Origin and Long-Term Trend of Italian Breeding Forest Birds in the Mediterranean Context

1. Introduction

From the ornithological point of view, the Mediterranean area is one of the most explored regions, but for at least two millennia it has also been among the most densely populated areas by humans and most exploited by agriculture at the expense of forest areas. As for the forests that used to cover Italian territory, much of them have been taken away to make room for agriculture; this has undoubtedly caused a decline in forest bird species, however, less than species living in other environments. Italian forest bird populations, like those in the rest of the Mediterranean, are still substantial and undoubtedly deserve special attention from a biogeographical and conservationist point of view.

Altogether, over the last two centuries, the populations of some species of Italy's avifauna have gone into definitive extinction and others have undergone an unprecedented decline, due to direct and indirect anthropic pressure. The extinction of species in Italy is mainly due to man's increasingly intrusive activities over the millennia, but especially in the 20^th century, when the vast majority of extinctions were recorded in the country. However, in the present century, as if to counterbalance the decline of some species, other birds are experiencing increases previously unreported in Italy, in some cases already recorded in other European countries. Recently, some forest species begun a process of colonization of environments that are covered by tree vegetation, but are generally planted by man, like urban habitats. For example, woodpigeon Columba palumbus, blackbird Turdus merula, magpie Pica pica, jay Garrulus glandarius and serin Serinus serinus since the 1990s have started to colonize urban areas and have become an integral part of the avifauna of built-up areas.

At the same time, it is difficult to understand the reasons for the decline of some species; it is not always clear whether it has been the excessive hunting, the destruction and fragmentation of some habitats, the climate change, or in the case of forest environments the fires, generally arson, that occur more frequently and violently each year. Increasing the extent of areas covered by large forest fires in Italy in the last fifteen years, in 2023 approaching 69,000 ha, including more than 10,000 ha of forest ecosystems; the forests involved are largely Mediterranean scrub and oakwood (61%) and areas covered by coniferous forests and afforestation (21%). Eighty-nine percent of the areas burned in 2023 are in Sicily (72%) and Calabria (17%) (data after the Istituto Superiore per la Protezione e la Ricerca Ambientale, https://www.isprambiente.gov.it/). Thus, undoubtedly the fires could be one of the main local causes of the decline of some forest and scrubland species, particularly those that are more demanding and have a rather specialized ecological niche (e.g., woodpeckers, treecreepers, etc.).

Italy has a total land area of 302,073 km², while its present wooded surface is about 120,000 km², amounting to ca. 40% of the total surface [1]. Forests historically occupied a large part of Italy's land area, but as early as Roman times they were reduced for various reasons (use of timber for shipbuilding, modification of the soil to make it arable, etc.). At the beginning of the last century, however, substantial afforestation activity took place that increased the wooded area. According to recent statistics, the surface of forests in Italy presently is increasing, but not all forests are equal, there is a big difference between natural forests and afforestation, of course. About 65,630 km² (22% of total Italian land area) of the contemporary forests surfaces do not have a natural origin, but are the result of secondary successions occurred on abandoned farmed land since 1888; ca. 10,000 km² (3.3%) are due to afforestation carried out between 1883 and 1939, and between 1952 and 1972. About 80% of them was done with conifers, mostly black pine, sometime replacing previous broadleaved woods [1].

During the course of our lives, it is rather difficult to have clear-cut answers as to the trend of species, but if we go through the past through the bibliography, we can gain a much better insight into the population dynamics of different species. The aim of this study was precisely to try to understand the old origin of Italian breeding forest birds and to investigate the evolution of their long-term trend over a fairly long period, from 1872 to 2022, i.e. 150 years, for which a conspicuous bibliography is available. Since, here we are talking about the entire Italian forest surface, it will not be possible to subdivide forests by essence and characteristics, but we will try to make some distinctions in the discussion.

2. Materials and Methods

Four periods were chosen between 1872 and 2022 in order to obtain an overall trend of breeding forest birds in Italy: a) before 1872 [2]; b) 1873-1929 [3,4,5]; c) 1930-1993 [6,7]; d) 1994-2022 [8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23]. The time periods were chosen on the basis of the available bibliography and therefore cover different periods of time, namely ca. 50, 56, 63, 28 years, respectively. By following the trend over 15 decades, and carefully studying species by species what the different authors have written, it was possible to understand the possible long-term status of each species (stable, increasing, decreasing, strongly decreasing, fluctuating). The choice to include some species within the fluctuating category may appear subjective, but it is the result of careful literature analysis and decades of personal experience; however, it is likely that another researcher had included some of them among different categories. The category of fluctuating species is generally overlooked by most ornithologists, but really there are species that have undergone positive and negative population number changes that are very difficult to understand (e.g., hazel grouse, hawfinch); other species, like the crossbill, due to the irregular cone seeds availability, fluctuate regularly in central-north Europe, however much less in the Mediterranean area.

The choice of forest species was established on the basis of their main habitat according to Brichetti and Fracasso [8,9,10,11,12,13,14,15,16,17,18] and Lardelli et al. [23]; e.g., some species, like blackbird, common redstart Phoenicurus phoenicurus, and European serin were excluded because although they live also in woody habitats, they occupy a very large part of arboreal habitats, including orchards and urban ones [23]. Additionally, African blue tit Cyanistes teneriffae and long-legged buzzard Buteo rufinus were excluded from the Italian list, being present outside their range only in the small island of Pantelleria (Sicily), just 80 km away from Tunisia (North Africa).

