Saudi Journal of Biological Sciences (2013) xxx, xxx–xxx

King Saud University

Saudi Journal of Biological Sciences www.ksu.edu.sa www.sciencedirect.com

ORIGINAL ARTICLE

Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia Mohammed Y. Shobrak a b

a,*

, Abdulhadi A. Aloufi

b

Biology Department, Faculty of Science, Taif University, P.O. Box 888, Zip Code 21974 Taif, Saudi Arabia Biology Department, Faculty of Science, Tabuk University, P.O. Box 741, 7149 Tabuk, Saudi Arabia

Received 9 June 2013; revised 1 November 2013; accepted 7 November 2013

KEYWORDS Seabirds; Breeding season; Northern Red Sea; Saudi Arabia

Abstract We undertook breeding surveys between 2010 and 2011 to assess the status of breeding birds on 16 islands in the northern Saudi Arabia. Sixteen bird species were found breeding at three different seasons; i.e. winter (Osprey), spring (Caspian and Saunder’s Terns), and summer (Lesser Crested, White-cheeked, Bridled Terns). It is postulated that food availability is an important factor influencing the breeding of seabirds in the northern Saudi Arabian Red Sea. Several species laid eggs earlier in northern parts of the Red Sea than in southern parts. The predicted increases in temperatures (Ta) could have a negative effect on species survival in the future, especially on those whose nests that are in the open. Finally, disturbance, predation and egg collection were probably the main immediate threats affecting the breeding seabird species in the northern Red Sea. ª 2013 Production and hosting by Elsevier B.V. on behalf of King Saud University.

1. Introduction Despite its importance as a breeding area for seabirds, few surveys have been carried out in the northern part of Saudi Arabian Red Sea (Shobrak et al., 2002a; PERSGA, 2003). The first systematic survey of seabirds was carried out by IUCN and MEPA during the summers of 1982 and 1983, and highlighted * Corresponding author. Tel.: +966 2 7241880; fax: +966 2 7241880. E-mail addresses: [email protected] (M.Y. Shobrak), aloufi@ut.edu.sa (A.A. Aloufi). Peer review under responsibility of King Saud University.

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the importance of Saudi Arabia for breeding terns and gulls (Evans, 1987). In 1996, the Saudi Wildlife Authority (SWA) (previously the National Commission for Wildlife Conservation and Development: NCWCD) carried out aerial and ground surveys to identify the important islands for breeding seabirds (Newton and As-Suhaibani, 1996). After that no seabird surveys have been carried out on the islands in the northern part of the Saudi Arabia Red Sea. However, parts of the central and the southern Red Sea were surveyed, including surveys of the island north of Yanbu (Meadows, 1993), the Umm al Qamari islands protected area survey (Symens, 1988a), several surveys of Kutambil Island between April and July (Stagg, 1984); and two surveys of the Farasan Islands during spring 1988 (Jennings, 1988; Symens, 1988b). In 1993 a joint expedition involving Manchester Metropolitan University (MMU) and the SWA undertook an aerial survey of seabirds covering the Farasan archipelago (Goldspink

1319-562X ª 2013 Production and hosting by Elsevier B.V. on behalf of King Saud University. http://dx.doi.org/10.1016/j.sjbs.2013.11.002

Please cite this article in press as: Shobrak, M.Y., Aloufi, A.A. Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia. Saudi Journal of Biological Sciences (2013), http://dx.doi.org/10.1016/j.sjbs.2013.11.002

2 et al., 1995). While in 1982/83 surveys covered 35 islands, the aerial survey in 1993 covered 117 islands. In addition, the aerial survey produced a list of islands suitable for breeding seabirds. The two surveys had only one species/island community in common: the Brown Noddy on Abu Shugur (Newton and As-Suhaibani, 1996). Two more studies were conducted in the region: on the breeding biology of the Bridle Tern Sterna anaethetus and White-cheeked Terns Sterna repressa (Sweet, 1994; Simmons, 1994). These studies indicated a possible effect of egg predation on tern’ species abundance in Farasan Islands. Recently, regular ornithological monitoring of Umm al-Qamari Island, a protected area, has been carried out in different seasons between 2001 and 2002 to determine which birds breed there, and assess their conservation status (Ostrowski et al., 2005). Several studies on Kentish Plover Charadrius alexandrines were conducted along the Saudi Arabian coast and on the Farasan Islands (AlRashidi et al., 2011a,b,c). However, no detailed research has been carried out to evaluate the status of breeding seabirds in the northern part of the Saudi Arabian Red Sea since the 1996 survey. Therefore, the aims of the present study were to determine the breeding seasons of the seabirds in the northern Red Sea of Saudi Arabia, and document the status and the threats of breeding seabirds in the Al Wajh archipelago islands. 2. Methodology and study area A pilot survey was carried out in the middle of July 2010 to determine the requirements of the study. As a result, we carried out five surveys on 16 islands between March and October 2011 (Fig. 1). Table 1 gives locations and descriptions of the islands visited. The descriptions of the islands were compiled

