New Data on Breeding Strategies and Reproductive Success of the Globally Threatened Turtle Dove Co-Occurring with the “Competitive” Collared Dove and the “Predatory” Maghreb Magpie in Olive Orchards

Wafae Squalli; Ismail Mansouri; Driss Ousaaid; Mohammed Hmidani; Hamid Achiban; Fatima Fadil; Mohamed Dakki

doi:10.1155/2022/2864178

New Data on Breeding Strategies and Reproductive Success of the Globally Threatened Turtle Dove Co-Occurring with the “Competitive” Collared Dove and the “Predatory” Maghreb Magpie in Olive Orchards

Squalli, Wafae;Mansouri, Ismail;Ousaaid, Driss;Hmidani, Mohammed;Achiban, Hamid;Fadil, Fatima;Dakki, Mohamed 2022-05-20 00:00:00 Hindawi International Journal of Zoology Volume 2022, Article ID 2864178, 11 pages https://doi.org/10.1155/2022/2864178 Research Article New Data on Breeding Strategies and Reproductive Success of the Globally Threatened Turtle Dove Co-Occurring with the “Competitive” Collared Dove and the “Predatory” Maghreb Magpie in Olive Orchards 1 1 2 1 Wafae Squalli , Ismail Mansouri , Driss Ousaaid , Mohammed Hmidani, 3 1 4 Hamid Achiban , Fatima Fadil, and Mohamed Dakki Laboratory of Functional Ecology and Genie of Environment, Faculty of Sciences and Technology, USMBA, Fez, Morocco Laboratory of Natural Substances, Pharmacology Environment, Modelisation, Health, and Quality of Life, Faculty of Sciences Dhar El Mahraz, University Sidi Mohamed Ben Abdellah, Fez, Morocco Laboratory of Geo-Environmental, Analysis Planning-Sustainable Development, Sidi Mohamed Ben Abdellah University, Fez, Morocco Laboratory of Go-Biodiversity and Naturel Patrimony, Scienti…c Institute, Mohammed V University, Av. Ibn Battota, 10 BP 703, Rabat, Morocco Correspondence should be addressed to Ismail Mansouri; mankhori@gmail.com Received 14 December 2021; Accepted 24 April 2022; Published 20 May 2022 Academic Editor: George A. Lozano Copyright © 2022 Wafae Squalli 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. Interactions between co-occurring species, including competition and predation, comprise critical processes regulating local community structure, habitat use, and diversity. We monitored nesting habitats, breeding chronology, and reproductive success rates to describe the patterns of spatiotemporal organization of three co-habiting species: the “native” turtle dove, the “invasive” collared dove, and the “predatory” Maghreb magpie. We de‡ned nesting site parameters, breeding chronology dates, and success rates to explain how these species are dispersed in space and time. Similarly, predation attacks were evaluated. Patterns of habitat use were best explained by fear of predation and competition. Both doves selected nesting sites far away from the predatory Magpie to protect their nests. Equally, sympatric Columbidae turtle dove and collared dove were segregated horizontally and vertically only in space to reduce competition inside olive orchards. On the other side, Maghreb magpie started the breeding activity ‡rst, most probably to bene‡t from food abundance targeted in doves’ nests (eggs and nestlings). Further, breeding success was higher in both doves, despite predation pressure exercised by the Magpie and other reptiles. Magpie nests were colonized by the great spotted cuckoo (Clamator glandarius). Finally, this study provides the ‡rst and only detailed data on nest-niche of the turtle dove co-occurring with competitor and predator species, in the entire Northwest Africa range. Additionally, our data provide an opportunity of large-scale comparative studies of the nesting niche and breeding performances of the turtle dove, collared dove, and Maghreb magpie complex. (−78%) [1, 2], Spain and Portugal (−70%) [3, 4], and Austria 1. Introduction (−54%) [4] between 1980 and 2020. Despite the ubiquity of Turtle dove Streptopelia turtur is the only long-distance dove distribution, the Asian population have also declined migratory Columbidae in the Western Palearctic that has [5]. In Europe, deterioration causes remain unclear [6]. su•ered a speedy and severe deterioration principally in the However, numerous factors have been suggested counting Northern slope of the Mediterranean. e European sub- intensive hunting [3], degradation breeding and foraging species S.. turtur has decreased severely in the Great Britain resources [7], and infection with parasites principally 2 International Journal of Zoology Trichomonas gallinae [8]. However, because impacting Atlas and Rif Mountainous chains, at an altitude of 600m. factors aﬀect diﬀerent stages in the life cycle of the turtle ,e monitored sites are bounded by diﬀerent aquatic eco- dove, more studies are needed to estimate the impact of each systems counting rivers (El Jawahir, Sebou, and Boufekrane) factor and involve other pressures counting predators and and dams (El Mahrez, Allal Fassi, and El Gaada dam) that invasive species [6] and these are suggested to increase the oﬀer required water sources (one of the most foraging el- eﬀectiveness of conservation measures [9]. ements conditioning the presence or absence of avian In North Africa, mainly in western zones, the turtle dove species). is a summer migrant and breeder [10–12]. Morocco hosts an Sa¨ıss plain is dominated by a semiarid climate with a important breeding population of doves, mainly Streptopelia strong continental impact. Annual precipitations are around turtur arenicola [13]. It is mostly observed in agricultural 800mm. Temperature varies widely between summer (July- ﬁelds that represent 1.5% of the total land area of Morocco August) dominated by hot temperatures (40–45 C) and cold [14–16] and woodland environments [17, 18] that represent winter (10–15 C). On the other hand, cereal crops (60%) 12.7% of the national surface [19]. In farmlands, breeding dominate the Saiss plain (main foraging seeds required by doves are mostly observed in irrigated perimeters dominated doves) and are used for both industrial purposes and food by oranges, olives, and apples [15, 20–22]. Despite its fa- beneﬁts. Cereals are dominated by wheat (Triticum turgidum vorable status when compared with European subspecies, and T. aestivum), maize (Zea mays), and fodder crops of S. t. arenicola is currently suﬀering from human stressors alfalfa (Medicago sativa). Orchards cover only 40% and are counting farming practices [21, 23] and natural enemies dominated by olives (Olea europaea) that occupy 14.4%. counting predators [24] and sympatric competitors [16, 25]. Olive orchards constituting potential nesting supports are In both farmlands and woodlands, S. t. arenicola is organized in form of patches (isolated farms or groups of mostly impacted by reptiles and raptors that attack breeding neighboring farms) throughout the plain. pairs and their clutches [21, 22]. ,ese natural enemies cause an annually loss of 15% to 30% of clutches in apples, olives, 2.2. Data Collection. Based on the previous observations of and orange orchards [15, 16, 24]. Equally, competitors, both doves in North African orchards [16] and the current principally sympatric Columbidae, were currently revealed breeding case of Magpie in olives [28], birds were partic- to impact negatively the breeding doves in Moroccan ularly monitored in olive orchards. Investigations of the farmlands [16, 24]. S. t. arenicola was dominated by invasive reproductive season were realized between the end of March collared dove (Streptopelia decaocto) [16], by sedentary and mid-September based on the phenological status of both laughing dove Streptopelia senegalensis [26], and by wood doves in Morocco [26]. ,ree potential olive orchards pigeon (Columba palumbus) [27] in agricultural and forest (Figure 1) were designated and monitored for two seasons ecosystems during breeding season. However, these studies (2017–2019). ,e selected olives were bordered by water did not clarify how the vulnerable migrant doves manage to streams and cereal plots (potential forage for both doves), in avoid the impacts of both predators and