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Breeding biology of a relictual Maghreb Magpie (Pica mauritanica) population in Tunisia

Breeding biology of a relictual Maghreb Magpie (Pica mauritanica) population in Tunisia Background: The Maghreb Magpie (Pica mauritanica) is an endemic North African species. Available knowledge on this species is limited to historic descriptive data with no ecological information provided. Populations continue to dramatically decline in Tunisia, where only one relic population survives. Investigating the breeding biology of this species is essential for conservation purposes. The purpose of this study was to increase our understanding of the Tunisian relic population and provide detailed data on breeding biology over two breeding seasons (2017 and 2018). Methods: This study occurred on a private farm of 650 ha, located 10 km from Dhorbania village at Kairouan Gov- ernorate, in central Tunisia. Active nests were monitored weekly during egg laying period and twice a week during hatching period. The Ivlev’s electivity index was used to assess whether the frequency of use of nesting trees and bushes matched their availability in the study area. We recorded nest measurements and positions, and compared them using Wilcoxon signed-rank test. Variations of breeding parameters as number of eggs laid, hatchlings, and fledglings over years were performed using Mann–Whitney U-test and χ tests. We used a Generalized Linear Mixed Model (GLMM) to investigate how egg volume varied with clutch size and laying date. Results: We investigated clutch size, egg size, hatching and fledging success, and evaluated how these parameters varied according to laying date and nest characteristics. Clutch size averaged 5.00 ± 0.19 but was significantly greater in 2017. Hatching success was 2.78 ± 0.34 eggs hatched per nest and fledging success reached 1.69 ± 0.30 young/ nest. Causes of nest failure included the depredation of nestlings by shrikes, cobras and rats (e.g. Lanius meridionalis, Naja haje and Rattus rattus), death of parents by the Black-shouldered Kite (Elanus caeruleus) and nest parasitism by the Great Spotted Cuckoo (Clamator glandarius). Clutch size, brood size and fledgling success were unaffected by lay- ing date, nest volume and nest elevation. Egg volume decreased with laying date but was unaffected by clutch. Conclusion: Our study provides the first and only detailed data on reproductive parameters of the Maghreb Magpie in its entire geographic range (North Africa). Information gleaned from this study provides valuable information for monitoring and long-term conservation plans of the endangered Tunisian Magpie population. Additionally, our data provide an avenue of large-scale comparative studies of the reproductive ecology of the magpie complex. Keywords: Clutch size, Laying date, Maghreb Magpie, Nesting habitat, Nest success, Relic population, Tunisia Background Investigating the breeding biology of bird species is an essential step for understanding their population dynam- ics and for focusing on conservation efforts. This is par - ticularly important for poorly known species, especially *Correspondence: aymennefla2007@yahoo.fr those showing signs of declining populations. Department of Biology, Faculty of Sciences of Tunis, University of Tunis El The Eurasian Magpie (Pica pica) is a common bird Manar, El Manar II, 2092 Tunis, Tunisia Full list of author information is available at the end of the article species in the Palearctic area. Until recently, the North © The Author(s) 2021. 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The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Nefla et al. Avian Res (2021) 12:12 Page 2 of 9 African population of this species was considered as  a chick survival to decrease with laying date, in line with subspecies (Pica pica mauritanica). However, Ebels the general trend known in birds (Bengtson 1972; Par- (2003) highlighted morphological and acoustic differ - sons 1972; Newton and Campbell 1975; Hill 1984; Sed- ences between the Maghreb population and those of inger 1992; Christians 2002; Verhulst and Nilsson 2008). Europe. Later, taxonomic and phylogenetic studies (Kry- This trend is more likely to occur in our arid study area ukov et  al. 2017; Song et  al. 2018) illustrated that the because food availability deteriorates rapidly as the North African clade is the most divergent compared to breeding season progresses. Moreover, we expected that other lines. Consequently the mauritanica subspecies is breeding success would be strongly related to nest posi- now considered as a separate species, the Maghreb Mag- tion, especially nest elevation, as this parameter is sup- pie (Pica mauritanica), endemic to North Africa (del posed to influence nest conspicuousness and accessibility Hoyo et al. 2018). to predators. At the beginning of the twentieth century, the Maghreb Magpie was locally widespread in North Africa. In the Methods past century, 12 isolated local populations were recorded Study area in Tunisia (Lavauden 1924; Heim de Balzac and Mayaud The relic population inhabits a private, 650  ha, farm 1962; Etchécopar and Hue 1964; Isenmann et  al. 2005), located 10 km from Dhorbania village (35° 58′ 16″ N–10° 16 in Algeria (Etchécopar and Hue 1964; Isenmann and 01′ 15″ E) at Kairouan Governorate, in central Tunisia Moali 2000) and approximately 30 in Morocco (Etché- (Fig.  1). The climate is semi-arid with annual rainfall of copar and Hue 1964; Thévenot et  al. 2003; Bergier et  al. 290 mm and an average summer (June, July and August) 2017). Nowadays, the distribution of this species in North temperature of 38  °C (Mougou et  al. 2011). The farm Africa is more fragmented and limited. For instance, comprises a mixture of cultivated land, including 150 ha only one relic population still survives in Tunisia, at the of fruit trees and 50  ha of vegetable crops, and pasture Sbikha region (Kairouan Governorate) (Ouni et al. 2018; area (450  ha) covered with bushy vegetation, includ- Nefla et al. 2020). However, despite this critical situation ing Sumac (Searsia tripartita) (76.5% of cover), African and the urgency of adequate conservation measures, the Wolfbane (Periploca angustifolia) (10.5%), Deciduous ecology and dynamics of this relic population remain Shrub (Ziziphus lotus) (9%), Ephedra (Ephedra sp.) (2%) poorly understood due to the lack of detailed studies. and European Boxthorn (Lycium europaeum) (1%). Other Indeed, available knowledge on this species is limited to trees [European Olive (Olea europaea), Almond (Pru- old descriptive data on its morphology and distribution nus dulcis), Pistachio (Pistacia vera), Atlas Mastic Tree (Lavauden 1924; Heim de Balzac and Mayaud 1962; Etch- (Pistacia atlantica), Wild Olive (Olea oleaster), Cyclops écopar and Hue 1964; Isenmann et al. 2005). Wattle (Acacia cyclops) and Cape Gum (Acacia horrida)] The breeding biology of the Eurasian Magpie has been comprised 1% of coverage. We also recorded White well studied throughout its whole geographic range, par- Wormwood (Artemisia herba alba), Rosemary (Rosmari- ticularly in the Palearctic region (Sachteleben et al. 1992; nus officinalis), Conehead Thyme (yTh mus capitatus), Eguchi 1995; Jerzak 