Distribution. &e Common Pochard was ob- served in a total of 118 wetlands (43% of the surveyed (iv) Sites of potential national importance (SPNI): they wetlands) (Table S1), mostly in the Northern half of the hosted, during at least winter, more than 1% of the country, along the Atlantic coast and Atlas region (Figure 4). national average. However, from year to year, the species was reported in 9 to 39 sites (Figure 1). Between 2010 and 2019, the northwest (31 3. Results sites) and northeast (16 sites) regions hosted the highest concentrations (37% and 33%, respectively). Amongst the 3.1. Populations’ Size and Trend. &e national average of the sites visited at least 19 winters over the 37 years study period, Common Pochard’s wintering population is 11.158 in the long the species occurrence percentage was the highest in five of term, the total annual numbers varying between 1.710 (in 2012) them (>85%): “Aguelmam Abekhane,” “Aguelmam Afen- and 20.458 ducks (in 2002) (Figure 1). During the last decade (2010–2019), the national average is lower (7.496 individuals), nourir,” “Merja de Sidi Bou Ghaba,” “Dayet Ifrah” and “Barrage de Smir.” &e highest total numbers (between 1983 but it represents 1.25% of the regional population “Central and NE Europe/Black Sea and Mediterranean” [37]. &e Common and 2019) were cumulated as follows: “Barrage Mohammed V,” “Barrage Al Massira,” and “Embouchure de Wad Pochard was present in 809 counts and absent in 991 counts Massa.” In the short term (amongst the sites visited at least 5 (no observed birds during visits), while 2.640 data are missing years out of 10), the highest average numbers were recorded (the unavailable records relative to the species’ known win- in “Barrage Mohammed V” and “Merja de Sidi Bou Ghaba” tering sites, which have not been visited during certain years) (Table 2). Some wetlands have known a decline in the (Table S1). Its population trend (Figure 1) is stable in the long species’ wintering numbers, such as “Embouchure de Wad term (additive slope � −0.0101± 0.0057; multiplicative slope � 0.9900± 0.0057), a significant moderate decline in the Massa;” others such as “Merja de Fouwarate” have hosted increasing numbers in recent years. &e highest concen- medium term (additive slope � −0.0727± 0.0117; multiplicative slope � 0.9299± 0.0109; p< 0, 01), and uncertain in the short tration ever recorded in Morocco (15.600 birds) was ob- served in the reservoir of “Barrage Mohammed V” in 2002. term (additive slope � −0.0226± 0.0279; multiplicative slope � 0.9776± 0.0273), but with a declining tendency. &is &is site has known high fluctuations of the Common Pochard’s numbers (zero to thousands), which is clearly decline is more evident during the last decade (2010–2019) reflected by its high standard deviation (Table 2). even though the census effort has significantly increased. &e Marbled Teal was observed in a total of 50 wetlands &e Marbled Teal’s national average is almost the (18% of the surveyed wetlands) (Table S2), mainly same, in the long term (3.071) and short term (3.070). International Journal of Zoology 5 25000 45 0 0 Years Total annual numbers Number of sites (a) 2.5 1.5 0.5 Years Model indices Imputed data (b) Figure 1: (a) Total annual numbers of the Common Pochard and number of wetlands where it has been observed in Morocco between 1983 and 2019. (b) Linear trend of the wintering population (TRIM analysis). distributed north and west to the Atlas Mountains and in the (i) “STEU Guelmim”: a wastewater treatment plant, northern part of the Sahara (Figure 5). Annual distribution only visited in 2016 (89 ducks) and in 2018 during varied between 2 and 19 sites (Figure 2). In the short term, which a high concentration of 1.748 was recorded. 67% of the national average was observed in the southern (ii) “Was As-Saqia Al Hamra a` La’youn”: observations region (in 15 wetlands), with particularly high concentra- varied between 0 individuals and the highest con- tions in 2013 (95%) and 2018 (62%). &e other regions centration ever recorded in Moroccan sites (3.557, hosted 8% to 15% of this number. &e highest occurrence of almost half of the national population in 2013). the species was recorded in “Merja de Sidi Bou Ghaba” (97% of the visits), “Lagunes de Sidi Moussa-Walidia” (83%), and Since its reappearance in Morocco in the early 2000s, the White-headed Duck was observed in 12 wetlands (17% of the “Embouchure de Wad Massa” (81%). &ree sites hosted each, more than 10% of the total numbers recorded between surveyed wetlands), mainly in the north of the country (Table S3; Figures 3 and 6). Its annual distribution did not 1983 and 2019: “Lagunes de Sidi Moussa-Walidia,” “Wad exceed six sites, and it was not observed in any wetland As-Saqia Al Hamra a` La’youn,” and “Merja de Sidi Bou visited in 2006, 2007, 2010, and 2012 (Figure 3). Most of its Ghaba.” &e highest standard deviations were recorded in population is located in the northwest region (73%). &e two sites (Table 3): Total annual numbers Indices values Number of sites 6 International Journal of Zoology 5000 20 4500 18 4000 16 3500 14 3000 12 2500 10 2000 8 1500 6 1000 4 500 2 0 0 Years Total annual numbers Number of sites (a) 2.5 1.5 0.5 Years Model indices Imputed data (b) Figure 2: (a) Total annual numbers of the Marbled Teal and the number of wetlands where it has been observed in Morocco between 1983 and 2019. (b) Linear trend of the wintering population (TRIM analysis). species was most regular in “Merja de Sidi Bou Ghaba” (75% the highest concentrations nationally were recorded (1.430 of the visits) and “Merja de Fouwarate” (45%). &ree wet- in 2018 and 500 in 2019). lands (“Merja de Fouwarate,” “Merja de Sidi Bou Ghaba,” and “Barrage Mohammed V”) hosted more than 10% of the 3.3. Sites of International and National Importance. &e wintering individuals. It is worth mentioning that the Common Pochard is a globally vulnerable species, which wetland “Plan d’eau de Dwiyate” is hard to access, since it is part of a royal domain. Except for a temporary lake on the makes all the sites hosting it of international importance (SII2 as we have defined in Methodology). None of the east (suffering from some disturbance, overgrazing, and recurrent droughts [29]), it is fenced and well-guarded and Moroccan wetlands verify the Ramsar criterion 6 for the species. Nevertheless, it is worth mentioning that “Barrage hence with no disturbance, which makes it a site of great importance for the species. &e highest standard deviation Mohammed V” could be of potential international impor- tance. In fact, in 2002, this site hosted a high concentration was recorded in “Merja de Fouwarate” (Table 4), where the species was not observed before 2014 (Table S3) and where of 15.600 ducks, which exceeded the estimated 1% of the Total annual numbers Indices values Number of sites International Journal of Zoology 7 2500 7 0 0 Years Total annual numbers Number of sites (a) Years Model indices Imputed data (b) Figure 3: (a) Total annual numbers of the White-headed Duck and the number of wetlands where it has been observed in Morocco between 2005 and 2019. (b) Linear trend of the wintering population (TRIM analysis). regional population at the time (10.000) [37]. &e reported (7.496) (Table 2), which makes them of national importance. species’ numbers in this wetland can be highly under- On the contrary, 15 others hosted wintering numbers ex- estimated due to a difficult access to many parts of the ceeding that threshold, during at least one winter (Table 2), reservoir, depending on the conditions. &erefore, it can, which makes them of potential national importance. more than likely, host regularly at least 1% of the Common &e Marbled Teal is a globally vulnerable species, which Pochard’s regional population. &is could also be the case for makes all the sites hosting it of international importance as well “Barrage Al Massira,” a reservoir often partially censused (SII2). Moreover, 18 wetlands hosted, at least once, more than and which hosted, in 2008, 5.500 ducks. Among the 118 1% of the regional population [5], three of them regularly: wetlands where the species was observed, 26 have average “Lagunes de Sidi Moussa-Walidia,” “Merja Zerga,” and “Wad numbers equal or superior to 1% the national average As-Saqia Al Hamra a` La’youn;” they are thus of international Total annual numbers Indices values Number of sites 8 International Journal of Zoology 0 25 50 100 150 200 Kilometers Average numbers 1983-2019 ≤28 Wetlands surveyed (with 29 – 103 no Common Pochard) 104 – 235 Hydrographic network 236 – 646 Regional boundaries 647 – 2331 Figure 4: Distribution map of the Common Pochard’s wintering population in Morocco (1983–2019). importance for the species (SII1) (Table 3). On the contrary, 26 main lists exist in the Moroccan legislation: a list of species for wetlands have average numbers equal or superior to 1% of the which hunting is banned (published through the “Annual Hunting Order”) and a list of species in which trade and national average (Table 3), which makes them of national importance. Among them, 11 hosted wintering numbers ex- transport is conditioned by a special governmental authori- zation (through the CITES Law “N ceeding that threshold during at least one winter (Table 3), 29–5”). &e hunting of the which makes them of potential national importance. White-headed Duck and Marbled Teal is prohibited in Mo- Because it is endangered, the White-headed Duck at- rocco, whilst the Common Pochard can still be hunted [38]. tributes an international importance to all the 12 sites National action plans for species can also be efficient tools hosting it (SII2). &e 1% of the regional population [37] was for the conservation of birds and their habitats. In Morocco, exceeded, at least one winter, in five wetlands, but regularly only the White-headed Duck has a national action plan [18]. in “Merja de Sidi Bou Ghaba” and “Merja de Fouwarate.” On In situ conservation mechanisms represent another the contrary, seven wetlands hosted, at least once, more than important measure for the conservation of the three species. 1% of the national average, cumulating 99.8% of this In addition to two international statuses for the conservation number. Among them, 6 are of national importance and one of wetlands: (i) Ramsar Sites and Important Bird and is of the potential national importance (Table 4). Biodiversity Areas (IBA), these mechanisms also consist, in For the three species, some sites need to be monitored Morocco, in the creation of three national statuses for which more regularly to verify and/or confirm their national/in- a high number of wetlands have been designated for. Several ternational importance since they have been visited less than bird species, including the three ducks subject of this article, 5 winters (Tables S1–S3). have been targeted by these statuses: (i) national parks (NPs); (ii) Sites of Biological and Ecological Interest (SBEI), defined in 1996 [39], with at least 84 wetlands, partly assessed using 3.4. Current Conservation Measures in Morocco towards the waterbirds; and (iii) permanent hunting reserves (PHRs). ;ree Species. An efficient legal conservation way consists in &e Common Pochard is found in 44 wetlands, with at least classifying a bird in an official list of protected species. Two one conservation status (Table 5); 22 of them are Ramsar sites, International Journal of Zoology 9 Table 2: Most important wintering sites of the Common Pochard (2010–2019). 