The habitat of each species was obtained from the bibliography and personal experience; the ecological niche fulfilled by each species was divided into three parts (trees, soil and undergrowth), in order to define the main activities (nesting, feeding) of the species in the three portions of the forest environment considered. Additionally, on the basis of species distribution and ability to colonize forest (or urban) habitats of little naturalistic interest the species was assigned one of the following three values: 1: of broad ecological value; 2: moderately ecologically demanding; 3: very ecologically demanding; a higher value of species corresponds to a greater number of ecologically demanding birds.

The conservation status of species in Europe has been obtained from BirdLife International (Red List) [24]. In order to carry out a comparison with forest birds of the Iberian and Balkan peninsulas, a list of forest birds breeding in those peninsulas was taken from the latest European Atlas [25] and other local references [26,27,28,29]. Sørensen's similarity index has been used, S = 2a/(2a+b+c), where a is the number of species in common in the two peninsulas considered, b and c are respectively the numbers of species found only in the first and only in the second peninsula compared. S can result between 0 (completely different) and 1 (identical) [30]. Concerning the trend of forest birds, a comparison has been tentatively carried out with the European trend simulated in the late 21^th century in the climatic Atlas by Huntley et al. [31]. The systematics follow Baccetti, Fracasso and COI [32].

3. Results

3.1. Breeding Forest Species in Italy

The species regularly breeding in Italian forests, i.e. mainly present in these environments, number 61 (Table 1) and represent a modest percentage (20.8%) of the 293 species found breeding in Italy [23]. They belong to 20 families, namely: Phasianidae Tetraoninae (3 species), Columbidae (2 species), Caprimulgidae (1 species), Scolopacidae (1 species), Strigidae (6 species), Accipitridae (6 species), Picidae (8 species), Falconidae (1 species), Corvidae (2 species), Paridae (6 species), Phylloscopidae (3 species), Aegithalidae (1 species), Sylviidae (4 species), Certhiidae (2 species), Sittidae (1 species), Troglodytidae (1 species), Turdidae (4 species), Muscicapidae (2 species), Regulidae (2 species), and Fringillidae (5 species) (Table 2). Except for 12 species (19.7%), i. e. the three species of Phasianidae Tetraoninae (capercaillie Tetrao urogallus, black grouse Lyrurus tetrix, hazel grouse Bonasa bonasia), boreal owl Aegolius funereus, pygmy owl Glaucidium passerinum, Ural owl Strix uralensis, grey-faced woodpecker Picus canus, three-toed woodpecker Picoides tridactylus, northern nutcracker Nucifraga caryocatactes, willow tit Poecile palustris, and fieldfare Turdus pilaris, absent south of Alps, the other 49 species (80.3%) are present in different regions of the Italian peninsula. However, 2 species (3.3%) are present only in north Italy (barred warbler Sylvia nisoria, and crested tit Lophophanes cristatus), while the other 47 species cover much of the peninsula area. Only in the islands (Sicily and Sardinia) the number of breeding forest species is reduced, due to insularity species impoverishment. Out of 61 species, none became extinct through 150 years (but this occurred locally), 28 (45.9%) resulted stable, 2 (3.3%) strongly decreasing, 8 (13.1%) decreasing, 18 (29.5%) increasing, and 5 (8.2%) fluctuating (Figure 1). Most species are sedentary, but at least 16 (26.2%) are migrant breeder and wintering. This means that in some cases breeding populations are very small (e.g., Eurasian woodcock Scolopax rusticola, rare breeder in Italy), but conspicuous populations arrive during the winter; in other cases wintering populations are added to already conspicuous breeding populations (e.g., European robin Erithacus rubecula). Only 8 (13.1%) are trans-Saharan species, that is breeding in Europe and wintering in tropical Africa.

Though they are species related to forest cover, do not all have similar ecology, habits and trophic requirements. In fact, if we look closely at the different families, we can see that the forest is the habitat, but the ecological niche is sometimes fulfilled in the undergrowth, in clearings, at the edge of the forest, where the species find food, which may consist of invertebrates, berries, small mammals, etc. Table 2 summarizes the essential data highlighting the importance of trees, soil (litter) and undergrowth for the different species belonging to 20 bird families. It seems clear that while there are species groups closely related to trees (e.g., woodpeckers, treecreepers and nuthatch), many other species use forest trees only to place their nests and may forage both on the ground and in the undergrowth. Overall, 56 species (91.8%) use the trees for nesting. The most specialized species resulted to be those belonging to Picidae family, which are characterized by the zygodactily, that is the presence of two fingers pointing forward and two backward, other than the hardened rectrices that allow to lean on logs.

3.2. Biogeographical Peculiarities of the Breeding Forest Avifauna in Italy and the Other Peninsulas

Considering the Mediterranean broadly, three peninsulas project southwards into this great sea, the Iberian peninsula (which touches the Atlantic to the west), the Balkan peninsula (which touches the Black Sea to the east) and the Italian peninsula, the only one completely within the Mediterranean and proportionately narrow and long compared to the other two (Figure 2). In these regions the fauna generally has a north-south impoverishment, known as the 'peninsula effect', a form of impoverishment in 'quasi-island' territories, sensu Mac Arthur and Wilson [36; cf. also 37,38]. With regard to forest birds on the Italian peninsula, a north-south gradient of depletion has not been observed. The Apennines of peninsular Italy are home to large forests of various species with breeding bird populations in the southernmost part not substantially different from those in the north, with the exceptions above recorded.