1995; Dolenec 2000; Soler et al. 2001; Crown Friar (Globularia alypum), White Horehound Antonov and Atanasova 2003; Ponz and Gil-Delgado (Marrubium vulgare), Esparrago (Asparagus alba) and 2004; Tucakov and Kucsera 2008; Wang et  al. 2008). Needle Grass (Stipa tenacissima). Overall, these studies showed that egg laying generally occurs from mid-March to mid-April. They also showed that clutch size varied among populations, with an aver- Nest monitoring age value ranging from five to six eggs per nest, but fledg - From March to late June in 2017 and 2018, we visited the ing success was always less than two fledglings per nest. study site to locate nests of breeding magpies. Located However, detailed data on the breeding parameters of the nests were visited weekly during the egg laying period (in endemic Maghreb Magpie are still lacking. order to minimize disturbance) and twice a week during The objective of this study was to increase our under - hatching until 25 days post-hatch. All active and unoccu- standing of the ecology of this relic population and pied nests were geo-referenced using GPS (Garmin Etrex provide detailed data on its breeding biology over two 75049). consecutive breeding seasons. Specifically, we aimed to: In 2017, we recorded the height (m), diameter (m) (1) describe nesting sites and nest characteristics; (2) and tree species the nest was in. For each nest, we also determine key breeding parameters, notably clutch size, recorded nest elevation (ground to nest distance) (m) and egg volume, hatching success and fledging success, and; nest to tree top distance (m). Nest volume (in liters) was (3) investigate how these parameters varied according 2 also calculated as: V = (4/3) × (π × a × b )/1000, where a to laying date. We expected clutch size, egg volume and Nefla  et al. Avian Res (2021) 12:12 Page 3 of 9 Fig. 1 Map showing the Maghreb Magpie breeding area in Tunisia (black triangle) is the largest radius of the ellipsoid nest (cm) and b half (± 0.01  mm) maximum length (L) and breadth (B; mm) nest width (cm) (Soler et al. 1995). of 35 eggs from seven clutches. We calculated egg volume 3 2 (mm ) following Hoyt (1979): V = 0.51 × L × B . Reproductive data collection We used an endoscopic camera to check nest contents. Data analyses For each nest we recorded the date when the first egg was We assessed whether the frequency of use of nesting laid, the number of eggs in each nest (i.e. clutch size) and trees and bushes matched their availability in the study the number of nestlings that survived to 25  days post- area, using the Ivlev’s electivity index: E = (r – p )/(r + p ), i i i i hatch (age at which nestlings scrambling made further where r is the relative abundance of the tree/shrub spe- visits impractical); we considered 25  days post-hatching cies i in the subset of trees/bushes used as nesting sup- as our operational criterion for fledging. The clutch was ports, while p denotes the relative abundance of this considered complete when there were no additional eggs tree/shrub species in the study area (Ivlev 1961). Values after two consecutive visits. We considered a nest unsuc- of E range from − 1 to + 1, with negative values indicat- cessful if it was found empty before the estimated hatch- ing avoidance, positive values suggesting active selection, ing/fledging date or with damaged eggs/nestlings, since and values close to zero indicating random use. Moreo- the incubation period was estimated to 15  days (Ouni ver, as an investigation of nest position within the nest 2018). We identified predators based on the nest con - tree, we compared nest elevation to nest distance from dition and evidence in the nest. For example, rats typi- tree top using the Wilcoxon signed-rank test. cally leave eggshell fragments, while snakes feed on nests We used data collected at active nests (during the two without leaving a trace (Pietz and Granfors 2000; Klug breeding seasons of 2017 and 2018), to determine clutch et al. 2010). In 2018, we used vernier calipers to measure size (number of eggs laid), hatching success (number of Nefla et al. Avian Res (2021) 12:12 Page 4 of 9 eggs hatched), and fledging success (number of fledglings produced). We assessed whether these parameters var- ied between the two years of study using Mann–Whit- ney U-test. Moreover, a series of colony-level parameters were also determined: egg hatching rate (total number of eggs hatched/total number of eggs laid in the colony), nestling survival rate (total number of fledglings/total number of eggs hatched) and breeding success (number of fledglings/number of eggs laid). We also calculated nest survival (number of nests with at least one hatched egg/total number of nests), fledging survival (number of nests raising at least one fledgling/number of nests with at least one hatched egg), and the rate of success- ful nests (number of nests raising at least one fledgling/ Fig. 2 Ivlev’s electivity index values corresponding to each selected total number of nests). χ tests were then conducted to nesting vegetal support species by Maghreb Magpie breeding pairs: check whether these rates varied between the two years negative values indicating avoidance, positive values suggesting active selection, and values close to zero indicating random use of study. Linear regressions were carried out to assess whether clutch size, brood size and the number of fledg - lings varied among nests according to laying date (Julian most abundant shrub species in the study area (10.5% of days, day 1 = January 1st), nest elevation and nest volume. potential nesting vegetation). This gives a negative Ivlev’s Finally, we used a Generalized Linear Mixed Model index value and indicates avoidance of this shrub species (GLMM) to investigate how egg volume varied with (Fig. 2). clutch size (three categories: four-egg clutches, five-egg Mean height and diameter of nesting shrubs (± SE) clutches and six-egg clutches) and laying date (days after were 2.87 ± 0.43 m (range 2.29–3.90 m) and 4.19 ± 1.17 m March 1st), while accounting for clutch identity as a ran- (range 2.50–6.80  m) respectively. Nest volume varied dom factor. All statistical tests and analyses were carried 3 3 between 0.08 and 0.52 m and averaged 0.25 ± 0.04 m . out using Statistica 12 software (StatSoft Inc 2013). Nest elevation ranged from 1.10 to 2.09 m, and averaged 1.54 ± 0.26 m. The height of the nest in the shrub was sig - Results nificantly higher than the distance from the nest to the Nesting sites shrub top (Z = 3.17, P < 0.01), showing that nests were In 2017 we recorded 119 nests: 13 (11%) active nest and built above the middle of the shrubs. 