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Fall-winter diet of the starling (Sturnus vulgaris) between foraging areas and resting areas near Algiers.

INTRODUCTION

The most important researches done on the Starling over the world were conducted mainly in Europe in the breeding area of this species as in Poland [1], in France [2,3,4,5,6,7,8], in several European countries [9] and in England [10]. Other studies were conducted in the USA [11], in New Zealand [12] and in Australia [13]. Very few researches about the Sturnus vulgaris were published in Algeria. However, it is possible to quote those of Doumandji and Doumandji-Mitiche [14], of Madagh [15], Doumandji and Doumandji-Mitiche [16], Moulai and Doumandji [17], Merrar and Doumandji [19], Djennas-Merrar and Doumandji [20], Berrai and Doumandji [21]. The main cause of choosing this subject is related with the Starling predatory behaviour against olive trees in Algeria (Olea europea) mentioned by several researchers [22,23,24,25,3]. Its mischief are reported on the vine (Vitis vinifera) by Heim de Balsac [22], Seurat [27], Spirhanzl-Duris and Solovjev [28] and Riba and Silvy [29] and on the date palm (Phoenix dactylifera) [27]. The qualification of this harmful or useful avian species is very complex. This study seeks to complement previous works particularly with regard to diet. Its aim is to refute or confirm the observations made by different researchers among others on its trophic bioecology and the relative importance of insect prey and vegetal intake.

Study area:

Two regions of Algiers are retained. The first is in the suburban area of the Algerian Sahel which corresponds to the botanical garden Hamma also known as "The test garden Hamma". The second is located in the piedmont of the Mitidja near Meftah. Situated deep in the bay of Algiers, in its southern part, the test garden Hamma (36[degrees]43' N.; 3[degrees] 5' E.) extends on 32 ha. It is characterized by a Mediterranean climate with a warm winter where minimum and maximum temperatures are significantly softened. Its rich vegetative coverage in tropical and xerophilic species adds its regulatory action. The region of Meftah (36[degrees]37' N.; 3[degrees]14' E.), located at the south-eastern part of Algiers and rises at an altitude of approximately 100 m. Its ground is for agricultural use, occupied by market gardens and citrus orchards in a sub- humid Mediterranean climate of a mild winter (Seltzer, 1946; Mutin, 1977).

MATERIALS AND METHODS

In the test garden Hamma, the outings have taken place since X 96 until I 97. During the daily readings, 48 items of the Sturnus vulgaris freshly dead lying on the ground under the resting areas are collected. In the area of Meftah, Bouamama station, one of the starling's foraging areas, 24 items are captured during XII 13 through an ornithological net (12m lengthand 3m height). Each collected item is put in a bag which carries a label showing the date and place of the picking. Brought back to the laboratory, and then placed in a refrigerator at 5 [degrees]C. Subsequently, the bird is carefully dissected. The digestive tracts is recover from the gizzard to the end of the cecum and put it in a glass petri dish containing ethanol. The identification process of the plants and animals fragments is performed at the laboratory of agricultural zoology from the Higher National School of Agronomy of El-Harrach through various identification keys.

The results analysis is made thanks to ecological indices such as the relative abundance, the Shannon-Weaver diversity and the equitability, as well as the variance analysis.

The relative abundance (R.A.%) is expressed in percentage with formula

R.A.% = n/N x 100

where (n) is the number of the species (i) taken into consideration and (N) the total number of individuals including all species [34]. In this case (n) corresponds to species number ratedin the stomach contents, where (N) represents all the invertebrates found in the stomach contents.

The Shannon-Weaver diversity indices are considered as the best means to reflect diversity. It is given by the Shannon-Weaver formula

H'(bits) = -[SIGMA] (ni/N) [Log.sub.2](ni/N)

Where (ni) is the number of individuals of the species (i) and (N) the total number of individuals including all species.

The equitability indices or equidistribution (E) is the ratio of the diversity calculated with the maximum diversity

E = H'/ H'max

Where H' is the de Shannon-Weaver diversity indices expressed in bits. H'max., the maximum diversity is evenly expressed in bits, given by

H' max. = [Log.sub.2] S

S the total richness which is the total number of the present species. The purpose of the one way analysis of variance or a single factor analysis of variance, is to compare averages of several populations presumably normal and of the same variance from random samples, simple and independent of each other [37].