Interestingly enough, are not the same northern species that have penetrated southwards into the peninsulas; for example, in the Iberian and Balkan peninsulas, crested tit has moved southwards, but in the Italian peninsula it has stopped in the northern Apennines. Conversely, Greece (latitude of S Italy) is the southernmost limit of western capercaillie, black grouse, hazel grouse, Eurasian pygmy-owl, boreal owl, grey-faced woodpecker, three-toed woodpecker, willow tit, and northern nutcracker [29], all species absent south of Italian Alps. Some species are present in the Balkan peninsula and northern Italy, but have not reached the Iberian peninsula: hazel grouse, grey-faced woodpecker, three-toed woodpecker, willow tit, northern nutcracker, wood warbler Phylloscopus sibilatrix, barred warbler, collared flycatcher Ficedula albicollis, and fieldfare. Others are present in the Balkan and Italian peninsulas, but reach only the north of Iberian peninsula: black woodpecker Dryocopus martius, middle spotted woodpecker Leiopicus medius, white-backed woodpecker Dendrocopos leucotos, ring ouzel Turdus torquatus, willow tit, and Eurasian treecreeper Certhia familiaris. Additionally, western Bonelli’s warbler Phylloscopus bonelli and western orphean warbler Sylvia hortensis are west Mediterranean species, present only in the Italian and Iberian peninsulas. Balkan peninsula has three forest birds not living in other Mediterranean areas: Syrian woodpecker Dendrocopos syriacus, Krüper’s nuthatch Sitta krueperi [living only on Lesvos Island (Greece), outside Turkey and Caucasus], and sombre tit Poecile lugubris [25]. Finally, Iberian peninsula has two endemic species, Iberian green woodpecker Picus sharpei (below discussed), and Iberian chiffchaff Phylloscopus ibericus.

The following numbers of breeding forest species were obtained from the Mediterranean peninsulas: Iberian peninsula 49 [25,26], Italian peninsula 61 [23], Balkan peninsula 64 [25,27,28,29]. The common component of the breeding forest avifauna of each peninsula is about 50%; altogether, 68 forest species breed in the three Mediterranean peninsulas, more or less equally distributed between them, but only part of species breeding in forests of each peninsula is in common with the other two (Sørensen's similarity index: 0.45-0.48; Table 3, Table 4, Figure 3, Figure 4). Seven species are trans-Saharan migrants in the Iberian and Balkan peninsulas, 14.3% and 10.9%, respectively, figures very similar to those obtained from Italian peninsula (13.1%).

Concerning the ecological value, in Table 3 are reported the sum of species values and their mean; while the sum of values may depend on the number of species, the mean is a more objective value. It resulted to be 2.0 for Iberian forest birds, and 2.1 for Italian and Balkan ones.

The conservation status of all Italian breeding forest birds resulted to be ‘Least Concern’ (LC), which means that no species is threatened.

4. Discussion

4.1. Comparison with the Trend Simulated in the late 21^th Century

An attempt was made to compare the data collected from the Italian bibliography over 150 years and the trend simulated in the late 21^st century by Huntley et al. [31]; it is not possible to make this comparison as the two methodologies are profoundly different. However, it is considered useful to make a few practical considerations. According to Huntley et al. [31] in the late 21^st century of the 61 forest species considered here 35 (57.4%) will be decreasing in southern Europe, 14 (22.9%) decreasing in central Europe, only 8 (13.1%) remain stable, 2 (3.3%) increasing in southern and central Europe, respectively (Figure 5). For 12 species (19.7%), the trend matches both with the literature search through 150 years and with the simulation in the late 21^st century; namely seven species (black grouse, capercaillie, eagle owl, stock dove, garden warbler, fieldfare, and ring ouzel) resulted to be decreasing in both the 150-year considered period and the late 21^st century simulations, two species (short-toed snake-eagle, and booted eagle) were found to be increasing, and three species (blue tit, great tit, and wren) resulted stable in the two time periods. It seems obvious that the two methodologies give different results; in particular the simulation for forest species based on climatic trend is very pessimistic, as altogether 80.3% are expected to decline in the late 21^st century, while the trend calculated through the bibliographic analysis gives a much lower figure (16.4%). Even if a predictive analysis that takes into account future climate projections should not disregard a bibliographic reference of long-term species trends, which implicitly includes information on each species' potential for possible adaptation to changes in habitat or climate, predictions for the late 21^st century may be sadly true.

4.2. Forest Birds on Italian Peninsula and Islands

Considering that the Iberian peninsula is the extreme western apex of Eurasia, a minimal depletion of species seems normal, which in contrast is not evident in the Balkan peninsula, an appendage of Asia. The higher number of forest birds in the Balkan peninsula can be explained by the fact that it is an area in continuity with Asia and suffers less from the peninsula effect, more evident in the other two Mediterranean peninsulas. In addition, the extreme south-western land of Eurasia (Iberian peninsula), with its isolation, allowed the evolution of two endemic species of forest birds, Iberian woodpecker (Pyrenees), and Iberian chiffchaff (westernmost French and Spanish Pyrenees and western parts of the peninsula). Concerning endemic taxa of Mediterranean Europe, another species lives in Corsica, the Corsican nuthatch Sitta whiteheadi, linked to black pine Pinus nigra forests, taxonomically related to other two forest endemic species, one living on Kabyle, the Algerian nuthatch Sitta ledanti linked to forest remains dominated by Abies numidica, and the other, Krüper nuthatch Sitta krueperi, linked to Turkish pine Pinus brutia, living in Turkey, Lesvos Is. (Greece), and Caucasus.