106 old unoccupied nests. One breeding pair has laid two clutches (initial and replacement) in two different nests. In 2018, we recorded 20 (15%) active nests with Reproductive parameters no replacement clutch. Among these 20 nests we distin- Egg laying occurred between mid-March and mid-April, guished 4 (20%) restored old nests, 3 (15%) reused nests with 69% of nests initiated during the second half of (from active nests in 2017) and 13 (65%) new built nests. March and 31% in the first half of April. u Th s the total number of nests recorded in the study area The breeding parameters remained consistent between in 2018 was 132, showing an increase of 11% from 2017 years, except for clutch size which was greater in 2017 to 2018. than 2018 (Table 1). All nests were located in the uncultivated part of Over the two years of study, 44% of eggs laid in the the study site and none were found in fruit trees. Nests colony were lost during incubation and 39% of hatch- were mainly built in Searsia tripartita shrubs (121 nests; lings were lost before fledging. The main causes of nest 91.6%), which is the most available nesting support in failure were depredation of nestlings by Southern Grey the area (76.5% of nesting supports), corresponding to Shrike (Lanius meridionalis) (34% of losses), Egyptian an Ivlev’s index value close to zero and suggesting a ran- Cobra (Naja haje) (24%) and rats (Rattus rattus) (18%). dom use of this shrub species (Fig.  2). Remaining nests The depredation of parents by raptors, particularly Black- were located in Ziziphus lotus (4 nests), Olea oleaster shouldered Kite (Elanus caeruleus) and nest parasitism (3 nests), Lycium europaeum (2 nests), Acacia cyclops (1 by the Great Spotted Cuckoo (Clamator glandarius) also nest) and Acacia horrida (1 nest). Together, these plant accounted for 6% and 9% of losses respectively. However, species accounted for 9.6% of potential nesting sites and we were unable to identify the cause of 9% of failed nests. supported 8.3% of magpie nests. By contrast, no nest Laying date had no effect on clutch was built in Periploca angustifolia, which is the second size (β ± SE = − 0.09 ± 0.30), brood size Nefla  et al. Avian Res (2021) 12:12 Page 5 of 9 Table 1 Breeding parameters of the Maghreb Magpie (Pica mauritanica) recorded during 2017 and 2018 breeding seasons in Tunisia (Sbikha) Breeding parameter 2017 2018 Years combined Test for difference between years Active nests 13 20 33 – Replacement clutches 1 0 1 – Range of clutch size 4–7 3–6 3–7 – Modal clutch 6 4 6 – Total number of eggs laid in the colony 75 90 165 – Mean clutch size ± SE 5.77 ± 0.69 4.50 ± 0.18 5.00 ± 0.19 Z = 3.56, P = 0.000 Egg hatching rate (%) 55% 57% 56% χ = 0.066, P = 0.796 Hatching success ± SE 3.15 ± 0.54 2.55 ± 0.44 2.78 ± 0.34 Z = 0.99, P = 0.321 Fledging success ± SE 2.07 ± 0.48 1.45 ± 0.38 1.69 ± 0.30 Z = 0.89, P = 0.369 Nestling survival rate (%) 66% 57% 61% χ = 0.771, P = 0.379 Breeding success (%) 36% 32% 34% χ = 0.260, P = 0.609 Nest survival (%) 85% 75% 79% χ = 0.435, P = 0.509 Fledging survival (%) 82% 73% 77% χ = 0.257, P = 0.611 Rate of successful nest (%) 69% 55% 61% χ = 0.668, P = 0.413 SE standard error (β ± SE = − 0.06 ± 0.30) and the number of fledg - β ± SE = − 0.06 ± 0.30 and β ± SE = − 0.07 ± 0.30) lings produced (β ± SE = − 0.40 ± 0.27). Moreo- nor with nest elevation (β ± SE = 0.26 ± 0.29, ver, none of these breeding parameters were related β ± SE = − 0.39 ± 0.27 and β ± SE = − 0.09 ± 0.30). to nest volume (respectively: β ± SE = 0.02 ± 0.30, Overall, clutch size was lower than those reported Table 2 Summary of main breeding parameters recorded in the studied population of Maghreb Magpie (current study) in comparison with those known in Eurasian Magpie populations Region Egg dimensions (mm) Mean (SD) clutch size Hatching success Fledging success Laying date Source (hatchlings per eggs (fledglings per Length Breadth laid) clutch) Tunisia 32.26 (2.05) 23.01 (3.96) 5.00 (1.09) 0.56 1.69 (1.72) Early March Present study Spain 33.10 23.30 6.35 – 1.45 Early April Arias de Reyna et al. (1984) Spain – – 6.80 (1.14) 0.57 1.84 (2.28) Mid April Ponz and Gil-Delgado (2004) Bulgaria – – 6.38 (1.15) 0.47 1.57 (2.34) Early April Antonov and Atanasova (2003) France – – 5.70 – – – Balanca (1984) Belgium 34.60 23.70 – – – – Verheyen (1967) Germany 33.30 23.61 6.70 – – – Hund and Prinzinger (1981) Germany – – – – 1.20 – Sachteleben et al. (1992) Poland 33.33 (2.43) 22.90 (0.68) 6.00 (1.09) – 1.13 Mid April Jerzak (1995) Netherlands 33.97 (0.16) 23.94 (0.07) 6.23 (0.89) 0.54 1.67 (1.46) Mid April Walters (1988) Britain – – 6.15 (1.09) 0.46 1.72 (2.13) Mid April Eden (1985) Britain – – – – 0.69–0.94 Mid March Vines (1981) Britain – – 5.60 (1.44) 0.46 1.67 Mid April Tatner (1982) Slovenia 33.60 (2.75) 23.20 (0.69) 6.00 (0.93) – – Mid April Vogrin (1998) Croatia 33.43 (1.38) 23.35 (0.52) 5.91 (1.08) – – – Dolenec (2000) Uzbekstan 35.50 24.10 6.20 – – – Abdreimov (1981) Kazakhstan 34.50 25.10 6.00 – – – Smetana (1978) Japan – – 6.19 (1.30) 0.62 0.73 Mid March Eguchi (1995) SD standard deviation Nefla et al. Avian Res (2021) 12:12 Page 6 of 9 for Eurasian Magpie populations in temperate areas food abundance is low. Secondly, we found that spring (Table  2), but values of hatching and fledging success rainfall (March to May) in 2017 (16 mm) was lower than were similar (Table 2). recorded in 2018 (34  mm). This is in accordance with Rodríguez and Bustamante (2003) demonstrating that Relationships of egg volume with clutch size and laying rainfall during the nestling period has a negative effect date on nest success rate. u Th s, spring rainfall at the time of Mean length, breadth and volume of Maghreb Mag- hatching cause temporal declines in foraging activity pie eggs (± SE) were 32.26 ± 2.05  mm (range: 28.60– (Dawson and Bortolotti 2000; Radford et  al. 2001) or in 35.00  mm), 23.01 ± 0.67  mm (range: 21.56–24.10  mm) food availability (Avery and Krebs 1984), causing mor- 3 3 and 8.74 ± 0.94 cm (range: 6.80–10.16 cm ) respectively. tality of complete clutches of recently hatched chicks. These data showed slight differences with egg volume According Senapathi et  al. (2011), spring rainfall affects recorded in the temperate Eurasian Magpie populations birds to breed later in the season. Delays in breeding (Table 2). cause reduction of reproductive success as birds get Accounting for clutch identity as a random factor, exposed to risks associated with adverse climatic condi- we found that egg volume decreased with laying date tions later in the breeding season, which reduce nesting (β ± SE = ‒ 0.52 ± 0.19, F = 7.65, P < 0.01) but was unaf- success. 1,31 fected by clutch size (β ± SE = 0.29 ± 0.18, F = 1.06, We showed that the depredation of Maghreb Magpie 2,31 P = 0.362). nestlings by Southern Grey Shrike was the main cause of nest failure. This species shared the same breeding habi - Discussion tat with Maghreb Magpie. Contrary to previous reports To our knowledge, this is the first investigation of the that state Magpies prey on shrikes nests (Cramp and Per- breeding ecology of the Maghreb Magpie. Our main rins 1994; Strnad et al. 2012), we found that shrikes were objective was to provide detailed data on the nesting hab- the most common magpie nest predators. Southern Grey its and breeding success of this declining relictual popu- Shrike nests inside thorny bushes showing a great abil- lation. We obtained new and valuable data describing ity to squeeze between thorns. Given the two bird spe- the nesting habitat use and the breeding performance of cies share the same breeding habitat, we believe shrikes the Maghreb Magpie. These results are the first and only kill the nestlings of neighboring   magpie pairs to cause provided data related to Maghreb Magpie in Tunisia and nest abandonment. This appears to be an active defense entire North African