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Hindawi International Journal of Zoology Volume 2021, Article ID 8737951, 8 pages https://doi.org/10.1155/2021/8737951 Research Article Breeding Biology, Chronology, and Reproductive Success of the European Serin (Serinus serinus) at Moulouya High Plain (Morocco) 1 1 2 1 Ismail Mansouri , Wafae Squalli , Mohamed Dakki , Amine Assouguem , 1 1 1 3 Abdelbari El Agy , Abderahim El Hassani , Chaimae Belarbi, Youssef Dbiba, 4 1 Hassnae Kouali , and Lahsen El Ghadraoui Laboratory of Functional Ecology and Genie of Environment, Faculty of Sciences and Technology, Sidi Mohamed Ben Abdellah University, Fez, Morocco Laboratory of Go-Biodiversity and Naturel Patrimony, Scientiﬁc Institute, Mohammed V University, Av. Ibn Battota, 10 BP 703, Rabat, Morocco Laboratory of Water, Biodiversity and Climate Change, Faculty of Science, Cadi Ayyad University, Marrakech, Morocco Environnement & Health Research Team, Department of Biology Polydisciplinaire Faculty, Cadi Ayyad University, Marrakech, Morocco Correspondence should be addressed to Ismail Mansouri; email@example.com Received 9 April 2021; Revised 12 June 2021; Accepted 30 June 2021; Published 8 July 2021 Academic Editor: Marco Cucco 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 European serin (Serinus serinus) is one of the best examples of a species in the western Palaearctic that has expanded its distribution ranges in current periods. However, the breeding features of serin are not well known and were restricted for some localities, as well as there have not been any deep and comparable studies on its mortality and menacing factors. &is study investigates breeding biology, including breeding chronology, nesting strategies, and reproductive success of the European serin in farmland and woodland habitats at Moulouya high plain (Morocco), during 2016. Results showed that, at high-altitude breeding habitats, the European serin started breeding activity lately by 25 April (construction of the ﬁrst nest) and continued until 19 July (last ﬂedging date). Moreover, most nests (96.42%) were found in farmlands, mainly in apple orchards. Two broods were recorded between April-May and June-July, and the clutch size was an average of 3.04± 0.13 eggs/nest. For reproductive success, among the 65 examined nests, 73.84% were active during the nest construction phase and 87.42% of eggs have succeeded during the incubation phase. Reproductive success was higher (93.83%) during ﬂedging. Clutches were failed due to predation (15.9%), nest desertion (14.35%), and destruction of nests (8.88%). Finally, our study highlights that the European serin breeds in high- altitude zones with late and shorter breeding seasons, which might allow this bird to avoid high lands’ vigorous climate conditions and their eﬀect on breeding success. conservation procedures . On the other hand, the study of 1. Introduction breeding biology allows to estimate breeding success and Information on breeding biology and reproductive perfor- productivity, which are likely useful in population dynamics. mances of avian species constitutes a central part in the &e serin (Serinus serinus) is a small, socially monoga- understanding of their population bio-ecology and adap- mous ﬁnch [4, 5], common in southern Europe, North tation, as it permits the academics and wild defenders to Africa, and some western parts of Asia, which sings in- identify problems [1, 2]. Equally, it has direct implications in tensively throughout the breeding period. &e serin is one of 2 International Journal of Zoology the best examples of a species in the western Palaearctic that wild rose due to their small surfaces) to seven km (∼9 has expanded its distribution ranges in recent times . &e transects for visit in Salix dominating the area), from 06.00 breeding biology, chronology, and success of the serin are to 18.00 hours, based on the surface of each habitat. not well known and were limited for some localities, and We recorded the nest placement (ﬁve descriptors: nest there have not been any comparable studies on its mortality height above the ground, nest distance to the central trunk, and failure factors mainly in the south of the Mediterranean nest inside or in the periphery of orchard, and nesting-tree) Basin . and nest dimension (three descriptors: big diameter, small In North Africa, the European serin is reported as diameter, and depth). Similarly, breeding chronology (three resident and breeding species . In Algeria, the species is descriptors: nest construction date (initiation of the ﬁrst nest well studied in terms of distribution ranges, habitat use, and per season), laying date of the ﬁrst egg, and hatching date of breeding seasons [8–10]. While in Morocco, the bird is less the ﬁrst chick per season), nest status (three descriptors: studied, and most observations were fragmented in time and new-empty, egg incubation, hatching and chick rearing), space [11, 12]. However, with the