competitors on addition to a dump of Ain Lbida where magpies were ob- diﬀerent stages of the life cycle in breeding habitats, which is served regularly from 2015 (unpublished data). Each farm suggested to oﬀer more data for conservationists and policy was divided into two areas (based on roads in the marginal makers [14]. Equally, the investigation of cohabitation be- zones of orchard and farming personnel abundant in the tween vulnerable bird and its natural enemies is suggested to periphery) (Figure 2): central sector (olive trees inside the serve as great model in ecology for animal species. orchard close to the epicenter) and marginal sector (ﬁrst In this study, we used ﬁeld investigations to document three olive-tree-lines situated in the orchard boundaries). the interactions among the native “vulnerable” turtle dove Monitored farms were assigned with speciﬁc identiﬁers. (Streptopelia turtur arenicola), the “invasive-competitor” Moreover, all monitored variables including tree density, Eurasian collared dove (Streptopelia decaocto), and the tree-lines, and farming practices were similar between “predatory” Maghreb magpie (Pica mauritanica) in marginal and central sectors. ,e separation of two sectors is Northwest Africa. We analyzed the patterns of (i) nesting a practical way to search for segregation between two or site selection of these birds to examine whether they are more species nesting in the same plot [16]. segregated on some nest site characteristics, (ii) breeding Each week, when weather conditions were favorable chronology to investigate if there is any temporal segrega- (absence of rain and moderate temperatures), surveys tion, and (iii) reproductive success to evaluate the impact of started from 06h00 to 18h00. We managed to identify nests predation attacks and competition on reproductive rates of and their status (new, incubation, rearing, or failure). We the migrant dove. More speciﬁcally, we searched if turtle found that nests were localized via phone GPS (Geotracker) doves manage spatially and temporally to avoid completion in all monitored sectors/orchards and olive trees. A nest was and predation in its breeding habitats. counted active when incubating adults, at least one egg, at least one nestling, or droppings were detected. ,e position 2. Materials and Methods of each nesting tree was referenced and then reported in an Open Source GIS (Quantum GIS 3.14 (2020)). 2.1. Study Area. ,e study was conducted in the irrigated zone (357 000ha) of the Saiss farming plain, placed in the neighborhood of the Fez empirical city (Central Morocco, 2.3. Nesting Strategies. To describe nesting strategies, we Figure 1). ,e study sites are located between the Middle focused on nesting site variables: (i) two variables for International Journal of Zoology 3 5°31′30″W 5°30′0″W 5°28′30″W 5°40′0″W 5°30′0″W 5°20′0″W Study area 5°40′0″W 5°30′0″W 5°20′0″W Cereals TD+CD nesting orchad1; orchad 2 Inhabited orchads Dump Magpie; orchad 3 5°31′30″W 5°30′0″W 5°28′30″W Figure 1: Map showing the location of the Saıss plain and breeding orchards used by turtle dove (TD), collared dove (CD), and Maghreb magpie (MGP) in the surrounding area of the Fes historical city (Morocco). Periphery Central olive trees Center Periphery Periphery Central olive trees Figure 2: Schematic diagram showing the marginal and central zones of the monitored olive orchards in the Fez agricultural zone. delimitation of macrohabitat, including nesting orchards useful for coexisting species inside the same orchard, zone, and nest location inside or in the marginal zone of the farm and/or olive-tree), including nesting-olive-tree height (to diﬀerentiate potential cohabitating species); (ii) Seven (NTH), elevation of the nest above the ground (NHG), variables for microhabitat breeding locations (cm) (very distance to lower canopy (NDLC), and the distance 37°40′0″N 37°50′0″N 38°0′0″N 38°10′0″N 12 m (First three olive lines) 37°40′0″N 37°50′0″N 38°0′0″N 38°10′0″N 37°48′0″N 37°45′0″N 37°46′30″N 4 International Journal of Zoology Figure 3: Measured parameters for nest placement and morphology. separating nest and tree central trunk (NDCT); and (iii) nest laying periods or rearing stages, laying time could not be morphology variables (cm), including nest big axis (NBD), conﬁrmed with exactitude. We therefore based on the nest small axis (NSD), and nest cup depth (NDP) (Figure 3). feature of both eggs and chicks (i.e., feathers of nestlings) Nest dimensions were measured because we expected that and we relied on descriptive accounts of known-aged nest morphology will be variable depending on the presence clutches in the surrounding population and breeding site to of the competitor doves on the same tree or nesting zone. conclude nearly nest laying time and then nesting date. When there were no birds in a nest when located, the three variables for nest position and three variables for nest di- 2.5. Reproductive Success. Breeding success rates were mensions were immediately measured using a clinometer. If assessed by the calculation of succeeded nests (active nests/ a bird was present, these measurements were taken early in built nests), hatching eggs (hatched eggs/laid eggs), and the morning, when birds often leave the nest to look for survived chicks (chicks leaving their nests/hatched chicks). food. In parallel, failure factors, including predation, desertion, To explicate any potential segregation of breeding sites, and others were recorded. Further, the nature of predators distances separating nest location to the adjacent regional (to estimate the attacks of Magpie on both doves) was road (DR), nearest infrastructures (buildings, households, searched via shells, meat fragments, feathers, fresh animals, and farming storages) (DH), and nearby cereal farms (DC) and human traces inside or in the neighborhood of nests. For were estimated for each species with QGIS (distances were example, rats typically leave eggshell fragments, while snakes estimated based on displayed maps). Equally, we noted the feed on nests without leaving a trace [29]. supporting tree (ST), and we quantiﬁed the number of farmers (daily encountered workers) inside each orchard (NP) for each visit, as well as herbaceous cover under nesting 2.6. Statistics. We checked for normality and homogeneity olives (VUCN). ,ese variables were measured only for of variance for all variables via the Kolmogorov–Smirnov turtle and collared doves because of the similarity in their test. ,e one-way ANOVA test was used to assess diﬀerences ecological requirements, while the Maghreb magpie is very in nest placement and dimension among studied species. diﬀerent in terms of food requirements (feed in the dump Similarly, breeding success rates, including nest occupation and from other bird’ nests, which make foraging sites un- (active nests/built nests), laying (hatched eggs/laid eggs), and clear to estimate distances) and human impact (North Af- ﬂedging (chicks leaving their nests/hatched chicks) were rican populations nest always far from the highly populated analyzed with ANOVA. For all these parameters, we con- area), and these make diﬃcult to compare between Magpie sidered three nesting orchards and two breeding seasons. and doves. Statistics were done in STATGRAPHICS Centurion soft- ware, version XVII, and results were given as sample size and 2.4. Breeding Chronology. To describe any segregation in the mean±SD. On the other hand, nest-niche parameters were breeding chronology of bird species; (i) ﬁrst to last nests per compared only between doves due to their cohabitation season, (ii) ﬁrst eggs to last laying date per season, and (iii) inside the same orchards and the possibility to compare between their nesting parameters, while Maghreb magpie ﬁrst chicks to last hatching date per season were monitored for each bird. On the other hand, for nests detected after nests were isolated and have diﬀerent foraging sites. International Journal of Zoology 5 4°58′15″W 4°58′10″W 