region, which is of great interest for strategy different from the known behavior of shrikes to the implementation of a possible monitoring and long- prevent predation of their nests by magpies: avoid attack- term conservation plan of the endangered Tunisian mag- ing predators that approach the nest so as not to show pie population. its location (Syrová et al. 2016). A more detailed study of Our results showed that magpie nests were built on the predatory interactions between these two species is thorny bushes, in particular Searsia tripartita which is warranted. the most available nest habitat in the area. Non-thorny Our preliminaries results showed that the breed- shrubs, such as Periploca angustifolia, were not used ing biology of Maghreb Magpie slightly differs from the despite their wide availability. In addition, nests were Eurasian Magpie by nesting earlier and laying smaller often built just above the middle of the bushes, which is clutches and eggs (Högstedt 1980; Tatner 1982; Arias de similar to what has been reported in the Eurasian Mag- Reyna et al. 1984; Redondo and Carranza 1989; Ponz and pie in temperate rural environments (e.g. Dolenec 2000; Gil-Delgado 2004; Birkhead 1991). Differences in laying Tucakov and Kucsera 2008). This tendency to place nests date may obey to a latitudinal gradient effect on birds in the middle of thorny shrubs might be a defense mech- breeding phenology (Lack 1947, 1968; Cardillo 2002; Jetz anism to limit the accessibility of mammalian and avian et al. 2008). More data and further analysis are needed to nest predators. verify this hypothesis. The earlier spring in the latitudes We found that clutch size and nest survival in 2018 of North Africa in comparison with the temperate zones were lower than those in 2017. Difference seem to be of Tunisia would explain the early entry into reproduc- related to weather condition mainly rainfall. Firstly, win- tion of the Maghreb Magpie compared to the popula- ter rainfall (September to February) in 2017 (109  mm) tions of Eurasian Magpie. According de Neve et al. (2004) was higher than in 2018 (46  mm). According Rodríguez food availability directly influences laying date in many and Bustamante (2003) nest success rate is influenced species, including the Eurasian Magpie, where food sup- positively by rainfall in winter. In fact, winter rainfall may plementation significantly advanced the onset of laying increase food availability during incubation since dry (Meijer and Drent 1999). winters will force birds to quit incubation to forage when Nefla  et al. Avian Res (2021) 12:12 Page 7 of 9 It is known that egg size of magpies significantly preservation of thornier bushes in protected areas, such increases in response to food supplementation (Högstedt as the private farm where the study population currently 1981; Hochachka and Boag 1987; Ramsay and Houston live, could ensure the increase of population size by pro- 1997; Meijer and Drent 1999; de Neve and Soler 2002; de viding it with more suitable and safe nesting habitat. This Neve et al. 2004) despite the relatively inflexibility within would require a short and medium-term conservation individual female birds showed by Christians (2002). The program, involving the responsible Tunisian authorities smaller clutches and eggs recorded in our population in (i.e. general directorate of forests) but also local envi- comparison with those known in the Eurasian Magpie ronmental NGOs, and aiming at sensitizing local farm- in temperate zones may be due to possible food scarcity ers and helping them to dedicate parts of their lands to in our arid study area and/or the shorter days at our lati- thorny bush plantations. tudes. Unfortunately, we did not assess food availability Acknowledgements in our study area to test this hypothesis and to investigate Our sincere thanks go to Mr Abdelaziz Mchala, the owner of the farm where more deeply the possible role of food availability in shap- the study was carried out, who allowed us free access to the site and for his permanent support for biodiversity. We also express our deep gratitude to ing the reproductive investment of the studied birds. Haifa Ouni who contributed to field mission in 2017. We also thank Zakher Egg volume varied significantly with laying date, being Bouragaoui for his contribution in paper finalization. larger earlier in the season. This pattern matches the gen - Authors’ contributions eral trend known in birds (Bengtson 1972; Parsons 1972; AN and RO conducted the field work and collected all data. AN statistically Newton and Campbell 1975; Hill 1984; Sedinger 1992; analyzed data. SN and SS contributed to results interpretation. AN and SS were Christians 2002). This might be due to poorer quality a major contributor in writing the manuscript. All authors read and approved the final manuscript. of late breeders compared to early ones. Indeed, some young and less experienced birds often start breeding Funding later and produce less-quality eggs compared to more Not applicable. experienced birds (Christians 2002; Williams 2012; Ver- Availability of data and materials hoeven et al. 2019). Alternatively, deteriorating breeding Not applicable. conditions, notably food availability, as the season pro- gress may also result in decreasing egg volume. These Declarations hypotheses were not investigated since no data on moni- Ethics approval and consent to participate tored breeding pairs ages and food availability seasonal Not applicable. changes were available. Because the number of eggs laid by a female could be Consent for publication Not applicable. traded-off their sizes, a negative relationship between egg size and clutch size could be expected (Blackburn Competing interests 1991; de Neve and Soler 2002; Ręk 2010). The opposite The authors declare that they have no competing interests. trend could also be expected as high-quality females Author details may lay larger clutches of larger eggs compared to low- 1 Department of Biology, Faculty of Sciences of Tunis, University of Tunis El quality females (de Neve and Soler 2002; de Neve et  al. Manar, El Manar II, 2092 Tunis, Tunisia. Tunisia Wildlife Conservation Society, Bejaoua, Sidi Thabit Tunis, Tunisia. Research Unit “Ecology of Terrestrial Fauna” 2004; Lifjeld et  al. 2005). Given that no significant rela - (UR17ES44), Faculty of Sciences, University of Gabes, Zrig, 6072 Gabes, Tunisia. tionship between egg volume and clutch size was found, our results did not give support to any of the previous Received: 11 September 2020 Accepted: 18 March 2021 hypotheses. Conclusion References In conclusion, we believe that without claiming to have Abdreimov T. Birds of deserts and lowlands of Amu Daria. Tashkent: Pub Fan completely filled a lack of information, our study pro - Uzbetskoy SRR Tashkent; 1981. Antonov A, Atanasova D. Small-scale differences in the breeding ecology of vides the first and only detailed data on the reproduc - urban and rural Magpies Pica pica. Ornis Fennica. 2003;80:21–30. tive parameters of the Maghreb Magpie in Tunisia and Arias de Reyna L, Recuerda P, Corvillo M, Cruz A. Reproduccion de la urraca whole North African region. In addition to their potential (Pica pica) en Sierra Morena (Andalucia). 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Breeding biology of a relictual Maghreb Magpie (Pica mauritanica) population in Tunisia