recent changes in climatic and failure factors (four descriptors: predation, desertion, destruction (natural and/or human impacts), or death of the conditions, intensiﬁcation of agricultural activities, and il- legal capture and trade of wildlife species [13, 14], the clutch) were recorded. However, for nests discovered during knowledge of the features that could impact the breeding the incubation or chick rearing stages, laying date could not performance and survival of this small Fringillidae is ur- be determined with precision. We thus relied on the aspect gently required. of eggs or chicks (feathers of nestlings), and we used de- In this study, we used ﬁeld prospects to uncover breeding scriptive accounts from known-aged nests in the same performances of the European serin in diﬀerent ecosystems. population and area to determine the nest laying date ap- We analysed the patterns of breeding biology, breeding proximately. Similarly, the nature of predators was searched chronology, and nesting strategies inside farmlands and via shell, meat fragments, feathers, fresh animals, and human woodlands. More speciﬁcally, we studied nesting trees, nest traces inside or in the vicinity of nests. For example, rats location, breeding chronology (nest construction dates, typically leave eggshell fragments, while snakes feed on nests without leaving a trace . To reduce the impact of our laying dates, and hatching dates), and breeding success in orchards and woody vegetation. &ese aspects are suggested investigations on the monitored nests, we used an endo- to ﬁll the gap of lacking data about this tiny bird in Morocco scopic camera to check nest contents, and measurements and North Africa. (nest dimensions) were realised via vernier calipers, during the morning when birds look for food out of the nest. In parallel, climatic conditions (diurnal temperatures and 2. Materials and Methods rainfall) were accessed from the Midelt Weather Station during 2016, to assess their impact on breeding chronology. 2.1. Study Area. Fieldwork was conducted in the northwest Moulouya high plain, situated at Midelt Province, Daraa- Taﬁlalet region, between the High Atlas mountains in the 2.3. Statistics. Statistics were done in STATGRAPHICS North and Middle Atlas in the Northeast (Figure 1). Geo- Centurion software, version XVI.I, and results were given as graphically, the study zone was at a high altitude ranging sample size and mean± SD. Moreover, breeding success between 1300 and 1600 m upon sea level . &e Moulouya rates were evaluated by the calculation of success nests zone is characterized by a cold arid climate with a moun- (active nests/built nests), hatching eggs (hatched eggs/laid tainous tendency, and the rainfall regime is marked by a eggs), survived chicks (chicks leaving their nests/ﬂedged variable and irregular low rainfall; stormy precipitation chicks) [15–17]. Clutch size was calculated as the number of brings eroded products upstream, the annual average ° eggs/total active nests. Preferences toward nesting trees were temperature and precipitations being about 29 C and 89 mm calculated by percentage (number of nest per supporting successively. Two sites were selected: farmlands including 16 tree/all nests). apple orchards and woodlands counting riparian habitats We checked for normality and homogeneity of variance and forest plantation (small islets’ vegetation around agri- for all variables via Kolmogorov–Smirnov test. Correlations cultural areas) (Table 1). among breeding chronology parameters (nest construction period (from ﬁrst nest to the last nest), laying period (from ﬁrst egg to the last egg), and hatching period (from ﬁrst chick 2.2. Data Collection. Based on results mentioned in  and to the last chick) were tested with Pearson correlation co- preliminary ﬁeld prospections during 2015, we searched for eﬃcient. To assess diﬀerences in breeding success among nests from early March to late August 2016 by means of breeding phases (nest construction, laying, hatching) and parental behavioral cues (mainly, the courtship of the mating birds) and Common Birds Census (CBC) methodology , among failure factors (predation, desertion, destruction), the ANOVA One way test was used, considering the 16 breeding based on both the acoustic calls and the observation of birds during the breeding season. Inside farmlands, nests or habitats inside farmlands (for breeding success). We analysed separately the relationship between breeding chronology breeding pairs were researched line by line based on apple (depending variables), including nest construction period, orchards’ tree-lines [12, 15] (Figure 2). In woodlands, nests laying period, hatching period, temperature, and rainfall and breeding birds were searched with a walked transect of (factors) by General linear Model, and all variables with P ﬁve (two to three transects for visit in Tamarix, poplar and International Journal of Zoology 3 5°15′0″W 5°10′0″W 5°5′0″W 5°0′0″W 4°55′0″W 4°50′0″W 