Volume 5 (3): 89-99 (2021) (http://www.wildlife-biodiversity.com/)

 Dietary niche comparison of raptors in northeastern Iran as an important zoogeographic zone

Ali Zarei1, Fatemeh Tabatabaei Yazdi1, Sakineh Rajaee2

1 Faculty of Natural Resources and Environment, Ferdowsi University of Mashhad, Mashhad, Iran

2 Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

*Email: f.tabatabaei@um.ac.ir

Received: 11 November 2020 / Revised: 05 March 2021 / Accepted: 07 March 2021 / Published online: 27 September 2021. Ministry of Sciences, Research and Technology, Arak University, Iran.

How to cite: Zarei, A., Tabatabaei Yazdi, F., Rajaee, S. (2021). Dietary niche comparison of raptors in NE Iran, as an important zoogeographic zone. Journal of Wildlife and Biodiversity, 5(3), 89-99. doi: 10.22120/jwb.2021.139673.1199

 Abstract

Diet analysis is one of the most basic requirements for understanding species' ecological niches and determining their feeding relationships in an ecosystem. Pellets are common material for investigating diets. In this study, to investigate the diets and food niche overlap of coexisting raptors in NE Iran, a total of 344 pellets were collected during 2017–18. The pellets belonged to common buzzard (Buteo buteo), long-legged buzzard (Buteo rufinus), a little owl (Athene noctua), common kestrel (Falco tinnunculus), golden eagle (Aquila chrysaetos), and Eurasian sparrowhawk (Accipiter nisus) from the Binalud protected area. Analysis of prey percent frequency showed that the pellets were predominantly composed of the remains of rodents, followed by birds and reptiles. The most frequently captured rodents were jirds (Meriones libycus and M. persicus), followed by a vole (Microtus arvalis). Although the raptors generally utilized small mammalian prey, they showed species-specific preferences and seasonal variations in prey species' share. According to three niche overlap indices, the most extensive food overlaps were found between long-legged buzzard with a common buzzard and golden eagle with a common buzzard. The smallest food overlap was found between the little owl and golden eagle. Seasonal comparison for common buzzard, common kestrel, and little owl showed that richness in the prey items was the highest in summer, followed by autumn. In addition to providing valuable information in terms of raptors' food habits and biodiversity, this study's results can be leveraged in conservation and management programs.

Keywords: Biodiversity, diet, feeding behavior, overlap index, pellets

Iran is characterized by great habitat diversity, making it one of the most important countries for conserving biodiversity in the Middle East and West Asia (Firouz, 2005). Since the loss of just one species may affect many other species, greater species diversity in an ecosystem and more complex food webs make an ecosystem more sustainable and self-regulated. Thus, the overall reduction of biodiversity caused by human activities has a destructive impact on ecosystem sustainability and biological resilience (Mitchell et al., 2002).

As an essential part of biodiversity, birds have evolved over millions of years (Kristin, 2004). So far, 49 species of birds of prey have been recorded among the 520 native and migratory bird species in Iran. However, several factors, such as hunting, habitat degradation, and pollution, have reduced these species' diversity and numbers (Khaleghizadeh et al., 2017). Obtaining dietary information is necessary to determine the status of a species in biological communities and achieve adequate protection (Bradley et al., 2007). In ecological and taphonomic studies, diet analysis is one of the most basic requirements for understanding species' biology and determining their nutritional relationships and roles in the ecosystem (Royer et al., 2018, Redpath et al., 2001, Deagle et al., 2005). Furthermore, more detailed knowledge of species' diets might be used to properly set up protective strategies (Marrero et al., 2004). Hence, the topic of dietary habits has found a special place in conservation.

Dietary studies are essential in understanding the different aspects of feeding ecology in raptors, and the results of such studies are often used for conservation and management purposes (Marti et al., 2007). One of the most common methods for investigating the diet of wildlife is the examination of pellets. Among traditional diet studies, pellet analysis is one of the best methods for determining raptors' diet composition, especially for species that cannot be hunted due to legal restrictions since pellet analysis is non-invasive and indirect (Khaleghizadeh & Javidkar, 2010; Hámori et al., 2017).