1% 1 2 Site name Average number Max. Importance Standard deviation NA Barrage Hassan Ad-Dakhil 850 1700 1 SNI/SII2 530 Barrage Mohammed V 626 15600 2 SNI/SII2 3816 Merja de Sidi Bou Ghaba 514 1200 8 SNI/SII2 258 Aguelmam Afennourir 468 2600 4 SNI/SII2 624 Merja de Wad Fouwarate 413 1000 8 SNI/SII2 308 Barrage Wad Al Makhazine 317 1101 3 SNI/SII2 345 Barrage de Smir 312 1689 4 SNI/SII2 462 Sadd Al Ajras 305 305 1 SNI/SII2 98 Barrage Asfalou 300 300 1 SNI/SII2 0 Aguelmam Abekhane 296 855 2 SNI/SII2 200 Barrage Al Massira 256 7038 3 SNI/SII2 1853 Aguelmam N’Tifounassine 227 652 1 SNI/SII2 145 Merja Zerga 210 1800 2 SNI/SII2 324 Barrage Hassan II 186 1100 2 SNI/SII2 327 Dayet Ifrah 180 860 3 SNI/SII2 218 Aguelmams Sidi Ali-Ta’nzoult 172 1700 4 SNI/SII2 360 Barrage Mechra’ Hommadi 126 290 2 SNI/SII2 82 Barrage Enjil 124 690 3 SNI/SII2 179 Barrage Oued Rmel 124 160 2 SNI/SII2 37 Dayet ‘Awa 122 1030 3 SNI/SII2 192 Embouchure de Wad Malwiya 104 224 5 SNI/SII2 67 Barrage Moulay Youssef 94 114 1 SNI/SII2 43 Merja Bargha 89 1590 4 SNI/SII2 323 Marais de Wad Smir 87 391 3 SNI/SII2 83 Barrage Sahla 85 164 1 SNI/SII2 80 Barrage Al Wahda 84 283 1 SNI/SII2 117 Barrage Hassar 74 148 3 SPNI/SII2 60 Mlalah du Bas Tahaddart 69 480 1 SPNI/SII2 96 Barrage Kheng El Hda 67 200 4 SPNI/SII2 61 Barrage Petit Tizil 52 250 2 SPNI/SII2 79 Dayet Hachlaf 45 163 1 SPNI/SII2 56 Barrage Zelmou 38 159 1 SPNI/SII2 44 Barrage’Arabat 38 94 1 SPNI/SII2 40 Barrage Idriss Premier 34 570 1 SPNI/SII2 156 Marais du bas Loukkos 34 410 1 SPNI/SII2 83 Merja des Wlad Khallouf 30 240 1 SPNI/SII2 53 Merja Al Halloufa 25 680 2 SPNI/SII2 220 Embouchure de Wad Massa 23 3330 1 SPNI/SII2 832 Merja des Wlad Skher 23 650 2 SPNI/SII2 143 Lagunes de Sidi Moussa-Walidia 16 2500 1 SPNI/SII2 431 Sebkha Bou Areg 12 406 1 SPNI/SII2 109 1 2 &e average (mean) of the species’ annual numbers counted in a site (their sum is divided by the number of years the site was censused). Maximum wintering number observed in a site since its first year of census. Number of winters during which 1% of the national average (7.496) exceeded. 34 are SBEI, 21 are IBA, 9 are part of national parks, and 18 are though regional populations’ trends differ from stable to part of permanent hunting reserves. &e Marbled Teal occupies unknown [8], the European population, which represents 25 wetlands having national and/or international conservation 35% to 40% of the global population, has decreased by statuses: 15 Ramsar sites, 20 SBEI, 16 IBAs, 3 are part of national 30–49% over three generations [8, 40, 41]. parks, and 10 are part of permanent hunting reserves. Among &e Moroccan wintering numbers show a significant the 9 wintering wetlands of the White-headed Duck with decline, especially during the two recent decades, which conservation statuses, 6 are Ramsar sites, 7 SBEI, 5 IBA, 3 are could be directly linked to the declining trend of the regional part of national parks, and 5 are part of permanent hunting population “Central and NE Europe/Black Sea and Medi- reserves. terranean” [37, 42–44], from which the wintering individ- uals in Morocco originate. In fact, according to the IUCN [37], the species’ decrease is mainly due to the loss of its 4. Discussion breeding habitat in Eastern Europe. In Central Europe, it appears that the major factors responsible for its decline are 4.1. Population Size and Trend. &e global population of the nest predation [37, 45] by natural (Vulpes vulpes and Sus Common Pochard is considered to be decreasing [8]. Even 10 International Journal of Zoology 0 75 150 225 300 Kilometers Average numbers 1983-2019 ≤28 Wetlands surveyed (with no Marbled Teal) 29 – 96 97 – 246 Hydrographic network 247 – 499 Regional boundaries 500 – 919 Figure 5: Distribution map of the Marbled Teal’s wintering population in Morocco (1983–2019). scrofa) and alien mammal species (i.e., Neovison vison, regional population (West Mediterranean/West Mediter- Nyctereutes procyonoides, and Procyon lotor) and a decline of ranean and West Africa), which is stable [42], but with a Dreissena polymorpha, the zebra mussel which is the pre- possible declining tendency [37]. &e global population of the species has decreased rapidly overtime [7]; only the ferred food of this duck [46–48]. Furthermore, Fox et al. (2016) [41] have summarized multiple factors influencing southwest Asian population knows a possible increase [37], albeit it may be due to an improvement in census coverage the breeding population in the old continent; they are mostly related to loss or changes in habitats, food availability, instead of actual changes within the population [7]. predation, alien species, hunting [9, 49, 50], fishing, dis- In Morocco, the Marbled Teal’s population often showed a turbance, and lead poisoning [51]. On the contrary, Folliot lot of fluctuations from one year to another. In fact, the species et al. (2018) [52] suggest that decreasing wintering numbers can have extreme fluctuations in its population’s size in Western Europe can also be due to the decline of the depending on rainfall’s annual variation [18]. It can therefore breeding population in the southwest Asian flyway (espe- relocate to other areas that may be unmonitored and vice versa cially in Siberia). In fact, analyses of ringing recoveries data and hence giving the impression of an increase or decrease in showed that large wintering numbers in the northwest numbers. &is relocation could occur between wetlands of the same country as well as at a larger scale, between wintering European flyway originate from the southwest Asian flyway, which brings to evidence the interactions and exchange areas of different countries. Moroccan wintering individuals between the different regional populations beyond the de- can come from breeding sites in Europe (e.g., Spain) and North termined limits of the flyways. In addition to the afore- Africa [59] (especially Algeria, which hosts important numbers mentioned factors that are possibly contributing to the of the species [60–62]). Nevertheless, the high records observed decline of the Common Pochard in Morocco, climate change sometimes are not necessarily caused by an influx from Spain can also play a crucial role in the species’ populations but could be explained by the presence of unknown breeding changes [53–58] at a larger scale, as well as the direct threats sites of great importance in the country or in North Africa [59]. faced by the species in Moroccan wetlands. &e sometimes declining numbers of the species in Morocco and other regions can also be function of the habitats’ quality &e evolution of the Marbled Teal’s wintering pop- ulation in Morocco is consistent with the trend of the and availability. In fact, the global population’s decrease was a International Journal of Zoology 11 Table 3: Most important wintering sites of the Marbled Teal (2010–2019). 1% 1 2 Site name Average number Max. Importance Standard deviation NA Wad As-Saqia Al Hamra a` La’youn 448 3557 9 SII1/SNI 708 Lagunes de Sidi Moussa-Walidia 157 1800 6 SII1/SNI 471 Merja Zerga 83 200 9 SII1/SNI 49 STEU Guelmim 919 1748 2 SII2/SNI 830 Barrage Moulay Abdellah 499 997 1 SII2/SNI 499 Barrage Hassan Ad-Dakhil 188 339 2 SII2/SNI 106 Sebkha Zima 148 950 3 SII2/SNI 185 Merja de Fouwarate 119 400 7 SII2/SNI 107 Merja de Sidi Bou Ghaba 74 1400 3 SII2/SNI 302 Barrage Mohammed V 50 230 2 SII2/SNI 49 STEP Tarfaya 44 44 1 SII2/SNI 0 Dayet Al Fahs 44 636 2 SII2/SNI 125 Radier de l’Oued Assaka 43 75 2 SII2/SNI 32 Barrage Al Massira 36 1973 3 SII2/SNI 355 Barrage Hassar 36 128 2 SII2/SNI 48 Plage Ras Takoumba-Bou Issafine 31 550 1 SII2/SPNI 161 Marais de Wad Al Maleh 22 248 1 SII2/SPNI 86 Embouchure de Wad Massa 20 397 3 SII2/SPNI 101 Plage Blanche 17 136 1 SII2/SPNI 32 Embouchure de Wad Malwiya 15 142 1 SII2/SPNI 27 Embouchure de Wad Bou Issafine 13 60 1 SII2/SPNI 16 Embouchure de Wad Assaka 13 52 1 SII2/SPNI 15 Marais du bas Loukkos 11 82 2 SII2/SPNI 18 Dayet Taras El Ghoul 8 350 1 SII2/SPNI 76 Daya Al Beyda 6 37 1 SII2/SPNI 9 Barrage Zelmou 5 37 1 SII2/SPNI 11 1 2 &e average (mean) of the species’ annual numbers counted in a site (their sum is divided by the number of years the site was censused). Maximum wintering number observed in a site since its first year of census. Number of winters during which 1% of the national average (3.070) exceeded. direct consequence of habitats’ loss and degradation [7, 59, 63] have different potential explanations and combined due mainly to drainage of wetlands for agricultural purposes factors: and hydrological work [7]. In our country, for example, one of (i) A flow of migrants from Spain: the conservation and the most important breeding sites, the Iriki Lake (where the protection efforts undertaken by Spain, over more than Marbled Teal used to breed in high numbers (hundreds of 30 years [29], have had a strong positive effect on the couples in the 1960s)), has disappeared because of the con- White-headed Duck’s population in Spain and may struction of a dam (Barrage Al Mansour Ad-Dahbi) [24]. have contributed to its return to Morocco and its Although this vulnerable duck is legally protected in Morocco increasing numbers in the country [29]. [24], it still faces many threats affecting negatively its pop- (ii) A flow of individuals from the regional population of ulation. &ese threats are mainly related to human activities, “Algeria and Tunisia,” which hosts significant breeding disturbing, degrading, or destructing its habitats, and changes numbers of the White-headed Duck [66]. &ere are, in water levels (caused by low precipitations, drainage, and currently, insufficient data to decide if there is any hydraulic work). In fact, the species’ wetlands occupancy in our exchange between the West Mediterranean and North country, especially in the breeding season, is closely dependent African subpopulations [66] that could also contribute on habitat-related factors, such as the number and diversity of to the species increase in Morocco. Nevertheless, our emergent vegetation species [22, 64, 65], which are more country is at an advantageous position between the predominant in Ramsar sites close to the coastline [65]. increasing Spanish population and the Algerian one, Since its return in Morocco, the White-headed Duck’s which hosts high numbers of the species during the population has known a moderate increase. Notwith- breeding season and throughout the year [66–70], but standing, the global population of the species is thought to faces many threats in the country, especially illegal be decreasing [6]. &is decline is estimated to be 50–79% killing [71]. in three generations [6] even though many subpopula- tions are not thoroughly recorded, which may lead to an (iii) &e decline in the population of the ruddy duck and underestimation of the species counts [6, 66]. &e increase its hybrids due to campaigns for its eradication in in this endangered duck’s population in Morocco, espe- Spain, Europe [29, 72], and Morocco [73]. cially the high numbers recorded in “Merja of Fouwarate” (iv) &e presence of favorable breeding sites in Mo- during the 2018 winter (1.430 individuals) [30], could rocco, thanks to wetlands conservation efforts and 12 International Journal of Zoology 0 20 40 80 120 160 Kilometers Average numbers 1983–2019 ≤13 Wetlands surveyed (with no White-headed Duck) 14 – 40 Hydrographic network 41 – 113 Regional boundaries 114 – 184 Figure 6: Distribution map of the White-headed Duck’s wintering population in Morocco (2005–2019). Table 4: Most important wintering sites of the White-headed Duck (2010–2019). 