Introduction

Human activities, from climate change and habitat destruction to overharvesting and the introduction of invasive species, are having a profound impact on the natural world (Parmesan & Yohe, 2003; Halpern et al., 2008; Wong & Candolin ,2014). The driving factors of environmental change include deforestation, urban sprawl, transport infrastructures, climate change and the control of water resources by dams, canals and reservoirs (Mclamb, 2009).

Birds have been the focus of intensive research because declines in Palearctic-African migrants have been recorded throughout the Palearctic (Sanderson et al., 2006; European Bird Census Council, 2012; Vickery et al., 2014). The effective conservation of this group poses a particular challenge since migratory birds exploit geographically distinct habitats throughout the annual cycle, including different refuelling sites along migratory corridors. Effective conservation plans therefore require coordinated strategies across disparate countries and biogeographic regions.

The European Turtle-dove Streptopelia turtur (henceforth ‘Turtle-dove’) is an example of a Palearctic-African migrant that has undergone rapid and serious decline across its European range (-78% during 1980–2013; PECBMS, 2015). It has been classified as ‘Vulnerable’ throughout Europe (and ‘Near Threatened’ within the EU27 countries) following recent assessment (BirdLife International, 2015).

Potential drivers responsible for the species' decline include nesting habitat degradation (Browne et al., 2004), changes in food availability (Browne & Aebischer, 2003) and in wintering grounds, agricultural intensification (Eraud et al., 2009), hunting (Boutin & Lutz, 2007), and variation in ecological conditions throughout the migration route (Browne & Aebischer, 2001, Eraud et al., 2009). Turtle-doves in Europe and Northwest Africa are classified as different subspecies: S. t. turtur and S. t. arenicola respectively (Cramp, 1985). Most research on population decline has focused on the European subspecies and comparatively little is known about the status of the Northwest African subspecies.

In Northwest Africa, Turtle-doves are common migratory breeding birds (Isenmann & Moali, 2000; Thévenot et al., 2003; Isenmann et al., 2005; Isenmann et al., 2016). Morocco holds a large and important Turtle-dove population (Hanane, 2003). Forest areas and fruit plantations represent respectively 12.7% (Mhirit & Blerot, 1999) and 1.5% (MAPM, 2014) of the total land area (TLA) of Morocco. There, although Turtle-doves are widely distributed in forests (Hanane, 2003; Vernon et al., 2005, Cherkaoui et al., 2007) and agricultural regions (Hanane & Baâmal, 2011; Hanane, 2016a, b), they are more densely concentrated in agricultural landscapes with irrigated areas (2.2% of TLA, MAPM 2014), olive and orange orchards being particularly favoured (Hanane & Baâmal, 2011; Hanane & Besnard, 2014). This proportion is higher than that recorded in Algeria (4.47 10^-6 % of TLA, FAOSTAT, 2015) and virtually identical to that in Tunisia [2.3% of TAC, FAOSTAT (2015)]. In Morocco, the Turtle-dove is a major game species, highly valued by national and international hunters (HCEFLCD, 2013).

Most studies on both European and Northwest African Turtle-doves have focused on breeding biology (Rocha & Hidalgo, 2002; Browne et al., 2004, 2005; Boukhemza et al., 2008; Eraud et al., 2009; Hanane & Baâmal, 2011; Hanane, 2012, 2014, 2015; Brahmia et al., 2015; Kafi et al., 2015; Hanane, 2016a, 2016b), breeding habitat use (Browne & Aebisher, 2004; Browne et al., 2004; Browne et al., 2005; Bakaloudis et al., 2009; Dunn & Morris, 2012; Sáenz de Buruaga et al., 2012; Dias et al., 2013; Yahiaoui et al., 2014; Dunn et al., 2016), foraging habitat use (Browne & Aebisher, 2003; Dunn et al., 2015; Rocha & Quillfeldt, 2015; Gutiérrez-Galán & Alonso, 2016) and migration (Eraud et al., 2013; Lormée et al., 2016; Marx et al., 2016). Both subspecies are granivorous and are true migrants, spending the winter period (late October to late March) mostly in the Sahel region of Africa, south of the Sahara in a broad band spanning the continent roughly between 10°N and 20°N (Browne & Aebischer, 2001). Moreover, both S. t. turtur and S. t. arenicola nest in forests (Sáenz de Buruaga et al., 2012; Dias et al., 2013; Yahyaoui et al., 2014; Hanane & Yassin, submitted paper), fruit orchards (Peiro, 2001; Hanane & Maghnouj, 2005; Hanane, 2009) and hedgerows (Dunn & Morris, 2012; Hanane, 2012).

