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New Data on Migration Time, Breeding Phenology, and Breeding Success of European Turtle Doves in Their Highest Breeding Habitats in North Africa

New Data on Migration Time, Breeding Phenology, and Breeding Success of European Turtle Doves in... Hindawi International Journal of Zoology Volume 2021, Article ID 6629285, 8 pages https://doi.org/10.1155/2021/6629285 Research Article New Data on Migration Time, Breeding Phenology, and Breeding Success of European Turtle Doves in Their Highest Breeding Habitats in North Africa 1 2 1 1 Ismail Mansouri , Driss Ousaaid , Wafae Squalli , Abdelbari El Agy, 1 3 1 Abderahim EL-Hassani, Mohamed Mounir , Lahsen Elghadraoui, and Mohamed Dakki Laboratory of Functional Ecology and Environment, Faculty of Sciences and Technology, Sidi Mohamed Ben Abdellah University, P.O. Box 2202, Imouzzer Street, Fez, Morocco Laboratory of Pharmacology and Environmental Health, Faculty of Science Dhar El Mahraz, USMBA Fez, B.P. 1796, Fez-Atlas 30003, Morocco Laboratory of Biotechnology and Valorisation of Phytogenetic Ressources, Faculty of Sciences and Technics, Sultan Moulay Sliman University, Beni Mellal, Morocco Laboratoire de G´eo-biodiversit´e et Patrimoine Naturel, Scientific Institute, Mohamed V University, Av. Ibn Battota, 10 BP 703, Rabat, Morocco Correspondence should be addressed to Ismail Mansouri; mankhori@gmail.com Received 10 November 2020; Revised 27 January 2021; Accepted 6 February 2021; Published 23 March 2021 Academic Editor: Hynek Burda Copyright © 2021 Ismail Mansouri 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. *e migration dates, breeding phenology, and reproductive success of the European turtle doves were studied in the highest breeding habitats at Midelt (1400 to 1600 m), Morocco. Data were recorded from March to October between 2015 and 2018, using the Common Bird Census methodology. Results showed that, at high-altitude breeding sites (n � 20), turtle doves arrived on 28.25± 2.05 March, while departure dates were on 28.00± 1.47 September. On the other hand, nesting activity began on 26.5± 0.64 April, and laying dates were only two days after the nest construction date on 28.00± 0.7 April. First fledged chicks were 17.50± 2.72 May, and chicks started flying on 3.50± 2.33 June. In addition, breeding chronology, including nesting and chick’s flight, was influenced by altitude and rainfall and more particularly controlled by temperature. For breeding success, among the 467 monitored nests, 73.87% survived during the nesting period and 71.16% of eggs have survived during incubation. Chicks’ survival rate was higher with 79.56%. Failure factors during breeding success were diverse. Predation caused the loss of 18.89% of eggs during incubation periods and 10.54% of chicks during the nestling phase. A few portions, including 4.41% of eggs and 4.39% of chicks, were deserted by their dove parents. Finally, our study highlights that the turtle dove breeds in high-altitude habitats with late and shorter breeding periods, which might allow this bird to avoid the vigorous climate conditions at mountains and their effect on reproductive success. this interconnectivity in conservation measures [5]. It is 1. Introduction becoming increasingly clear that the timing of spring mi- *e current advances in the study of avian migration have gration, breeding chronology, and feeding quality can underscored the important linkages between wintering, greatly influence reproductive success and population trends stopover, and breeding zones [1–4] and the need to consider [6–8], especially for long-distance migratory species [9]. 2 International Journal of Zoology highest breeding habitats. We examine the evidence that Birds are hypothesized to adopt their migration dates and breeding chronology in agreement with environmental elevations in altitudinal parameters have coincided with late migration dates and breeding chronology in doves as re- factors dominating in wintering and breeding grounds [10]. *is means that migration dates and breeding chronology ported in many other avian species. In the Western Atlantic were selected early and/or lately in order to avoid the harsh Red Knot (Calidris canutus rufa) and Savannah Sparrows conditions, counting temperatures, and rainfall of such (Passerculus sandwichensis), the migration and breeding habitat [11]. In fact, many Anatidae and Palearctic migrant chronology were late in high-altitude mountains and species have coincided their migration dates with suitable influenced rate of success [39, 40]. *erefore, if the change in spring climate conditions and food availability during breeding chronology occurs, then how it will influence breeding success in the ‘vulnerable’ turtle dove. summer in breeding quarters, in order to maximize their breeding success [12]. Since climate change, mainly high 2. Methods temperatures can result in missed foraging opportunities, loss of body condition, and impaired parental care [13]. Also, 2.1. Study Area. *e present study was carried out in Midelt avian responses to increasing temperatures may include ° ° province, Ait Ayach valley (32 41′N, 4 44′W) Morocco. *e breeding earlier in the season [14] or selecting cooler nest monitored sites were located at the Northern foot of Jbel microsites [15]. Ayachi Mountains, in the Molouya high plateau, 1400 to With the development of technologies, especially sat- 1600 m altitude above sea level (Figure 1). Midelt was ellite telemetry, the examination of individuals and their dominated by forests that cover 17095 ha, including Xero- migration and/or breeding strategies facing