1% 1 3 Site name Average number Max. Importance Standard deviation NA Merja de Sidi Bou Ghaba 170 8 351 SII1/SNI 120 Merja de Wad Fouwarate 225 5 1430 SII2/SNI 419 Barrage Mohammed V 106 3 426 SII2/SNI 145 Dayet Ifrah 15 2 59 SII2/SNI 19 Dayet Hachlaf 15 1 88 SII2/SNI 31 Barrage’Arabat 9 2 22 SII2/SNI 9 Barrage El Mehraz 2 1 6 SII2/SPNI 3 Dayet’Awa 1 0 3 SII2 1 1 2 &e average of the species’ annual numbers counted in a site (their sum is divided by the number of years during which the site was censused). Maximum wintering number observed in a site since its first year of census. Number of winters during which 1% of the national average (542) exceeded. suitable climate conditions that contribute to good many other threats; the most imminent one is the hybrid- water levels [74] and more developed vegetation ization with the ruddy duck. In fact, this introduced species cover. has been observed in Morocco on many occasions, and the last documented observation was in 2013, where 2 indi- In Morocco, many factors have contributed to the for- viduals were observed in Merja Al Halloufa [75]. Never- mer disappearance of this endangered duck and halted its theless, unpublished data (Hassani H. and Dakki M. in litt.) expansion. Overgrazing and repeated cutting of reed beds have reported the ruddy duck, during recent years in Barrage caused a regression of emergent vegetation in permanent Al Mehraz in 2014 and 2015, one of the sites where breeding wetlands [29], which is crucial for this duck’s breeding. White-headed Ducks have been observed [31]. &e second According to El Hamoumi et al. [31], the species still faces most imminent threat to the survival of the species in International Journal of Zoology 13 Table 5: Conservation statuses of the three species’ hosting wetlands. 1 2 3 4 5 6 7 Site name Types of habitat Region Ramsar IBA SBEI NP PHR Aytfer Marang Oxyleu Aguelmam Abekhane Inland lake Atlas — — X — — X — — Aguelmam Afennourir Inland lake Atlas X — X I X X X — Aguelmam Azegza Inland lake Atlas — — X — — X — — Aguelmam N’Tifounassine Inland lake Atlas X X X I X X — — Aguelmam Wiwane Inland lake Atlas — — X — — X — — Aguelmams Sidi Ali-Ta’nzoult Inland lake Atlas — X X — — X — — (a) 13 Baie d’Ad-Dakhla Bay South X X X D — X — — (b) Barrage Al Mansour Ad-Dahbi Artificial reservoir South — X X — — X X — Center (b) Barrage Al Massira Artificial reservoir X X X — X X X — Atlantic Center (b) Barrage de Wad Al Mellah Artificial reservoir — — X — — X — — Atlantic (b) 8 Barrage de Smir Artificial reservoir Northwest X — — — — X — — (b) Barrage Idriss Premier Artificial reservoir Northwest — X X — — X X — (b) Barrage Mohammed V Artificial reservoir Northeast X X X — X X X X Center (c) Cote ˆ et Archipel d’Essawira Coastal wetland X X X — — X X — Atlantic Dayet Ar-Roumi Inland lake Northwest — — X — — X — — 9 12 Dayet’Awa Inland lake Atlas X — X I X X X X 9 12 Dayet Hachlaf Inland lake Atlas X — — I X X — X 9 12 Dayet Ifrah Inland lake Atlas X — X I X X — X (d) Embouchure de Wad Al Wa’er River mouth South — — X — — X — — (d) Embouchure de Wad Assaka River mouth South — — X — X X X — (d) Embouchure de Wad Chbeyka River mouth South — X X — X X X — (d) Embouchure de Wad Dr’a River mouth South X — X — — — X — (d) Embouchure de Wad Malwiya River mouth Northeast X X X — — X X X (d) Embouchure de Wad Martil River mouth Northwest — X — — — X — — (d) 14 Embouchure de Wad Massa River mouth South X — — SM X X — — (e) 15 Lac de Tislite Inland lake Atlas X X HAO — X — — (e) 15 Lac d’Isly Inland lake Atlas X HAO — X — — Lagoon/ (f) 16 Lagune de Khnifiss South X X X K — — X — marshland Lagunes de Sidi Moussa- Lagoon/ Center X X X — X X — — (f) Walidia marshland Atlantic Center (g) Marais de Wad Al Maleh Marshland X — — — — X X — Atlantic (g) 8 Marais de Wad Smir Marshland Northwest X — — — — X X — (g) Marais du bas Loukkos Marshland Northwest X — — — — X X — Merja Al Halloufa Marshland Northwest X X X — — X — — Merja Bargha Marshland Northwest X X — — — X X X Merja Boukka Marshland Northwest — — X — X X — — Merja de Fouwarate Marshland Northwest X — X — — X X X Merja de Sidi Bou Ghaba Marshland Northwest X X X — X X X X Merja des Wlad Khallouf Marshland Northwest — — — — X X — — Merja des Wlad Skher Marshland Northwest X — X — — X X — Merja Zerga Marshland Northwest X X X — X X X — Mlalah du Bas Tahaddart Marshland Northwest X X X — X X — — (h) Plan d’eau de Dwiyate Inland lake Northwest — X X — — X X X (h) 11 Plan d’eau de Zerrouqa Inland lake Atlas X — X — — X — — Sebkha Bou Areg Lagoon Northeast — X X — X X X — Center Sebkha Zima Saline lake — X X — X X X — Atlantic Depression Center Sehb El Mejnoun — X X — — — X — wetland Atlantic Wad As-Saqia Al Hamra a` River South X X — — — X X — La’youn (a) (b) (c) (d) (e) (f) (g) (h) Baie � bay; Barrage � dam; Cote ˆ � coast; Archipel � archipelago; Embouchure � river mouth; Lac � lake; Lagune � lagoon; Marais � marsh; 1 2 3 4 Plan d’eau � waterbody. Important bird and biodiversity areas; Sites of Biological and Ecological Importance; national parks; permanent hunting reserves; 5 6 7 8 Common Pochard (Aythya ferina); Marbled Teal (Marmaronetta angustirostris); White-headed Duck (Oxyura leucocephala); Ramsar site: “Lagune et 9 10 11 12 barrage de Smir;” Ramsar site: “Lacs d’Imouzzer du Kandar;” Ramsar site: “Marais et Cote ˆ du Plateau de Rmel;” Ramsar site: “Oued Tizguite;” Ifrane 13 14 15 16 National Park; Dakhla National Park (project); Souss-Massa National Park; Haut Atlas Oriental National Park; Khnifiss National Park. 14 International Journal of Zoology Morocco is the excessive pumping [31], from artificial and conservation of this endangered waterbird and the resto- natural wetlands, as well as groundwater. &is leads to lower ration of a viable population on the long term. Similar water levels or even the drying-out of the wetlands, making it actions should be undertaken for the marble teal and the difficult for the species to thrive in such conditions. &e Common Pochard, as well as all globally threatened birds in other threats are mainly related to different disturbances that Morocco, targeting the specific threats for each species in can affect the species population directly (illegal or acci- each site. However, efforts must be deployed for a rigorous dental hunting and stray dogs that feed on ducklings or eggs) implementation of these conservation action plans and their or indirectly (recreational activities and inadequate man- evaluation on a regular basis. While the hunting of the agement policies). White-headed Duck and the Marbled Teal is prohibited, the Most of the key wintering wetlands of the three wa- Common Pochard can still be hunted. Given the current terfowls benefit from at least one conservation status. &e trend of this duck’s population, at the national and inter- attribution of these conservation statuses represents an national levels, more restrictions should be placed on its important step in their conservation. In fact, some of these hunting. sites also have management plans that allow enhanced land So far, we have discussed the populations’ changes and water management and the protection against an- inherent to factors at the national level. However, some of thropogenic threats. &is begs the following question: if the these changes can be related to factors at a larger scale and most important sites for the species benefit from conser- outside the national territory (e.g., threats and conser- vation statuses and measures, on what scale should we also vation measures in other countries). Furthermore, climate focus to improve the populations’ size? change and meteorological conditions can also have an impact on the national population. Kleijn et al. [76] have, for example, reported a positive correlation between 4.2. Conservation Stakes. For each of three species presented waterbirds’ population trends in Morocco and precipi- in this article, the population changes are often multifac- tations in the Sahel zone that may have a potential impact torial and can be in situ or ex situ. In fact, these ducks are on birds’ migratory strategies. &erefore, some pop- highly dependent on their habitats, especially during the ulations’ changes are probably more related to shifts in breeding season. As we have discussed above, any negative migratory routes and wintering areas than actual changes change, be it natural (e.g., drought and flood) or anthro- in birds’ numbers [76]. pogenic (e.g., drainage, vegetation cutting, and hydraulic More thorough research could lead to the exact reasons work) can potentially result in their decrease or redistri- behind the three studied ducks’ populations’ trends. Com- bution to other sites. &e designation of Ramsar and im- prehensive studies should be conducted to understand the portant bird and biodiversity sites is one of the important effects of ecological and anthropogenic factors on the distri- measures for the waterbirds and wetlands conservation and bution, abundance, and population dynamics of waterbirds’ among the good indicators of its success. In Morocco, 49 species [12], such as water quality, food availability, predation, wetlands are important bird biodiversity areas, 38 are weather, and conservation statuses. Furthermore, with the in- Ramsar sites, and at least 84 are Sites of Biological and creasing challenges that may hinder our monitoring programs Ecological Interest (SBEI), among which many are part of [77] and the effectiveness of conservation plans, we must de- national parks and/or permanent hunting reserves. While velop new effective methods for waterbirds’ census (wintering these statuses are important, if no ensuing effective man- and breeding populations) with more precision and coverage, agement plans are developed and implemented, their deg- coupled with other programs such as ringing-recovery/capture- radation, thus their biodiversity’s decline, is an inevitable recapture, continent/flyway, or region-wide series of aerial consequence, especially for those subject to many anthro- survey transects as has been suggested by Fox