Results:

The contents analysis of the Sturnus vulgaris digestive tracts taken under the resting areas in the test garden Hamma in 1997 and in the foraging area (Meftah) in 2013 shows the presence of several plants and animals trophic factors (Tab.I). The food-plants, the most sought in 1997, are Pistacia lentiscus (Anacardiaceae) with 249 fruits, followed by Olea europea (Oleaceae) with 35 fruits, Triticum sp. (Poaceae) and Ficus sp. (Moraceae) are less ingested. In 2013, the high consumption of the pistachio mastic tree fruits is confirmed, in the foraging area.

In the digestive tracts of the individuals taken within the resting areas, the animal part ingested consists of Formicidae including Messor barbarus, followed by Larinus sp. (Curculionidae) and Cochlicella sp. (Gastropoda) with 17 individuals. The other species are weakly represented. In the foraging area (Meftah), the animal part is well represented by the Formicidae such as Messor barbarus followed by a bug Sehirus sp. (Pentatomidae).

Composition of the diet according to the classes and orders:

The listed preys belong to 5 classes, those of Gastropoda, Arachnida, Myriapoda, Crustacea and Insecta (Fig. 1). Insecta is the most significant in the test garden Hamma (56.1%) and even in items captured in Meftah foraging area (58.6%).

The insects identified during the present study belong to 7 orders, those of Orthoptera, Dermaptera, Heteroptera, Coleoptera, Hymenoptera, Lepidoptera and Diptera (Fig. 2). The most represented order in the test garden Hamma is Hymenoptera (72.4%), followed by Coleoptera (23.7%). These orders are dominant also in Meftah foraging area (38.2% each one).

Relative abundance of the main species ingested by the Sturnus vulgaris:

In the digestive tracts of the Sturnus vulgaris, the dominant species found in the Starling within the resting places (test garden Hamma) are Messor barbarous (in the swarming period), Pistacia lentiscus, Larinus sp.,Cochlicella sp., Tapinoma simrothi and Tetramorium biskrensis. In Meftah area, the dominant species are Pistacia lentiscus, Messor barbarus, Sehirus sp.and Cochlicella ventricosa (Tab. II).

Diversity of the Sturnus vulgaris diet:

The values of the Shannon-Weaver (H') diversity calculated according to the number of the various components of starling trophical diet vary from one station to another. But they are relatively high (H' > 3 bits) (Tab. III). The equitability (E) tends in most cases to 1, which means that the numbers of the prey-species tend to be in balance among themselves.

Applied analysis of variance on the ingested species:

The exploitation of the trophic elements foundin the Sturnus vulgaris diet, captured within the test garden Hamma and the region of Meftah by an analysis of the variance shows that there is a significant difference between the two areas, knowing that F = 21.13 ; ddl = 1 ; P = 0.001.

Discussions:

Gromadzki has examined the feeding behaviour of the Starling in its breeding range in Poland. During the analysis of 85 stomach contents of this species along with the nesting period, this author finds 71 species including 61 of animal origin and 10 of plant species, that to say 3953 individuals. The species number listed in the present study within the resting area of the test garden Hamma is higher than that reported by Gromadzki. Actually, the differences of ingested species numbers depend on many factors, such as the sacrified subject numbers and the climatic conditions. In Algiers during the fall-winter period, the temperatures are low thus leads to a reduction in the richness of the entomofauna. On the contrary the spring-summer thermal conditions are favourable for the activity of several insect species. Thus, the Sturnus vulgaris is in its breeding area in front of a wide range of preys. Apparently, it chooses its preys among those that are most appropriate, by their consistency and by their richness in nutrients to feed its young in the nest. Doumandji and Merrar [38] during the autumn 1996 and the winter 1997 report the presence of 1153 feed components in the Sturnus vulgaris droppings, collected from the test garden Hamma (Algiers) and 507 trophic elements in those collected at the People's Palace of Algiers in autumn 1997. In the eastern part of Mitidja, Berrai and Doumandji [21] report between October 2006 and March 2007, 1123 individuals in 50 Starling digestive tracts. The obtained results in the resting area of the test garden Hamma confirms those of the authors previously quoted. On the other hand, the numbers counted from the starlings sacrified at the foraging area in Meftah are much weaker. This is due probably to the low number of the birds captured and dissected. The obtained values in Meftah are of the same order of magnitude of those of Rahmouni-Berrai and Doumandji [39] observed in the eastern part of Mitidja. The last quoted authors stresses that in 2006 in Rouiba, 271 individuals are listed in the digestive tracts content of 10 starlings trapped and sacrified in the foraging areas. They also mention that in 2007 in Larbaa, 282 trophic elements are found in 10 digestive tracts. As well in Meftah as in the test garden Hamma, the starling seems to have a preference for the Hymenoptera including Messor barbarus and for the beetles. Indeed, Mayaud [40] announces that the order of the class of insects which is the best represented by the numbers consumed is that of the Hymenoptera with a prevalence of the ants. Doumandji and Doumandji-Mitiche [14] notice on the shoreline the acrobatic flights of the Sturnus vulgaris in the early autumn, to capture the ants Messor barbarus while swarming.