different cli- phytes with 4 772 ha, Holm oak 3375 ha, and Red juniper matic, as well as geographical conditions, has greatly ad- 2280 ha, while irrigated perimeter cover more than 1000 ha vanced with more abilities from wintering to breeding [33]. *e orchards were dominated by fruit trees, including grounds [16, 17]. However, the field monitoring of the apples, plums, and peach trees. strategies adopted by these populations needs an exhaustive In terms of climate, the temperature in Midelt ranges presence in the field [18, 19]. Additionally, many ecological ° ° from 8 to 21.2 C with an annual average of 16.9 C, and and biological aspects must be monitored for a long period precipitations vary largely between 65 mm and 481 mm from before conclusions. *is is particularly important in the case one year to another (data were extracted from 1957 to 2010 of rapidly declining species, where threatening factors are from Midelt Weather Station). All these characteristics, still unclear in both breeding and wintering zones [20, 21]. including vegetation cover and climatic parameters, would European turtle doves (Streptopelia turtur) are the only play a major role in the bioecology of the turtle dove. migrant Columbidae that winters in Sub-Saharan Africa and breeds in North Africa and Europe [22, 23]. Based on 2.2.DataCollection. Twenty apple orchards (7.47 ha in total) breeding and wintering areas, this game has undergone at Ait Ayach (Midelt) were selected and monitored during long-term declines, especially in Western Europe [24, 25]. four years, from 2015 to 2018. For each season, the survey of Over the past decades, the intensification of agriculture and dove’s arrival dates (first observed birds during spring) habitat loss are classified as principal causes leading to the started from early March and continued to the building of declining of turtle doves [22, 26, 27]. *ese factors cause a the first nest. Equally, departure dates (date of last observed failure of breeding success and reduction of migration ca- birds in the breeding site) were recorded at the leaving of the pacities. Although the breeding ecology and migration dates last birds from the whole breeding area. After the installation of turtle doves have been examined in detail [28,29], there of doves in the designated sites (after the arrival of breeding has been no comparable examination of the detailed pairs), the nest initiation (first nest recorded after the arrival breeding chronology and reproductive success in high-al- date), laying date (first egg after the nest initiation), hatching titude habitats [22]. In all previous studies, research con- (first fledged chick), and chicks’ nest leaving (first chick to cerning breeding ecology was limited to an altitude ranging leave its nest) were surveyed with three visits per month from 100 to 600 m in both Europe and North Africa (each visit with three days in field), based on turtle dove [22, 23, 30–37]. *erefore, understanding the migration and breeding biology reported in North Africa [30, 31, 41, 42]: (i) breeding phenology at high-altitude habitat will open a new the first visit was conducted at the beginning of every month, th th window in conservation measures, in particular with recent (ii) the second visit from 10 to 20 days, (iii) the third visit th th evidence indicating that turtle doves breed and feed in from 20 to 30 days. Common Bird Census (CBC) mountainous zones [22, 23]. In parallel, [38] have reported a methodology [36], instigated to provide sound and obser- significant shifting in migration dates and breeding chro- vational information on farmland bird populations in ag- nology between high and low altitude breeding sites. ricultural lands, was used and research took place from 06.00 *erefore, the clarification of migration dates and breeding to 18.00 hours. In our case, this methodology was adopted success, as well as the impact of the principal environmental inside apple orchards and nests or breeding pairs were factors dominating, will situate the high-altitude zones in researched line by line based on the tree lines of apple trees. terms of suitability, mainly rate of breeding success, and in In every single visit, recorded nests were monitored from the terms of habitat that deserves more attention in conservation construction to the nest leaving or nest failure. Furthermore, concern for declining doves. reproductive success rates were evaluated by the calculation In this paper, we present a four-year analysis of breeding of hatching eggs (hatched eggs/laid eggs), fledging, and phenology and migration dates of turtle doves in their flying chicks (chicks leaving their nests/fledged chicks). International Journal of Zoology 3 5°20′0″W 5°10′0″W 5°0′0″W 4°50′0″W 4°40′0″W 4°30′0″W 32°50′0″N 32°50′0″N 32°40′0″N 32°40′0″N 32°30′0″N 32°30′0″N 5°20′0″W 5°10′0″W 5°0′0″W 4°50′0″W 4°40′0″W 4°30′0″W Coordinate system: GCS WGS 1984 Datum: WGS 1984 Units: degree Ayt ayach valley Altitude value 906–1,314 Habitats 2,155–2,464 River 1,315–1,529 2,465–2,894 Floodplain 1,530–1,708 2,895–3,714 Hassan II Dam 1,709–1,910 City 1,911–2,154 Breeding orchards Figure 1: Studied orchards in Ait Ayach valley, Midelt province, Morocco, between 2015 and 2018. Moreover, failure factors were cited (basing on carcasses and Statistical analysis was performed using the STAT- other aspects, such as the status of the nest and feathers in or GRAPHICS Centurion software (version XVI.I), and graphs outside the nest) along with breeding stages, in order to were created by GraphPad Prism Mac 6.0 h software. compare between breeding phases. 