Pellets are mainly spindly or oval-shaped, containing the undigested parts of the birds' food such as bones, teeth, claws, and hair. These materials are regurgitated through the mouth and are entirely different from droppings. Therefore, by collecting and analyzing pellets, it is possible to determine prey items. For raptors, this method provides extensive information about the food composition, prey species diversity, dominant prey, food preferences, archaeology, ecotoxicology, and differences in food habits (Ghiasyi 1996; Zerunian et al., 1982; Carevic et al., 2003; Van den Brink et al., 2003; Shao et al., 2008; Charter et al., 2012; Pocora et al., 2012; Rajaei et al., 2014; Rey-Rodríguez et al., 2019). Additionally, this method can provide information on the distribution of small mammals as prey species, the impact of annual and seasonal changes in prey availability, fluctuations in the relative abundance of prey populations, and the niche overlap among raptors in a region. For instance, Goutner et al. (2003) studied the diet of the barn owl (Tyto alba) and little owl (Athene noctua) in the wetlands of northeastern Greece and found the greatest niche overlap in the summer, mainly in mammalian prey items. Romanowski and Lesiński (2020) compared the trophic niches of sympatric raptors in central Poland and showed that the niches and hunting habitats of coexisting kestrels and long-eared owls overlapped almost completely. Zhao (2011) studied the dietary overlap between little owls and long-eared owls in northwestern China, demonstrating that the main prey items overlapped extensively. Kitowski (2013) investigated food niche overlap between barn owls and long-eared owls in Poland and discovered an 83.2% overlap between the two wintering species in main prey items. Numerous studies on the diet of birds of prey have been published worldwide during the last few decades with various aims. However, such studies have been rare in Western Asia and the Middle East. Rey-Rodríguez et al. (2019) performed a modern analysis on barn owl pellets in the Middle East. Ghiasyi (1996), Obuch and Kristin (2004), and Rajaei et. al. (2014) also determined food composition for little owl (Athene noctua) in Iran, Syria, and Egypt. The pellets were collected from 34 roosting sites, 17 of which were located in Iran. Obuch and Khaleghizadeh (2011) identified rodent fauna based on one raptor species' pellets (Tyto alba) in Iran, finding remarkable differences in the 26 studied prey taxa. In 1996, Ghiasyi studied the rodent fauna of northern Khorasan based on nearly 500 pellets collected from near the cities of Sarakhs, Torbate Jam, Dargaz, and Quchan.

Niche overlap is the shared use of a resource by two or more species (Varasteh et al., 2017). Niche overlap can be relevant to species density and the community structure (Rajaei et al., 2014). There are several methods for measuring niche overlap (Krebs, 2001; Romanowski & Lesiński, 2020). Most previous studies on the diet of sympatric raptors have been carried out on two bird species. Although a comprehensive investigation of several sympatric raptors' diets based on pellets has been undertaken by Romanowski and Lesiński (2020) in Poland, no such research has been conducted in Iran so far. In contrast with previous studies in Iran, which included one or two species (e.g., Varasteh et al., 2017; Anushiravani & Sepehri Roshan, 2017), in the present study, dietary niches of several coexisting raptors were investigated in NE Iran (Binalud protected area in Khorasan Razavi Province). This study aimed to determine the food composition and dietary overlaps in these raptors based on pellets and provide data on this critical zoogeographic area (Misonne, 1959).

The study area (Binalud protected area) has a total area of 61,936 hectares. It is located at 58°53' to 59°25' E and 36°6' to 36°28' N, between the cities of Torqabeh-Shandiz, Neyshabur and Chenaran (Fig. 1).

Considerable variation exists in the area's vegetation, including various trees and shrubs (genera Astragalus, Artemisia, Juniperus, Salix and Berberis) (Moghaddam & Koocheki, 2003). The hydrological conditions and the rivers in the study area (e.g., Dowlat Abad, Zoshk, Kang, and Jaghargh rivers) have provided suitable habitats for various species wolves, foxes, cats, pikas, buzzards, owls, and kestrels.