4°56′32″W 4°56′24″W Orchard 1 Orchard 2 W E W E 0 25 50 m 05025 m 4°58′15″W 4°58′10″W 4°56′32″W 4°56′24″W Tree Tree Nest of Turtle Dove Nest of Turtle Dove Nest of Collared Dove Nest of Collared Dove Figure 4: Map showing the nest location of turtle doves (Streptopelia turtur arenicola) and collared doves (Streptopelia decaocto) in olive orchards. chick has emancipated) and 0 (no chicks produced)), and To assess the main factors of nest-niche separation be- tween doves, distances separating nests of each bird to the examined via binomial error structure (generalized linear adjacent cereal farms (DC), adjacent vehicle road (DR), model) with a log it link function. adjacent infrastructure (homes or other constructions) (DH), active employees inside groves (NP) (documented for each visit), herbaceous cover under nesting-olives (VUCN) 3. Results (assessed by super‡cial covered by plants in the circle of three m around nesting tree), type of supporting tree (ST), 3.1. Nest-Niche Selection. Columbidae, turtle, and collared and the elevation of nesting-olives (NTH) were considered dove selected the same breeding habitats inside olive or- as illustrative factors (principal factors), while the nest chards N1 and N2, while the Maghreb magpie was isolated position in the central sector (OC) or in the peripheral sector alone inside orchard N3 (Figure 1). However, the migrant (OP) of the farms for each bird was counted as response dove selected mostly nesting trees in the central sector of the variables (1: nest located in the periphery or interior, 0: nest olive farms (87%; 96 nests), while the invasive dove selected not located in the periphery or interior), and were examined principally olive nesting trees in the marginal area of or- with PCA (only factors with eigenvalues >1.0 were chards (79%; 40 nests) (Figure 4). Further, turtle dove nests considered). were placed far from human impact, counting infrastruc- Similarly, to examine the relevance of threatening factors tures, roads, and farmers (Figure 5). On the opposite, the to in©uence the productivity of each bird during the collared dove nested close to infrastructures and in the areas breeding season, desertion, predation attacks, demolition, dominated by farmers. and infestation (only for magpie infested by the parasite) Breeding species selected di•erent nest positions on were counted as predictors of ©edging likelihood in olive-supporting trees (except distance from the nest to the Columbidae and magpie (responses: with 1 (at least one central trunk of the tree NDCT) (Table 1). Both doves 33°58′45″N 33°58′50″N 33°58′45″N 33°58′50″N 34°0′32″N 34°0′32″N 6 International Journal of Zoology Periphery of orchards Center of orchards Governing factors Figure 5: Segregation of nesting sites and supporting-trees (OC: center of the orchard; OP: periphery of the orchard) between turtle dove (TD) and collared dove (CD), and predicting factors of sampled nests (DC: distance to adjacent cereals; DH: distance to adjacent human infrastructure; DR: distance to adjacent road; NP: number of the employees in the orchard; NTH: nesting-tree-height; ST: supporting tree; VCUN: herbaceous plants under the nesting tree). Table 1: Comparison of nest placement and dimension (n �60 nests) parameters between dove species and magpie (mean±SE) was tested using one-way ANOVA. (NBD: big nest diameter, NDLC: distance between nest and the lower canopy, NDCT: distance of nest to tree center, NDP: nest depth, NSD: small nest diameter, NHG: nest height upon the ground, NTH: nesting tree height). Species Test Nesting parameters Turtle dove Collared dove Magpie F P NBD 18.65±2.60 17.80±3.87 25.90±1.79 23.791 P<0.001 NSD 15.05±2.65 14.58±3.51 20.00±.00 13.937 P<0.001 NDP 5.08±1.53 6.42±2.18 10.70±1.63 26.379 P<0.001 NDCT 106.10±38.28 116.70±34.58 92.00±15.95 1.579 0.225 NDLC 154.00±32.02 204.80±43.48 168.00±10.54 6.822 0.004 NHG 225.30±48.87 286.90±100.16 300.00±48.07 3.240 0.055 NTH 4.88±0.56 5.82±1.58 4.50±0.21 4.822 0.016 selected taller olive trees but nested at a lower height in 3.3.ReproductiveRatesandFailureFactors. Productivity was comparison with magpie. Similarly, nest dimensions were variable among monitored species (Table 2). Migrant and variables among species. Magpie nests were characterized by resident doves have the highest breeding success rates during nesting (N �7, DF �2, F �140.21, P<0.001), laying (N �7, grater dimensions, while doves’ nests were comparable and categorized by medium-sized platforms. DF �2, F �82.34, P<0.001), and ﬂedging phases (N �7, DF �2, F �12.79, P<0.001) in comparison with Maghreb magpie. However, the invasive dove showed the highest 3.2. Breeding Dates. ,e breeding timeline of studied spe- breeding success during nesting and laying phases in cies, counting nest construction, laying, and hatching dates comparison to the native dove. at Fez are summarized in (Figure 6). Magpie started nesting Predation, mainly magpie attacks were the most failure activities ﬁrst during the fourth week of March. Turtle dove causing loss of both doves’ clutches. Predators attacked and collared dove nesting dates were on the fourth week of 29.25% of turtle dove and 25.31% of collared dove clutches. April. Similarly, laying activities were earlier in Magpie Human disturbance, desertion, and destruction have caused (third week of April), while T. dove and C. dove were late loss of 18.98% and 5.83% of clutches in turtle doves, as well (second week of May). On the other hand, hatching dates as 13.45% and 2% of collared dove clutches successively. On were diﬀerent among studied birds. First chicks were the other hand, Maghreb magpie clutches were failed mainly recorded for the magpie (ﬁrst week of May), followed by due to desertion (38.46% of nests), destruction (15.38% of collared dove (fourth week of May) and later turtle dove nests), and parasitism (3.84% of nests, 20.83% of eggs, and (ﬁrst week of June). 25% of nestlings) (Table 3). International Journal of Zoology 7 Nesting Laying 150 200 0 0 Dates (10 days) Dates (10 days) TD: Turtle dove TD: Turtle dove CD: Collared dove CD: Collared dove MGP: Maghreb Magpie MGP: Maghreb Magpie Hatching Dates (10 days) TD: Turtle dove CD: Collared dove MGP: Maghreb Magpie Figure 6: Breeding chronology (nest construction, laying, and breeding dates) of turtle dove, collared dove, and Maghreb magpie at Fez between 2017 and 2019. ,is study revealed the signiﬁcant segregation of nest- 4. Discussion niche and breeding chronology between turtle doves and co- To our knowledge, this is the deep study of the nest-niche occurring collared dove and Maghreb magpie. Both doves ecology of the vulnerable turtle dove in the presence of its nested jointly in orchards N1 and N2, while the magpie was sympatric competitor and predator [16, 25]. Our main goal isolated in the orchard N3. Similarly, nest placement was was to provide comprehensive data on the segregation of diﬀerent among monitored birds. Despite the use of the nesting sites, breeding dates, and reproductive success of same orchards, T. doves have nested mainly on olive trees turtle dove co-occurring with collared dove and Maghreb situated in the central sector of the orchards, while C. dove magpie. ,ese ﬁndings are the ﬁrst and only provided results nests were abundant in the peripheral areas of the olive related to nest-niche ecology of turtle dove, collared dove, orchards. ,e spatial segregation between both doves and and magpie in Morocco and the entire Northwest African Maghreb magpie is suggested to separate between nests of zone, which is of great interest for future comparative studies both Columbidae and predatory Maghreb magpie consid- and the employment of a possible conservation plan of the ered as a direct predator for passerine birds [30], and to endangered Moroccan Turtle dove (globally threatened) and protect clutches from predation risk [31]. Moreover, the endemic North African Maghreb magpie populations. spatial segregation recorded between nests of