3. Results 2.3. Data Analysis. *e normality of data was checked for all variables with the Kolmogorov–Smirnov test. Arrival and 3.1. Migration and Breeding Chronology. During four years, departure dates were defined and means were calculated (all the first arrival dates in spring were on 28.25± 2.05 March, arrival or departure dates during four years). Results were while the last doves were observed on 28.00± 1.47 Sep- given as mean± SD. Climatic conditions (temperature and tember at Midelt. On the other hand, turtle doves arrived rainfall) were accessed from the Midelt Weather Station solitary, particularly during the first weeks of April. After from 2015 to 2018. We analysed separately the relationship these periods, doves were observed in groups, especially in between breeding chronology, including nesting, laying, pairs. hatching, nest leaving and habitat characteristics, counting *e breeding chronology of turtle doves, including nest altitude, temperature, and rainfall by simple regression initiation, laying, fledging, and chick’s flying dates at Midelt (linear model), and all variables with P walue greater than is summarized in Figure 2. Nesting (initiation of nest 0.5 were eliminated. In parallel, the analysis of variance with construction) began during the last week of April at Midelt the lack-of-fit test was conducted to evaluate the best-fit for (26.5± 0.64 April), and the nesting period dated from 26 models by considering chronology (nesting, laying, hatch- April to 6 August. Similarly, laying dates were earlier, and ing, and nest leaving dates) as dependent variables and the first eggs were found on 28.00± 0.7 April, only two days habitat parameters (altitude, temperature, and rainfall) as after the nest construction date. *e last laying date was on factors. Rates of breeding success were compared between 12 August. On the other hand, the first fledged chicks were breeding phases, including nesting, laying, and rearing, via on 17.50± 2.72 May, and chicks started flying on 3.50± 2.33 one-way ANOVA test, considering twenty apple orchards. June. 4 International Journal of Zoology Nesting Laying 30 30 20 20 10 10 0 0 Dates (10 days) Dates (10 days) hatching nest leaving 40 30 0 0 Figure 2: Breeding chronology of turtle dove at Midelt between 2015 and 2018. (nesting: mean± SD number of nests by decades (10 days) from April to September; laying: mean± SD number of laid eggs by decades (10 days) from April to September; hatching: mean± SD number of hatched chicks by decades (10 days) from April to September; nest leaving: mean± SD number of chicks that survived by decades (10 days) from April to September). 3.2. Breeding Success. Among the 467 monitored nests at hatching dates) and climatic parameters at Midelt are Midelt (Table 1), only 73.87% were survived. During the summarized in Figure 3 and Table 2. *e breeding chro- incubation stage, the hatching success rate was 71.16%. In nology of turtle doves, mainly nesting dates were earlier with addition, during the rearing period, chicks’ survival rate was increasing temperatures. On the contrary, elevated altitudes and increasing temperatures shifted lately nesting and higher with 79.56% of chicks (n � 20 (orchards), F � 3.696, P � 0.031). On the other hand, failure factors of breeding fledging dates of turtle doves at Midelt. success were diverse. Predation presented the most risk menacing turtle dove’s breeding success, causing loss of 4. Discussion 18.89% of eggs during incubation periods and 10.54% of chicks during the nestling phase. Additionally, 5.03% of eggs Previous studies have noted that turtle doves breed in warm were unhatched and 5.49% of chicks have died inside their and lowlands, preferring farmlands and forests nests. Few portions, including 4.41% of eggs and 4.39% of [31, 40, 43–47]. However, no previous effort has been made chicks were deserted by their dove parents. to investigate the breeding attempt in high-altitude habitats, particularly in North Africa [29]. Our findings clearly indicate that the European turtle 3.3. Relationships between Breeding Parameters and Climatic doves breed in Midelt as a mountainous zone with an al- Conditions. *e relationships between the breeding chro- titude ranging between 1400 and 1600 m. *is species ar- nology of turtle doves (nest initiation, laying dates, and rived on 28.25± 2.05 March and started its breeding season Chicks Nests April-1 April-1 April-02 April-02 April-03 April-03 May-01 May-01 May-02 May-02 May-03 May-03 June-01 June-01 June-02 June-02 June-03 June-03 July-01 July-01 July-02 July-02 July-03 July-03 August-01 August-01 August-02 August-02 August-03 August-03 September-01 September-01 September-02 September-02 Chick’s leaving Eggs April-1 April-1 April-02 April-02 April-03 April-03 May-01 May-01 May-02 May-02 May-03 May-03 June-01 June-01 June-02 June-02 June-03 June-03 July-01 July-01 July-02 July-02 July-03 July-03 August-01 August-01 August-02 August-02 August-03 August-03 September-01 September-01 September-02 September-02 International Journal of Zoology 5 Table 1: Breeding success of turtle doves from 2015 to 2018 at Midelt, Morocco. Parameters Number % Total 467 100 Succeed 345 73.87 Nests Predated 98 20.98 Abandoned 24 5.14 Total 635 100 Succeed 455 71.16 Predated 120 18.89 Eggs Abandoned 28 4.41 Destruction 0 0 Unhatched 32 5.03 Total 455 100 Succeed 362 79.56 Chicks Predated 48 10.54 Died 25 5.49 Abandoned 20 4.39 29/03/18 03/03/18 28/03/17 28/03/17 27/03/16 27/03/16 26/03/15 26/03/15 25/03/15 25/03/15 Nesting = –10584.6 + 21.5499 ∗ altitude Nesting = –30535.8 – 610 ∗ temperature 24/03/15 24/03/15 1590 1600 1610 1620 1630 1640 1650 9.5 9.8 10.1 10.4 10.7 11 Altitude Temperature (a) (b) 29/03/18 09/06/18 Nesting = –24785.4 + 22.753.1 ∗ rainfall 07/06/17 28/03/17 05/06/16 27/03/16 03/06/15 26/03/15 01/06/15 25/03/15 28/05/15 Midelt = –31.8893 + 3.5722 ∗ temperature 24/03/15 28/05/15 17 18 19 20 21 0 10 20 30 40 Temperature Rainfall (c) (d) Figure 3: Relationship between the environmental factors and turtle dove chronology at Midelt during 2015 to 2018. (a) Between nesting dates and altitude. (b) Between Nesting dates and temperature. (c) Between nesting dates and rainfall. (d) Between nest leaving dates and temperatures (the lack of fit test is designed to determine whether the selected model is adequate to describe the observed data). Table 2: Models of the relationship between the breeding chronology of turtle doves (dates) and habitat conditions (altitude, temperature, and rainfall) during 2015 to 2018 (the lack of fit test is designed to determine whether the selected model is adequate to describe the observed variables). Model Sum of squares Df Mean square F P value Nesting × altitude 643077 1 643077 47.51 0.0204 Nesting × temperature 602802 1 602802 17.90 0.0516 Nesting × rainfall 248772 1 248772 1.18 0.3907 Nest leaving × temperature 88.1441 1 88.1441 38.27 0.0251 Nesting Nesting Nesting Nest leaving 6 International Journal of Zoology (a) (b) Figure 4: Predation of eggs (a) and chicks (b) of turtle doves in apple orchards during breeding seasons between 2015 and 2018. by nesting activity on 26.5± 0.64 April. *e laying period desertion of nests (5.14% of nests were deserted, counting 28 took place two days after nest initiation on 28.00± 0.7 April. eggs (4.41%) and 20 chicks (4.39%)). Furthermore, 32 eggs *is breeding chronology is in agreement with results cited were unhatched and 25 dead chicks were lost (chicks were by [33], while previous studies have noted a variation in the found died every cold morning). Similar results were cited in breeding chronology of turtle doves. At Tadla (514 m altitude Orange orchards. In fact, [29, 39, 48] have reported that the human disturbance in orange orchards at Tadla (150 km to and 150 km to Midelt), the first doves arrived early on 19± 0.6 March [48, 49], at Haouz (452 m altitude and Midelt) counting fruit harvesting, tree pruning, and the overuse of pesticides in coincidence with turtle dove 300 km to Midelt) 15 to 16 March [50], and in Moroccan North Atlantic (100 m above sea level and 450 km to Midelt) breeding periods, are the main factors causing nest 24± 0.16 March [51]. In all these preceding studies, par- desertion. ticularly those cited in low breeding sites (between 100 m and 514 m above sea level), nesting and laying dates ranged 5. Conclusion between 19 to 23 March and 10 to 20 April, respectively. *erefore, despite the limitation of this study to one high- In summary, this study provides a deep analysis of turtle altitude site, the cited literature confirms that the arrival and doves’ arrival dates, breeding chronology, and reproductive breeding chronology dates are later in high-altitude breeding success in its North African highest breeding zone. Results lands. At this point, the latitudinal influence on arrival and reveal the late arrival and breeding seasons in high-altitude breeding dates was excluded, because Tadla where Dove’s habitats compared to lowlands. However, breeding success chronology was earlier being in the same latitudinal level was similar between low- and high-altitude zones. All these with Midelt, while the northern Atlantic is in the North of strategies, including late arrival and breeding chronology, Midelt. *e suggested reason behind this late breeding prevent turtle doves against low temperatures in high chronology at Midelt is the environmental factors accom- habitats (protection of eggs and chicks) and human dis- panying the elevation of the altitude (Figure 3). In fact, high turbance in managed agricultural farms. temperatures and low rainfall promote an early nesting and check nest leaving (Table 2). Such results were mentioned in many other migratory birds [52–54]. In the barn swallow Data Availability (Hirundo rustica), the arrival dates vary from 12 April at 110 *e data used to support the findings of this study are in- altitude to 24 April at 760 m [55]. Furthermore, the tem- cluded within the article. perature was warm at lowlands and predicted the arrival dates of swallows. On the other hand, departure dates were on 28.00± 1.47 September, before the installation of cold Conflicts of Interest temperatures in dove’s breeding site. Across three breeding seasons, breeding success was *e authors declare that there are no conflicts of interest different from nesting to chicks rearing (Table 1). In total, regarding the publication of this paper. 71.16% of eggs were hatched, and 79.56% of chicks have flown. Moreover, 57% of chicks (flown chicks/laid eggs) have References flown at Midelt, which is comparable to previous results cited in other North African breeding habitats [35, 38, 45]. In [1] J. A. Gill, K. Norris, P. M. Potts, T. G. Gunnarsson, Algeria, the nesting success varies between 56% and 60.32% P. W. Atkinson, and W. J. Sutherland, “*e buffer effect and [36, 37, 46], and in Morocco success rate varies between 54,1 large-scale population regulation in migratory birds,” Nature, % and 55.5% [39, 48, 56]. 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New Data on Migration Time, Breeding Phenology, and Breeding Success of European Turtle Doves in Their Highest Breeding Habitats in North Africa

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Copyright © 2021 Ismail Mansouri et al. This 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.