Figure 1. Map showing the geographical location of the study area. Khorasan Razavi Province,

Iran (A), and Binalud protected area (B).

 

A total of 358 pellets, belonging to common buzzard (Buteo buteo), long-legged buzzard (Buteo rufinus), little owl (Athene noctua), common kestrel (Falco tinnunculus), golden eagle (Aquila chrysaetos), and Eurasian sparrowhawk (Accipiter nisus) were collected during the autumn and winter of 2017 and spring and summer of 2018. Although pellets are more likely to be regurgitated at roosting sites and are often found around abandoned buildings, at the base of trees and mud walls, holes in cliffs, and around utility poles, all other locations showing signs of raptor presence were also explored for collection of pellets. Pellets were collected in separate bags and were transferred to the laboratory of the Faculty of Natural Resources and Environment, Ferdowsi University of Mashhad (FUM). Subsequently, the external features and structure (shape, color, weight, length, and diameter) of the collected pellets were measured and recorded (Fig. 2).

 

Figure 2. Pellets collected during different seasons: spring (A), summer (B), autumn (C) and winter (D), photographed by authors.

The characteristics of the collected pellets and prey remains were checked with the literature (Brown et al., 1999; Darvish et al., 2006).

Data on the weight, length, and diameter of pellets were statistically analyzed. The pellets were soaked, and prey remains in the pellets were teased apart for further identification following the protocol used by Carevic et al. (2013). All the remains were identified to the lowest possible taxonomic level. Prey items were clustered into eight groups based on taxonomic similarities, including rodents (Muridae), birds (passerine), birds (poultry), reptiles, hedgehogs and shrews, ground squirrel, insects, and hares and pikas (Lagomorpha).

Rodents' remains in the pellets were identified based upon skull, jawbone, and dental formula using an identification key (Darvish et al., 2006). Some pellets lacked enough skeletal and cranial remains, so it was only possible to detect an anonymous rodent. Since insects were not our specialty and given the conservation and management concerns of this study, we did not attempt to identify insects precisely.

 

Table 1. Dimensions of pellets from six raptor species in NE Iran.

           Length (mm)                     Diameter (mm)                      Weight (g)           

 

species                 Season      N      Mean±SD     Min    Max    Mean ±SD     Min    Max   Mean ±SD   Min    Max

 

Common buzzard (Buteo buteo)

 

  Spring      42     38.16±9.05      22      57.8     23.87±4.7       12       37      2.56±1.36     0.6      7.8

  Summer   118   47.25±12.4      21       89      31.37±7.67      15       54      5.06±3.24      1        18

  Autumn  41   40.09±12.53     19       75      24.41±7.38      13       40      3.76±4.96     0.9       17

  Winter      82     31.05±6.49    14.5      47     47.91±11.37     24       82      4.24±1.99      1        10

 

 

 

Total

292

38.54±11.87

22

82

35.46±13.64

11.3

89

4.24±3.12

0.6

33

Little owl

Spring

7

42±8.5

32

56

16.7±5.3

12

25

1.87±0.34

1.4

2.4

(Athene noctua)

Summer

1

36

36

36

15

15

15

1.7

1.7

1.7

 

Autumn

3

40.66±7.02

 

 

17.1±2.47

 

 

2.8±1.61

 

 

 

 

 

 

Common kestrel (Falco tinnunculus)

 

Long-legged buzzard (Buteo rufinus)

  Winter      11   39.18±10.87     15       56      18.57±7.17      12       36      2.11±0.88     1.4      4.6

Total         22     40.20±7.82    27.66 49.33      17.5±2.3       13      25.3      2.4±1.2       1.5      2.9

  Spring       4     33.57±5.15      31      41.3     15.22±1.15    13.5    15.8      1.35±0.1      1.2      1.4

 

Summer

1

24

24

24

14

14

14

1.4

1.4

1.4

Autumn     3     29.66±2.31                            17.53±3                             1.4±0.02

  Winter       2     35.65±17.46   23.3      48       37.5±3.35       35       40       2.6±0.14      2.5      2.7

Total         10     31.23±7.51      14      41.3    20.88±10.19   13.5      48      1.62±0.52     1.2      2.7