both Nests Mar-04 April-01 April-02 April-03 April-04 May-01 May-02 Chicks May-03 May04 June-01 Mar-04 June-02 April-01 June-03 April-02 june04 April-03 July-01 April-04 July-02 May-01 July-03 May-02 May-03 Eggs May04 June-01 Mar-04 June-02 April-01 June-03 April-02 june04 pri A l-03 July-01 April-04 July-02 May-01 July-03 May-02 May-03 May04 June-01 June-02 June-03 june04 July-01 July-02 July-03 8 International Journal of Zoology Table 2: Comparison of breeding success and failure factors among turtle dove (n �120 nests), collared dove (n �50 nests), and magpie (n �26 nests) in olive orchards at Fez. Streptopelia turtur Streptopelia decaocto Pica mauritanica Phase Parameter Number % Number % Number % Total 120 100 50 100.00 26 100 Succeeded 93 77.75 39 78.00 5 19.23 Predated 9 07.5 6 12.00 0 0 Nests Deserted 11 09.16 4 08.00 10 38.46 Parasited 0 0 0 0 1 3.84 Destructed 7 05.83 1 02.00 4 15.38 Total 186 100 78 100.00 24 100 Succeeded 142 76.34 69 88.46 15 62.5 Predated 30 16.12 7 08.97 0 0 Eggs Deserted 10 5.37 2 02.56 0 0 Destructed 0 0 0 0.00 4 16.66 Parasited 0 0 0 0 5 20.83 Unhatched 4 5.03 0 0.00 0 0 Total 142 100 69 100.00 20 100 Succeeded 133 93.66 64 92.65 15 75 Predated 8 5.63 3 04.34 0 0 Chicks Died 1 00.70 0 0.00 0 0 Infested 0 0 0 0 5 25 Deserted 0 4.39 2 02.89 0 0 Table 3: Failure causes decreasing the probability to emancipate ﬂedglings of collared dove, turtle dove, and Maghreb magpie. Estimate Standard error Wald test P Intercept −1.084 0.421 3.231 <0.05 Predation −0.236 0.049 8.412 0.002 Desertion −1.045 0.038 4.786 0.034 Turtle dove Destruction −0.001 0.002 0.525 0.469 Unhatched 0.626 0.026 10.243 <0.001 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 Collared dove Destruction −0.011 0.012 0.735 0.621 Unhatched 0.116 0.056 11.183 0.431 Scale 1.000 0.044 Intercept −1.205 0.359 3.564 0.051 Predation −0.042 0.015 0.567 0.455 Desertion −0.056 0.032 0.631 0.513 Maghreb magpie Destruction −0.065 0.092 8.653 0.002 Parasitism −0.064 0.024 10.432 0.011 Scale 1.000 0.021 Columbidae is suggested to reduce competition between the comparison with both doves. Magpie started nesting ac- invasive collared dove and the native turtle dove, as men- tivities in March, while both doves initiated the construction tioned currently in Moroccan farmlands [16, 25], Algeria of their nests on the last week of April. Similarly, ﬁrst chicks [32], and previously in the west of the Iberian Peninsula [33], were occurred ﬁrstly for the magpie during May, followed by where the expansions of the invasive dove in urban areas collared dove and later the turtle dove. ,e early breeding have forced T. dove to select breeding sites far away in forest chronology recorded in the Maghreb magpie is most likely ecosystems, to avoid competition for available food and related to food abundance targeted in both doves’ nests; the nesting resources [1, 7]. In our case, the competition magpie started breeding activities ﬁrst to beneﬁt from eggs and nestlings of both doves (particularly late nests) to ensure avoidance is also achieved via vertical segregation recorded in nest placement; the collared dove selected nest placement suﬃcient food for its own nestlings (this is conﬁrmed in at a greater height and taller trees compared to turtle doves mentioned failure factors). ,ese earliest breeding dates as revealed currently by [16] in the same area. On the other have been mentioned in other predators; the boreal owl hand, Maghreb magpie breeding chronology was earlier in species start their breeding early to beneﬁt from the International Journal of Zoology 9 nests of both doves and other neighboring species. On the other hand, breeding success was higher in doves despite predation attacks conducted by the Maghreb magpie and human disturbance. Correspondingly, the intelligent strat- egy of early breeding adopted by the magpie is broken by parasitic colonization of its nests by the great spotted cuckoo. Finally, predation fear and competition avoidance were more important in explaining spatial partitioning of breeding habitats among studied species, while food avail- ability was more important in explaining temporal segre- gation. However, all these aspects, including the relationship between magpie attacks and breeding chronology of doves and potential segregation of foraging resources in co-oc- curring doves, need deep and close monitoring to get the real picture of these complex ecological issues. Data Availability Figure 7: Magpie nest totally colonized by the great spotted cuckoo. All necessary data are included within the article with clear careful statement. ,e full data are available from corre- sponding author upon reasonable request for any future abundance and availability of prey species’ nests (they attack studies. eggs and nestlings) [34]. On the other hand, the similarity of breeding chronology between competitive doves is expected Conflicts of Interest since these Columbidae are so close in their biological and ecological features include breeding [1, 7]. On behalf of all authors, the corresponding author states that Breeding success was signiﬁcantly higher in doves there are no conﬂicts of interest. compared to the magpie during all breeding stages. Clutches of both doves were highly threatened by predation attacks, Authors’ Contributions mainly from the magpie and reptiles, as well as from human disturbance, including olive-tree cutting and pulverization WS and IM conducted the ﬁeld work and collected all data. of pesticides in coincidence with breeding activities. ,ese IM, HA, and MH statistically analyzed data. FF, DO, and results conﬁrm the eﬀect of predation on both doves MD contributed to results’ interpretation. WS, IM, MD, and [15, 21, 24] and highlight the attacks conducted by the North FF were major contributors in writing the manuscript. All African magpie (despite the absence of precise statistical authors read and approved the ﬁnal manuscript. evidence, ﬁeld observations were suﬃcient to conﬁrm predation attacks). On the other hand, Maghreb magpie Acknowledgments clutches were lost mainly due to human disturbance and parasitism. Magpie nests were attacked and colonized by the ,e authors thank the owners of the farms for kindly great spotted cuckoo (Clamator glandarius) (Figure 7), and allowing them to work on their properties. ,is study was this is widely reported in Europe and recently in Africa, supported by the Regional Department of High Commission where the great spotted cuckoo (Clamator glandarius) is for Water, Forests and Desertiﬁcation Control, in Fez, considered as an obligate clutch parasite and the Eurasian Morocco. magpie (Pica pica) population as the regular host [28, 30, 35, 36] due to the lack of antiparasitic defenses. References [1] J. C. Dunn, J. E. Stockdale, R. J. Moorhouse-Gann et al., “,e 5. Conclusion decline of the turtle dove: dietary associations with body condition and competition with other columbids analysed ,is is the ﬁrst study providing deep insights into the using high-throughput sequencing,” Molecular Ecology, breeding habitat use, time partitioning, breeding success of vol. 27, no. 16, pp. 3386–3407, 2018. the native turtle dove co-occurring with the invasive collared [2] J. C. Dunn and A. J. Morris, “Which features of UK farmland dove and the predatory Maghreb magpie in Morocco and are important in retaining territories of the rapidly declining entire North Africa. We have shown that both doves select turtle dove Streptopelia turtur?” Bird Study, vol. 59, no. 4, nesting sites far away from the magpie to protect their pp. 394–402, 2012. clutches. Equally, competitive doves partitioned nesting sites [3] L. Moreno-Zarate, B. Arroyo, and W. 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Publisher: Hindawi Publishing Corporation
Copyright: Copyright © 2022 Wafae Squalli 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.
ISSN: 1687-8477
eISSN: 1687-8485
DOI: 10.1155/2022/2864178
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Abstract