et al. (2019) [77]. pogenic pressures. &e Moroccan Department of Water and &is is crucial since the movements occurring within and be- Forestry has developed management plans for many wet- tween the regional populations of the species are still not well lands: some are finalized, and others are still in progress. &e understood. Large-scale information on birds’ populations’ implementation of these plans can face many challenges trends and habitats’ use is insufficient, which affects negatively inherent to the multiplicity of actors involved and the co- the conservation process [78]. Cooperative and coordinated operation of the local populations, whose livelihoods may efforts, such as the Mediterranean Waterbirds Network [79], are depend on the ecosystem services those wetlands provide. the key to improve data quality and quantity and to successful &e designation of SBEI in Morocco was a strategic measure and adequate conservation measures, for both waterbirds and and a starting point to prioritize the conservation of the wetlands. ecosystems with the highest biodiversity indices and hosting the most endangered, rare, or endemic species. But as we 5. Conclusions have pointed out above, the implementation of management and conservation action plans remains crucial. &rough this article, we presented the current status of three globally threatened waterfowls’ populations in Morocco. On the species’ level, the adoption of the National Law N 29–05, enforcing the CITES Convention, is a particularly While the White-headed Duck’s numbers are increasing and the Marbled Teal’s are mostly stable, the Common Pochard successful measure deterring all illegal actions threatening endangered species. Furthermore, the national action plan has known a decline in its wintering population and its breeding range is very limited in the country. for the White-headed Duck [31] is a crucial step to the International Journal of Zoology 15 Another important result of this synthesis is the iden- Supplementary Materials tification of the Moroccan wetlands that play a major role as Table S1. National counts of the Common Pochard’s win- hosting key sites of the three species. &ese results can direct tering individuals per year and per site. Table S2. National and focus the short-term conservation efforts on these key counts of the Marbled Teal’s wintering individuals per year sites, to enhance the survival and thriving of these species in and per site. Table S3. National counts of the White-headed Morocco. Duck’s wintering individuals per year and per site. Table S4. A better understanding of these ducks’ populations’ List of observers who contributed to the IWC program in dynamics, which is crucial to prevent their decline, requires Morocco between 1983 and 2019. (Supplementary Materials) further studies on the ecological and anthropogenic factors influencing them. Furthermore, cooperative efforts, coupled with more effective census methods, should be carried out to References enhance the knowledge on the species on the flyway/regional levels. &ese threatened waterbirds’ survival depends, in fact, [1] A. 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Distribution and Numbers of Three Globally Threatened Waterbird Species Wintering in Morocco: The Common Pochard, Marbled Teal, and White-Headed Duck

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Hindawi International Journal of Zoology Volume 2021, Article ID 8846203, 17 pages https://doi.org/10.1155/2021/8846203 Research Article Distribution and Numbers of Three Globally Threatened Waterbird Species Wintering in Morocco: The Common Pochard, Marbled Teal, and White-Headed Duck 1 1 1 Asmaaˆ Ouassou , Mohamed Dakki , Mohammed-Aziz El Agbani, 1 2,3 Abdeljebbar Qninba , and R’himou El Hamoumi Study Centre of Bird Migration, Geo-Biodiversity and Natural Patrimony Laboratory, Department of Zoology and Animal Ecology, Scientific Institute, Mohammed V University in Rabat, Rabat 10106, Morocco Laboratory of Ecology and Environment, Ben M’sik Faculty of Sciences, Hassan II University, Casablanca, Morocco GREPOM/BirdLife Morocco, Sale´, Morocco Correspondence should be addressed to Asmaaˆ Ouassou; asmaa.ouassou@gmail.com Received 3 August 2020; Revised 25 December 2020; Accepted 31 December 2020; Published 21 January 2021 Academic Editor: Marco Cucco Copyright © 2021 Asmaaˆ Ouassou et al. &is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Morocco plays a key role in the life of many migratory birds and their survival, thanks to the diversity and richness of its ecosystems. &e International Waterbird Census (IWC) has been regularly implemented in Morocco since 1983. &anks to this program, a large database on wintering waterbirds’ populations has been collected. In this article, we summarize the wintering data of three globally threatened waterbirds: Aythya ferina, Marmaronetta angustirostris, and Oxyura leucocephala. &e pop- ulation of Aythya ferina, which is declining, is largely distributed in the country, in over a hundred wetlands, 26 of which verify the national importance criteria. Marmaronetta angustirostris has a stable trend over the years even though its population can know high annual fluctuations; it winters in more or less 50 wetlands, among which 18 host more than 1% of its regional population and 16 verify the criteria for national importance. On the contrary, Oxyura leucocephala, a globally endangered bird only encountered in a dozen wetlands, shows a moderate increase in its numbers; only two wetlands verify the Ramsar criterion 6, while a total of six can be considered of national importance. Furthermore, given the conservation statuses of these waterbirds and according to the Ramsar criterion 2, all their hosting sites are of international importance. &e results presented in this paper are a crucial step for the adoption and implementation of adequate conservation measures for the species and their key sites. Nevertheless, com- prehensive research and coordinated efforts on the factors (ecological and anthropogenic) influencing the species, at the national and international levels, are required for a better understanding of their populations’ dynamics. Waterbird Agreement, the country undertakes regular water- 1. Introduction bird censuses that provide an appropriate basis for effective Morocco is a North African country, with highly diversified decision-making in their conservation. In fact, Morocco has ecosystems and coastlines along both Atlantic Ocean and been regularly participating, since 1983, in the International Mediterranean Sea [1, 2]. It is located at the crossroads of many Waterbird Census (IWC), one of the largest biodiversity bird migration routes between Europe and Tropical Africa, and monitoring programs in the world, thanks to the coordination its wetlands play a crucial role for thousands of birds as of the Study Centre of Bird Migration (in the Scientific Institute) stopover, wintering, and breeding areas [3, 4]. &e country has and the collaboration of GREPOM/BirdLife Morocco, which ratified almost all international and regional agreements for the provides the majority of field volunteers. conservation of these birds and their habitats. In the context of &is article provides new syntheses on three globally the Ramsar Convention and the African-Eurasian Migratory threatened species of Anseriformes [5]: the White-headed 2 International Journal of Zoology Duck Oxyura leucocephala (Scopoli, 1769), an endangered Nevertheless, given the large number of wetlands to be bird [6], and two vulnerable species the Marbled Teal censused, some missions can start in late December (es- ´ ´ ´ Marmaronetta angustirostris (Menetries, 1832) [7] and the pecially in the Saharan region). Moreover, in some rare st Common Pochard Aythya ferina (Linnaeus, 1758) [8]. cases, data from censuses during the 1 week of February &e Common Pochard is a Eurasian duck found in a were accepted; they were conducted in some sites (Atlas wide variety of wetlands (marshes, lagoons, lakes, artificial lakes) that were not accessible, during January, because of reservoirs, and rivers), with eutrophic to pH neutral waters, heavy snow. &e number of wetlands censused, at least once, but it mostly prefers large open bodies of water with in the context of this program is 272 (IWC wetlands net- abundant emergent vegetation [8–10]. In Morocco, it is a work). However, not all of them are visited every year, winter visitor, passage migrant, and occasional to regular depending on the availability of human, financial, and lo- breeder [4, 11, 12]. Evident nesting cases have been observed gistical resources. &e priority is always given to the wet- in five Northern marshlands: “Plan d’eau de Dwiyate” lands with the highest waterbirds’ numbers and specific [4, 13], “Merja Bargha” [4, 14], “Marais de Smir” [15], “Merja richness. de Sidi Bou Ghaba” (with the highest number of breeding During each visit, the observers (Table S4) counted all pairs, nationally: 25 in 2011) [16], “Merja de Fouwarate” waterbirds on the grounds, in the water, and even those [17], and in two Atlas lakes (“Aguelmam Afennourir” and flying inside the site, using binoculars and telescopes. “Dayet ‘Awa’” [4]). &e threats faced by the species and its Counting points and transects are determined for each limited breeding population have rendered it vulnerable in wetland, depending on its configuration and accessibility. Morocco [16]. When some wetlands are close to one another, in a way that &e Marbled Teal is commonly found in shallow allows frequent bird exchange between them, they are brackish wetlands [18], with rich emergent and submerging considered as complex sites and are covered during the same vegetation [9, 19, 20], avoiding open-water areas [20–22]. visit. Over the years (especially since the 1990s), most However, its distribution largely varies with seasons, espe- wetlands have been censused by the same group of ob- cially depending on its dietary needs [18]. In Morocco, it is a servers, using the same protocol; this makes the obtained resident breeder, winter visitor, and passage migrant [4, 11]. data more homogenous, comparable, and reliable. &e Its breeding population was estimated to 50–250 pairs [23], observers participating in the IWC program are ornithol- distributed in a dozen wetlands situated in the north and ogists, qualified and trained for bird identification. New south of the country [4, 16, 17, 23–25]. Nevertheless, it is the observers can join the program after going through training most regularly breeds in four wetlands [16, 17, 24]: “Merja de sessions on bird identification and counting methods, both Sidi Bou Ghaba,” “Merja de Fouwarate,” “Plan d’eau de theoretical and practical. During their learning phase, they Dwiyate,” and “Embouchure de Wad Massa.” &e species is can join the established observers’ teams during their census considered endangered in Morocco [16] mainly because of campaigns to strengthen their training. its habitat degradation and modification [16]. &e White-headed