The forests of peninsular Italy do not host any endemic representatives among the birds; all the species can be found in forest environments elsewhere in Europe. However, the Apennines are home to forest bird species that are most likely relicts of the last ice age, i.e. around 18,000-20,000 years old. Among these there is the trans-Adriatic subspecies of the white-backed woodpecker Dendrocopos leucotos lilfordi. This taxon, distributed in the Iberian and French Pyrenees to Asia Minor, Caucasus and Transcaucasia, may have arrived from the Balkans to Apennines and Pyrenees during the last ice age; the typical subspecies (leucotos), widespread across Eurasia from north, central and eastern Europe to northeast Asia, may instead have arrived in central Europe from the north. A similar case is that of the Eurasian green woodpecker; the species-complex consists of Picus viridis, distributed from western Europe to the Caucasus and Iran, the Iberian green woodpecker, distributed in the Iberian and French Pyrenees, and the related Le Vaillant’s woodpecker P. vaillantii, distributed in north-western Africa from central Morocco to Tunisia (Maghreb). The divergence event between the Iberian and the European lineages took place during the mid-Pleistocene (0.7–1.2 Ma), and a post-glacial range expansion of two lineages from distinct refugia located in the Iberian peninsula and in eastern Europe occurred. During the Pleistocene much of the forests suitable for green woodpeckers in central and northern Europe were covered by ice, tundra, steppe or other unsuitable habitat; thus, the woodpeckers might have occupied the current range during the past 20,000 years [39,40]. A similar case is reported also for a mammal, the chamois, present with Rupicapra rupicapra in the Alps and with another species, Rupicapra pyrenaica (subdivided into two subspecies, pyrenaica and ornata) in Pyrenees and Apennines, respectively [41].

Other possible relicts of the last ice age in the Apennines are black woodpecker, middle spotted woodpecker (Figure 6), goldcrest, Eurasian treecreeper, collared flycatcher (Figure 7), the western European subspecies of the bullfinch Pyrrhula pyrrhula europoea, howfinch Coccothraustes coccothraustes (with sedentary populations also in Sardinia), Eurasian siskin Spinus spinus (with a small breeding population also in Sicily, on Etna) (Figure 8) and red crossbill Loxia curvirostra ‘sensu lato’. The latter, unlike the northern populations (linked to cone seeds of larch and spruce pines), is associated with the black pine (with bigger cones than spruces and larches) and characterized by a more massive beak, smaller size, evident discoloration in both males and females, and marked sedentariness (Figure 9). Similar populations of sedentary crossbills evolved not only in the Italian peninsula, but also in the Iberian and Balkan peninsulas, Corsica, Sicily (Etna), Cyprus, and North Africa. Some of them live at the expense of the cones of the Aleppo pine Pinus halepensis, also characterized by big size. Polytypical species status has recently been proposed for the three main sedentary populations on Mediterranean peninsulas, islands and North Africa (L. balearica in the Balearics and Iberian peninsula, L. poliogyna in North Africa, Italian peninsula and Corsica, L. guillemardi in Cyprus and Balkan peninsula), as was previously the case for Loxia scotica [42].

The situation is different on the large Italian islands, which are poorer in species than peninsular Italy. Sicily has been definitively an island for only 20 thousand years [43], so it is assumed that numerous species reached it earlier and then remained isolated for around twenty thousand generations. However, this was enough to give rise to local endemic forms, as below reported. Far more isolated is Sardinia, which, in accordance with the reconstructions of Alvarez et al. [44], together with Corsica and other microplates (among which those that formed the Kabyle in Algeria) would have broken away from the Iberian peninsula and migrated towards the center of the Tyrrhenian Sea. This would have happened over 20 million years ago; this ancient isolation undoubtedly allowed numerous invertebrate species to differentiate, but as far as forest birds are concerned, there must have been some gene flow with other Mediterranean populations in fairly recent times. However, the isolation allowed the subspecific differentiation of some forest birds: jay Garrulus glandarius ichnusae, coal tit Periparus ater sardus, blue tit Cyanistes caeruleus ogliastrae, great tit Parus major corsus, wren Troglodytes troglodytes koenigi, sparrowhawk Accipiter nisus wolterstorffi, goshawk Accipiter gentilis arrigonii, and great spotted woodpecker Dendrocopos major harterti. Three of them are non-Passeriformes, which generally require longer isolation times than Passeriformes to differentiate themselves from continental populations. Most of them are subspecies in the Sardinian-Corsican system, recognized by taxonomists [45,46].

In Sicily, by far more recent island than Sardinia, live some isolated populations not yet taxonomically recognized, but certainly differentiated from continental ones. For example, Sicilian great and blue tits are smaller in size compared to continental individuals [pers. obs.]. The smaller size of these birds can be explained by Bergmann's rule according to which there is an inverse correlation between body size and average temperature in the geographical area of origin. The relict populations of the above-mentioned sedentary species may have remained isolated for several millennia, although for some of them probably there may have been mixing with more recent northern immigrant populations. It would be interesting to establish whether the isolation caused adaptations and differentiations or whether the gene flow was maintained, a fact that would deserve to be studied in depth with genomic investigations. A particular case is represented by the Sicilian population of long-tailed tit Aegithalos caudatus siculus (Figure 10), a taxon found mainly in broadleaved woods; its isolation in Sicily for at least 20,000 years has led to a clear differentiation, not only in the grey back, but also in the coloring of the head, which generally lacks the characteristic dark lateral bands, in the grey (not reddish) scapulars and in the size of the wing and tail, which are on average shorter than those of continental individuals [47,48]. It seems that interbreeding with peninsular populations does not occur, thanks to the 3 km long sea arm of the Strait of Messina between Sicily and south Italy. A similar case of isolation, but not occurred in a forest insular species, is that of the Sicilian rock partridge Alectoris graeca whitakeri, clearly differentiated from the peninsular taxon.