The goals of this review are twofold. First, I summarise existing literature on the natural history, ecology and status of the Turtle-dove in North Africa. Second, I identify the most important research gaps that need to be addressed to assist the future conservation of S. t. arenicola, and propose a framework for developing research and monitoring over the coming years. The proposals will help orient scientific research to address issues of Turtle-dove conservation on both the national and regional scales.

Scientific research on the Turtle-dove in North Africa

In Northwest Africa, 20 peer-reviewed papers have studied the Turtle-dove (Table 1) and have addressed eight topics: nest position within trees, nest density, nest success and habitat, potential competition with other dove species, age-ratio, breeding phenology, the methodological of nest detection and biometry. Of these studies, 70% (n = 14) have involved the Moroccan population and 30% (n = 6) the Algerian population. No studies were found for populations in Tunisia, Libya and Mauritania. I have therefore focused primarily on data from the Moroccan and Algerian Turtle-dove populations in this review. Research in Morocco was mostly conducted in fruit orchards. Only one study has been conducted in a forest habitat.

Current knowledge

Estimation of population size: the case of the Tadla irrigated area

Turtle-doves are a valuable game species in Morocco. Determining the game population size is a basic prerequisite for determining adequate hunting management and conservation strategies and for setting up appropriate hunting quotas. In 2013, a study was conducted in the Tadla region of central Morocco (Figure 1) to estimate the minimum population size in this area (Hanane & Besnard, 2011). The study was conducted in olive and orange orchards at the peak of the breeding season (from 27 May to 10 June, Hanane & Baâmal, 2011). The authors found that nest density in orange orchards was three times higher than in olive orchards (Hanane & Besnard, 2014) and the size of the breeding population in the Tadla region was estimated to be 58,969 pairs (range 46,281-75,183; Hanane & Besnard, 2014). Olive hedgerows (olive hedge lines) adjacent to crops of cereal (wheat and barley) and forage (alfalfa and com) promote the settlement of Turtle-doves by providing food in close proximity to their nest sites (Hanane, 2009, 2014). The difference in nest density between orange and olive trees is likely to be driven by the degree of human disturbance. The Turtle-dove breeding period coincides with the presence of fruits in orange orchards, which are highly protected against human intrusions, particularly before the harvests. Such protection is non-existent in olive groves (Hanane & Baâmal, 2011; Hanane & Besnard, 2014) and greater human disturbance in olive groves relative to orange groves may result in lower nest densities.

Table 1

Synthesis of published papers on the Turtle-dove Streptopelia turtur arenicola in North Africa.

[Síntesis de los artículos publicados sobre la tórtola europea Streptopelia turtur en el norte de África.]

Although this estimate did not considered belated and precocious breeding pairs, it clearly shows that the Tadla irrigated area is one of the most important breeding grounds for Turtle-doves in the Mediterranean basin. To provide an order of magnitude, the estimate of population size in Tadla is much higher than that for many European countries, including Greece (Snow & Perrins, 1998), Slovenia (Tucker & Heath, 1994) and Cyprus (BirdLife International, 2004), although lower than the overall population sizes reported for Spain and France (Rocha et al., 2006; Comolet-Tirman et al., 2015). The Tadla data confirms that Morocco is one of the most important breeding areas since it holds high densities of birds, particularly since other irrigated areas in the country, such as the Souss valley (Taroudant Region) in the southwest and the Triffa plain (Berkane Region) in the northeast (I. Cherkaoui, pers. comm.), are known to have similar densities of breeding doves (Hanane, 2009). A comparison with nest densities reported in Algerian populations (Table 2) further demonstrates the importance of Moroccan irrigated areas as a high-density nesting zone for African Turtle-doves. In studying the main landscape metrics affecting abundance of game species in a semi-arid agroecosystem in the Mediterranean region, Belda et al. (2011) have also reported the great abundance of Turtle-doves in irrigated fruit orchards in Europe.