Duck is the only Palearctic species of the Oxyurini tribe [26]. Breeding birds are usually found in 2.2. Data Analysis. &e wintering waterbirds’ numbers are freshwater and brackish or eutrophic lakes with dense entered in an information system, which generates auto- matically tables per species and sites. emergent vegetation [22, 27], shallow and permanent or semipermanent [9], while wintering birds can be found in To calculate populations’ trends, we used the TRIM (TRends and Indices for Monitoring Data) freeware [36] deeper and larger wetlands, alkaline or saline, and with less vegetation [28]. In Morocco, it is a winter visitor, resident (version 3.54). TRIM generates estimations for missing counts and can analyze data for 4000 sites, over 100 years; breeder, and suspected passage migrant [11]. It is used to th breed in Morocco until the 20 century, before becoming this makes it very suitable for our large dataset, especially since not all sites are visited every year (Table 1). &e missing scarce and disappearing, due its habitats’ loss by agricultural development and droughts [25]. Since the 1990s, the species data imputations take into account a site effect and a time effect, assuming the counts in a year depend on those of the reappeared in “Plan d’eau de Dwiyate” [4, 29] and then expanded progressively to several other breeding sites year before (serial correlation). &e counts are assumed to be Poisson distributed and are converted into annual indices to [30, 31]: “Merja de Sidi Bou Ghaba,” “Merja de Fouwarate,” simulate the missing data and calculate trends, based on the “Barrage ‘Arabat’,” “Barrage El Mehraz,” “Merja Bargha,” completed dataset (with the first year as base year, to which cumulating about 60 couples. It is still vulnerable in Mo- the index 1 or 0 is attributed). &e overdispersion (when the rocco [12]. variance is larger than expected for a Poisson distribution) and the serial correlation can be estimated by TRIM, 2. Methodology through a generalized estimating equation (GEE) approach. &e recommended overall slope by TRIM is based on the 2.1. Counting Procedure. Our study is based on the dataset of the waterbirds’ winter census, between 1983 and 2019. &e imputed data and given with the results of the additive slope and the multiplicative slope, which reflects the magnitude of counting procedure was adopted according to standard bird monitoring techniques [32], and the protocol was refined annual change, as well as their standard errors. It is con- verted into one of six trend categories: (i) strong increase: an over the years [14, 33–35]. &e censuses are conducted increase significantly greater than 5% per year; (ii) moderate annually, usually during January, to avoid recounts. International Journal of Zoology 3 Table 1: Number and percentage of wetlands visited per year. Year Number of surveyed wetlands % of the IWC wetlands network (272) Average 73 27 1983 47 17 1984 82 30 1985 49 18 1986 35 13 1987 69 25 1988 69 25 1989 56 21 1990 71 26 1991 94 35 1992 86 32 1993 94 35 1994 77 28 1995 89 33 1996 46 17 1997 70 26 1998 65 24 1999 65 24 2000 62 23 2001 65 24 2002 56 21 2003 62 23 2004 65 24 2005 59 22 2006 66 24 2007 77 28 2008 85 31 2009 79 29 2010 62 23 2011 100 37 2012 43 16 2013 78 29 2014 115 42 2015 70 26 2016 88 32 2017 76 28 2018 99 36 2019 131 48 increase: a significant increase, but not significantly more To better understand the species evolution, we used than 5% per year; (iii) stable: no significant increase or different parameters, mainly as follows: decline, and it is certain that trends are less than 5% per year; (i) &e average number of a species in each site is (iv) uncertain: no significant increase or decline, but not calculated for the long term and short term and certain if trends are less than 5% per year; (v) moderate corresponds to the arithmetic mean. decline: significant decline, but not significantly more than (ii) &e national average corresponds to the sum of the 5% year; (vi) steep decline: decline significantly greater than average numbers in each site. 5% year. A significance threshold is also provided for the increasing and declining trends: (i) highly significant: (iii) &e total annual numbers correspond to the sum of p< 0.01 (i.e., confidence level of 99%); (ii) significant: the species numbers in each site for every year. p< 0.05 (i.e., confidence level of 95%). (iv) &e total number per site is the sum of all the For the Common Pochard and the Marbled Teal TRIM species numbers observed per year in said site. analyses, three periods were considered: long term (v) &e occurrence of a species in a site corresponds to (1983–2019), medium term (2000–2019), and short term the number of winters it has been observed in this (2010–2019). For the White-headed Duck, which has been site. regularly observed in Morocco only starting 2005, the trend (vi) &e census number of a site corresponds to the was calculated for the periods of 2005–2019 (long term) and number of years during which it has been visited. 2010–2019 (short term). 4 International Journal of Zoology (vii) &e occurrence percentage of a species in a site However, this number hides very high interannual fluc- corresponds to the ratio of its occurrence to the tuations (Figure 2), knowing that the total annual num- bers vary between 27 (in 1996) and 3.755 ducks (in 2013). site’s census number. Morocco hosts 47% of the regional population “West (viii) &e 1st census of a site corresponds to the first year Mediterranean/West Mediterranean and West Africa” during which it has been visited. [37]. &e species was present in 295 counts and absent in (ix) &e standard deviation was calculated for each site, 651 counts (no observed birds during visits), while 904 to determine the deviation of the numbers ob- data are missing (Table S2). Its population trend (Figure 2) served annually from the average. is stable in the long term (additive slope � −0.0050 ± 0.0092; multiplicative slope � 0.9950± 0.0092), whilst it 􏽳��������� is uncertain in the medium term (additive slope � - 􏽐 x − x􏼁 0.0208± 0.00169; multiplicative slope � 0.9794± 0.0166) (1) σ � , and short term (additive slope � 0.0097± 0.0447; multi- plicative slope � 1.0097± 0.0452). where x is the observed number in site i, x is the arithmetic i &e White-headed Duck’s national average is 445 between mean, and N is the number of observations. 2005 and 2019 and 542 individuals during the last decade To prioritize future conservation measures, we have (2010–2019). Morocco hosts 22% of the regional population identified for each species, categories of key sites, based on “Spain and Morocco” [37]. &e observed total annual numbers recent data (2010–2019): varied between 1 and 1.730 (Figure 3). &e species was ob- served, in the context of IWC, during the period 2005–2019 (i) Sites of international importance, priority 1 (SII1): and was present in 29 counts and absent in 58 counts (no wetlands verifying the 6th Ramsar criterion (the observed birds during visits), while 45 records are missing species’ numbers reach or exceed regularly (5 (Table S3). &e population’s trend (Figure 3), for the 2005–2019 winters or more) 1% of its regional population. period, is a moderate increase (additive slope � 0.2749± 0.1181; (ii) Sites of international importance, priority 2 (SII2), multiplicative slope � 1.3164± 0.1554; p< 0, 05). In the short verifying the 2nd Ramsar criterion (sites supporting term, it is uncertain (additive slope � 0.3899± 0.4609; multi- vulnerable, endangered, or critically endangered plicative slope � 1.4768± 0.6807), but with an increasing species). tendency. (iii) Sites of national importance (SNI): the species’ average number, in those sites, equals or exceeds the 1% of the national average. 3.2. Spatial Distribution. &e Common Pochard was ob- served in a total of 118 wetlands (43% of the surveyed (iv) Sites of potential national importance (SPNI): they wetlands) (Table S1), mostly in the Northern half of the hosted, during at least winter, more than 1% of the country, along the Atlantic coast and Atlas region (Figure 4). national average. However, from year to year, the species was reported in 9 to 39 sites (Figure 1). Between 2010 and 2019, the northwest (31 3. Results sites) and northeast (16 sites) regions hosted the highest concentrations (37% and 33%, respectively). Amongst the 3.1. Populations’ Size and Trend. &e national average of the sites visited at least 19 winters over the 37 years study period, Common Pochard’s wintering population is 11.158 in the long the species occurrence percentage was the highest in five of term, the total annual numbers varying between 1.710 (in 2012) them (>85%): “Aguelmam Abekhane,” “Aguelmam Afen- and 20.458 ducks (in 2002) (Figure 1). During the last decade (2010–2019), the national average is lower (7.496 individuals), nourir,” “Merja de Sidi Bou Ghaba,” “Dayet Ifrah” and “Barrage de Smir.” &e highest total numbers (between 1983 but it represents 1.25% of the regional population “Central and NE Europe/Black Sea and Mediterranean” [37]. &e Common and 2019) were cumulated as follows: “Barrage Mohammed V,” “Barrage Al Massira,” and “Embouchure de Wad Pochard was present in 809 counts and absent in 991 counts Massa.” In the short term (amongst the sites visited at least 5 (no observed birds during visits), while 2.640 data are missing years out of 10), the highest average numbers were recorded (the unavailable records relative to the species’ known win- in “Barrage Mohammed V” and “Merja de Sidi Bou Ghaba” tering sites, which have not been visited during certain years) (Table 2). Some wetlands have known a decline in the (Table S1). Its population trend (Figure 1) is stable in the long species’ wintering numbers, such as “Embouchure de Wad term (additive slope � −0.0101± 0.0057; multiplicative slope � 0.9900± 0.0057), a significant moderate decline in the Massa;” others such as “Merja de Fouwarate” have hosted increasing numbers in recent years. &e highest concen- medium term (additive slope � −0.0727± 0.0117; multiplicative slope � 0.9299± 0.0109; p< 0, 01), and uncertain in the short tration ever recorded in Morocco (15.600 birds) was ob- served in the reservoir of “Barrage Mohammed V” in 2002. term (additive slope � −0.0226± 0.0279; multiplicative slope � 0.9776± 0.0273), but with a declining tendency. &is &is site has known high fluctuations of the Common Pochard’s numbers (zero to thousands), which is clearly decline is more evident during the last decade (2010–2019) reflected by its high standard deviation (Table 2). even though the census effort has significantly increased. &e Marbled Teal was observed in a total of 50 wetlands &e Marbled Teal’s national average is almost the (18% of the surveyed wetlands) (Table S2), mainly same, in the long term (3.071) and short term (3.070). International Journal of Zoology 5 25000 45 0 0 Years Total annual numbers Number of sites (a) 2.5 1.5 0.5 Years Model indices Imputed data (b) Figure 1: (a) Total annual numbers of the Common Pochard and number of wetlands where it has been observed in Morocco between 1983 and 2019. (b) Linear trend of the wintering population (TRIM analysis). distributed north and west to the Atlas Mountains and in the (i) “STEU Guelmim”: a wastewater treatment plant, northern part of the Sahara (Figure 5). Annual distribution only visited in 2016 (89 ducks) and in 2018 during varied between 2 and 19 sites (Figure 2). In the short term, which a high concentration of 1.748 was recorded. 