Compared to the contents of the 34 starling collected during the second decade of october under the perches in the gardens of the national agronomic Institute of El-Harrach, The diet of this predator includes especially ants such the Messor barbarus in swarming (84.1%), Aphaenogaster testaceo-pilosa (0.6%), Tapinoma simrothi (0.6%) and Monomorium salomonis(0.6%) [16]. These authors report that the Coleoptera are less listed like Otiorrhynchus sp. and Sitona sp. as well as the Aranea, Oniscidae and Helicidae. Milla and al. [17] in the Sahel of Algiers underline that the Hymenoptera appeared at the first place in the menu of Sturnus vulgaris with 98 individuals (49.5%) followed by Coleoptera with 77 individuals (38.9%).

In Poland, Gromadzki reports in 85 stomach contents, high frequencies for the Diptera (45.6%), the Coleoptera (31.2%) and the Lepidoptera (13.2%). In the breeding area, 1112 samples from the throat and digestive tracts of the young Sturnus vulgaris, that Kluijverquoted by Gramet examined, belong to 313 animal species which 267 are insects (85.3%), the remainder being consisted of gastropods, worms, isopods, myriapods, arachnids, amphibians and even by lezards. Gramet (1976) reports the prevalence of the Diptera (39.7%) and Coleoptera (25.1%). They are followed by the Lepidoptera (18.5%). In the wintering area in particular the Mitidja (Algiers), the starling feeds itself, in the fall-winter, with olives and mature pistachio mastic tree fruits. Indeed, according the present study, Pistacia lentiscusis consumed in big proportions. It is found as well in the digestive tracts of the birds taken from the resting area as in the foraging areas, in the presence of epicarps and olive pits. It would appear that the Sturnus vulgaris has a preference for olives and the mastic tree fruits. Also, Doumandji and Doumandji-Mitiche [16] report the presence of the pulp of 14 olives and the rests of a hackberry fruit (Celtis australis) in the faeces of the Sturnus vulgaris. In the same way, this bird rejects many small oleaster nuclei (Olea europea oleaster), big olive pits (Olea europea europea) and Palmaceae seeds such as Washingtonia filifera and Washingtonia robusta. These rather recent observations confirm those of Heim de Balsac [22] and of Heim de Balsac and Mayaud [23] which report that in Algeria, in october the Sturnus vulgaris attacks the vineyard and the olive trees in Mitidja. Previously, Seurat [30] and Brimont [42] reported that this species consumed fruits berries stating that the starling visits the pistachio mastic tree, the olive tree and the ornamental palms. The plant part can become significant in the autumn where the fruits and the seeds constitute most of the Sturnus vulgaris menu. According to several authors, the starlings can eat different berries and fruits of grown plants such as tomatoes, strawberries, blueberries, peaches, apples, pears, figs, grapes, cherries and ornamental plants as elderberries and blackberries [43,5,44]. Depenbusch and al. [11] note that starlings can be feeded by mature seeds of Medicago plants. However, Tahon [46] reports that in winter, the starlings consume all kinds of food. In times of extreme cold, starling completes its diet with soft seeds. He looked for them in-feed maize silage for cattle or in plots recently planted as winter cereals where he takes the seed that he has just germinated [8]. According to Clergeau [5] and Latham and Latham [12], this gregarious bird shows a food opportunism which partly explains its success and its wintering survival

Other authors like Havlin and Folk quoted by Cramp and Perruis [10] report, compared to 336 Sturnus vulgaris stomach contents between march and november 1964, the strong presence of Hymnoptera (24.2%) including 22.6% of Formicidae, accompanied by Coleoptera (21.5%). To these preys, it is necessary to add wild fruits (15.2%). Karasov [47] and Starck [48] in New-York, notice that the vegetable part takes a big proportion in the autumn and winter starling diet. It should be recalled that in the nesting area, this species also ingests plants. Indeed, Debont quoted by Gramet report a food intake based only on cherries. Previously in 1957, Lohrl report the discovery of 438 nuclei of Avium sp. in a starling nest.