  Spring       9      41.78±8.6       28       56      25.78±4.66      21       35      3.42±1.12     2.2      6.1

  Summer                                                                                                                                     

  Autumn                                                                                                                                     

  Winter                                                                                                                                      

 

 

Total

9

41.78±8.6

28

56

25.78±4.66

21

35

3.42±1.12

2.2

6.1

 

Golden eagle (Aquila chrysaetos)

 

  Spring       9      77.7±8.69       65       89      46.17±3.16      42       52     21.47±8.83   11.3      39

  Summer     2        34±4.29        31       37       71±11.31       63       79       9.9±0.14      9.9       10

  Autumn  11   50.68±11.03     42       79     69.75±19.35     31       89     19.36±9.19    9.8       39

  Winter                                                                                                                                       Total                 22      55.2±8.51       46     68.33                       45.33 73.33                      10.33 29.33

 

Eurasian sparrowhawk Spring       2        19±2.83        17       21       13±1.414       12       14       0.6±0.00                                                        0.6     0.6

 

(Accipiter nisus)

 

Summer     1            20            20       20            12            12       12          0.62        0.62     0.62

  Autumn                                                                                                                                     

  Winter                                                                                                                                       Total  3                  19.5±2.7               18.5     20.5      12.5±1.4       12       13          0.61        0.61     0.61

 

 

All the obtained data, including length, weight, diameter, color, and texture of the pellets and the detected items for each specimen, were entered into Microsoft Excel 2019 and analyzed in SPSS version 16.

In order to study the diet of raptors and investigate their food niche overlap, the common method for examining pellets of raptors (Obuch & Khaleghizadeh, 2011; Carevic et al., 2013), i.e., determination of the proportion of prey items, was used. The relationship between species and the physical characteristics of pellets was analyzed using SPSS ver. 16. Since the data for weight, length, and diameter had normal distributions, one-way analysis of variance (ANOVA) was used to test differences in these variables among the raptors. We used Duncan's multiple range test to test pairwise differences in pellet characteristics between raptors (DMRT). Additionally, we investigated seasonal variation in food items' richness and how prey items are utilized in different seasons by a common buzzard, common kestrel, and little owl. The association between the contents pellets and season were tested using a chi-square test in SPSS ver. 16. The pellets of Eurasian sparrow hawk were excluded because of limited sample size. Finally, we evaluated food niche overlap for five raptor species (excluding Eurasian sparrowhawk) based on several indexes. Pianka's niche overlap index (Pianka, 1974) was calculated from the presence-absence matrix, and Horn's overlap index (Horn, 1966) was calculated based on the proportion of the resources utilized by each species. Lastly, simplified Morisita's original index of overlap (Morisita, 1959) was applied to the numbers of prey species in Software for Ecological Methodology ver.7.2 (Krebs, 2001).

 

The collected pellets belonged to the common buzzard, long-legged buzzard, little owl, kestrel, golden eagle, and sparrow hawk. One-way ANOVA shows significant differences among raptors in the weight, length, and pellets' diameter (Table2).

 

Table 2. The results of ANOVA' test on the dimensions of the raptors' pellets, length (mm), diameter (mm), and weigth (g); (Sig=0, α=0.05)

 

Sig.

 

F              Mean              df

 

Sum of

 

 

 

 

 

 

 

 

 

 

 

 

 

Square

 

Squares

 

0

22.324

3012.438

4

18074.63

(Combined)

Between Groups

Length*Species

 

 

134.939

356

45339.447

 

Within Groups

 

 

 

 

352

63414.077

 

Total

 

0

24.845

1350.263

4

8101.576

(Combined)

Between Groups

Diameter*Species

 

 

54.347

356

18260.533

 

Within Groups

 

 

 

 

352

26362.109

 

Total

 

0

42.919

471.101

4

2826.608

(Combined)

Between Groups

Weight*Species

 

 

10.976

356

3688.094

 

Within Groups

 

 

 

 

352

6514.702

 

Total

 

 

 

The results of DMRT demonstrate homogenous subsets which are significantly different from each other. In all measured characteristics, the common buzzard and long-legged buzzard were placed in the same homogenous subset. The maximum pellet length, weight and diameter belonged to golden eagles, and the minimum belonged to little owls (Table 1). The pellets of golden eagles were significantly (P < 0.05) heavier than those of other raptors (for more details about dimensions of pellets, see Table 1).