67% of the national average was observed in the southern (ii) “Was As-Saqia Al Hamra a` La’youn”: observations region (in 15 wetlands), with particularly high concentra- varied between 0 individuals and the highest con- tions in 2013 (95%) and 2018 (62%). &e other regions centration ever recorded in Moroccan sites (3.557, hosted 8% to 15% of this number. &e highest occurrence of almost half of the national population in 2013). the species was recorded in “Merja de Sidi Bou Ghaba” (97% of the visits), “Lagunes de Sidi Moussa-Walidia” (83%), and Since its reappearance in Morocco in the early 2000s, the White-headed Duck was observed in 12 wetlands (17% of the “Embouchure de Wad Massa” (81%). &ree sites hosted each, more than 10% of the total numbers recorded between surveyed wetlands), mainly in the north of the country (Table S3; Figures 3 and 6). Its annual distribution did not 1983 and 2019: “Lagunes de Sidi Moussa-Walidia,” “Wad exceed six sites, and it was not observed in any wetland As-Saqia Al Hamra a` La’youn,” and “Merja de Sidi Bou visited in 2006, 2007, 2010, and 2012 (Figure 3). Most of its Ghaba.” &e highest standard deviations were recorded in population is located in the northwest region (73%). &e two sites (Table 3): Total annual numbers Indices values Number of sites 6 International Journal of Zoology 5000 20 4500 18 4000 16 3500 14 3000 12 2500 10 2000 8 1500 6 1000 4 500 2 0 0 Years Total annual numbers Number of sites (a) 2.5 1.5 0.5 Years Model indices Imputed data (b) Figure 2: (a) Total annual numbers of the Marbled Teal and the number of wetlands where it has been observed in Morocco between 1983 and 2019. (b) Linear trend of the wintering population (TRIM analysis). species was most regular in “Merja de Sidi Bou Ghaba” (75% the highest concentrations nationally were recorded (1.430 of the visits) and “Merja de Fouwarate” (45%). &ree wet- in 2018 and 500 in 2019). lands (“Merja de Fouwarate,” “Merja de Sidi Bou Ghaba,” and “Barrage Mohammed V”) hosted more than 10% of the 3.3. Sites of International and National Importance. &e wintering individuals. It is worth mentioning that the Common Pochard is a globally vulnerable species, which wetland “Plan d’eau de Dwiyate” is hard to access, since it is part of a royal domain. Except for a temporary lake on the makes all the sites hosting it of international importance (SII2 as we have defined in Methodology). None of the east (suffering from some disturbance, overgrazing, and recurrent droughts [29]), it is fenced and well-guarded and Moroccan wetlands verify the Ramsar criterion 6 for the species. Nevertheless, it is worth mentioning that “Barrage hence with no disturbance, which makes it a site of great importance for the species. &e highest standard deviation Mohammed V” could be of potential international impor- tance. In fact, in 2002, this site hosted a high concentration was recorded in “Merja de Fouwarate” (Table 4), where the species was not observed before 2014 (Table S3) and where of 15.600 ducks, which exceeded the estimated 1% of the Total annual numbers Indices values Number of sites International Journal of Zoology 7 2500 7 0 0 Years Total annual numbers Number of sites (a) Years Model indices Imputed data (b) Figure 3: (a) Total annual numbers of the White-headed Duck and the number of wetlands where it has been observed in Morocco between 2005 and 2019. (b) Linear trend of the wintering population (TRIM analysis). regional population at the time (10.000) [37]. &e reported (7.496) (Table 2), which makes them of national importance. species’ numbers in this wetland can be highly under- On the contrary, 15 others hosted wintering numbers ex- estimated due to a difficult access to many parts of the ceeding that threshold, during at least one winter (Table 2), reservoir, depending on the conditions. &erefore, it can, which makes them of potential national importance. more than likely, host regularly at least 1% of the Common &e Marbled Teal is a globally vulnerable species, which Pochard’s regional population. &is could also be the case for makes all the sites hosting it of international importance as well “Barrage Al Massira,” a reservoir often partially censused (SII2). Moreover, 18 wetlands hosted, at least once, more than and which hosted, in 2008, 5.500 ducks. Among the 118 1% of the regional population [5], three of them regularly: wetlands where the species was observed, 26 have average “Lagunes de Sidi Moussa-Walidia,” “Merja Zerga,” and “Wad numbers equal or superior to 1% the national average As-Saqia Al Hamra a` La’youn;” they are thus of international Total annual numbers Indices values Number of sites 8 International Journal of Zoology 0 25 50 100 150 200 Kilometers Average numbers 1983-2019 ≤28 Wetlands surveyed (with 29 – 103 no Common Pochard) 104 – 235 Hydrographic network 236 – 646 Regional boundaries 647 – 2331 Figure 4: Distribution map of the Common Pochard’s wintering population in Morocco (1983–2019). importance for the species (SII1) (Table 3). On the contrary, 26 main lists exist in the Moroccan legislation: a list of species for wetlands have average numbers equal or superior to 1% of the which hunting is banned (published through the “Annual Hunting Order”) and a list of species in which trade and national average (Table 3), which makes them of national importance. Among them, 11 hosted wintering numbers ex- transport is conditioned by a special governmental authori- zation (through the CITES Law “N ceeding that threshold during at least one winter (Table 3), 29–5”). &e hunting of the which makes them of potential national importance. White-headed Duck and Marbled Teal is prohibited in Mo- Because it is endangered, the White-headed Duck at- rocco, whilst the Common Pochard can still be hunted [38]. tributes an international importance to all the 12 sites National action plans for species can also be efficient tools hosting it (SII2). &e 1% of the regional population [37] was for the conservation of birds and their habitats. In Morocco, exceeded, at least one winter, in five wetlands, but regularly only the White-headed Duck has a national action plan [18]. in “Merja de Sidi Bou Ghaba” and “Merja de Fouwarate.” On In situ conservation mechanisms represent another the contrary, seven wetlands hosted, at least once, more than important measure for the conservation of the three species. 1% of the national average, cumulating 99.8% of this In addition to two international statuses for the conservation number. Among them, 6 are of national importance and one of wetlands: (i) Ramsar Sites and Important Bird and is of the potential national importance (Table 4). Biodiversity Areas (IBA), these mechanisms also consist, in For the three species, some sites need to be monitored Morocco, in the creation of three national statuses for which more regularly to verify and/or confirm their national/in- a high number of wetlands have been designated for. Several ternational importance since they have been visited less than bird species, including the three ducks subject of this article, 5 winters (Tables S1–S3). have been targeted by these statuses: (i) national parks (NPs); (ii) Sites of Biological and Ecological Interest (SBEI), defined in 1996 [39], with at least 84 wetlands, partly assessed using 3.4. Current Conservation Measures in Morocco towards the waterbirds; and (iii) permanent hunting reserves (PHRs). ;ree Species. An efficient legal conservation way consists in &e Common Pochard is found in 44 wetlands, with at least classifying a bird in an official list of protected species. Two one conservation status (Table 5); 22 of them are Ramsar sites, International Journal of Zoology 9 Table 2: Most important wintering sites of the Common Pochard (2010–2019). 1% 1 2 Site name Average number Max. Importance Standard deviation NA Barrage Hassan Ad-Dakhil 850 1700 1 SNI/SII2 530 Barrage Mohammed V 626 15600 2 SNI/SII2 3816 Merja de Sidi Bou Ghaba 514 1200 8 SNI/SII2 258 Aguelmam Afennourir 468 2600 4 SNI/SII2 624 Merja de Wad Fouwarate 413 1000 8 SNI/SII2 308 Barrage Wad Al Makhazine 317 1101 3 SNI/SII2 345 Barrage de Smir 312 1689 4 SNI/SII2 462 Sadd Al Ajras 305 305 1 SNI/SII2 98 Barrage Asfalou 300 300 1 SNI/SII2 0 Aguelmam Abekhane 296 855 2 SNI/SII2 200 Barrage Al Massira 256 7038 3 SNI/SII2 1853 Aguelmam N’Tifounassine 227 652 1 SNI/SII2 145 Merja Zerga 210 1800 2 SNI/SII2 324 Barrage Hassan II 186 1100 2 SNI/SII2 327 Dayet Ifrah 180 860 3 SNI/SII2 218 Aguelmams Sidi Ali-Ta’nzoult 172 1700 4 SNI/SII2 360 Barrage Mechra’ Hommadi 126 290 2 SNI/SII2 82 Barrage Enjil 124 690 3 SNI/SII2 179 Barrage Oued Rmel 124 160 2 SNI/SII2 37 Dayet ‘Awa 122 1030 3 SNI/SII2 192 Embouchure de Wad Malwiya 104 224 5 SNI/SII2 67 Barrage Moulay Youssef 94 114 1 SNI/SII2 43 Merja Bargha 89 1590 4 SNI/SII2 323 Marais de Wad Smir 87 391 3 SNI/SII2 83 Barrage Sahla 85 164 1 SNI/SII2 80 Barrage Al Wahda 84 283 1 SNI/SII2 117 Barrage Hassar 74 148 3 SPNI/SII2 60 Mlalah du Bas Tahaddart 69 480 1 SPNI/SII2 96 Barrage Kheng El Hda 67 200 4 SPNI/SII2 61 Barrage Petit Tizil 52 250 2 SPNI/SII2 79 Dayet Hachlaf 45 163 1 SPNI/SII2 56 Barrage Zelmou 38 159 1 SPNI/SII2 44 Barrage’Arabat 38 94 1 SPNI/SII2 40 Barrage Idriss Premier 34 570 1 SPNI/SII2 156 Marais du bas Loukkos 34 410 1 SPNI/SII2 83 Merja des Wlad Khallouf 30 240 1 SPNI/SII2 53 Merja Al Halloufa 25 680 2 SPNI/SII2 220 Embouchure de Wad Massa 23 3330 1 SPNI/SII2 832 Merja des Wlad Skher 23 650 2 SPNI/SII2 143 Lagunes de Sidi Moussa-Walidia 16 2500 1 SPNI/SII2 431 Sebkha Bou Areg 12 406 1 SPNI/SII2 109 1 2 &e average (mean) of the species’ annual numbers counted in a site (their sum is divided by the number of years the site was censused). Maximum wintering number observed in a site since its first year of census. Number of winters during which 1% of the national average (7.496) exceeded. 