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10.1155/2021/6629285
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Abstract

Hindawi International Journal of Zoology Volume 2021, Article ID 6629285, 8 pages https://doi.org/10.1155/2021/6629285 Research Article New Data on Migration Time, Breeding Phenology, and Breeding Success of European Turtle Doves in Their Highest Breeding Habitats in North Africa 1 2 1 1 Ismail Mansouri , Driss Ousaaid , Wafae Squalli , Abdelbari El Agy, 1 3 1 Abderahim EL-Hassani, Mohamed Mounir , Lahsen Elghadraoui, and Mohamed Dakki Laboratory of Functional Ecology and Environment, Faculty of Sciences and Technology, Sidi Mohamed Ben Abdellah University, P.O. Box 2202, Imouzzer Street, Fez, Morocco Laboratory of Pharmacology and Environmental Health, Faculty of Science Dhar El Mahraz, USMBA Fez, B.P. 1796, Fez-Atlas 30003, Morocco Laboratory of Biotechnology and Valorisation of Phytogenetic Ressources, Faculty of Sciences and Technics, Sultan Moulay Sliman University, Beni Mellal, Morocco Laboratoire de G´eo-biodiversit´e et Patrimoine Naturel, Scientific Institute, Mohamed V University, Av. Ibn Battota, 10 BP 703, Rabat, Morocco Correspondence should be addressed to Ismail Mansouri; mankhori@gmail.com Received 10 November 2020; Revised 27 January 2021; Accepted 6 February 2021; Published 23 March 2021 Academic Editor: Hynek Burda Copyright © 2021 Ismail Mansouri 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. *e migration dates, breeding phenology, and reproductive success of the European turtle doves were studied in the highest breeding habitats at Midelt (1400 to 1600 m), Morocco. Data were recorded from March to October between 2015 and 2018, using the Common Bird Census methodology. Results showed that, at high-altitude breeding sites (n � 20), turtle doves arrived on 28.25± 2.05 March, while departure dates were on 28.00± 1.47 September. On the other hand, nesting activity began on 26.5± 0.64 April, and laying dates were only two days after the nest construction date on 28.00± 0.7 April. First fledged chicks were 17.50± 2.72 May, and chicks started flying on 3.50± 2.33 June. In addition, breeding chronology, including nesting and chick’s flight, was influenced by altitude and rainfall and more particularly controlled by temperature. For breeding success, among the 467 monitored nests, 73.87% survived during the nesting period and 71.16% of eggs have survived during incubation. Chicks’ survival rate was higher with 79.56%. Failure factors during breeding success were diverse. Predation caused the loss of 18.89% of eggs during incubation periods and 10.54% of chicks during the nestling phase. A few portions, including 4.41% of eggs and 4.39% of chicks, were deserted by their dove parents. Finally, our study highlights that the turtle dove breeds in high-altitude habitats with late and shorter breeding periods, which might allow this bird to avoid the vigorous climate conditions at mountains and their effect on reproductive success. this interconnectivity in conservation measures [5]. It is 1. Introduction becoming increasingly clear that the timing of spring mi- *e current advances in the study of avian migration have gration, breeding chronology, and feeding quality can underscored the important linkages between wintering, greatly influence reproductive success and population trends stopover, and breeding zones [1–4] and the need to consider [6–8], especially for long-distance migratory species [9]. 2 International Journal of Zoology highest breeding habitats. We examine the evidence that Birds are hypothesized to adopt their migration dates and breeding chronology in agreement with environmental elevations in altitudinal parameters have coincided with late migration dates and breeding chronology in doves as re- factors dominating in wintering and breeding grounds [10]. *is means that migration dates and breeding chronology ported in many other avian species. In the Western Atlantic were selected early and/or lately in order to avoid the harsh Red Knot (Calidris canutus rufa) and Savannah Sparrows conditions, counting temperatures, and rainfall of such (Passerculus sandwichensis), the migration and breeding habitat [11]. In fact, many Anatidae and Palearctic migrant chronology were late in high-altitude mountains and species have coincided their migration dates with suitable influenced rate of success [39, 40]. *erefore, if the change in spring climate conditions and food availability during breeding chronology occurs, then how it will influence breeding success in the ‘vulnerable’ turtle dove. summer in breeding quarters, in order to maximize their breeding success [12]. Since climate change, mainly high 2. Methods temperatures can result in missed foraging opportunities, loss of body condition, and impaired parental care [13]. Also, 2.1. Study Area. *e present study was carried out in Midelt avian responses to increasing temperatures may include ° ° province, Ait Ayach valley (32 41′N, 4 44′W) Morocco. *e breeding earlier in the season [14] or selecting cooler nest monitored sites were located at the Northern foot of Jbel microsites [15]. Ayachi Mountains, in the Molouya high plateau, 1400 to With the development of technologies, especially sat- 1600 m altitude above sea level (Figure 1). Midelt was ellite telemetry, the examination of individuals and their dominated by forests that cover 17095 ha, including Xero- migration and/or breeding strategies facing different cli- phytes with 4 772 ha, Holm oak 3375 ha, and Red juniper