4°45′0″W 4°40′0″W 33°0′0″N 32°55′0″N 32°50′0″N 32°45′0″N 5°0′0″W 4°0′0″W 3°0′0″W 2°0′0″W 1°0′0″W 35°0′0″N 32°40′0″N 34°0′0″N 32°35′0″N 33°0′0″N 32°30′0″N 32°0′0″N Coordinate System: GCS WGS 1984 Datum: WGS 1984 Units: degree 32°25′0″N Floodplain Hassan II dam Moulouya watershed Figure 1: Localization of Moulouya high plain in Morocco. apple orchards, 81.35% of nests were located in the center of Table 1: Principal agricultural lands and woody vegetation monitored at Moulouya high plain. groves, while only 18.64% of nests were located in the pe- riphery (n � 16 orchards, t � 2.75357 P Habitat Type Vegetation Surfaces (Ha) value � 0.013) (Figure 3(b)). Salix 330 Generally, the Serin’s nests were cup-shaped, with an Riparian Tamarix 15 Woodland external diameter of 8.30± 0.29 cm (n � 65 nests), an internal Poplar 8 diameter of 7.03± 0.29 cm, and a cup depth of Forest Wild rose 14 5.82± 0.35 cm. Nest height above the ground was Farmland Orchards Apple trees 3.5 214.15± 0.09 cm and 95.4± 0.09 cm (n � 65 nests) far from the tree center trunk. values lesser than 0.5 were considered as predicting factors. To investigate the relevance of failure factors to 3.2. Breeding Chronology. &e breeding chronology of the impact the breeding success of the serin, during breeding European serin, including nesting, laying, and hatching phases, predation, desertion, destruction, death and un- dates at Moulouya, is summarized in Figure 4. After the hatched nests were considered as predictors of success formation of breeding pairs (based on acoustic courtship (response variables: with 0 (no ﬂedglings produced for nest, and visual mating), initiation of nest construction began no hatching of eggs, no occupation of nest) and 1 (at least during the last week of April at Midelt (the ﬁrst nest was one ﬂedgling produced for nest, at least one egg has hatched recorded on 25 April), and the nesting period dated from 25 and at least the nest was occupied for once), then a model April to 5 July (last new-built nest of the season). In parallel, with a binomial error structure and log it link function was laying activity was observed on 28 April (the ﬁrst egg), only applied. three days after the construction of the ﬁrst nest. &e last laying date was on 15 July and the laying period was 78 days. On the other hand, the ﬁrst observed chick was on 9 May, 3. Results and eggs’ hatching continues to 19 July. High correlations 3.1. Nesting Strategies. At the end of the breeding season, were revealed among breeding periods (Table 2). However, 96.42% of nests (n � 54) were recorded on orchards (50% on breeding periods were note inﬂuenced by temperatures and Golden delicious (n � 28 nests) and 46.42% Starkrimson rainfall (Table 3). At the end of breeding season, two broods delicious (n � 26 nests)) and 3.52% woodlands (1.78% on were observed; the ﬁrst between April and May, and the poplar and 1.78% on wild rose) (Figure 3(a)). Moreover, in second between June and July. 4 International Journal of Zoology Hedgerow Nest placement Apples Periphery Apple tree Golden delicious Central apple trees Hedgerow NDLC Starking NTH delicious NHG NDCT Nest morphology Nesting parameters NTH: nesting-tree height NHG: nest height above the ground NDLC: lower canopy distance NDCT: distance of nest to tree center NBD: nest big diameter NSD: nest small diameter NDP: nest cup depth Figure 2: Studied parameters, nesting sites, nest placement and morphology of the European serin in Moulouya. 30 60 20 40 10 20 0 0 Centre Periphery Golden Starkrimson Poplar Wild rose Nesting-trees Nest placement inside orchards (a) (b) Figure 3: (a) Nesting-tree and (b) nest placement of European serin at Moulouya high plain. 3.3. Clutch Size and Breeding Success. In summary, the Eu- total, success rates were higher during chicks rearing (n � 15, ropean serin’s clutch size ranged between three and ﬁve eggs F � 699.14, Df � 2, P< 0.001)(Figure 5). with a medium size of 3.04± 0.13 eggs. On the other hand, Failure factors were variable (Table 5). In summary, 15.9% among the 65 recorded nests (Table 4), 73.84% were suc- of clutches were failed due to predation attacks (7.69% of nests, ceeded (were active during all breeding phases) at Moulouya 4.79% of eggs, 3.42% of chicks), 14.35% of clutches were failed high plain. During the incubation period, the ﬂedging success due to nest desertion by parents (10.76% of nests, 3.59% of eggs) rate was more signiﬁcant, with 87.42% hatched eggs. Equally, and 8.88% of clutch due to destruction of nests (7.69% of nests, during the rearing phase, 93.83% of chicks have survived. In 1.19% of eggs) (n � 15 orchards, F � 1.08, Df � 2, P � 0.349). Nests Nests International Journal of Zoology 5 Dates (10 days) Nesting Laying Hatching Figure 4: Breeding chronology of the European serin at Moulouya high plain. Table 2: Pearson correlation coeﬃcients among breeding periods of the European serin at Moulouya high plain. Hatching (chicks) Laying (eggs) Nesting (nests) Hatching (chicks) — 