34 are SBEI, 21 are IBA, 9 are part of national parks, and 18 are though regional populations’ trends differ from stable to part of permanent hunting reserves. &e Marbled Teal occupies unknown [8], the European population, which represents 25 wetlands having national and/or international conservation 35% to 40% of the global population, has decreased by statuses: 15 Ramsar sites, 20 SBEI, 16 IBAs, 3 are part of national 30–49% over three generations [8, 40, 41]. parks, and 10 are part of permanent hunting reserves. Among &e Moroccan wintering numbers show a significant the 9 wintering wetlands of the White-headed Duck with decline, especially during the two recent decades, which conservation statuses, 6 are Ramsar sites, 7 SBEI, 5 IBA, 3 are could be directly linked to the declining trend of the regional part of national parks, and 5 are part of permanent hunting population “Central and NE Europe/Black Sea and Medi- reserves. terranean” [37, 42–44], from which the wintering individ- uals in Morocco originate. In fact, according to the IUCN [37], the species’ decrease is mainly due to the loss of its 4. Discussion breeding habitat in Eastern Europe. In Central Europe, it appears that the major factors responsible for its decline are 4.1. Population Size and Trend. &e global population of the nest predation [37, 45] by natural (Vulpes vulpes and Sus Common Pochard is considered to be decreasing [8]. Even 10 International Journal of Zoology 0 75 150 225 300 Kilometers Average numbers 1983-2019 ≤28 Wetlands surveyed (with no Marbled Teal) 29 – 96 97 – 246 Hydrographic network 247 – 499 Regional boundaries 500 – 919 Figure 5: Distribution map of the Marbled Teal’s wintering population in Morocco (1983–2019). scrofa) and alien mammal species (i.e., Neovison vison, regional population (West Mediterranean/West Mediter- Nyctereutes procyonoides, and Procyon lotor) and a decline of ranean and West Africa), which is stable [42], but with a Dreissena polymorpha, the zebra mussel which is the pre- possible declining tendency [37]. &e global population of the species has decreased rapidly overtime [7]; only the ferred food of this duck [46–48]. Furthermore, Fox et al. (2016) [41] have summarized multiple factors influencing southwest Asian population knows a possible increase [37], albeit it may be due to an improvement in census coverage the breeding population in the old continent; they are mostly related to loss or changes in habitats, food availability, instead of actual changes within the population [7]. predation, alien species, hunting [9, 49, 50], fishing, dis- In Morocco, the Marbled Teal’s population often showed a turbance, and lead poisoning [51]. On the contrary, Folliot lot of fluctuations from one year to another. In fact, the species et al. (2018) [52] suggest that decreasing wintering numbers can have extreme fluctuations in its population’s size in Western Europe can also be due to the decline of the depending on rainfall’s annual variation [18]. It can therefore breeding population in the southwest Asian flyway (espe- relocate to other areas that may be unmonitored and vice versa cially in Siberia). In fact, analyses of ringing recoveries data and hence giving the impression of an increase or decrease in showed that large wintering numbers in the northwest numbers. &is relocation could occur between wetlands of the same country as well as at a larger scale, between wintering European flyway originate from the southwest Asian flyway, which brings to evidence the interactions and exchange areas of different countries. Moroccan wintering individuals between the different regional populations beyond the de- can come from breeding sites in Europe (e.g., Spain) and North termined limits of the flyways. In addition to the afore- Africa [59] (especially Algeria, which hosts important numbers mentioned factors that are possibly contributing to the of the species [60–62]). Nevertheless, the high records observed decline of the Common Pochard in Morocco, climate change sometimes are not necessarily caused by an influx from Spain can also play a crucial role in the species’ populations but could be explained by the presence of unknown breeding changes [53–58] at a larger scale, as well as the direct threats sites of great importance in the country or in North Africa [59]. faced by the species in Moroccan wetlands. &e sometimes declining numbers of the species in Morocco and other regions can also be function of the habitats’ quality &e evolution of the Marbled Teal’s wintering pop- ulation in Morocco is consistent with the trend of the and availability. In fact, the global population’s decrease was a International Journal of Zoology 11 Table 3: Most important wintering sites of the Marbled Teal (2010–2019). 1% 1 2 Site name Average number Max. Importance Standard deviation NA Wad As-Saqia Al Hamra a` La’youn 448 3557 9 SII1/SNI 708 Lagunes de Sidi Moussa-Walidia 157 1800 6 SII1/SNI 471 Merja Zerga 83 200 9 SII1/SNI 49 STEU Guelmim 919 1748 2 SII2/SNI 830 Barrage Moulay Abdellah 499 997 1 SII2/SNI 499 Barrage Hassan Ad-Dakhil 188 339 2 SII2/SNI 106 Sebkha Zima 148 950 3 SII2/SNI 185 Merja de Fouwarate 119 400 7 SII2/SNI 107 Merja de Sidi Bou Ghaba 74 1400 3 SII2/SNI 302 Barrage Mohammed V 50 230 2 SII2/SNI 49 STEP Tarfaya 44 44 1 SII2/SNI 0 Dayet Al Fahs 44 636 2 SII2/SNI 125 Radier de l’Oued Assaka 43 75 2 SII2/SNI 32 Barrage Al Massira 36 1973 3 SII2/SNI 355 Barrage Hassar 36 128 2 SII2/SNI 48 Plage Ras Takoumba-Bou Issafine 31 550 1 SII2/SPNI 161 Marais de Wad Al Maleh 22 248 1 SII2/SPNI 86 Embouchure de Wad Massa 20 397 3 SII2/SPNI 101 Plage Blanche 17 136 1 SII2/SPNI 32 Embouchure de Wad Malwiya 15 142 1 SII2/SPNI 27 Embouchure de Wad Bou Issafine 13 60 1 SII2/SPNI 16 Embouchure de Wad Assaka 13 52 1 SII2/SPNI 15 Marais du bas Loukkos 11 82 2 SII2/SPNI 18 Dayet Taras El Ghoul 8 350 1 SII2/SPNI 76 Daya Al Beyda 6 37 1 SII2/SPNI 9 Barrage Zelmou 5 37 1 SII2/SPNI 11 1 2 &e average (mean) of the species’ annual numbers counted in a site (their sum is divided by the number of years the site was censused). Maximum wintering number observed in a site since its first year of census. Number of winters during which 1% of the national average (3.070) exceeded. direct consequence of habitats’ loss and degradation [7, 59, 63] have different potential explanations and combined due mainly to drainage of wetlands for agricultural purposes factors: and hydrological work [7]. In our country, for example, one of (i) A flow of migrants from Spain: the conservation and the most important breeding sites, the Iriki Lake (where the protection efforts undertaken by Spain, over more than Marbled Teal used to breed in high numbers (hundreds of 30 years [29], have had a strong positive effect on the couples in the 1960s)), has disappeared because of the con- White-headed Duck’s population in Spain and may struction of a dam (Barrage Al Mansour Ad-Dahbi) [24]. have contributed to its return to Morocco and its Although this vulnerable duck is legally protected in Morocco increasing numbers in the country [29]. [24], it still faces many threats affecting negatively its pop- (ii) A flow of individuals from the regional population of ulation. &ese threats are mainly related to human activities, “Algeria and Tunisia,” which hosts significant breeding disturbing, degrading, or destructing its habitats, and changes numbers of the White-headed Duck [66]. &ere are, in water levels (caused by low precipitations, drainage, and currently, insufficient data to decide if there is any hydraulic work). In fact, the species’ wetlands occupancy in our exchange between the West Mediterranean and North country, especially in the breeding season, is closely dependent African subpopulations [66] that could also contribute on habitat-related factors, such as the number and diversity of to the species increase in Morocco. Nevertheless, our emergent vegetation species [22, 64, 65], which are more country is at an advantageous position between the predominant in Ramsar sites close to the coastline [65]. increasing Spanish population and the Algerian one, Since its return in Morocco, the White-headed Duck’s which hosts high numbers of the species during the population has known a moderate increase. Notwith- breeding season and throughout the year [66–70], but standing, the global population of the species is thought to faces many threats in the country, especially illegal be decreasing [6]. &is decline is estimated to be 50–79% killing [71]. in three generations [6] even though many subpopula- tions are not thoroughly recorded, which may lead to an (iii) &e decline in the population of the ruddy duck and underestimation of the species counts [6, 66]. &e increase its hybrids due to campaigns for its eradication in in this endangered duck’s population in Morocco, espe- Spain, Europe [29, 72], and Morocco [73]. cially the high numbers recorded in “Merja of Fouwarate” (iv) &e presence of favorable breeding sites in Mo- during the 2018 winter (1.430 individuals) [30], could rocco, thanks to wetlands conservation efforts and 12 International Journal of Zoology 0 20 40 80 120 160 Kilometers Average numbers 1983–2019 ≤13 Wetlands surveyed (with no White-headed Duck) 14 – 40 Hydrographic network 41 – 113 Regional boundaries 114 – 184 Figure 6: Distribution map of the White-headed Duck’s wintering population in Morocco (2005–2019). Table 4: Most important wintering sites of the White-headed Duck (2010–2019). 1% 1 3 Site name Average number Max. Importance Standard deviation NA Merja de Sidi Bou Ghaba 170 8 351 SII1/SNI 120 Merja de Wad Fouwarate 225 5 1430 SII2/SNI 419 Barrage Mohammed V 106 3 426 SII2/SNI 145 Dayet Ifrah 15 2 59 SII2/SNI 19 Dayet Hachlaf 15 1 88 SII2/SNI 31 Barrage’Arabat 9 2 22 SII2/SNI 9 Barrage El Mehraz 2 1 6 SII2/SPNI 3 Dayet’Awa 1 0 3 SII2 1 1 2 &e average of the species’ annual numbers counted in a site (their sum is divided by the number of years during which the site was censused). Maximum wintering number observed in a site since its first year of census. Number of winters during which 1% of the national average (542) exceeded. suitable climate conditions that contribute to good many other threats; the most imminent one is the hybrid- water levels [74] and more developed vegetation ization with the ruddy duck. In fact, this introduced species cover. has been observed in Morocco on many occasions, and the last documented observation was in 2013, where 2 indi- In Morocco, many factors have contributed to the for- viduals were observed in Merja Al Halloufa [75]. Never- mer disappearance of this endangered duck and halted its theless, unpublished data (Hassani H. and Dakki M. in litt.) expansion. Overgrazing and repeated cutting of reed beds have reported the ruddy duck, during recent years in Barrage caused a regression of emergent vegetation in permanent Al Mehraz in 2014 and 2015, one of the sites where breeding wetlands [29], which is crucial for this duck’s breeding. White-headed Ducks have been observed [31]. &e second According to El Hamoumi et al. [31], the species still faces most imminent threat to the survival of the species in International Journal of Zoology 13 Table 5: Conservation statuses of the three species’ hosting wetlands. 