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10.1186/s40657-021-00249-6
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Abstract

Background: The Maghreb Magpie (Pica mauritanica) is an endemic North African species. Available knowledge on this species is limited to historic descriptive data with no ecological information provided. Populations continue to dramatically decline in Tunisia, where only one relic population survives. Investigating the breeding biology of this species is essential for conservation purposes. The purpose of this study was to increase our understanding of the Tunisian relic population and provide detailed data on breeding biology over two breeding seasons (2017 and 2018). Methods: This study occurred on a private farm of 650 ha, located 10 km from Dhorbania village at Kairouan Gov- ernorate, in central Tunisia. Active nests were monitored weekly during egg laying period and twice a week during hatching period. The Ivlev’s electivity index was used to assess whether the frequency of use of nesting trees and bushes matched their availability in the study area. We recorded nest measurements and positions, and compared them using Wilcoxon signed-rank test. Variations of breeding parameters as number of eggs laid, hatchlings, and fledglings over years were performed using Mann–Whitney U-test and χ tests. We used a Generalized Linear Mixed Model (GLMM) to investigate how egg volume varied with clutch size and laying date. Results: We investigated clutch size, egg size, hatching and fledging success, and evaluated how these parameters varied according to laying date and nest characteristics. Clutch size averaged 5.00 ± 0.19 but was significantly greater in 2017. Hatching success was 2.78 ± 0.34 eggs hatched per nest and fledging success reached 1.69 ± 0.30 young/ nest. Causes of nest failure included the depredation of nestlings by shrikes, cobras and rats (e.g. Lanius meridionalis, Naja haje and Rattus rattus), death of parents by the Black-shouldered Kite (Elanus caeruleus) and nest parasitism by the Great Spotted Cuckoo (Clamator glandarius). Clutch size, brood size and fledgling success were unaffected by lay- ing date, nest volume and nest elevation. Egg volume decreased with laying date but was unaffected by clutch. Conclusion: Our study provides the first and only detailed data on reproductive parameters of the Maghreb Magpie in its entire geographic range (North Africa). Information gleaned from this study provides valuable information for monitoring and long-term conservation plans of the endangered Tunisian Magpie population. Additionally, our data provide an avenue of large-scale comparative studies of the reproductive ecology of the magpie complex. Keywords: Clutch size, Laying date, Maghreb Magpie, Nesting habitat, Nest success, Relic population, Tunisia Background Investigating the breeding biology of bird species is an essential step for understanding their population dynam- ics and for focusing on conservation efforts. This is par - ticularly important for poorly known species, especially *Correspondence: aymennefla2007@yahoo.fr those showing signs of declining populations. Department of Biology, Faculty of Sciences of Tunis, University of Tunis El The Eurasian Magpie (Pica pica) is a common bird Manar, El Manar II, 2092 Tunis, Tunisia Full list of author information is available at the end of the article species in the Palearctic area. Until recently, the North © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Nefla et al. Avian Res (2021) 12:12 Page 2 of 9 African population of this species was considered as  a chick survival to decrease with laying date, in line with subspecies (Pica pica mauritanica). However, Ebels the general trend known in birds (Bengtson 1972; Par- (2003) highlighted morphological and acoustic differ - sons 1972; Newton and Campbell 1975; Hill 1984; Sed- ences between the Maghreb population and those of inger 1992; Christians 2002; Verhulst and Nilsson 2008). Europe. Later, taxonomic and phylogenetic studies (Kry- This trend is more likely to occur in our arid study area ukov et  al. 2017; Song et  al. 2018) illustrated that the because food availability deteriorates rapidly as the North African clade is the most divergent compared to breeding season progresses. Moreover, we expected that other lines. Consequently the mauritanica subspecies is breeding success would be strongly related to nest posi- now considered as a separate species, the Maghreb Mag- tion, especially nest elevation, as this parameter is sup- pie (Pica mauritanica), endemic to North Africa (del posed to influence nest conspicuousness and accessibility Hoyo et al. 2018). to predators. At the beginning of the twentieth century, the Maghreb Magpie was locally widespread in North Africa. In the Methods past century, 12 isolated local populations were recorded Study area in Tunisia (Lavauden 1924; Heim de Balzac and Mayaud The relic population inhabits a private, 650  ha, farm 1962; Etchécopar and Hue 1964; Isenmann et  al. 2005), located 10 km from Dhorbania village (35° 58′ 16″ N–10° 16 in Algeria (Etchécopar and Hue 1964; Isenmann and 01′ 15″ E) at Kairouan Governorate, in central Tunisia Moali 2000) and approximately 30 in Morocco (Etché- (Fig.  1). The climate is semi-arid with annual rainfall of copar and Hue 1964; Thévenot et  al. 2003; Bergier et  al. 290 mm and an average summer (June, July and August) 2017). Nowadays, the distribution of this species in North temperature of 38  °C (Mougou et  al. 2011). The farm Africa is more fragmented and limited. For instance, comprises a mixture of cultivated land, including 150 ha only one relic population still survives in Tunisia, at the of fruit trees and 50  ha of vegetable crops, and pasture Sbikha region (Kairouan Governorate) (Ouni et al. 2018; area (450  ha) covered with bushy vegetation, includ- Nefla et al. 2020). However, despite this critical situation ing Sumac (Searsia tripartita) (76.5% of cover), African and the urgency of adequate conservation measures, the Wolfbane (Periploca angustifolia) (10.5%), Deciduous ecology and dynamics of this relic population remain Shrub (Ziziphus lotus) (9%), Ephedra (Ephedra sp.) (2%) poorly understood due to the lack of detailed studies. and European Boxthorn (Lycium europaeum) (1%). Other Indeed, available knowledge on this species is limited to trees [European Olive (Olea europaea), Almond (Pru- old descriptive data on its morphology and distribution nus dulcis), Pistachio (Pistacia vera), Atlas Mastic Tree (Lavauden 1924; Heim de Balzac and Mayaud 1962; Etch- (Pistacia atlantica), Wild Olive (Olea oleaster), Cyclops écopar and Hue 1964; Isenmann et al. 2005). Wattle (Acacia cyclops) and Cape Gum (Acacia horrida)] The breeding biology of the Eurasian Magpie has been comprised 1% of coverage. We also recorded White well studied throughout its whole geographic range, par- Wormwood (Artemisia herba alba), Rosemary (Rosmari- ticularly in the Palearctic region (Sachteleben et al. 1992; nus officinalis), Conehead Thyme (yTh mus capitatus), Eguchi 1995; Jerzak 1995; Dolenec 2000; Soler et al. 2001; Crown