The results of DMRT indicate that pellet diameter is significantly different among the raptors. Based on the results of DMRT for pellet diameter, the golden eagle did not cluster with any other species.

A total of 850 individual prey remains were identified. The proportion of prey items was significantly different among the raptors. However, remains of murids were most common in general, followed by birds (passerine). The least common prey items were ground squirrels and birds (poultry). Overall, the results indicated that during the four seasons, the diets of the studied raptors contained 48.8 % rodents (Muridae), 17.8% birds (passerine), 4.7% birds (poultry), 5.6% lagomorphs (1.5% tolai hare (Lepus tolai) and 4.1% Afghan pika (Ochotona rufescens)), 8.9% insects (spiders, beetles, grasshoppers, and ants), 10.5% reptiles (snakes and lizards, especially Gekkonidae spp), 4.9% hedgehogs and shrews (4.4% shrews, and 0.5% long-eared hedgehogs (Hemiechinus auratus), and 3.1% yellow ground squirrel (Spermophilus fulvus) (Table 3). Among the rodents, genus Meriones (mostly M. persicus and less than 10% M. libycus), 38% relative frequency, and genus Microtus (mostly M. socialis and M. arvalis), with 36% relative frequency, had the highest percentages in pellets. Indian crested porcupine (Hystrix indica), house mouse (Mus musculus), and short-tailed nesokia (Nesokia indica) with 2, 4.1, and 5%, respectively, had the lowest frequency among rodent remains in the studied pellets.

 

Golden eagle

Pray item           (Aquila chrysaetos)

Little owl (Athene

noctua)

Common kestrel (Falco

tinnunculus)

Common buzzard (Buteo

rufinus)

Long-legged buzzard (Buteo

rufinus)

Eurasian sparrowhawk

(Accipiter nisus)

Rodents                58

61

38

40

46

47

Birds(pass              18

6

15

16

15

33

Ground                 4

5

3

10

2

0

Insects 1                 1

7

13

2

4

4

Reptiles 2                4

11

11

11

22

10

Hedgehog

s and                   3

shrews

 

5

 

2

 

4

 

2

 

0

Birds                   4

1

7

8

3

3

Lagomorp               5

1

8

6

3

3

 

 

 

 The results of the chi-square test showed that prey items were significantly different among the raptors (P < 0.05), without significant differences between seasons. Although statistically insignificant, notable patterns were observed in different seasons. In spring, the pellets (especially little owl pellets) contained considerable percentages of insects. In summer, pellets contained a substantial richness of rodent species, and rodents had the highest frequency. In spring, birds (passerine) showed similar frequency in raptors' pellets, except for the little owl. Seasonal comparison for common buzzard, common kestrel, and little owl showed that richness in prey items was highest in summer, followed by autumn.

Pianka's overlap index (ranging from 0–1) shows that the largest food overlap exists between a long-legged buzzard and common buzzard (0.97), and golden eagle with a common buzzard (0.87); the smallest food overlap exists between the little owl and golden eagle (0.22). Morisita's index revealed similar results since the largest overlap was found between the little owl and common buzzard (0.884), and the golden eagle with common buzzard (0.87); the smallest food overlap was found between the little owl and golden eagle  (0.21). Based upon Horn's index, maximum niche overlaps were based upon Horn's index, maximum niche overlaps were between a long-legged buzzard and common buzzard (0.89), and a common buzzard with a common kestrel. A minimum food overlap (0.18) was observed between a little owl with a golden eagle (similar to other food overlap indexes). All food overlap indexes showed a small overlap between the golden eagle with the little owl (Table 4).

Table 4. Food overlap indexes for all the raptors.