The results of the present study shows an equitability value which tend to 1, which emplies that the consumed numbers of the animal and plant species tend to be in balance between each other. Berrai and Doumandji [21] in the Mitidja plain, report also an equitability value (E) close to 1. The results of analysis of the variance provesa significant difference between the two stations (Pr<0,05). Contrary to our results, in the Mitidja plain, Berrai and Doumandji [21] show that there is no significant difference.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Conclusion:

Contrary to the ideas which prevail in the North Africa, where the Sturnus vulgaris causes only damages on the olives and dates in the fall-winter period, two observations made during this study undermine these insertions. Indeed, it is shown that in the area of Algiers which belongs to their wintering area, the starlings strongly consume the Pistacia lentiscus fruits. Furthermore, it is to be noticed in this same area, the strong ingestion of animal preys in addition to the requested vegetable part.

AKNOWLEDGMENTS

My sincere thanks and gratitude are addressed to Professor Doumandji Salaheddine of Higher National School of Agronomy to have corrected this document. My sincere gratitude is addressed to Berrai Hassiba and Marniche Faiza to bring some remarks after reading this document. I would certainly like to express my thanks to Djennas Abdelkrim, Engineer of fauna at the National Agency of Natural Conservation (ANN) in the test garden Hamma to have always been by my side during these researches and for his valuable advices.

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(1) Katia DJENNAS-MERRAR, (2) Hassiba BERRAI, (3) Faiza MARNICHE and (4) Salaheddine DOUMANDJI

(1) Higher National School of Agronomy, El-Harrach, DZ-16200, Algiers, Algeria

(2) Department of Biotechnology, Faculty of Science of Nature and Life, University Blida 1, Blida, Algeria

(3) Higher National School of Veterinary, El-Alia, Algiers, Algeria

(4) Lab. Researches "protection of plant in agricultural and natural environments "Higher National School of Agronomy, El-Harrach, DZ16200, Algiers, Algeria

Address For Correspondence:

Katia DJENNAS-MERRAR, Higher National School of Agronomy, El-Harrach, DZ-16200, Algiers, Algeria E-mail: merrark@yahoo.fr

Received 22 June 2016; Accepted 28 August 2016; Available online 31 August 2016
Table I: List of items contained in Sturnus vulgaris digestive tracts

Stations Catches                                      Test garden
                                                      Hamma

Number of Guts Examined                               48

Classes               Orders        Families          Numbers

Gastropoda            Pulmonata     Helicellidae      6
                                    Helicidae         2
                                    Cochlicellidae    26
Arachnida             Aranea        Aranea sp.        3
                                    Gnaphosidae       0
                                    Lycosidae         0
                      Phalangidae   Phalangidae sp.   1
                      Acari         Acari sp.         2
                                    Oribatidae        0
Myriapoda             Diplopoda     Iulidae           9
                                    Polydesmidae      0
                      Chilopoda     Chilopodasp.      2
Crustacea             Isopoda       Oniscidae         3
Arthropoda cl. ind.   O. ind.       F. ind.           1
                      Orthoptera    Acrididaesp.      4
                      Dermaptera    Forficulidae      1
                                    Labiduridae       2
                                    Labiidae          1
                                    Anisolabidae      1
                      Heteroptera   F. ind.           1
                                    Pentatomidae      1