1 2 3 4 5 6 7 Site name Types of habitat Region Ramsar IBA SBEI NP PHR Aytfer Marang Oxyleu Aguelmam Abekhane Inland lake Atlas — — X — — X — — Aguelmam Afennourir Inland lake Atlas X — X I X X X — Aguelmam Azegza Inland lake Atlas — — X — — X — — Aguelmam N’Tifounassine Inland lake Atlas X X X I X X — — Aguelmam Wiwane Inland lake Atlas — — X — — X — — Aguelmams Sidi Ali-Ta’nzoult Inland lake Atlas — X X — — X — — (a) 13 Baie d’Ad-Dakhla Bay South X X X D — X — — (b) Barrage Al Mansour Ad-Dahbi Artificial reservoir South — X X — — X X — Center (b) Barrage Al Massira Artificial reservoir X X X — X X X — Atlantic Center (b) Barrage de Wad Al Mellah Artificial reservoir — — X — — X — — Atlantic (b) 8 Barrage de Smir Artificial reservoir Northwest X — — — — X — — (b) Barrage Idriss Premier Artificial reservoir Northwest — X X — — X X — (b) Barrage Mohammed V Artificial reservoir Northeast X X X — X X X X Center (c) Cote ˆ et Archipel d’Essawira Coastal wetland X X X — — X X — Atlantic Dayet Ar-Roumi Inland lake Northwest — — X — — X — — 9 12 Dayet’Awa Inland lake Atlas X — X I X X X X 9 12 Dayet Hachlaf Inland lake Atlas X — — I X X — X 9 12 Dayet Ifrah Inland lake Atlas X — X I X X — X (d) Embouchure de Wad Al Wa’er River mouth South — — X — — X — — (d) Embouchure de Wad Assaka River mouth South — — X — X X X — (d) Embouchure de Wad Chbeyka River mouth South — X X — X X X — (d) Embouchure de Wad Dr’a River mouth South X — X — — — X — (d) Embouchure de Wad Malwiya River mouth Northeast X X X — — X X X (d) Embouchure de Wad Martil River mouth Northwest — X — — — X — — (d) 14 Embouchure de Wad Massa River mouth South X — — SM X X — — (e) 15 Lac de Tislite Inland lake Atlas X X HAO — X — — (e) 15 Lac d’Isly Inland lake Atlas X HAO — X — — Lagoon/ (f) 16 Lagune de Khnifiss South X X X K — — X — marshland Lagunes de Sidi Moussa- Lagoon/ Center X X X — X X — — (f) Walidia marshland Atlantic Center (g) Marais de Wad Al Maleh Marshland X — — — — X X — Atlantic (g) 8 Marais de Wad Smir Marshland Northwest X — — — — X X — (g) Marais du bas Loukkos Marshland Northwest X — — — — X X — Merja Al Halloufa Marshland Northwest X X X — — X — — Merja Bargha Marshland Northwest X X — — — X X X Merja Boukka Marshland Northwest — — X — X X — — Merja de Fouwarate Marshland Northwest X — X — — X X X Merja de Sidi Bou Ghaba Marshland Northwest X X X — X X X X Merja des Wlad Khallouf Marshland Northwest — — — — X X — — Merja des Wlad Skher Marshland Northwest X — X — — X X — Merja Zerga Marshland Northwest X X X — X X X — Mlalah du Bas Tahaddart Marshland Northwest X X X — X X — — (h) Plan d’eau de Dwiyate Inland lake Northwest — X X — — X X X (h) 11 Plan d’eau de Zerrouqa Inland lake Atlas X — X — — X — — Sebkha Bou Areg Lagoon Northeast — X X — X X X — Center Sebkha Zima Saline lake — X X — X X X — Atlantic Depression Center Sehb El Mejnoun — X X — — — X — wetland Atlantic Wad As-Saqia Al Hamra a` River South X X — — — X X — La’youn (a) (b) (c) (d) (e) (f) (g) (h) Baie � bay; Barrage � dam; Cote ˆ � coast; Archipel � archipelago; Embouchure � river mouth; Lac � lake; Lagune � lagoon; Marais � marsh; 1 2 3 4 Plan d’eau � waterbody. Important bird and biodiversity areas; Sites of Biological and Ecological Importance; national parks; permanent hunting reserves; 5 6 7 8 Common Pochard (Aythya ferina); Marbled Teal (Marmaronetta angustirostris); White-headed Duck (Oxyura leucocephala); Ramsar site: “Lagune et 9 10 11 12 barrage de Smir;” Ramsar site: “Lacs d’Imouzzer du Kandar;” Ramsar site: “Marais et Cote ˆ du Plateau de Rmel;” Ramsar site: “Oued Tizguite;” Ifrane 13 14 15 16 National Park; Dakhla National Park (project); Souss-Massa National Park; Haut Atlas Oriental National Park; Khnifiss National Park. 14 International Journal of Zoology Morocco is the excessive pumping [31], from artificial and conservation of this endangered waterbird and the resto- natural wetlands, as well as groundwater. &is leads to lower ration of a viable population on the long term. Similar water levels or even the drying-out of the wetlands, making it actions should be undertaken for the marble teal and the difficult for the species to thrive in such conditions. &e Common Pochard, as well as all globally threatened birds in other threats are mainly related to different disturbances that Morocco, targeting the specific threats for each species in can affect the species population directly (illegal or acci- each site. However, efforts must be deployed for a rigorous dental hunting and stray dogs that feed on ducklings or eggs) implementation of these conservation action plans and their or indirectly (recreational activities and inadequate man- evaluation on a regular basis. While the hunting of the agement policies). White-headed Duck and the Marbled Teal is prohibited, the Most of the key wintering wetlands of the three wa- Common Pochard can still be hunted. Given the current terfowls benefit from at least one conservation status. &e trend of this duck’s population, at the national and inter- attribution of these conservation statuses represents an national levels, more restrictions should be placed on its important step in their conservation. In fact, some of these hunting. sites also have management plans that allow enhanced land So far, we have discussed the populations’ changes and water management and the protection against an- inherent to factors at the national level. However, some of thropogenic threats. &is begs the following question: if the these changes can be related to factors at a larger scale and most important sites for the species benefit from conser- outside the national territory (e.g., threats and conser- vation statuses and measures, on what scale should we also vation measures in other countries). Furthermore, climate focus to improve the populations’ size? change and meteorological conditions can also have an impact on the national population. Kleijn et al. [76] have, for example, reported a positive correlation between 4.2. Conservation Stakes. For each of three species presented waterbirds’ population trends in Morocco and precipi- in this article, the population changes are often multifac- tations in the Sahel zone that may have a potential impact torial and can be in situ or ex situ. In fact, these ducks are on birds’ migratory strategies. &erefore, some pop- highly dependent on their habitats, especially during the ulations’ changes are probably more related to shifts in breeding season. As we have discussed above, any negative migratory routes and wintering areas than actual changes change, be it natural (e.g., drought and flood) or anthro- in birds’ numbers [76]. pogenic (e.g., drainage, vegetation cutting, and hydraulic More thorough research could lead to the exact reasons work) can potentially result in their decrease or redistri- behind the three studied ducks’ populations’ trends. Com- bution to other sites. &e designation of Ramsar and im- prehensive studies should be conducted to understand the portant bird and biodiversity sites is one of the important effects of ecological and anthropogenic factors on the distri- measures for the waterbirds and wetlands conservation and bution, abundance, and population dynamics of waterbirds’ among the good indicators of its success. In Morocco, 49 species [12], such as water quality, food availability, predation, wetlands are important bird biodiversity areas, 38 are weather, and conservation statuses. Furthermore, with the in- Ramsar sites, and at least 84 are Sites of Biological and creasing challenges that may hinder our monitoring programs Ecological Interest (SBEI), among which many are part of [77] and the effectiveness of conservation plans, we must de- national parks and/or permanent hunting reserves. While velop new effective methods for waterbirds’ census (wintering these statuses are important, if no ensuing effective man- and breeding populations) with more precision and coverage, agement plans are developed and implemented, their deg- coupled with other programs such as ringing-recovery/capture- radation, thus their biodiversity’s decline, is an inevitable recapture, continent/flyway, or region-wide series of aerial consequence, especially for those subject to many anthro- survey transects as has been suggested by Fox et al. (2019) [77]. pogenic pressures. &e Moroccan Department of Water and &is is crucial since the movements occurring within and be- Forestry has developed management plans for many wet- tween the regional populations of the species are still not well lands: some are finalized, and others are still in progress. &e understood. Large-scale information on birds’ populations’ implementation of these plans can face many challenges trends and habitats’ use is insufficient, which affects negatively inherent to the multiplicity of actors involved and the co- the conservation process [78]. Cooperative and coordinated operation of the local populations, whose livelihoods may efforts, such as the Mediterranean Waterbirds Network [79], are depend on the ecosystem services those wetlands provide. the key to improve data quality and quantity and to successful &e designation of SBEI in Morocco was a strategic measure and adequate conservation measures, for both waterbirds and and a starting point to prioritize the conservation of the wetlands. ecosystems with the highest biodiversity indices and hosting the most endangered, rare, or endemic species. But as we 5. Conclusions have pointed out above, the implementation of management and conservation action plans remains crucial. &rough this article, we presented the current status of three globally threatened waterfowls’ populations in Morocco. On the species’ level, the adoption of the National Law N 29–05, enforcing the CITES Convention, is a particularly While the White-headed Duck’s numbers are increasing and the Marbled Teal’s are mostly stable, the Common Pochard successful measure deterring all illegal actions threatening endangered species. Furthermore, the national action plan has known a decline in its wintering population and its breeding range is very limited in the country. for the White-headed Duck [31] is a crucial step to the International Journal of Zoology 15 Another important result of this synthesis is the iden- Supplementary Materials tification of the Moroccan wetlands that play a major role as Table S1. National counts of the Common Pochard’s win- hosting key sites of the three species. &ese results can direct tering individuals per year and per site. Table S2. National and focus the short-term conservation efforts on these key counts of the Marbled Teal’s wintering individuals per year sites, to enhance the survival and thriving of these species in and per site. Table S3. National counts of the White-headed Morocco. Duck’s wintering individuals per year and per site. Table S4. A better understanding of these ducks’ populations’ List of observers who contributed to the IWC program in dynamics, which is crucial to prevent their decline, requires Morocco between 1983 and 2019. (Supplementary Materials) further studies on the ecological and anthropogenic factors influencing them. Furthermore, cooperative efforts, coupled with more effective census methods, should be carried out to References enhance the knowledge on the species on the flyway/regional levels. &ese threatened waterbirds’ survival depends, in fact, [1] A. 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Journal

International Journal of ZoologyHindawi Publishing Corporation

Published: Jan 21, 2021

References