Friar (Globularia alypum), White Horehound Antonov and Atanasova 2003; Ponz and Gil-Delgado (Marrubium vulgare), Esparrago (Asparagus alba) and 2004; Tucakov and Kucsera 2008; Wang et  al. 2008). Needle Grass (Stipa tenacissima). Overall, these studies showed that egg laying generally occurs from mid-March to mid-April. They also showed that clutch size varied among populations, with an aver- Nest monitoring age value ranging from five to six eggs per nest, but fledg - From March to late June in 2017 and 2018, we visited the ing success was always less than two fledglings per nest. study site to locate nests of breeding magpies. Located However, detailed data on the breeding parameters of the nests were visited weekly during the egg laying period (in endemic Maghreb Magpie are still lacking. order to minimize disturbance) and twice a week during The objective of this study was to increase our under - hatching until 25 days post-hatch. All active and unoccu- standing of the ecology of this relic population and pied nests were geo-referenced using GPS (Garmin Etrex provide detailed data on its breeding biology over two 75049). consecutive breeding seasons. Specifically, we aimed to: In 2017, we recorded the height (m), diameter (m) (1) describe nesting sites and nest characteristics; (2) and tree species the nest was in. For each nest, we also determine key breeding parameters, notably clutch size, recorded nest elevation (ground to nest distance) (m) and egg volume, hatching success and fledging success, and; nest to tree top distance (m). Nest volume (in liters) was (3) investigate how these parameters varied according 2 also calculated as: V = (4/3) × (π × a × b )/1000, where a to laying date. We expected clutch size, egg volume and Nefla  et al. Avian Res (2021) 12:12 Page 3 of 9 Fig. 1 Map showing the Maghreb Magpie breeding area in Tunisia (black triangle) is the largest radius of the ellipsoid nest (cm) and b half (± 0.01  mm) maximum length (L) and breadth (B; mm) nest width (cm) (Soler et al. 1995). of 35 eggs from seven clutches. We calculated egg volume 3 2 (mm ) following Hoyt (1979): V = 0.51 × L × B . Reproductive data collection We used an endoscopic camera to check nest contents. Data analyses For each nest we recorded the date when the first egg was We assessed whether the frequency of use of nesting laid, the number of eggs in each nest (i.e. clutch size) and trees and bushes matched their availability in the study the number of nestlings that survived to 25  days post- area, using the Ivlev’s electivity index: E = (r – p )/(r + p ), i i i i hatch (age at which nestlings scrambling made further where r is the relative abundance of the tree/shrub spe- visits impractical); we considered 25  days post-hatching cies i in the subset of trees/bushes used as nesting sup- as our operational criterion for fledging. The clutch was ports, while p denotes the relative abundance of this considered complete when there were no additional eggs tree/shrub species in the study area (Ivlev 1961). Values after two consecutive visits. We considered a nest unsuc- of E range from − 1 to + 1, with negative values indicat- cessful if it was found empty before the estimated hatch- ing avoidance, positive values suggesting active selection, ing/fledging date or with damaged eggs/nestlings, since and values close to zero indicating random use. Moreo- the incubation period was estimated to 15  days (Ouni ver, as an investigation of nest position within the nest 2018). We identified predators based on the nest con - tree, we compared nest elevation to nest distance from dition and evidence in the nest. For example, rats typi- tree top using the Wilcoxon signed-rank test. cally leave eggshell fragments, while snakes feed on nests We used data collected at active nests (during the two without leaving a trace (Pietz and Granfors 2000; Klug breeding seasons of 2017 and 2018), to determine clutch et al. 2010). In 2018, we used vernier calipers to measure size (number of eggs laid), hatching success (number of Nefla et al. Avian Res (2021) 12:12 Page 4 of 9 eggs hatched), and fledging success (number of fledglings produced). We assessed whether these parameters var- ied between the two years of study using Mann–Whit- ney U-test. Moreover, a series of colony-level parameters were also determined: egg hatching rate (total number of eggs hatched/total number of eggs laid in the colony), nestling survival rate (total number of fledglings/total number of eggs hatched) and breeding success (number of fledglings/number of eggs laid). We also calculated nest survival (number of nests with at least one hatched egg/total number of nests), fledging survival (number of nests raising at least one fledgling/number of nests with at least one hatched egg), and the rate of success- ful nests (number of nests raising at least one fledgling/ Fig. 2 Ivlev’s electivity index values corresponding to each selected total number of nests). χ tests were then conducted to nesting vegetal support species by Maghreb Magpie breeding pairs: check whether these rates varied between the two years negative values indicating avoidance, positive values suggesting active selection, and values close to zero indicating random use of study. Linear regressions were carried out to assess whether clutch size, brood size and the number of fledg - lings varied among nests according to laying date (Julian most abundant shrub species in the study area (10.5% of days, day 1 = January 1st), nest elevation and nest volume. potential nesting vegetation). This gives a negative Ivlev’s Finally, we used a Generalized Linear Mixed Model index value and indicates avoidance of this shrub species (GLMM) to investigate how egg volume varied with (Fig. 2). clutch size (three categories: four-egg clutches, five-egg Mean height and diameter of nesting shrubs (± SE) clutches and six-egg clutches) and laying date (days after were 2.87 ± 0.43 m (range 2.29–3.90 m) and 4.19 ± 1.17 m March 1st), while accounting for clutch identity as a ran- (range 2.50–6.80  m) respectively. Nest volume varied dom factor. All statistical tests and analyses were carried 3 3 between 0.08 and 0.52 m and averaged 0.25 ± 0.04 m . out using Statistica 12 software (StatSoft Inc 2013). Nest elevation ranged from 1.10 to 2.09 m, and averaged 1.54 ± 0.26 m. The height of the nest in the shrub was sig - Results nificantly higher than the distance from the nest to the Nesting sites shrub top (Z = 3.17, P < 0.01), showing that nests were In 2017 we recorded 119 nests: 13 (11%) active nest and built above the middle of the shrubs. 