Probably due to the loss of mature woodland areas in Sicily, the eagle owl and three woodpecker species became extinct in the 20^th century, namely black woodpecker, Eurasian green woodpecker, and lesser spotted woodpecker Dryobates minor [49]; the latter seems that disappeared also from Sardinia [22,33].

4.3. Palaeogeographical Vicissitudes of the Mediterranean

The Mediterranean sea is subject to very complex tectonic activities, due primarily to the strong collision between the large Eurasian Plate to the north and the African Plate to the south. Between them there are other microplates; the Hellenic Arc is an arc-shaped tectonic structure about 1,000 km long that stretches from the Ionian Islands, located north-west of Greece, to the island of Rhodes from which the Cyprus Arc originates.

Generating this complex structure was the subduction (still ongoing) of the African plate, moving S-N at a rate of about 10 mm/year, under the Aegean microplate, which in turn moves in a NE-SW direction by about 45 mm/year [50].

In order to understand the origin of the breeding forest avifauna in Italy, it should useful to trace the various vicissitudes that Mediterranean vegetation has gone through since the Tertiary. During the Late Cretaceous and Paleocene periods, tropical and subtropical forests dominated by oaks, laurels and palms covered the lower-middle latitudes of Eurasia and North America; at the beginning of the Tertiary period, North Africa was characterized by tropical forests and savannah. With the expansion of drier climates in Europe and Asia, xerophyllous species appeared in the Middle Eocene, which include ancestor species of today's woody plants with leathery leaves. In the early Oligocene, xerophyllous floras were widespread; environmental conditions from Spain to Central Asia favored Mediterranean-type plants [48,51].

In the Miocene (around seven million years ago), the climate of much of the earth's surface was torrid and the waters were inhabited by tropical species. In the second half of the Messinian (between about five and six million years ago), an exceptional event occurred: the Messinian salinity crisis, i.e. the drying up of the Mediterranean Sea. The relationship between the Atlantic Ocean and the Mediterranean Sea was interrupted; only a few large brackish lagoons remained, water was scarce for at least half a million years, and lions, buffalos, monkeys and elephants moved to the only areas where water still existed [51]. The pollen research carried out by Fauquette et al. [52] established that the Mediterranean area was then characterized by two types of vegetation: in the southernmost part conditions were dry and warm and the vegetation was relatively open, while in the northernmost part the warm-humid conditions allowed the growth of forest-type vegetation. The researchers were also able to establish that the salinity crisis was not directly caused by the climate and that the climate did not change substantially during this period, particularly in the southernmost part of the area, where it remained very dry and warm before, during and after the salinity crisis [52].

The Quaternary was a period of exceptional climatic instability [53]. During the cold-dry episodes, forests were replaced by steppes and tundra in the north and by savannah-like formations from the tropics to southern Europe; the continental vertebrate faunas of peninsular Italy and Sicily included elephants, lions and hippos, indicating a savannah environment even at our latitudes. In the Pliocene (between four and two and half million years ago), the climate must still have been relatively warm; the Mediterranean climate stabilized more or less three million years ago, but considerable climatic changes also occurred in the Pleistocene (between two and half million and eleven thousand seven hundred years ago), particularly during glaciations and interglacial periods.

The effects of each glaciation on the fauna were cancelled out by the next one, so that the last glaciation explains the distribution and diversification patterns of today's avifauna. Although the deciduous forests of Europe were reduced and compressed in the Mediterranean peninsulas during the Pleistocene, areas covered by forests remained in North Africa and the Middle East. During glacial periods there was a drop in sea level of the order of 60 meters in the first glaciation and as much as 130 meters in the last (Würm, around eighteen thousand years ago); the maximum temperatures would have allowed the coexistence of European vegetation and associated fauna [54]. It is from the period before the first glaciation (around 50,000 years ago) that pollen shows the presence of a Mediterranean-type vegetation, i.e. scrubland characterized by Quercus ilex (or Q. coccifera/calliprinos), Pistacia and Ericaceae (mainly represented by Arbutus unedo) [55]. Pollens dating back to the Würmian glaciation (30,000-25,000 years ago) show that much of southern Europe was composed of Artemisia steppes with scattered patches of forest (the average temperature was ca. 8 °C lower than today) and only later, after the retreat of the glaciers, 15,000 years ago, there was an expansion of Juniperus and Pinus, while 13,500 years ago, a re-growth of Quercus forests was observed [56]. This kind of vegetation favored the spread of bird species associated to coniferous (e.g., crossbills, siskin) and to evergreen broadleaved (many species of passerines, woodpeckers, etc.) (see Table 1).