Hindawi International Journal of Zoology Volume 2022, Article ID 2864178, 11 pages https://doi.org/10.1155/2022/2864178 Research Article New Data on Breeding Strategies and Reproductive Success of the Globally Threatened Turtle Dove Co-Occurring with the “Competitive” Collared Dove and the “Predatory” Maghreb Magpie in Olive Orchards 1 1 2 1 Wafae Squalli , Ismail Mansouri , Driss Ousaaid , Mohammed Hmidani, 3 1 4 Hamid Achiban , Fatima Fadil, and Mohamed Dakki Laboratory of Functional Ecology and Genie of Environment, Faculty of Sciences and Technology, USMBA, Fez, Morocco Laboratory of Natural Substances, Pharmacology Environment, Modelisation, Health, and Quality of Life, Faculty of Sciences Dhar El Mahraz, University Sidi Mohamed Ben Abdellah, Fez, Morocco Laboratory of Geo-Environmental, Analysis Planning-Sustainable Development, Sidi Mohamed Ben Abdellah University, Fez, Morocco Laboratory of Go-Biodiversity and Naturel Patrimony, Scienti…c Institute, Mohammed V University, Av. Ibn Battota, 10 BP 703, Rabat, Morocco Correspondence should be addressed to Ismail Mansouri; mankhori@gmail.com Received 14 December 2021; Accepted 24 April 2022; Published 20 May 2022 Academic Editor: George A. Lozano Copyright © 2022 Wafae Squalli 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. Interactions between co-occurring species, including competition and predation, comprise critical processes regulating local community structure, habitat use, and diversity. We monitored nesting habitats, breeding chronology, and reproductive success rates to describe the patterns of spatiotemporal organization of three co-habiting species: the “native” turtle dove, the “invasive” collared dove, and the “predatory” Maghreb magpie. We de‡ned nesting site parameters, breeding chronology dates, and success rates to explain how these species are dispersed in space and time. Similarly, predation attacks were evaluated. Patterns of habitat use were best explained by fear of predation and competition. Both doves selected nesting sites far away from the predatory Magpie to protect their nests. Equally, sympatric Columbidae turtle dove and collared dove were segregated horizontally and vertically only in space to reduce competition inside olive orchards. On the other side, Maghreb magpie started the breeding activity ‡rst, most probably to bene‡t from food abundance targeted in doves’ nests (eggs and nestlings). Further, breeding success was higher in both doves, despite predation pressure exercised by the Magpie and other reptiles. Magpie nests were colonized by the great spotted cuckoo (Clamator glandarius). Finally, this study provides the ‡rst and only detailed data on nest-niche of the turtle dove co-occurring with competitor and predator species, in the entire Northwest Africa range. Additionally, our data provide an opportunity of large-scale comparative studies of the nesting niche and breeding performances of the turtle dove, collared dove, and Maghreb magpie complex. (−78%) [1, 2], Spain and Portugal (−70%) [3, 4], and Austria 1. Introduction (−54%) [4] between 1980 and 2020. Despite the ubiquity of Turtle dove Streptopelia turtur is the only long-distance dove distribution, the Asian population have also declined migratory Columbidae in the Western Palearctic that has [5]. In Europe, deterioration causes remain unclear [6]. su•ered a speedy and severe deterioration principally in the However, numerous factors have been suggested counting Northern slope of the Mediterranean. e European sub- intensive hunting [3], degradation breeding and foraging species S.. turtur has decreased severely in the Great Britain resources [7], and infection with parasites principally 2 International Journal of Zoology Trichomonas gallinae [8]. However, because impacting Atlas and Rif Mountainous chains, at an altitude of 600m. factors aﬀect diﬀerent stages in the life cycle of the turtle ,e monitored sites are bounded by diﬀerent aquatic eco- dove, more studies are needed to estimate the impact of each systems counting rivers (El Jawahir, Sebou, and Boufekrane) factor and involve other pressures counting predators and and dams (El Mahrez, Allal Fassi, and El Gaada dam) that invasive species [6] and these are suggested to increase the oﬀer required water sources (one of the most foraging el- eﬀectiveness of conservation measures [9]. ements conditioning the presence or absence of avian In North Africa, mainly in western zones, the turtle dove species). is a summer migrant and breeder [10–12]. Morocco hosts an Sa¨ıss plain is dominated by a semiarid climate with a important breeding population of doves, mainly Streptopelia strong continental impact. Annual precipitations are around turtur arenicola [13]. It is mostly observed in agricultural 800mm. Temperature varies widely between summer (July- ﬁelds that represent 1.5% of the total land area of Morocco August) dominated by hot temperatures (40–45 C) and cold [14–16] and woodland environments [17, 18] that represent winter (10–15 C). On the other hand, cereal crops (60%) 12.7% of the national surface [19]. In farmlands, breeding dominate the Saiss plain (main foraging seeds required by doves are mostly observed in irrigated perimeters dominated doves) and are used for both industrial purposes and food by oranges, olives, and apples [15, 20–22]. Despite its fa- beneﬁts. Cereals are dominated by wheat (Triticum turgidum vorable status when compared with European subspecies, and T. aestivum), maize (Zea mays), and fodder crops of S. t. arenicola is currently suﬀering from human stressors alfalfa (Medicago sativa). Orchards cover only 40% and are counting farming practices [21, 23] and natural enemies dominated by olives (Olea europaea) that occupy 14.4%. counting predators [24] and sympatric competitors [16, 25]. Olive orchards constituting potential nesting supports are In both farmlands and woodlands, S. t. arenicola is organized in form of patches (isolated farms or groups of mostly impacted by reptiles and raptors that attack breeding neighboring farms) throughout the plain. pairs and their clutches [21, 22]. ,ese natural enemies cause an annually loss of 15% to 30% of clutches in apples, olives, 2.2. Data Collection. Based on the previous observations of and orange orchards [15, 16, 24]. Equally, competitors, both doves in North African orchards [16] and the current principally sympatric Columbidae, were currently revealed breeding case of Magpie in olives [28], birds were partic- to impact negatively the breeding doves in Moroccan ularly monitored in olive orchards. Investigations of the farmlands [16, 24]. S. t. arenicola was dominated by invasive reproductive season were realized between the end of March collared dove (Streptopelia decaocto) [16], by sedentary and mid-September based on the phenological status of both laughing dove Streptopelia senegalensis [26], and by wood doves in Morocco [26]. ,ree potential olive orchards pigeon (Columba palumbus) [27] in agricultural and forest (Figure 1) were designated and monitored for two seasons ecosystems during breeding season. However, these studies (2017–2019). ,e selected olives were bordered by water did not clarify how the vulnerable migrant doves manage to streams and cereal plots (potential forage for both doves), in avoid the impacts of both predators and competitors on addition to a dump of Ain Lbida where magpies were ob- diﬀerent stages of the life cycle in breeding habitats, which is served regularly from 2015 (unpublished data). Each farm suggested to oﬀer more data for conservationists and policy was divided into two areas (based on roads in the marginal makers [14]. Equally, the investigation of cohabitation be- zones of orchard and farming personnel abundant in the tween vulnerable bird and its natural enemies is suggested to periphery) (Figure 2): central sector (olive trees inside the serve as great model in ecology for animal species. orchard close to the epicenter) and marginal sector (ﬁrst In this study, we used ﬁeld investigations to document three olive-tree-lines situated in the orchard boundaries). the interactions among the native “vulnerable” turtle dove Monitored farms were assigned with speciﬁc identiﬁers. (Streptopelia turtur arenicola), the “invasive-competitor” Moreover, all monitored variables including tree density, Eurasian collared dove (Streptopelia decaocto), and the tree-lines, and farming practices were similar between “predatory” Maghreb magpie (Pica mauritanica) in marginal and central sectors. ,e separation of two sectors is Northwest Africa. We analyzed the patterns of (i) nesting a practical way to search for segregation between two or site selection of these birds to examine whether they are more species nesting in the same plot [16]. segregated on some nest site characteristics, (ii) breeding Each week, when weather conditions were favorable chronology to investigate if there is any temporal segrega- (absence of rain and moderate temperatures), surveys tion, and (iii) reproductive success to evaluate the impact of started from 06h00 to 18h00. We managed to identify nests predation attacks and competition on reproductive rates of and their status (new, incubation, rearing, or failure). We the migrant dove. More speciﬁcally, we searched if turtle found that nests were localized via phone GPS (Geotracker) doves manage spatially and temporally to avoid completion in all monitored sectors/orchards and olive trees. A nest was and predation in its breeding habitats. counted active when incubating adults, at least one egg, at least one nestling, or droppings were detected. ,e position 2. Materials and Methods of each nesting tree was referenced and then reported in an Open Source GIS (Quantum GIS 3.14 (2020)). 