matic, as well as geographical conditions, has greatly ad- 2280 ha, while irrigated perimeter cover more than 1000 ha vanced with more abilities from wintering to breeding [33]. *e orchards were dominated by fruit trees, including grounds [16, 17]. However, the field monitoring of the apples, plums, and peach trees. strategies adopted by these populations needs an exhaustive In terms of climate, the temperature in Midelt ranges presence in the field [18, 19]. Additionally, many ecological ° ° from 8 to 21.2 C with an annual average of 16.9 C, and and biological aspects must be monitored for a long period precipitations vary largely between 65 mm and 481 mm from before conclusions. *is is particularly important in the case one year to another (data were extracted from 1957 to 2010 of rapidly declining species, where threatening factors are from Midelt Weather Station). All these characteristics, still unclear in both breeding and wintering zones [20, 21]. including vegetation cover and climatic parameters, would European turtle doves (Streptopelia turtur) are the only play a major role in the bioecology of the turtle dove. migrant Columbidae that winters in Sub-Saharan Africa and breeds in North Africa and Europe [22, 23]. Based on 2.2.DataCollection. Twenty apple orchards (7.47 ha in total) breeding and wintering areas, this game has undergone at Ait Ayach (Midelt) were selected and monitored during long-term declines, especially in Western Europe [24, 25]. four years, from 2015 to 2018. For each season, the survey of Over the past decades, the intensification of agriculture and dove’s arrival dates (first observed birds during spring) habitat loss are classified as principal causes leading to the started from early March and continued to the building of declining of turtle doves [22, 26, 27]. *ese factors cause a the first nest. Equally, departure dates (date of last observed failure of breeding success and reduction of migration ca- birds in the breeding site) were recorded at the leaving of the pacities. Although the breeding ecology and migration dates last birds from the whole breeding area. After the installation of turtle doves have been examined in detail [28,29], there of doves in the designated sites (after the arrival of breeding has been no comparable examination of the detailed pairs), the nest initiation (first nest recorded after the arrival breeding chronology and reproductive success in high-al- date), laying date (first egg after the nest initiation), hatching titude habitats [22]. In all previous studies, research con- (first fledged chick), and chicks’ nest leaving (first chick to cerning breeding ecology was limited to an altitude ranging leave its nest) were surveyed with three visits per month from 100 to 600 m in both Europe and North Africa (each visit with three days in field), based on turtle dove [22, 23, 30–37]. *erefore, understanding the migration and breeding biology reported in North Africa [30, 31, 41, 42]: (i) breeding phenology at high-altitude habitat will open a new the first visit was conducted at the beginning of every month, th th window in conservation measures, in particular with recent (ii) the second visit from 10 to 20 days, (iii) the third visit th th evidence indicating that turtle doves breed and feed in from 20 to 30 days. Common Bird Census (CBC) mountainous zones [22, 23]. In parallel, [38] have reported a methodology [36], instigated to provide sound and obser- significant shifting in migration dates and breeding chro- vational information on farmland bird populations in ag- nology between high and low altitude breeding sites. ricultural lands, was used and research took place from 06.00 *erefore, the clarification of migration dates and breeding to 18.00 hours. In our case, this methodology was adopted success, as well as the impact of the principal environmental inside apple orchards and nests or breeding pairs were factors dominating, will situate the high-altitude zones in researched line by line based on the tree lines of apple trees. terms of suitability, mainly rate of breeding success, and in In every single visit, recorded nests were monitored from the terms of habitat that deserves more attention in conservation construction to the nest leaving or nest failure. Furthermore, concern for declining doves. reproductive success rates were evaluated by the calculation In this paper, we present a four-year analysis of breeding of hatching eggs (hatched eggs/laid eggs), fledging, and phenology and migration dates of turtle doves in their flying chicks (chicks leaving their nests/fledged chicks). International Journal of Zoology 3 5°20′0″W 5°10′0″W 5°0′0″W 4°50′0″W 4°40′0″W 4°30′0″W 32°50′0″N 32°50′0″N 32°40′0″N 32°40′0″N 32°30′0″N 32°30′0″N 5°20′0″W 5°10′0″W 5°0′0″W 4°50′0″W 4°40′0″W 4°30′0″W Coordinate system: GCS WGS 1984 Datum: WGS 1984 Units: degree Ayt ayach valley Altitude value 906–1,314 Habitats 2,155–2,464 River 1,315–1,529 2,465–2,894 Floodplain 1,530–1,708 2,895–3,714 Hassan II Dam 1,709–1,910 City 1,911–2,154 Breeding orchards Figure 1: Studied orchards in Ait Ayach valley, Midelt province, Morocco, between 2015 and 2018. Moreover, failure factors were cited (basing on carcasses and Statistical analysis was performed using the STAT- other aspects, such as the status of the nest and feathers in or GRAPHICS Centurion software (version XVI.I), and graphs outside the nest) along with breeding stages, in order to were created by GraphPad Prism Mac 6.0 h software. compare between breeding phases. 