Insecta                             Coreidae          2
                                    Tingidae          1
                                    Scutellaridae     0
                      Coleoptera    F. ind.           9
                                    Chrysomelidae     26
                                    Curculionidae     35
                                    Apionidae         5
                                    Tenebrionidae     12
                                    Scarabeidae       8
                                    Caraboidae        18
                                    Staphylinidae     2
                                    Elateridae        2
                                    Nitidulidae       2
                                    Dermestidae       2
                                    Buprestidae       1
                      Hymenoptera   F. ind.           0
                                    Apidae            2
                                    Formicidae        370
                      Lepidoptera   F. ind.           3
                      Diptera       F. ind.           2
                                    Stratiomyidae     0
                      O. ind.       F. ind.           1
Plantae                             Anacardiaceae     249
                                    Oleaceae          36
                                    Moraceae          14
                                    Poaceae           29
                                    Solanaceae        3
                                    Cupressaceae      1
                                    Rosaceae          1
                                    Ericaceae         1
                                    F. ind.           13
Total Numbers of Individus                            916
Total Numbers of Species                              87

Stations Catches                                      Meftah

Number of Guts Examined                               24

Classes               Orders        Families          Numbers

Gastropoda            Pulmonata     Helicellidae      1
                                    Helicidae         1
                                    Cochlicellidae    3
Arachnida             Aranea        Aranea sp.        4
                                    Gnaphosidae       1
                                    Lycosidae         2
                      Phalangidae   Phalangidae sp.   0
                      Acari         Acari sp.         0
                                    Oribatidae        2
Myriapoda             Diplopoda     Iulidae           2
                                    Polydesmidae      1
                      Chilopoda     Chilopodasp.      0
Crustacea             Isopoda       Oniscidae         2
Arthropoda cl. ind.   O. ind.       F. ind.           0
                      Orthoptera    Acrididaesp.      1
                      Dermaptera    Forficulidae      0
                                    Labiduridae       1
                                    Labiidae          0
                                    Anisolabidae      0
                      Heteroptera   F. ind.           5
                                    Pentatomidae      5

Insecta                             Coreidae          0
                                    Tingidae          0
                                    Scutellaridae     3
                      Coleoptera    F. ind.           5
                                    Chrysomelidae     2
                                    Curculionidae     8
                                    Apionidae         1
                                    Tenebrionidae     1
                                    Scarabeidae       1
                                    Caraboidae        4
                                    Staphylinidae     4
                                    Elateridae        0
                                    Nitidulidae       0
                                    Dermestidae       0
                                    Buprestidae       0
                      Hymenoptera   F. ind.           1
                                    Apidae            1
                                    Formicidae        24
                      Lepidoptera   F. ind.           0
                      Diptera       F. ind.           0
                                    Stratiomyidae     1
                      O. ind.       F. ind.           0
Plantae                             Anacardiaceae     27
                                    Oleaceae          0
                                    Moraceae          0
                                    Poaceae           2
                                    Solanaceae        0
                                    Cupressaceae      0
                                    Rosaceae          0
                                    Ericaceae         0
                                    F. ind.           0
Total Numbers of Individus                            116
Total Numbers of Species                              47

Table II: Relative abundance (RA%) of the most significant species
consumed by the Starling.

Stations Catches                Test garden Hamma   Meftah

Species                         RA%                 RA%
Cochlicella barbara             0.98                0
Cochlicella ventricosa          0                   2.58
Cochlicella sp.                 1.85                0
Iulussp.                        0.98                0
Sehirus sp.                     0                   3.44
Larinus sp.                     2.07                0
Sitona sp.                      0.87                0
Messor barbarus                 35.48               14.65
Tapinoma simrothi               1.20                0
Tetramorium biskrense           1.20                0
Aphaenogaster testaceo-pilosa   0.76                0
Pheidole pallidula              0.76                0
Pistacia lentiscus              27.18               23.27
Olea europea                    3.82                0

Table III: Diversity indices values of the species ingested by the
Sturnus vulgaris in the catches stations.

Stations            NumbersGuts              H'       H'max
Catches             Dissected     N     S    (bits)   (bits)   E

Test garden Hamma   48            916   87   3.23     6.47     0.49
Meftah              24            116   47   4.46     5.57     0.79

N: numbers of individuals consumed; S: total wealth; H': diversity
index of Shannon-Weaver; H' max: maximum diversity; E: equitability
index
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Author:Djennas-Merrar, Katia; Berrai, Hassiba; Marniche, Faiza; Doumandji, Salaheddine
Publication:Advances in Environmental Biology
Article Type:Report
Geographic Code:6ALGE
Date:Aug 1, 2016
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