In Mediterranean habitats today evergreen sclerophylls are found, which have adapted to the abundant winter rains that alternate with very dry summers; they have small, thick, evergreen leaves, usually with a villous covering and frequently with a robust cuticle, which allow them to retain moisture during long dry periods [57]. Their deep root systems allow them to capture water at depth; in addition, many species are well adapted to withstand fire disturbance, promoting rapid re-growth of vegetation after fire. This type of structure seems to have originated in relatively warm and moderately mesic conditions and has pre-adapted different species to climates with shorter periods of rainfall and greater temperature variability. Such modifications are ancient, as can be judged from the presence of essentially modern scrub and woodland evergreen sclerophyll taxa in the Miocene and Oligocene floras, which experienced very wet summers. These characters are therefore not an evolutionary response to an ancient and persistent Mediterranean-type climate; from a functional point of view, adaptation to the Mediterranean climate is a fine-tuning when considering the ability to reproduce in a short period of wet weather during the coldest part of the year [57]. Aridity in summer is the major limiting factor for plant activity, not the cold of winter; flowering and growth take place mainly in winter and spring and only a few species and rare individuals vegetate in summer [51,53]. The Mediterranean climate is therefore much younger than the sclerophylls, as it only appeared after the first glacial events.

4.4. The Climatic Phases

The climatic phases have been studied both by sampling and identifying fossil pollen, and by analyzing the ratio of oxygen ¹⁸O to ¹⁶O, which changes with changing temperatures. When temperatures are very low due to ice caps, i.e. during glaciations, water and marine organisms are enriched in ¹⁸O and thus the ratio between ¹⁸O and ¹⁶O is in favor of the former; the opposite occurs when temperatures rise, i.e. during interglacial stages [52]. Thanks to the study of the ratio between ¹⁸O and ¹⁶O, it was discovered that glacial and interglacial stages amount to about sixty and glaciations to about thirty. These periodic climatic changes make us understand how shifts in the range of fauna and flora could have taken place southwards and then northwards, and also how so many endemic invertebrate species could have formed in mountainous areas of the Mediterranean peninsulas, where populations could remain imprisoned and isolated for long periods of time and thus undergo differentiation, thanks to small adaptive changes. Examples are the Iberian mountains, the Apennines in Italy and the Balkans in the east, areas rich in taxa of endemic invertebrates but with only single cases of endemic forest bird species [25,58,59]. It is difficult to explain why certain species did not reach the central and southern Apennines (e.g., crested tit), especially when one considers that they were able to colonize the other two Mediterranean peninsulas; however, the recent expansion in north Apennines of crested tit [23] shows its present ability to live at lower Apennine latitudes.

It is very interesting to highlight that when comparing the entire breeding avifauna with the forest birds of the three peninsulas the same Sørensen's similarity index values were found [59]; in a sense, the forest species represent a significant sample of the entire avifauna of the three peninsulas and show that a similar biogeographical story occurred.

As stated above, corroborated by paleobotanical and paleontological data, at least during the last two million years the expansion and contraction phases of glacial and Arctic conditions and the consequent expansion of ecological zones forced the entire European avifauna to take refuge in the Mediterranean [60]. Thirteen thousand years ago deciduous oak forests were located at the southern tip of the Balkan, Italian and Iberian peninsulas; they reached Scandinavia only six thousand years later. Mediterranean vegetation never completely disappeared during the Pleistocene, even under the most severe climatic conditions. During the interglacial period, Mediterranean forests at low to medium altitudes were widespread, mainly dominated by deciduous and non-evergreen broadleaf trees. The expansion of vegetation took place between twelve thousand and nine thousand five hundred years ago [53]. This has allowed the majority of species to continue living in these Mediterranean-type habitats.

4.5. Man's Influence On Present-Day Forest Avifauna

The great naturalist Gaius Plinius Secundus (Pliny the Elder) wrote ‘Summum munus homini datum arbores silvaeque intelligebantur’ [translated from Latin: Trees and forests must be understood as the supreme gift given to mankind]. It seems clear that already at the beginning of the first millennium, men of science were aware of the importance of forests and individual trees. The Mediterranean, and in particular the three peninsulas, were then covered with important forests, which, due to overexploitation and the need to obtain cultivable land, were considerably reduced over the following hundreds of years. It is obvious that the animal populations that were linked to those forests also declined; however, to the best of our knowledge, no forest birds have become extinct in historical times, except for in single insular regions.

The present extension of the maquis is associated with deforestation by man, which has not stopped since the beginning of the Neolithic period, nine thousand years ago. The most favorable time for the natural expansion of the maquis was probably in the Xerothermal period, between eight and four thousand years ago, when the climate was drier and warmer than today [51]. At the beginning of the Holocene, 10,000 years ago, the warming of the climate became more pronounced, the incident solar radiation at Mediterranean latitudes was about 7% higher than today, and precipitation more numerous. It should be noted that in the Fezzan (Matkandush, Sahara, Libya) there are rock carvings of species such as giraffes, elephants, dating back some seven thousand years, indicating the existence of a savannah where today there is a rocky desert (Figure 11). This is evidence of the natural relatively rapid climate change a few thousand years ago, and the youth of the Sahara desert. This was the most important period for the pedogenesis of the Mediterranean where there was a climatic optimum; it was during this period that the first Neolithic cultures and the very first agricultural activities were born. The pastoralism and agricultural practices marked the first changes to the environment that would later become increasingly accentuated. According to Le Houérou [60], between twelve and four thousand years ago, during the Neolithic and Protohistoric revolutions, man exerted a very important transformative action on vegetation, initially in the eastern and then in the western Mediterranean. The definition of ‘revolution’ is due to the fact that in the 2,500 years of that period there was a large increase in the world’s human population, which grew from 10 million to 100 million [60].