Fig. 1.

The location of the Tadla irrigated area in Morocco (Hanane, 2015).

[Mapa de la localización de la zona de regadíos de Tadla en Marruecos (Hanane, 2015).]

Table 2

Turtle-dove nest densities (ha-1) in olive and orange plantations in Morocco and Algeria.

[Densidad de nidos (ha-1) en cultivos de olivos y naranjos en Marruecos y Argelia.]

Occurrence during the annual cycle

Several studies have monitored the timing of spring arrival at irrigated areas throughout Morocco. Turtle-doves arrive earliest in southern Morocco, particularly in the Souss valley irrigated area: in 2009 one at Taroudant on 22 February was followed by birds in the central regions of the Haouz and Tadla: respectively one at Marrakech on 8th March and two at Beni Mellal on 27th March (Hanane, 2009). Regular censuses throughout the season show three important temporal phases in the Turtledove breeding cycle (Figure 2): (i) prenuptial migration (March-May) and (ii) postnuptial migration (September-October), in which a somewhat lower number of Turtle-doves were recorded (Fig. 2), and (iii) a stable period (June-August) characterised by a large number of breeding Turtle-doves (Fig. 2) (Hanane, 2009; Hanane & Maghnouj, 2005). A significant difference in the number of Turtledoves sighted per 4 km transect was also recorded between the three irrigated study areas, with higher densities found in the Souss and Tadla (94.2 ± 25.9 and 70.9 ± 27.5 respectively) than in Haouz (27.9 ± 9.00) (own unpublished data).

Fig. 2.

Mean number of Turtle-Doves sighted per transect throughout an annual cycle (in 2009) in the Souss, Haouz and Tadla irrigated areas.

[Número medio de tórtolas europeas registradas por transecto durante un ciclo anual (en 2009) en los perímetros irrigados de Souss, Haouz y Tadla.]

Nesting success

Future research directions

Identification of migration flyways and Wintering Areas

Knowledge of the migratory patterns of the Northwest African population of S. t. arenicola is very limited or non-existent. Many questions remain unanswered, including: (i) what are the main migratory routes of North African Turtle-doves? (ii) where are their major stopover sites? (iii) where are their principal wintering areas? (iv) do North African populations use the same wintering grounds and migratory routes as the European subspecies? If so, to what extent do the two races overlap in habitat and diet? Such questions require research to clarify the Turtle-dove migration system and to develop appropriate conservation strategies.

New technologies, such as light-level geolocators (e.g. Bächler et al., 2010; Catry et al., 2011; Akesson et al., 2012; Bairlein et al., 2012; Kristensen et al., 2013) and satellite tracking [Geo Location Sensor (GLS),Eraud et al., 2013; López-López, 2016; Lormee et al., 2016)], are now used for tracking Afro-Palearctic migratory birds, including Turtledoves (Eraud et al., 2013; Lormee et al., 2016). Application of these emerging tracking technologies to North African Turtle-doves would help identify their migratory pathways and strategies (Vickery et al., 2014).

Breeding ecology

Nest sites provide the basic needs of breeding adults, eggs and young, including protection from inclement weather (Sadoti, 2008) human disturbance (Hanane et al., 2012; Hanane & Besnard, 2014) and predators (Hatchwell et al., 1999) and offering proximity to food sources (Wiehn & Korpimaki, 1997). Identifying the ecological factors associated with nest site selection in both natural and artificial habitats and at diverse spatial scales: including nest-tree, nest-site, territory and landscape, is therefore important for determining high-priority protected areas. Such information is also useful in assessing the effects of nest predation on the productivity and abundance of Turtle-dove populations.