2.1. Study Area. ,e study was conducted in the irrigated zone (357 000ha) of the Saiss farming plain, placed in the neighborhood of the Fez empirical city (Central Morocco, 2.3. Nesting Strategies. To describe nesting strategies, we Figure 1). ,e study sites are located between the Middle focused on nesting site variables: (i) two variables for International Journal of Zoology 3 5°31′30″W 5°30′0″W 5°28′30″W 5°40′0″W 5°30′0″W 5°20′0″W Study area 5°40′0″W 5°30′0″W 5°20′0″W Cereals TD+CD nesting orchad1; orchad 2 Inhabited orchads Dump Magpie; orchad 3 5°31′30″W 5°30′0″W 5°28′30″W Figure 1: Map showing the location of the Saıss plain and breeding orchards used by turtle dove (TD), collared dove (CD), and Maghreb magpie (MGP) in the surrounding area of the Fes historical city (Morocco). Periphery Central olive trees Center Periphery Periphery Central olive trees Figure 2: Schematic diagram showing the marginal and central zones of the monitored olive orchards in the Fez agricultural zone. delimitation of macrohabitat, including nesting orchards useful for coexisting species inside the same orchard, zone, and nest location inside or in the marginal zone of the farm and/or olive-tree), including nesting-olive-tree height (to diﬀerentiate potential cohabitating species); (ii) Seven (NTH), elevation of the nest above the ground (NHG), variables for microhabitat breeding locations (cm) (very distance to lower canopy (NDLC), and the distance 37°40′0″N 37°50′0″N 38°0′0″N 38°10′0″N 12 m (First three olive lines) 37°40′0″N 37°50′0″N 38°0′0″N 38°10′0″N 37°48′0″N 37°45′0″N 37°46′30″N 4 International Journal of Zoology Figure 3: Measured parameters for nest placement and morphology. separating nest and tree central trunk (NDCT); and (iii) nest laying periods or rearing stages, laying time could not be morphology variables (cm), including nest big axis (NBD), conﬁrmed with exactitude. We therefore based on the nest small axis (NSD), and nest cup depth (NDP) (Figure 3). feature of both eggs and chicks (i.e., feathers of nestlings) Nest dimensions were measured because we expected that and we relied on descriptive accounts of known-aged nest morphology will be variable depending on the presence clutches in the surrounding population and breeding site to of the competitor doves on the same tree or nesting zone. conclude nearly nest laying time and then nesting date. When there were no birds in a nest when located, the three variables for nest position and three variables for nest di- 2.5. Reproductive Success. Breeding success rates were mensions were immediately measured using a clinometer. If assessed by the calculation of succeeded nests (active nests/ a bird was present, these measurements were taken early in built nests), hatching eggs (hatched eggs/laid eggs), and the morning, when birds often leave the nest to look for survived chicks (chicks leaving their nests/hatched chicks). food. In parallel, failure factors, including predation, desertion, To explicate any potential segregation of breeding sites, and others were recorded. Further, the nature of predators distances separating nest location to the adjacent regional (to estimate the attacks of Magpie on both doves) was road (DR), nearest infrastructures (buildings, households, searched via shells, meat fragments, feathers, fresh animals, and farming storages) (DH), and nearby cereal farms (DC) and human traces inside or in the neighborhood of nests. For were estimated for each species with QGIS (distances were example, rats typically leave eggshell fragments, while snakes estimated based on displayed maps). Equally, we noted the feed on nests without leaving a trace [29]. supporting tree (ST), and we quantiﬁed the number of farmers (daily encountered workers) inside each orchard (NP) for each visit, as well as herbaceous cover under nesting 2.6. Statistics. We checked for normality and homogeneity olives (VUCN). ,ese variables were measured only for of variance for all variables via the Kolmogorov–Smirnov turtle and collared doves because of the similarity in their test. ,e one-way ANOVA test was used to assess diﬀerences ecological requirements, while the Maghreb magpie is very in nest placement and dimension among studied species. diﬀerent in terms of food requirements (feed in the dump Similarly, breeding success rates, including nest occupation and from other bird’ nests, which make foraging sites un- (active nests/built nests), laying (hatched eggs/laid eggs), and clear to estimate distances) and human impact (North Af- ﬂedging (chicks leaving their nests/hatched chicks) were rican populations nest always far from the highly populated analyzed with ANOVA. For all these parameters, we con- area), and these make diﬃcult to compare between Magpie sidered three nesting orchards and two breeding seasons. and doves. Statistics were done in STATGRAPHICS Centurion soft- ware, version XVII, and results were given as sample size and 2.4. Breeding Chronology. To describe any segregation in the mean±SD. On the other hand, nest-niche parameters were breeding chronology of bird species; (i) ﬁrst to last nests per compared only between doves due to their cohabitation season, (ii) ﬁrst eggs to last laying date per season, and (iii) inside the same orchards and the possibility to compare between their nesting parameters, while Maghreb magpie ﬁrst chicks to last hatching date per season were monitored for each bird. On the other hand, for nests detected after nests were isolated and have diﬀerent foraging sites. International Journal of Zoology 5 4°58′15″W 4°58′10″W 4°56′32″W 4°56′24″W Orchard 1 Orchard 2 W E W E 0 25 50 m 05025 m 4°58′15″W 4°58′10″W 4°56′32″W 4°56′24″W Tree Tree Nest of Turtle Dove Nest of Turtle Dove Nest of Collared Dove Nest of Collared Dove Figure 4: Map showing the nest location of turtle doves (Streptopelia turtur arenicola) and collared doves (Streptopelia decaocto) in olive orchards. chick has emancipated) and 0 (no chicks produced)), and To assess the main factors of nest-niche separation be- tween doves, distances separating nests of each bird to the examined via binomial error structure (generalized linear adjacent cereal farms (DC), adjacent vehicle road (DR), model) with a log it link function. adjacent infrastructure (homes or other constructions) (DH), active employees inside groves (NP) (documented for each visit), herbaceous cover under nesting-olives (VUCN) 3. Results (assessed by super‡cial covered by plants in the circle of three m around nesting tree), type of supporting tree (ST), 3.1. Nest-Niche Selection. Columbidae, turtle, and collared and the elevation of nesting-olives (NTH) were considered dove selected the same breeding habitats inside olive or- as illustrative factors (principal factors), while the nest chards N1 and N2, while the Maghreb magpie was isolated position in the central sector (OC) or in the peripheral sector alone inside orchard N3 (Figure 1). However, the migrant (OP) of the farms for each bird was counted as response dove selected mostly nesting trees in the central sector of the variables (1: nest located in the periphery or interior, 0: nest olive farms (87%; 96 nests), while the invasive dove selected not located in the periphery or interior), and were examined principally olive nesting trees in the marginal area of or- with PCA (only factors with eigenvalues >1.0 were chards (79%; 40 nests) (Figure 4). Further, turtle dove nests considered). were placed far from human impact, counting infrastruc- Similarly, to examine the relevance of threatening factors tures, roads, and farmers (Figure 5). On the opposite, the to in©uence the productivity of each bird during the collared dove nested close to infrastructures and in the areas breeding season, desertion, predation attacks, demolition, dominated by farmers. and infestation (only for magpie infested by the parasite) Breeding species selected di•erent nest positions on were counted as predictors of ©edging likelihood in olive-supporting trees (except distance from the nest to the Columbidae and magpie (responses: with 1 (at least one central trunk of the tree NDCT) (Table 1). Both doves 33°58′45″N 33°58′50″N 33°58′45″N 33°58′50″N 34°0′32″N 34°0′32″N 6 International Journal of Zoology Periphery of orchards Center of orchards Governing factors Figure 5: Segregation of nesting sites and supporting-trees (OC: center of the orchard; OP: periphery of the orchard) between turtle dove (TD) and collared dove (CD), and predicting factors of sampled nests (DC: distance to adjacent cereals; DH: distance to adjacent human infrastructure; DR: distance to adjacent road; NP: number of the employees in the orchard; NTH: nesting-tree-height; ST: supporting tree; VCUN: herbaceous plants under the nesting tree). Table 1: Comparison of nest placement and dimension (n �60 nests) parameters between dove species and magpie (mean±SE) was tested using one-way ANOVA. (NBD: big nest diameter, NDLC: distance between nest and the lower canopy, NDCT: distance of nest to tree center, NDP: nest depth, NSD: small nest diameter, NHG: nest height upon the ground, NTH: nesting tree height). Species Test Nesting parameters Turtle dove Collared dove Magpie F P NBD 18.65±2.60 17.80±3.87 25.90±1.79 23.791 P<0.001 NSD 15.05±2.65 14.58±3.51 20.00±.00 13.937 P<0.001 NDP 5.08±1.53 6.42±2.18 10.70±1.63 26.379 P<0.001 NDCT 106.10±38.28 116.70±34.58 92.00±15.95 1.579 0.225 NDLC 154.00±32.02 204.80±43.48 168.00±10.54 6.822 0.004 NHG 225.30±48.87 286.90±100.16 300.00±48.07 3.240 0.055 NTH 4.88±0.56 5.82±1.58 4.50±0.21 4.822 0.016 selected taller olive trees but nested at a lower height in 3.3.ReproductiveRatesandFailureFactors. Productivity was comparison with magpie. Similarly, nest dimensions were variable among monitored species (Table 2). Migrant and variables among species. Magpie nests were characterized by resident doves have the highest breeding success rates during nesting (N �7, DF �2, F �140.21, P<0.001), laying (N �7, grater dimensions, while doves’ nests were comparable and categorized by medium-sized platforms. DF �2, F �82.34, P<0.001), and ﬂedging phases (N �7, DF �2, F �12.79, P<0.001) in comparison with Maghreb magpie. However, the invasive dove showed the highest 3.2. Breeding Dates. ,e breeding timeline of studied spe- breeding success during nesting and laying phases in cies, counting nest construction, laying, and hatching dates comparison to the native dove. at Fez are summarized in (Figure 6). Magpie started nesting Predation, mainly magpie attacks were the most failure activities ﬁrst during the fourth week of March. Turtle dove causing loss of both doves’ clutches. Predators attacked and collared dove nesting dates were on the fourth week of 29.25% of turtle dove and 25.31% of collared dove clutches. April. Similarly, laying activities were earlier in Magpie Human disturbance, desertion, and destruction have caused (third week of April), while T. dove and C. dove were late loss of 18.98% and 5.83% of clutches in turtle doves, as well (second week of May). On the other hand, hatching dates as 13.45% and 2% of collared dove clutches successively. On were diﬀerent among studied birds. First chicks were the other hand, Maghreb magpie clutches were failed mainly recorded for the magpie (ﬁrst week of May), followed by due to desertion (38.46% of nests), destruction (15.38% of collared dove (fourth week of May) and later turtle dove nests), and parasitism (3.84% of nests, 20.83% of eggs, and (ﬁrst week of June). 