Between five and four thousand years ago there was also a climatic deterioration towards aridity throughout the Mediterranean, and for at least 2,500-4,000 years shepherds and farmers have been burning down forests to obtain better pastures and new land for cultivation. This has had a particular significance on Mediterranean vegetation, which can undoubtedly be considered fragile and vulnerable, due to the climatic conditions in which it lives (relatively mild winter, long aridity in summer), especially susceptible to fire and overgrazing. In much of the Mediterranean region historically logging and fire have degraded the original oak forests to the maquis stage and altered the relative abundance of other smaller tree species. Overgrazing and inappropriate cultivation practices subsequently caused the disappearance of shrub species, changing maquis into garrigue, a type of woody Mediterranean vegetation consisting of very low evergreen shrubs (e.g., rosemary, thyme, broom, dwarf palm, etc.) and allowing soil erosion. Thus, little by little the ancient forest landscape was converted into heaths covered with grasses and other wind-resistant and undemanding herbaceous species. Human activity has produced vast expanses of garrigue; bare spaces and small rocky areas are often interspersed among the plants. Due to regular fires or overgrazing, garrigue can cover large expanses and is perhaps one of the most widespread environments in the Mediterranean because of these very negative factors.

The present extent of forests in Italy amounts to 120,000 km², accounting for ca. 40% of the country's area. Most forests are found in the Alps and Apennines, but a fair amount of forest cover also exists in coastal (e.g., pine forests), lowland areas, and islands. Over nearly a century, humans have also reforested, mostly with conifers, and in many cases terraced hillsides and mountainsides in order to plant trees. Thus a fair percentage of Italy's forest cover is made by tree planting.

Throughout the Mediterranean area, and particularly in islands characterized by rugged hills and mountains, man has sought to obtain arable land by terracing with great difficulty and powerful manpower the slopes, even steep hills and mountains, in order to obtain soils where to cultivate. Cyprus, Crete, Sicily have mountain terraces that have served both for the planting of coniferous forests and for the cultivation of olive groves (Figure 12). Eventually, although tree cover of limited ecological value, these have served for the establishment of some of the most widespread species of forest birds. These events have contributed in no small measure to the recent distribution of bird species, especially those associated with tree vegetation.

According to available statistics, tree cover in Italy is increasing, mainly since 1980’ [1; Figure 13]; recently the extent of the forest has increased remarkably, rising from 91,414 km² in 1990, to 94.704 km² in 2000, and reaching 96,532 km² in 2008 (for all three dates, the error standard of the estimate is very small, amounting to 0.1%) [61]. Thus, during the period 1990-2008, there was an increase in forest area of 5,1 km². It was certainly the same phenomenon of progressive abandonment of rural land that sees the triggering of processes natural recolonization by shrub and tree species in marginal areas [61]. However, it should be noted that while it is true that due to the abandonment of agriculture, mainly in central and northern Italy, forests are expanding naturally, much of the recent forest increase (22%, according to Agnoletti et al. [1]) is due to afforestation, mainly with conifers.

There is an obvious difference between natural forests and afforestation; many species of invertebrates or even herbaceous or shrubby plants established within natural forests are lacking in afforestation, and thus some bird species select only certain forest environments and not others. Data collected in the Iberian peninsula [62] allowed to find out the relationships between a series of environmental variables and the abundance of individual species of forest birds. The variable most highly correlated with the abundance of species was floristic composition and the diameter of trees; bird density was also correlated with mean annual rainfall (positive correlation: e. g., chiffchaff, goldcrest, robin, bullfinch; negative correlation: e. g., Bonelli’s warbler) [62]. This shows that obviously each forest has its own characteristics, and these in turn allow the presence of certain species and not others.

Although, in general, from 1980 to 2003 populations of many common forest birds in some parts of Europe appeared to be declining by 13-18% [63], in particular in Great Britain [64], Gil-Tena et al. [65] found a certain degree of variation across the Iberian peninsula. Interestingly, the percentage of diminution is very similar both for species and populations. Overall, in Italy a similar percentage (16.4%) of forest bird species resulted to be decreasing, both over a long time (150 years) and in present times [23], also similar to that found (20%) by Gil-Tena et al. [65] in Spanish forest bird populations. Latter authors highlighted that forest maturation is most influencing dynamic of forest birds, which are more related with advanced forest development stages than with initial succession stages as those of young forests. Overall, species that inhabit a forest do not remain in that forest forever; the greatest species diversity can be found in forests where different stages of succession are represented at all times [66]. In conclusion, presently this may depend on the forest management by man, as well as on the age of the trees, the presence of permanent open spaces (important to birds), and other characteristics at the edge of woodland.

The forest consists of numerous microhabitats that depend on forest species (conifers, broadleaf trees of different species, etc.), age, exposure, altitude, amount of litter, and the presence of undergrowth and clearings. These ecological factors enable the establishment of different species of birds. An afforestation of allochthonous Eucalyptus is certainly unattractive to most forest species, not only birds; however, it can be easily understood that the most ecologically demanding species are found only in certain types of forest. Generally if a species is uncommon then it will occur only in wide woods with singular ecological characteristics.

Additionally, it is very difficult to know the true increase in forest area in Italy, as this should be offset by that lost to fires; statistics on the area of forest destroyed by fire are very poor and in some cases absent. The Italian regions more affected by fire generally are Sicily, Calabria, and Sardinia. In terms of percentage, the habitats more affected by fires from 2000 to 2023 are Mediterranean pine forests, and Italy resulted to be the 3^rd country more affected by forest fires in Europe (after Spain and Portugal) [67]; ca. 1,784,000 hectares of Italian land have been fired, mainly arson, between 2000 and 2023, that is 5.9% of total Italian land area (Figure 14). Of course, not all of the fire passed through forests, some of it affected pastures, shrubs, garrigue, and even cultivated land; the majority of the forests traversed by the fire, however, were coniferous afforestation, which once burned are obliterated forever.