106 old unoccupied nests. One breeding pair has laid two clutches (initial and replacement) in two different nests. In 2018, we recorded 20 (15%) active nests with Reproductive parameters no replacement clutch. Among these 20 nests we distin- Egg laying occurred between mid-March and mid-April, guished 4 (20%) restored old nests, 3 (15%) reused nests with 69% of nests initiated during the second half of (from active nests in 2017) and 13 (65%) new built nests. March and 31% in the first half of April. u Th s the total number of nests recorded in the study area The breeding parameters remained consistent between in 2018 was 132, showing an increase of 11% from 2017 years, except for clutch size which was greater in 2017 to 2018. than 2018 (Table 1). All nests were located in the uncultivated part of Over the two years of study, 44% of eggs laid in the the study site and none were found in fruit trees. Nests colony were lost during incubation and 39% of hatch- were mainly built in Searsia tripartita shrubs (121 nests; lings were lost before fledging. The main causes of nest 91.6%), which is the most available nesting support in failure were depredation of nestlings by Southern Grey the area (76.5% of nesting supports), corresponding to Shrike (Lanius meridionalis) (34% of losses), Egyptian an Ivlev’s index value close to zero and suggesting a ran- Cobra (Naja haje) (24%) and rats (Rattus rattus) (18%). dom use of this shrub species (Fig.  2). Remaining nests The depredation of parents by raptors, particularly Black- were located in Ziziphus lotus (4 nests), Olea oleaster shouldered Kite (Elanus caeruleus) and nest parasitism (3 nests), Lycium europaeum (2 nests), Acacia cyclops (1 by the Great Spotted Cuckoo (Clamator glandarius) also nest) and Acacia horrida (1 nest). Together, these plant accounted for 6% and 9% of losses respectively. However, species accounted for 9.6% of potential nesting sites and we were unable to identify the cause of 9% of failed nests. supported 8.3% of magpie nests. By contrast, no nest Laying date had no effect on clutch was built in Periploca angustifolia, which is the second size (β ± SE = − 0.09 ± 0.30), brood size Nefla  et al. Avian Res (2021) 12:12 Page 5 of 9 Table 1 Breeding parameters of the Maghreb Magpie (Pica mauritanica) recorded during 2017 and 2018 breeding seasons in Tunisia (Sbikha) Breeding parameter 2017 2018 Years combined Test for difference between years Active nests 13 20 33 – Replacement clutches 1 0 1 – Range of clutch size 4–7 3–6 3–7 – Modal clutch 6 4 6 – Total number of eggs laid in the colony 75 90 165 – Mean clutch size ± SE 5.77 ± 0.69 4.50 ± 0.18 5.00 ± 0.19 Z = 3.56, P = 0.000 Egg hatching rate (%) 55% 57% 56% χ = 0.066, P = 0.796 Hatching success ± SE 3.15 ± 0.54 2.55 ± 0.44 2.78 ± 0.34 Z = 0.99, P = 0.321 Fledging success ± SE 2.07 ± 0.48 1.45 ± 0.38 1.69 ± 0.30 Z = 0.89, P = 0.369 Nestling survival rate (%) 66% 57% 61% χ = 0.771, P = 0.379 Breeding success (%) 36% 32% 34% χ = 0.260, P = 0.609 Nest survival (%) 85% 75% 79% χ = 0.435, P = 0.509 Fledging survival (%) 82% 73% 77% χ = 0.257, P = 0.611 Rate of successful nest (%) 69% 55% 61% χ = 0.668, P = 0.413 SE standard error (β ± SE = − 0.06 ± 0.30) and the number of fledg - β ± SE = − 0.06 ± 0.30 and β ± SE = − 0.07 ± 0.30) lings produced (β ± SE = − 0.40 ± 0.27). Moreo- nor with nest elevation (β ± SE = 0.26 ± 0.29, ver, none of these breeding parameters were related β ± SE = − 0.39 ± 0.27 and β ± SE = − 0.09 ± 0.30). to nest volume (respectively: β ± SE = 0.02 ± 0.30, Overall, clutch size was lower than those reported Table 2 Summary of main breeding parameters recorded in the studied population of Maghreb Magpie (current study) in comparison with those known in Eurasian Magpie populations Region Egg dimensions (mm) Mean (SD) clutch size Hatching success Fledging success Laying date Source (hatchlings per eggs (fledglings per Length Breadth laid) clutch) Tunisia 32.26 (2.05) 23.01 (3.96) 5.00 (1.09) 0.56 1.69 (1.72) Early March Present study Spain 33.10 23.30 6.35 – 1.45 Early April Arias de Reyna et al. (1984) Spain – – 6.80 (1.14) 0.57 1.84 (2.28) Mid April Ponz and Gil-Delgado (2004) Bulgaria – – 6.38 (1.15) 0.47 1.57 (2.34) Early April Antonov and Atanasova (2003) France – – 5.70 – – – Balanca (1984) Belgium 34.60 23.70 – – – – Verheyen (1967) Germany 33.30 23.61 6.70 – – – Hund and Prinzinger (1981) Germany – – – – 1.20 – Sachteleben et al. (1992) Poland 33.33 (2.43) 22.90 (0.68) 6.00 (1.09) – 1.13 Mid April Jerzak (1995) Netherlands 33.97 (0.16) 23.94 (0.07) 6.23 (0.89) 0.54 1.67 (1.46) Mid April Walters (1988) Britain – – 6.15 (1.09) 0.46 1.72 (2.13) Mid April Eden (1985) Britain – – – – 0.69–0.94 Mid March Vines (1981) Britain – – 5.60 (1.44) 0.46 1.67 Mid April Tatner (1982) Slovenia 33.60 (2.75) 23.20 (0.69) 6.00 (0.93) – – Mid April Vogrin (1998) Croatia 33.43 (1.38) 23.35 (0.52) 5.91 (1.08) – – – Dolenec (2000) Uzbekstan 35.50 24.10 6.20 – – – Abdreimov (1981) Kazakhstan 34.50 25.10 6.00 – – – Smetana (1978) Japan – – 6.19 (1.30) 0.62 0.73 Mid March Eguchi (1995) SD standard deviation Nefla et al. Avian Res (2021) 12:12 Page 6 of 9 for Eurasian Magpie populations in temperate areas food abundance is low. Secondly, we found that spring (Table  2), but values of hatching and fledging success rainfall (March to May) in 2017 (16 mm) was lower than were similar (Table 2). recorded in 2018 (34  mm). This is in accordance with Rodríguez and Bustamante (2003) demonstrating that Relationships of egg volume with clutch size and laying rainfall during the nestling period has a negative effect date on nest success rate. u Th s, spring rainfall at the time of Mean length, breadth and volume of Maghreb Mag- hatching cause temporal declines in foraging activity pie eggs (± SE) were 32.26 ± 2.05  mm (range: 28.60– (Dawson and Bortolotti 2000; Radford et  al. 2001) or in 35.00  mm), 23.01 ± 0.67  mm (range: 21.56–24.10  mm) food availability (Avery and Krebs 1984), causing mor- 3 3 and 8.74 ± 0.94 cm (range: 6.80–10.16 cm ) respectively. tality of complete clutches of recently hatched chicks. These data showed slight differences with egg volume According Senapathi et  al. (2011), spring rainfall affects recorded in the temperate Eurasian Magpie populations birds to breed later in the season. Delays in breeding (Table 2). cause reduction of reproductive success as birds get Accounting for clutch identity as a random factor, exposed to risks associated with adverse climatic condi- we found that egg volume decreased with laying date tions later in the breeding season, which reduce nesting (β ± SE = ‒ 0.52 ± 0.19, F = 7.65, P < 0.01) but was unaf- success. 1,31 fected by clutch size (β ± SE = 0.29 ± 0.18, F = 1.06, We showed that the depredation of Maghreb Magpie 2,31 P = 0.362). nestlings by Southern Grey Shrike was the main cause of nest failure. This species shared the same breeding habi - Discussion tat with Maghreb Magpie. Contrary to previous reports To our knowledge, this is the first investigation of the that state Magpies prey on shrikes nests (Cramp and Per- breeding ecology of the Maghreb Magpie. Our main rins 1994; Strnad et al. 2012), we found that shrikes were objective was to provide detailed data on the nesting hab- the most common magpie nest predators. Southern Grey its and breeding success of this declining relictual popu- Shrike nests inside thorny bushes showing a great abil- lation. We obtained new and valuable data describing ity to squeeze between thorns. Given the two bird spe- the nesting habitat use and the breeding performance of cies share the same breeding habitat, we believe shrikes the Maghreb Magpie. These results are the first and only kill the nestlings of neighboring   magpie pairs to cause provided data related to Maghreb Magpie in Tunisia and nest abandonment. This appears to be an active defense entire North African region, which is of great interest for