3. Results 2.3. Data Analysis. *e normality of data was checked for all variables with the Kolmogorov–Smirnov test. Arrival and 3.1. Migration and Breeding Chronology. During four years, departure dates were defined and means were calculated (all the first arrival dates in spring were on 28.25± 2.05 March, arrival or departure dates during four years). Results were while the last doves were observed on 28.00± 1.47 Sep- given as mean± SD. Climatic conditions (temperature and tember at Midelt. On the other hand, turtle doves arrived rainfall) were accessed from the Midelt Weather Station solitary, particularly during the first weeks of April. After from 2015 to 2018. We analysed separately the relationship these periods, doves were observed in groups, especially in between breeding chronology, including nesting, laying, pairs. hatching, nest leaving and habitat characteristics, counting *e breeding chronology of turtle doves, including nest altitude, temperature, and rainfall by simple regression initiation, laying, fledging, and chick’s flying dates at Midelt (linear model), and all variables with P walue greater than is summarized in Figure 2. Nesting (initiation of nest 0.5 were eliminated. In parallel, the analysis of variance with construction) began during the last week of April at Midelt the lack-of-fit test was conducted to evaluate the best-fit for (26.5± 0.64 April), and the nesting period dated from 26 models by considering chronology (nesting, laying, hatch- April to 6 August. Similarly, laying dates were earlier, and ing, and nest leaving dates) as dependent variables and the first eggs were found on 28.00± 0.7 April, only two days habitat parameters (altitude, temperature, and rainfall) as after the nest construction date. *e last laying date was on factors. Rates of breeding success were compared between 12 August. On the other hand, the first fledged chicks were breeding phases, including nesting, laying, and rearing, via on 17.50± 2.72 May, and chicks started flying on 3.50± 2.33 one-way ANOVA test, considering twenty apple orchards. June. 4 International Journal of Zoology Nesting Laying 30 30 20 20 10 10 0 0 Dates (10 days) Dates (10 days) hatching nest leaving 40 30 0 0 Figure 2: Breeding chronology of turtle dove at Midelt between 2015 and 2018. (nesting: mean± SD number of nests by decades (10 days) from April to September; laying: mean± SD number of laid eggs by decades (10 days) from April to September; hatching: mean± SD number of hatched chicks by decades (10 days) from April to September; nest leaving: mean± SD number of chicks that survived by decades (10 days) from April to September). 3.2. Breeding Success. Among the 467 monitored nests at hatching dates) and climatic parameters at Midelt are Midelt (Table 1), only 73.87% were survived. During the summarized in Figure 3 and Table 2. *e breeding chro- incubation stage, the hatching success rate was 71.16%. In nology of turtle doves, mainly nesting dates were earlier with addition, during the rearing period, chicks’ survival rate was increasing temperatures. On the contrary, elevated altitudes and increasing temperatures shifted lately nesting and higher with 79.56% of chicks (n � 20 (orchards), F � 3.696, P � 0.031). On the other hand, failure factors of breeding fledging dates of turtle doves at Midelt. success were diverse. Predation presented the most risk menacing turtle dove’s breeding success, causing loss of 4. Discussion 18.89% of eggs during incubation periods and 10.54% of chicks during the nestling phase. Additionally, 5.03% of eggs Previous studies have noted that turtle doves breed in warm were unhatched and 5.49% of chicks have died inside their and lowlands, preferring farmlands and forests nests. Few portions, including 4.41% of eggs and 4.39% of [31, 40, 43–47]. However, no previous effort has been made chicks were deserted by their dove parents. to investigate the breeding attempt in high-altitude habitats, particularly in North Africa [29]. Our findings clearly indicate that the European turtle 3.3. Relationships between Breeding Parameters and Climatic doves breed in Midelt as a mountainous zone with an al- Conditions. *e relationships between the breeding chro- titude ranging between 1400 and 1600 m. *is species ar- nology of turtle doves (nest initiation, laying dates, and rived on 28.25± 2.05 March and started its breeding season Chicks Nests April-1 April-1 April-02 April-02 April-03 April-03 May-01 May-01 May-02 May-02 May-03 May-03 June-01 June-01 June-02 June-02 June-03 June-03 July-01 July-01 July-02 July-02 July-03 July-03 August-01 August-01 August-02 August-02 August-03 August-03 September-01 September-01 September-02 September-02 Chick’s leaving Eggs April-1 April-1 April-02 April-02 April-03 April-03 May-01 May-01 May-02 May-02 May-03 May-03 June-01 June-01 June-02 June-02 June-03 June-03 July-01 July-01 July-02 July-02 July-03 July-03 August-01 August-01 August-02 August-02 August-03 August-03 September-01 September-01 September-02 September-02 International Journal of Zoology 5 Table 1: Breeding success of turtle doves from 2015 to 2018 at Midelt, Morocco. Parameters Number % Total 467 100 Succeed 345 73.87 Nests Predated 98 20.98 Abandoned 24 5.14 Total 635 100 Succeed 455 71.16 Predated 120 18.89 Eggs Abandoned 28 4.41 Destruction 0 0 Unhatched 32 5.03 Total 455 100 Succeed 362 79.56 Chicks Predated 48 10.54 Died 25 5.49 Abandoned 20 4.39 29/03/18 03/03/18 28/03/17 28/03/17 27/03/16 27/03/16 26/03/15 26/03/15 25/03/15 25/03/15 Nesting = –10584.6 + 21.5499 ∗ altitude Nesting = –30535.8 – 610 ∗ temperature 24/03/15 24/03/15 1590 1600 1610 1620 1630 1640 1650 9.5 9.8 10.1 10.4 10.7 11 Altitude Temperature (a) (b) 29/03/18 09/06/18 Nesting = –24785.4 + 22.753.1 ∗ rainfall 07/06/17 28/03/17 05/06/16 27/03/16 03/06/15 26/03/15 01/06/15 25/03/15 28/05/15 Midelt = –31.8893 + 3.5722 ∗ temperature 24/03/15 28/05/15 17 18 19 20 21 0 10 20 30 40 Temperature Rainfall (c) (d) Figure 3: Relationship between the environmental factors and turtle dove chronology at Midelt during 2015 to 2018. (a) Between nesting dates and altitude. (b) Between Nesting dates and temperature. (c) Between nesting dates and rainfall. (d) Between nest leaving dates and temperatures (the lack of fit test is designed to determine whether the selected model is adequate to describe the observed data). Table 2: Models of the relationship between the breeding chronology of turtle doves (dates) and habitat conditions (altitude, temperature, and rainfall) during 2015 to 2018 (the lack of fit test is designed to determine whether the selected model is adequate to describe the observed variables). Model Sum of squares Df Mean square F P value Nesting × altitude 643077 1 643077 47.51 0.0204 Nesting × temperature 602802 1 602802 17.90 0.0516 Nesting × rainfall 248772 1 248772 1.18 0.3907 Nest leaving × temperature 88.1441 1 88.1441 38.27 0.0251 Nesting Nesting Nesting Nest leaving 6 International Journal of Zoology (a) (b) Figure 4: Predation of eggs (a) and chicks (b) of turtle doves in apple orchards during breeding seasons between 2015 and 2018. by nesting activity on 26.5± 0.64 April. *e laying period desertion of nests (5.14% of nests were deserted, counting 28 took place two days after nest initiation on 28.00± 0.7 April. eggs (4.41%) and 20 chicks (4.39%)). Furthermore, 32 eggs *is breeding chronology is in agreement with results cited were unhatched and 25 dead chicks were lost (chicks were by [33], while previous studies have noted a variation in the found died every cold morning). Similar results were cited in breeding chronology of turtle doves. At Tadla (514 m altitude Orange orchards. In fact, [29, 39, 48] have reported that the human disturbance in orange orchards at Tadla (150 km to and 150 km to Midelt), the first doves arrived early on 19± 0.6 March [48, 49], at Haouz (452 m altitude and Midelt) counting fruit harvesting, tree pruning, and the overuse of pesticides in coincidence with turtle dove 300 km to Midelt) 15 to 16 March [50], and in Moroccan North Atlantic (100 m above sea level and 450 km to Midelt) breeding periods, are the main factors causing nest 24± 0.16 March [51]. In all these preceding studies, par- desertion. ticularly those cited in low breeding sites (between 100 m and 514 m above sea level), nesting and laying dates ranged 5. Conclusion between 19 to 23 March and 10 to 20 April, respectively. *erefore, despite the limitation of this study to one high- In summary, this study provides a deep analysis of turtle altitude site, the cited literature confirms that the arrival and doves’ arrival dates, breeding chronology, and reproductive breeding chronology dates are later in high-altitude breeding success in its North African highest breeding zone. Results lands. At this point, the latitudinal influence on arrival and reveal the late arrival and breeding seasons in high-altitude breeding dates was excluded, because Tadla where Dove’s habitats compared to lowlands. However, breeding success chronology was earlier being in the same latitudinal level was similar between low- and high-altitude zones. All these with Midelt, while the northern Atlantic is in the North of strategies, including late arrival and breeding chronology, Midelt. *e suggested reason behind this late breeding prevent turtle doves against low temperatures in high chronology at Midelt is the environmental factors accom- habitats (protection of eggs and chicks) and human dis- panying the elevation of the altitude (Figure 3). In fact, high turbance in managed agricultural farms. temperatures and low rainfall promote an early nesting and check nest leaving (Table 2). Such results were mentioned in many other migratory birds [52–54]. In the barn swallow Data Availability (Hirundo rustica), the arrival dates vary from 12 April at 110 *e data used to support the findings of this study are in- altitude to 24 April at 760 m [55]. Furthermore, the tem- cluded within the article. perature was warm at lowlands and predicted the arrival dates of swallows. On the other hand, departure dates were on 28.00± 1.47 September, before the installation of cold Conflicts of Interest temperatures in dove’s breeding site. Across three breeding seasons, breeding success was *e authors declare that there are no conflicts of interest different from nesting to chicks rearing (Table 1). In total, regarding the publication of this paper. 71.16% of eggs were hatched, and 79.56% of chicks have flown. Moreover, 57% of chicks (flown chicks/laid eggs) have References flown at Midelt, which is comparable to previous results cited in other North African breeding habitats [35, 38, 45]. In [1] J. A. Gill, K. Norris, P. M. Potts, T. G. Gunnarsson, Algeria, the nesting success varies between 56% and 60.32% P. W. Atkinson, and W. J. Sutherland, “*e buffer effect and [36, 37, 46], and in Morocco success rate varies between 54,1 large-scale population regulation in migratory birds,” Nature, % and 55.5% [39, 48, 56]. 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International Journal of ZoologyHindawi Publishing Corporation

Published: Mar 23, 2021

References