25% of nestlings) (Table 3). International Journal of Zoology 7 Nesting Laying 150 200 0 0 Dates (10 days) Dates (10 days) TD: Turtle dove TD: Turtle dove CD: Collared dove CD: Collared dove MGP: Maghreb Magpie MGP: Maghreb Magpie Hatching Dates (10 days) TD: Turtle dove CD: Collared dove MGP: Maghreb Magpie Figure 6: Breeding chronology (nest construction, laying, and breeding dates) of turtle dove, collared dove, and Maghreb magpie at Fez between 2017 and 2019. ,is study revealed the signiﬁcant segregation of nest- 4. Discussion niche and breeding chronology between turtle doves and co- To our knowledge, this is the deep study of the nest-niche occurring collared dove and Maghreb magpie. Both doves ecology of the vulnerable turtle dove in the presence of its nested jointly in orchards N1 and N2, while the magpie was sympatric competitor and predator [16, 25]. Our main goal isolated in the orchard N3. Similarly, nest placement was was to provide comprehensive data on the segregation of diﬀerent among monitored birds. Despite the use of the nesting sites, breeding dates, and reproductive success of same orchards, T. doves have nested mainly on olive trees turtle dove co-occurring with collared dove and Maghreb situated in the central sector of the orchards, while C. dove magpie. ,ese ﬁndings are the ﬁrst and only provided results nests were abundant in the peripheral areas of the olive related to nest-niche ecology of turtle dove, collared dove, orchards. ,e spatial segregation between both doves and and magpie in Morocco and the entire Northwest African Maghreb magpie is suggested to separate between nests of zone, which is of great interest for future comparative studies both Columbidae and predatory Maghreb magpie consid- and the employment of a possible conservation plan of the ered as a direct predator for passerine birds [30], and to endangered Moroccan Turtle dove (globally threatened) and protect clutches from predation risk [31]. Moreover, the endemic North African Maghreb magpie populations. spatial segregation recorded between nests of both Nests Mar-04 April-01 April-02 April-03 April-04 May-01 May-02 Chicks May-03 May04 June-01 Mar-04 June-02 April-01 June-03 April-02 june04 April-03 July-01 April-04 July-02 May-01 July-03 May-02 May-03 Eggs May04 June-01 Mar-04 June-02 April-01 June-03 April-02 june04 pri A l-03 July-01 April-04 July-02 May-01 July-03 May-02 May-03 May04 June-01 June-02 June-03 june04 July-01 July-02 July-03 8 International Journal of Zoology Table 2: Comparison of breeding success and failure factors among turtle dove (n �120 nests), collared dove (n �50 nests), and magpie (n �26 nests) in olive orchards at Fez. Streptopelia turtur Streptopelia decaocto Pica mauritanica Phase Parameter Number % Number % Number % Total 120 100 50 100.00 26 100 Succeeded 93 77.75 39 78.00 5 19.23 Predated 9 07.5 6 12.00 0 0 Nests Deserted 11 09.16 4 08.00 10 38.46 Parasited 0 0 0 0 1 3.84 Destructed 7 05.83 1 02.00 4 15.38 Total 186 100 78 100.00 24 100 Succeeded 142 76.34 69 88.46 15 62.5 Predated 30 16.12 7 08.97 0 0 Eggs Deserted 10 5.37 2 02.56 0 0 Destructed 0 0 0 0.00 4 16.66 Parasited 0 0 0 0 5 20.83 Unhatched 4 5.03 0 0.00 0 0 Total 142 100 69 100.00 20 100 Succeeded 133 93.66 64 92.65 15 75 Predated 8 5.63 3 04.34 0 0 Chicks Died 1 00.70 0 0.00 0 0 Infested 0 0 0 0 5 25 Deserted 0 4.39 2 02.89 0 0 Table 3: Failure causes decreasing the probability to emancipate ﬂedglings of collared dove, turtle dove, and Maghreb magpie. Estimate Standard error Wald test P Intercept −1.084 0.421 3.231 <0.05 Predation −0.236 0.049 8.412 0.002 Desertion −1.045 0.038 4.786 0.034 Turtle dove Destruction −0.001 0.002 0.525 0.469 Unhatched 0.626 0.026 10.243 <0.001 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 Collared dove Destruction −0.011 0.012 0.735 0.621 Unhatched 0.116 0.056 11.183 0.431 Scale 1.000 0.044 Intercept −1.205 0.359 3.564 0.051 Predation −0.042 0.015 0.567 0.455 Desertion −0.056 0.032 0.631 0.513 Maghreb magpie Destruction −0.065 0.092 8.653 0.002 Parasitism −0.064 0.024 10.432 0.011 Scale 1.000 0.021 Columbidae is suggested to reduce competition between the comparison with both doves. Magpie started nesting ac- invasive collared dove and the native turtle dove, as men- tivities in March, while both doves initiated the construction tioned currently in Moroccan farmlands [16, 25], Algeria of their nests on the last week of April. Similarly, ﬁrst chicks [32], and previously in the west of the Iberian Peninsula [33], were occurred ﬁrstly for the magpie during May, followed by where the expansions of the invasive dove in urban areas collared dove and later the turtle dove. ,e early breeding have forced T. dove to select breeding sites far away in forest chronology recorded in the Maghreb magpie is most likely ecosystems, to avoid competition for available food and related to food abundance targeted in both doves’ nests; the nesting resources [1, 7]. In our case, the competition magpie started breeding activities ﬁrst to beneﬁt from eggs and nestlings of both doves (particularly late nests) to ensure avoidance is also achieved via vertical segregation recorded in nest placement; the collared dove selected nest placement suﬃcient food for its own nestlings (this is conﬁrmed in at a greater height and taller trees compared to turtle doves mentioned failure factors). ,ese earliest breeding dates as revealed currently by [16] in the same area. On the other have been mentioned in other predators; the boreal owl hand, Maghreb magpie breeding chronology was earlier in species start their breeding early to beneﬁt from the International Journal of Zoology 9 nests of both doves and other neighboring species. On the other hand, breeding success was higher in doves despite predation attacks conducted by the Maghreb magpie and human disturbance. Correspondingly, the intelligent strat- egy of early breeding adopted by the magpie is broken by parasitic colonization of its nests by the great spotted cuckoo. Finally, predation fear and competition avoidance were more important in explaining spatial partitioning of breeding habitats among studied species, while food avail- ability was more important in explaining temporal segre- gation. However, all these aspects, including the relationship between magpie attacks and breeding chronology of doves and potential segregation of foraging resources in co-oc- curring doves, need deep and close monitoring to get the real picture of these complex ecological issues. Data Availability Figure 7: Magpie nest totally colonized by the great spotted cuckoo. All necessary data are included within the article with clear careful statement. ,e full data are available from corre- sponding author upon reasonable request for any future abundance and availability of prey species’ nests (they attack studies. eggs and nestlings) [34]. On the other hand, the similarity of breeding chronology between competitive doves is expected Conflicts of Interest since these Columbidae are so close in their biological and ecological features include breeding [1, 7]. On behalf of all authors, the corresponding author states that Breeding success was signiﬁcantly higher in doves there are no conﬂicts of interest. compared to the magpie during all breeding stages. Clutches of both doves were highly threatened by predation attacks, Authors’ Contributions mainly from the magpie and reptiles, as well as from human disturbance, including olive-tree cutting and pulverization WS and IM conducted the ﬁeld work and collected all data. of pesticides in coincidence with breeding activities. ,ese IM, HA, and MH statistically analyzed data. FF, DO, and results conﬁrm the eﬀect of predation on both doves MD contributed to results’ interpretation. WS, IM, MD, and [15, 21, 24] and highlight the attacks conducted by the North FF were major contributors in writing the manuscript. All African magpie (despite the absence of precise statistical authors read and approved the ﬁnal manuscript. evidence, ﬁeld observations were suﬃcient to conﬁrm predation attacks). On the other hand, Maghreb magpie Acknowledgments clutches were lost mainly due to human disturbance and parasitism. Magpie nests were attacked and colonized by the ,e authors thank the owners of the farms for kindly great spotted cuckoo (Clamator glandarius) (Figure 7), and allowing them to work on their properties. ,is study was this is widely reported in Europe and recently in Africa, supported by the Regional Department of High Commission where the great spotted cuckoo (Clamator glandarius) is for Water, Forests and Desertiﬁcation Control, in Fez, considered as an obligate clutch parasite and the Eurasian Morocco. magpie (Pica pica) population as the regular host [28, 30, 35, 36] due to the lack of antiparasitic defenses. References [1] J. C. Dunn, J. E. Stockdale, R. J. Moorhouse-Gann et al., “,e 5. 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Journal