Following Blondel [68] Mediterranean forest birds originated in the large forest blocks of Eurasia; every species living in the Italian forests, as well as in the other Mediterranean peninsulas, are almost certainly also found in central European forest environments. For the reasons stated above, species of true Mediterranean origin are hardly found in mature evergreen oak forests today. The nearly absence of endemic taxa among Mediterranean Europe forest birds is surprising, especially when one considers how many endemic plants there are and how many opportunities species have had to isolate themselves [68,69]. Overall, the Mediterranean avifauna is no different from that of Europe today, but barely impoverished, probably due to the fact that the Mediterranean region falls on the south-western edge of Eurasia [68]. Only in the Iberian peninsula two endemic forest birds live; however, the fact that all forest species present in Italy are Least Concern [24] also means that generally researchers who dealt with the red lists did not consider them to be at risk because these birds are widespread in Europe and do not face any kind of present threat. However, according to the Italian red list [70] six forest bird species are considered at local risk: barred warbler (Critically Endangered), black grouse (Endangered), western capercaillie (Vulnerable), middle spotted woodpecker (Vulnerable), white-backed woodpecker (Vulnerable), and garden warbler (Vulnerable); in addition the Sardinian subspecies of goshawk Accipiter gentilis arrigonii is considered Endangered, while the other forest species are listed as Least Concern. The long-term study calculated over 150 years, however, shows a less risky trend for the two woodpecker species above cited (‘stable’ in Table 1), while for the other four species in Italy the status is not at all positive. Also, the mean ecological value (2.0-2.1; Table 2) shows a good presence of ecologically demanding species in all the three peninsulas.

More recently, in the last few decades, perhaps due to climate change or the increased trophic availability within cities, some forest species have begun to colonize the tree cover of towns and have become heavily urbanized. Some species (e.g., woodpigeon, blackbird, serin) had already carried out this urban colonization process many years earlier in central Europe, others (e.g., jay) have begun to do so in Italian towns. The reasons for this recent immigration may be many: better winter temperatures inside cities compared to forests, less likelihood of predation for some species, greater availability of trophic resources, which allow a greater number of reproductions per year (e.g., woodpigeon, three times a year and sometimes from January to November) [71], and finally lower mortality of fledglings. In addition, other species, like siskin, benefited from recent conifer afforestation, mainly in south Italy [G. Congi, pers. comm.].

Among the causes of the expansion of bird species there are creation of new habitats, increase in trophic availability, and climatic fluctuations. It is not always easy to understand the cause of the expansion of certain species, but certainly new trophic factors and probably, at least as far as urban environments are concerned, significantly higher average temperatures in association with the anthropic activities from which the birds sometimes benefit, contribute. This takes place because in nature, animal populations undergo colonization events, declines, increases or simple fluctuations over time [72,73,74].

5. Conclusions

Overall, today the Mediterranean forest avifauna is no different from that of Europe, but hardly impoverished, very likely due to the fact that the Mediterranean region falls on the south-western edge of Eurasia. The nearly absence of endemic species among Mediterranean forest birds is unexpected, especially when one considers how many endemic plants there are and how many opportunities species have had to isolate themselves. However, from the reconstruction made in the preceding pages, it can be understood that the avifauna of the forests of Mediterranean Europe is of fairly recent origin and, above all, the result of the isolation of Eurasian populations during the ice ages. The effects of each glaciation on the fauna were cancelled out by the next one, so that the last glaciation explains the distribution and diversification patterns of presently forest avifauna. Most species became definitively established during the last ice age and can be considered in this sense as glacial relicts. A portion of species that colonized the Balkan peninsula in turn colonized the Italian peninsula via the trans-Adriatic route and are therefore absent from the Alps. However, those which have differentiated from north-eastern populations should be considered neo-endemic taxa, dating back some 18-20,000 years. Thus, this time frame was sufficient for differentiation of isolated populations of some species, at the subspecific or specific level. This took place in the Iberian peninsula, Sicily and probably the Apennines. Only the Iberian peninsula has two endemic species, which have become isolated due to the Pyrenean barrier and the fact that the Iberian peninsula is the extreme south-western apex of Eurasia, separated from North Africa by the Strait of Gibraltar. It remains quite unknown what has happened in the Sardinian-Corsican system, which, although very old, presently hosts only a few differentiated populations of some forest species of birds, except for Corsican nuthatch, a species endemic to Corsica, and absent elsewhere, related to Algerian nuthatch (Kabyle) and Krüper nuthatch (Turkey, Caucasus and Lesvos islet). Here briefly another Mediterranean forest species deserves to be mentioned, Le Vaillant woodpecker in North-West Africa, belonging to green woodpecker group and isolated in the Maghreb, probably when the Strait of Gibraltar reopened around 5 million years ago. This woodpecker, and the three species of nuthatches mentioned above are undoubtedly among the oldest forest species in the Mediterranean, and may be considered paleo-endemic taxa.

Italian forest species, like those in the rest of the Mediterranean, will face some challenges in the coming decades because of the problems faced by their elective habitat, the forest. The main threats to forests are climate change, global warming, reduction of old-growth forests, increased fires and CO₂ emissions (Figure 15). As we have seen above Huntley et al. [31] have attempted to simulate the future of European avifauna in the late 21^st century; the very pessimistic vision they present, much more than the trend currently calculated on the basis of the bibliography consulted, may be grimly realistic, but this will depend only on humans making important decisions for environmental protection.