 

Pairwise comparisons

Pianka

Morisita

Horn

 

 

Long-legged buzzard -Common buzzard

0.97

0.676

0.89

 

 

Long-legged buzzard -Little owl

0.585

0.23

0.38

 

 

Long-legged buzzard -Common kestrel

0.414

0.403

0.626

 

 

Long-legged buzzard -Golden eagle

0.771

0.768

0.818

 

 

Long-legged buzzard -Eurasian sparrowhawk

0.23

0.22

0.22

 

 

Common buzzard-Little owl

0.85

0.884

0.71

 

 

Common buzzard-Common kestrel

0.78

0.86

0.79

 

 

Common buzzard-Golden eagle

0.87

0.87

0.862

 

 

Common buzzard-Eurasian sparrowhawk

0.25

0.24

0.22

 

 

Little owl-Common kestrel

0.64

0.74

0.782

 

 

Little owl-Golden eagle

0.22

0.21

0.18

 

 

Little owl-Eurasian sparrowhawk

0.37

0.279

0.345

 

 

Common kestrel-Golden eagle

0.62

0.618

0.657

 

 

Common kestrel-Eurasian sparrowhawk

0.433

0.344

0.408

 

 

Golden eagle-Eurasian sparrowhawk

0.433

0.22

0.21

 

 

Various studies have been conducted in Iran and throughout the world on raptors' diets based on pellet analysis. Most of these studies have been carried out on a particular species (e.g., Bakaloudis et al., 2012). Rarely have such studies dealt with dietary niche' overlap and comparison of food habits for sympatric raptors, as recently done by Romanowski and Lesiński (2020). This study examined a total of 358 pellets belonging to six raptors. The results demonstrated that the raptors mainly feed on rodents throughout the year. This study's results are consistent with those of Obuch and Kristin (2004), who showed that prey remains in pellets mostly belonged to invertebrates, mammals, and birds. Since the highest frequency of prey items was found for rodents, our findings are also in concordance with the results of Davis (1975), Ghiasyi (1996), Shao and Lio (2008), and Zhao (2011).

However, our observed prey item frequencies were not in agreement with the results of Hounsome et al. (2004) and Souttou et al. (2006), who found insects to have the highest percentage. These differences could be attributed to various reasons. For instance, Obuch and Kristin (2004) observed that the prey composition of one species (little owl) could be different between different localities in arid climates (Egypt, Syria, and Iran). Another reason might be the small sample size; researchers such as Souttou et al. (2006) and Pocora et al. (2012) have studied only 35 and 103 pellets, respectively. Although we had a small sample size for the long-legged buzzard, we observed similar results to Bakaloudis et al. (2012), showing reptile remains were more frequent than avian remains.

Despite the similarity between our findings and those of Romanowski and Lesiński (2020) in terms of species dietary niches and richness of prey items, the results of this study demonstrated that there was a significant difference between the foods eaten by the studied raptors. Murids made up the majority of the diets, and passerines were the most common prey during summer. The frequency of prey items (especially in owls) is similar to what has been observed by Shao et al. (2007) in northwestern China. Seasonal patterns for common buzzard, common kestrel, and little owl in this study agree with Hussain Khan et al. (2016), who demonstrated that the richness of prey items is highest in summer, followed by autumn.

The study of niche overlaps revealed food competition among most raptors in the study area. However, we believe that sympatric species (even those in the same guild) undergo niche partitioning, at least in prey size (Romanowski & Lesiński, 2020). Although human settlements provide various habitats for the raptors, land-use change and habitat fragmentation during the last decade have caused the local extinction of these species. To protect raptors in the Binalud protected area, we recommend that landscape fragmentation be controlled and managed first. Secondly, the birds' food sources in the region, including small mammal species, need to be managed. Moreover, given the role of raptors in the biological control of rodents as pests of agricultural areas in the Binalud region, more effective management of prey-predator relationships and protection of raptors in this region should be pursued. Based on the results of our work and similar studies, Iran's Department of Environment can plan for the conservation of Iran's avian fauna.

This work was financially supported by Ferdowsi University of Mashhad, Iran (project # 41999). We thank the anonymous reviewers for their careful reading of our manuscript and their many insightful comments and suggestions, which helped us improve the manuscript.