International Journal of Zoology – Hindawi Publishing Corporation

Published: May 20, 2022

References

The decline of the turtle dove: dietary associations with body condition and competition with other columbids analysed using high-throughput sequencing,

J. C. Dunn, J. E. Stockdale, R. J. Moorhouse-Gann et al.
Which features of UK farmland are important in retaining territories of the rapidly declining turtle dove Streptopelia turtur?

J. C. Dunn and A. J. Morris
Effectiveness of hunting regulations for the conservation of a globally-threatened species: the case of the European turtle-dove in Spain,

L. Moreno-Zarate, B. Arroyo, and W. Peach
Spatial heterogeneity in population change of the globally threatened European turtle dove in Spain: the role of environmental favourability and land use,

L. M. Zarate, A. Estrada, W. Peach, and B. Arroyo
European turtle-dove (Streptopelia turtur)—bird life species factsheet,

Birdlife International
The historical and socioeconomic perspective of calcareous grasslands—lessons from the distant and recent past,

P. Poschlod and M. F. WallisDeVries
Breeding habitat use and conservation status of the turtle dove Streptopelia turtur in northern Spain,

M. S. D. Buruaga, A. Onrubia, J. M. Fernández-García, M. Á. Campos, F. Canales, and J. M. Unamuno
The protozoan parasite Trichomonas gallinae causes adult and nestling mortality in a declining population of European turtle doves, Streptopelia turtur,

J. E. Stockdale, J. C. Dunn, S. J. Goodman et al.
Distribution of the European turtle dove (Streptopelia turtur) at the edge of the south-western palaearctic: transboundary differences and conservation prospects,

J. L. Tellería, R. Carbonell, G. Fandos et al.
Avifauna diversity in the gate between humid Atlas and saharan desert: midelt province, Morocco,

I. Mansouri, W. Squalli, A. El Agy et al.
Analysis of Moroccan breeding and wintering population of the vulnerable European turtle dove Streptopelia turtur: breeding habitats, wintering sites, and governing factors,

I. Mansouri, W. Squalli, A. E. Agy et al.
The European turtle-dove Streptopelia turtur in northwest Africa: a review of current knowledge and priorities for future research,

S. Hanane
Migratory dates, breeding phenology, and reproductive success of European turtle doves between lowlands and highest breeding habitats in north Africa,

I. Mansouri, M. Mounir, W. Squalli, L. Elhanafi, M. Dakki, and L. El Ghadraoui
Macro-habitat, micro-habitat segregation and breeding success of the “vulnerable

W. Squalli, I. Mansouri, A. El Hassani et al.
Birds of cork oak forest of ma’amora (Morocco): phenology, status of breeding species and evolution since the beginning of the 20th century,

S. I. Cherkaoui, M. Dakki, R. I. Hamid, and M. Thévenot
Le grand livre de la forêt marocaine,

O. Mhirit and P. Blerot
Diversity of feeding habitats and diet composition in the turtle doves Streptopelia turtur to buffer loss and modification of natural habitats during breeding season,

I. Mansouri, M. K. Al-Sadoon, M. Rochdi, B. A. Paray, M. Dakki, and L. Elghadraoui
The turtle dove (Streptopelia turtur) in midelt plain, Morocco: nesting preferences and breeding success versus the impact of predation and agricultural practices,

I. Mansouri, D. Ousaaid, W. Squalli, H. Sqalli, L. E. Ghadraoui, and M. Dakki
Chronologie de la reproduction de la tourterelle des bois Streptopelia turtur arenicola dans la région de taroudant (maroc),

A. EL Hassani, M. Dakki, and L. El Ghadraoui
Effects of location, orchard type, breeding period and nest position on the reproductive performance of turtle doves (Streptopelia turtur) on intensive farmland,

S. Hanane
New data on migration time, breeding phenology, and breeding success of European turtle doves in their highest breeding habitats in north Africa,

I. Mansouri, D. Ousaaid, W. Squalli et al.
Segregation of breeding habitats and feeding resources among five north African game species in Midelt province, Morocco,

I. Mansouri, W. Squalli, H. Achiban, M. Mounir, L. El Ghadraoui, and M. Dakki
Nest-niche differentiation in two sympatric Streptopelia species from a north African agricultural area: the role of human presence,

S. Hanane
Nest-niche differentiation in two sympatric columbid species from a mediterranean tetraclinis woodland: considerations for forest management,

S. Hanane and M. Yassin
Breeding biology of a relictual maghreb magpie (Pica mauritanica) population in Tunisia,

A. Nefla, R. Ouni, S. Selmi, and S. Nouira
Identifying predators and fates of grassland passerine nests using miniature video cameras,

P. J. Pietz and D. A. Granfors
Evolution of tolerance by magpies to brood parasitism by great spotted cuckoos,

J. J. Soler, D. Martin-Galvez, J. G. Martinez et al.
Safety first: terrestrial predators drive selection of highly specific nesting sites in colonial-breeding birds,

D. J. D. Natusch, J. A. Lyons, and R. Shine
Landscape composition governs the abundance patterns of native and invasive columbidae species along an urban–rural gradient and contribute to their partitioning,

N. Saâd, S. Hanane, M. D. El Hak Khemis, and K. Farhi
The spread of the collared dove Streptopelia decaocto in Europe: colonization patterns in the west of the Iberian Peninsula,

G. Rocha-Camarero and S. de Trucios
The impact of climate and cyclic food abundance on the timing of breeding and brood size in four boreal owl species,

A. Lehikoinen, E. Ranta, H. Pietiainen et al.
Factors affecting natal and breeding magpie dispersal in a population parasitized by the great spotted cuckoo,

M. Molina-Morales, J. G. Martínez, J. M. Avilés, and J. Avilés
Absence of anti-parasitic defenses in an Asian population of the magpie, a regular host of the great spotted cuckoo in Europe,

C. Yang, J. Huang, W. Liang, and A. P. Møller

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New Data on Breeding Strategies and Reproductive Success of the Globally Threatened Turtle Dove Co-Occurring with the “Competitive” Collared Dove and the “Predatory” Maghreb Magpie in Olive Orchards

New Data on Breeding Strategies and Reproductive Success of the Globally Threatened Turtle Dove Co-Occurring with the “Competitive” Collared Dove and the “Predatory” Maghreb Magpie in Olive Orchards

Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

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New Data on Breeding Strategies and Reproductive Success of the Globally Threatened Turtle Dove Co-Occurring with the “Competitive” Collared Dove and the “Predatory” Maghreb Magpie in Olive Orchards

New Data on Breeding Strategies and Reproductive Success of the Globally Threatened Turtle Dove Co-Occurring with the “Competitive” Collared Dove and the “Predatory” Maghreb Magpie in Olive Orchards

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