0.7004 0.7494 P value — 0.0116 0.0069 Laying (eggs) 0.7004 — 0.9299 P value 0.0116 — 0.0008 Nesting (nests) 0.7494 0.9299 — P value 0.0069 0.0008 — Table 3: Relationship between breeding periods and climatic variables (rainfall and temperatures) analysed via General linear Model. Periods Factors Sum of squares Df Mean square F-ratio P value Rainfall 64.0168 1 64.0168 2.92 0.1157 Temperature 16.456 1 16.456 0.75 0.4051 Nest construction Residual 241.441 11 21.9492 Total (corrected) 337.214 13 Rainfall 104.636 1 104.636 0.55 0.4756 Temperature 0.713529 1 0.713529 0 0.9525 Laying periods Residual 2109.98 11 191.816 Total (corrected) 2580.93 13 Rainfall 246.61 1 246.61 1.81 0.2054 Temperature 152.906 1 152.906 1.12 0.3119 Hatching periods Residual 1497.31 11 136.119 Total (corrected) 1749.43 13 To date, it is known that the European serin is a resident- 4. Discussion breeding species in Morocco and Algeria [11, 18], since this &e study highlights the European Serin’s reproductive bird was recorded in forest areas and farmlands, mainly biology at Moulouya high plain Morocco, occupying oases [8, 19]. Similarly, in our case, nests of the European farmlands and woodlands. &ough a common species, the serin were found inside orchards and woodlands. However, study parameters were poorly studied in the area. the higher portion of nests was placed inside apple orchards Breeding activities April 02 April 03 May 01 May 02 May 03 June 01 June 02 June 03 July 01 July 02 July 03 August 01 August 02 August 03 6 International Journal of Zoology Table 4: Breeding success of the European Serin and failure factors at Moulouya high plain. Moulouya Phase Parameter Number % Total 65 100 Succeeded 48 73.84 Nests Predated 5 7.69 Deserted 7 10.76 Destructed 5 7.69 Total 167 100 Succeeded 146 87.42 Predated 8 4.79 Eggs Deserted 6 3.59 Destructed 2 1.19 Unhatched 5 2.99 Total 146 100 Succeeded 137 93.83 Chicks Predated 5 3.42 Died 4 2.73 Deserted 0 0 Box-and-Whisker plot Chicks Eggs Nests 71 76 81 86 91 96 101 Response Figure 5: Comparison (graphical ANOVA) of reproductive success among breeding phases (nest construction, laying of eggs, and hatching of chicks) at Moulouya. Table 5: Failure factors reducing the breeding success (success of chicks � emancipation of chicks, success of eggs � hatching of chicks, success of nests � occupied by the breeders) of the European serin. Estimate Standard error Wald test Intercept −0.075 0.334 2.253 0.007 Predation −0.236 0.039 6.452 0.032 Desertion −1.043 0.057 9.765 0.004 Nest construction Destruction −0.061 0.022 6.452 0.047 Unhatched −0.021 0.028 0.243 0.653 Scale 1.000 0.013 Intercept −1.164 0.432 3.321 0.034 Predation −1.522 0.027 10.634 0.001 Desertion 0.037 0.042 6.876 0.030 Hatching of eggs Destruction −0.011 0.012 0.735 0.621 Unhatched −1.832 0.037 10.536 0.001 Scale 1.000 0.043 Intercept −1.232 0.154 2.136 0.034 Predation −2.417 0.014 9.342 0.022 Emancipation of chicks Desertion −0.052 0.041 0.152 0.714 Died −1.062 0.003 10.016 0.026 Scale 1.000 0.043 in comparison with woody habitats. &e high incidence of study area [15, 20]. Additionally,  have reported the Serin inside apple orchards (on Golden delicious and breeding of Serin in apple orchards in Midelt province. On Starkrimson delicious) is related to their abundance in the the other hand, nests were cup-shaped, with small International Journal of Zoology 7 dimensions, and were placed at an important height above and population trends are needed to establish proper the ground to avoid ground stressors [21–23]. management strategies . Breeding activities of the European serin started during the last week of April (construction of ﬁrst nests) at Data Availability Moulouya high plain and continued till the second week of July (the hatching of last chicks). Our results are similar to &e data used to support the ﬁndings of this study are in- those cited in Europe, while they are diﬀerent from those cluded within the article. cited in North Africa. In Morocco (Marrakech, only 280 km to Moulouya) and in Algeria (Regha¨ ıa in North), serin Conflicts of Interest started breeding activities from February and March [8, 11], which is earlier by two months. On the contrary, in Europe, &e authors declare they have no conﬂicts of interest. mainly France and Spain, the breeding activities of the serin were between April and May [7, 8, 24], and these are close to Acknowledgments our results. However, the authors of [15, 16] have reported late breeding dates in other passerines, including the Eu- &e authors are grateful to their colleagues who helped in ropean turtle dove in the same area due to the eﬀect of collecting data. climatic conditions that delay breeding attempts in birds to avoid the vigorous climate in the area and its impact on broods [15, 16, 25]. To verify this issue, we have tested the References eﬀect of rainfall and temperatures on breeding periods (nest  A. Margalida, L. M. Gonzalez, ´ R. 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