Regarding survival, it has been noticed that nest desertion is the most important source of reproductive failure for breeding Turtle-doves in Northwest Africa (Hanane & Maghnouj, 2005; Hanane & Baâmal, 2011; Boukhamza et al., 2008). For this reason, it is essential to identify the factors leading to nest desertion within both natural and man-made habitats in order to minimise their impact on breeding success. Three factors contributing to nest desertion are agricultural disruption, hunting and children searching for nests. This last activity overlaps with the breeding season during the latter half of the nesting season period (26.8%). Turtle-doves in orchards are disturbed by several forms of human activity (Mitchell et al., 1996; Hanane & Baâmal, 2011). Agricultural practices (e.g. tillage, grazing, fruit harvesting, tree pruning, application of pesticides and herbicides) are known to impact bird populations directly through mortality or indirectly by modifying food availability and affecting breeding success (O’Connor & Shrubb, 1986; Newton, 2004; Vanbeek et al., 2014; Hanane, 2016a). It would therefore be important to investigate, for instance, how orange orchards constitute an optimal breeding habitat during the first part of the breeding season but thereafter become markedly sub-optimal. Examining the relationship between different types of agricultural habitats and activities and the breeding density, reproductive success and nest desertion rates of Turtle-doves is thus highly important. Since most previous research has focused on irrigated regions, it would be interesting to compare nest density and nesting success in Moroccan agricultural habitats where irrigation is absent.

Genetic research

The subspecies category was developed to enhance understanding of geographic variation and speciation, and to refine taxonomic distinction (Torstrom et al., 2014). Two subspecies of Turtle-doves occur in Northwest Africa, S. t. arenicola which breeds in the region and S. t. turtur which nests in Europe and crosses the region; two other subspecies are extralimital. However, under the influence of both global changes and anthropogenic landscape modification, it is possible that the distributions of the two local subspecies are shifting. No comparative genetic research has been conducted on the Northwest African or European subspecies (but see, Calderon et al., 2016). Using genetic analysis to assess ecological factors such as population connectivity and migration routes would help target conservation efforts on the most important regions.

Parasites and disease research

Recent studies of Turtle-doves in Britain (Lennon et al., 2013; Stockdale et al., 2015) have shown that the protozoan parasite Trichomonas gallinae causes mortality of adults and chicks. For this reason, identifying and studying the sources and prevalence of parasitic diseases is of great importance, not only in North Africa, but in all countries frequented by the Turtle-dove. Comparing the prevalence levels of T. gallinae between the two local subspecies would constitute another good way of understanding differences in population dynamics.

Further needs

Coordinating research efforts among countries is recommended to reach the ultimate objective of conserving Turtle-doves. Although a scientific monitoring network focused on migratory birds is well-established in Europe (e.g.  http://www.ebcc.info/pecbm.html, French ACT programme, Spanish SACRE programme), no similar network exists in North Africa. Setting up a similar scientific monitoring scheme in this region would benefit not just the Turtle-dove but also other migrant species (e.g. the Common Quail Coturnix coturnix) as well as residents (e.g. the Barbary Partridge Alectoris barbara and Woodpigeon Columba palumbus). Comprehensive data on abundance, habitats, predators, food supplies and climatic influences will help implement an effective management strategy. Moreover, standardising methodological approaches will facilitate broad analysis and implementation of conservation benchmarks across countries.

Conclusions

This review provides a comprehensive synthesis of the current state of knowledge of the Turtle-dove, an important game species in North African intensive farmlands. It highlights priority areas for future research to assist in the conservation of the species. As global climate change and anthropogenic landscape modification progress, scientific vigilance is required to maintain biodiversity. Indeed, there is an urgent need to set up an integrated programme of long-term ecological monitoring in North African farmlands and forests and to apply new technologies to address pressing conservation problems. This approach will enable researchers and policymakers: (i) to assess the importance of different ecosystems for the maintenance of biodiversity, (ii) to identify population trends of species of conservation concern, and (iii) to quantify over time the impact of human disturbance on habitat quality, breeding performance and population size of species of conservation concern. This approach requires the existence, on a national scale, of networks for monitoring Afro-Palearctic migrant bird populations.

Overall, the role of scientific research in providing an evidence base for management actions is of paramount importance. Scientific collaboration among research institutions, both at regional and international scales, is to be encouraged and strengthened in order to share knowledge, skills and techniques.