strategy different from the known behavior of shrikes to the implementation of a possible monitoring and long- prevent predation of their nests by magpies: avoid attack- term conservation plan of the endangered Tunisian mag- ing predators that approach the nest so as not to show pie population. its location (Syrová et al. 2016). A more detailed study of Our results showed that magpie nests were built on the predatory interactions between these two species is thorny bushes, in particular Searsia tripartita which is warranted. the most available nest habitat in the area. Non-thorny Our preliminaries results showed that the breed- shrubs, such as Periploca angustifolia, were not used ing biology of Maghreb Magpie slightly differs from the despite their wide availability. In addition, nests were Eurasian Magpie by nesting earlier and laying smaller often built just above the middle of the bushes, which is clutches and eggs (Högstedt 1980; Tatner 1982; Arias de similar to what has been reported in the Eurasian Mag- Reyna et al. 1984; Redondo and Carranza 1989; Ponz and pie in temperate rural environments (e.g. Dolenec 2000; Gil-Delgado 2004; Birkhead 1991). Differences in laying Tucakov and Kucsera 2008). This tendency to place nests date may obey to a latitudinal gradient effect on birds in the middle of thorny shrubs might be a defense mech- breeding phenology (Lack 1947, 1968; Cardillo 2002; Jetz anism to limit the accessibility of mammalian and avian et al. 2008). More data and further analysis are needed to nest predators. verify this hypothesis. The earlier spring in the latitudes We found that clutch size and nest survival in 2018 of North Africa in comparison with the temperate zones were lower than those in 2017. Difference seem to be of Tunisia would explain the early entry into reproduc- related to weather condition mainly rainfall. Firstly, win- tion of the Maghreb Magpie compared to the popula- ter rainfall (September to February) in 2017 (109  mm) tions of Eurasian Magpie. According de Neve et al. (2004) was higher than in 2018 (46  mm). According Rodríguez food availability directly influences laying date in many and Bustamante (2003) nest success rate is influenced species, including the Eurasian Magpie, where food sup- positively by rainfall in winter. In fact, winter rainfall may plementation significantly advanced the onset of laying increase food availability during incubation since dry (Meijer and Drent 1999). winters will force birds to quit incubation to forage when Nefla  et al. Avian Res (2021) 12:12 Page 7 of 9 It is known that egg size of magpies significantly preservation of thornier bushes in protected areas, such increases in response to food supplementation (Högstedt as the private farm where the study population currently 1981; Hochachka and Boag 1987; Ramsay and Houston live, could ensure the increase of population size by pro- 1997; Meijer and Drent 1999; de Neve and Soler 2002; de viding it with more suitable and safe nesting habitat. This Neve et al. 2004) despite the relatively inflexibility within would require a short and medium-term conservation individual female birds showed by Christians (2002). The program, involving the responsible Tunisian authorities smaller clutches and eggs recorded in our population in (i.e. general directorate of forests) but also local envi- comparison with those known in the Eurasian Magpie ronmental NGOs, and aiming at sensitizing local farm- in temperate zones may be due to possible food scarcity ers and helping them to dedicate parts of their lands to in our arid study area and/or the shorter days at our lati- thorny bush plantations. tudes. Unfortunately, we did not assess food availability Acknowledgements in our study area to test this hypothesis and to investigate Our sincere thanks go to Mr Abdelaziz Mchala, the owner of the farm where more deeply the possible role of food availability in shap- the study was carried out, who allowed us free access to the site and for his permanent support for biodiversity. We also express our deep gratitude to ing the reproductive investment of the studied birds. Haifa Ouni who contributed to field mission in 2017. We also thank Zakher Egg volume varied significantly with laying date, being Bouragaoui for his contribution in paper finalization. larger earlier in the season. This pattern matches the gen - Authors’ contributions eral trend known in birds (Bengtson 1972; Parsons 1972; AN and RO conducted the field work and collected all data. AN statistically Newton and Campbell 1975; Hill 1984; Sedinger 1992; analyzed data. SN and SS contributed to results interpretation. AN and SS were Christians 2002). This might be due to poorer quality a major contributor in writing the manuscript. All authors read and approved the final manuscript. of late breeders compared to early ones. Indeed, some young and less experienced birds often start breeding Funding later and produce less-quality eggs compared to more Not applicable. experienced birds (Christians 2002; Williams 2012; Ver- Availability of data and materials hoeven et al. 2019). Alternatively, deteriorating breeding Not applicable. conditions, notably food availability, as the season pro- gress may also result in decreasing egg volume. These Declarations hypotheses were not investigated since no data on moni- Ethics approval and consent to participate tored breeding pairs ages and food availability seasonal Not applicable. changes were available. Because the number of eggs laid by a female could be Consent for publication Not applicable. traded-off their sizes, a negative relationship between egg size and clutch size could be expected (Blackburn Competing interests 1991; de Neve and Soler 2002; Ręk 2010). The opposite The authors declare that they have no competing interests. trend could also be expected as high-quality females Author details may lay larger clutches of larger eggs compared to low- 1 Department of Biology, Faculty of Sciences of Tunis, University of Tunis El quality females (de Neve and Soler 2002; de Neve et  al. Manar, El Manar II, 2092 Tunis, Tunisia. Tunisia Wildlife Conservation Society, Bejaoua, Sidi Thabit Tunis, Tunisia. Research Unit “Ecology of Terrestrial Fauna” 2004; Lifjeld et  al. 2005). Given that no significant rela - (UR17ES44), Faculty of Sciences, University of Gabes, Zrig, 6072 Gabes, Tunisia. tionship between egg volume and clutch size was found, our results did not give support to any of the previous Received: 11 September 2020 Accepted: 18 March 2021 hypotheses. Conclusion References In conclusion, we believe that without claiming to have Abdreimov T. Birds of deserts and lowlands of Amu Daria. Tashkent: Pub Fan completely filled a lack of information, our study pro - Uzbetskoy SRR Tashkent; 1981. Antonov A, Atanasova D. Small-scale differences in the breeding ecology of vides the first and only detailed data on the reproduc - urban and rural Magpies Pica pica. Ornis Fennica. 2003;80:21–30. tive parameters of the Maghreb Magpie in Tunisia and Arias de Reyna L, Recuerda P, Corvillo M, Cruz A. Reproduccion de la urraca whole North African region. In addition to their potential (Pica pica) en Sierra Morena (Andalucia). 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