M.Y. Shobrak, A.A. Aloufi from our observations and from Al Ghazzawy et al. (2007). The number of breeding pairs was estimated using four methods: vantage point observations, flush counts, walk-through count, and quadrats (Symens and Al Suhaibany, 1996; PERSGA, 2004). The vantage point method was used at the cliff island of Mardunah and for part of Riykhah Island. At these sites, a boat or a suitable elevated location on land was used as a vantage point from where the breeding Brown Boobies Sula leucogaster and Sooty Gull Larus hemprichii nesting on the cliffs were counted. The flush count method was used for the majority of incubating seabirds on sandy or flat rocky islands (as upon approach by humans they rise up almost synchronously and fly around above the colony in a relatively compact flock). Validation of this method was calculated according to Bullock and Gomersall (1981), who gave a conversion factor of 1.5 for temperate nesting. This method was used commonly to survey White-cheeked Tern S. repressa and Bridled Terns S. anaethetus in the Arabian Gulf (Symens and Al Suhaibany, 1996). The walk-through count method was used to survey Whitecheeked Terns, Bridled Terns and the small colony of Lesser Crested Terns Sterna bengalensis. Finally, quadrats method was used to survey lesser-crested terns. For this method light weight frame of rigid wire measuring 1 · 1 m was laid carefully down at randomly selected locations within the colony, and the number of nests within the frame was counted. Counts were then used to determine the average density of nests (nest/m), and this was used to estimate the size of the colony. The breeding seasons were determined by compiling our observations of eggs and nestling size with published information on incubation and fledging periods, such as those in Jennings (2010) and Del Hoyo et al. (1996). Egg measurements

Figure 1 Map shows the islands visited. (1) Al Nabageyah; (2) Al Uwandiyah; (3) Riykhah; (4) Mardunah; (5) Ad Dahrah; (6) Sheikh Marbat; (7) Mrumah; (8) Mezebeyah; (9) Harr; (10) Ber-reem; (11) Umm al Malek; (12) Jazayah; (13) Attaweel; (14) Umm Qshaiyat; (15) Al Munqaleb and (16) Umm Khadav.

Please cite this article in press as: Shobrak, M.Y., Aloufi, A.A. Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia. Saudi Journal of Biological Sciences (2013), http://dx.doi.org/10.1016/j.sjbs.2013.11.002

Location and description of the islands visited. Location

Size (Km2)#

Island discretion

Al Nabageyah

N 26 44.427 E 36 02.579

0.02

Al Uwandiyah

N 26 35.920 E 36 06.608

0.015

Riykhah

N 26 11.068 E 36 21.696

1.2

Mardunah Ad Dahrah

N 26 03.940 E 36 28.888 N 26 09.165 E 36 26.787

0.06 12.5

Sheikh Marbat

N 25 52.810 E 36 35.955

0.09

Mrumah

N 25 42.000 E 36 36.104

12.6

Mezabeyah Harr

N 25 41.893 E 36 32.637 N 25 40.257 E 36 31.436

0.3 0.3

Ber-reem

N 25 39.550 E 36 30.775

19

Attaweel Jazayah

N 25 12.333 E 37 10.629 N 25 12.945 E 37 10.269

0.7 0.1

Umm Al Malek Al-Munqaleb

N 25 13.829 E 37 08.794 N 25 09.974 E 37 08.987

0.02 0.005

Umm Khadav Umm Qshaiyat

N 25 09.673 E 37 09.691 N 25 10.110 E 37 10.170

0.05 0.01

Low circle-shaped atoll with sandy surface mostly covered with Avicennia marina mangrove bushes. Small rocky part at the edge of the north west of the island Low atoll with sandy surface covered with A. marina mangrove bushes and small rocky part at the edge of the north west of the island A longitudinal atoll with sandy flat surface in the south eastern part and rocky (coral) edge 9 to 10 m high in the middle and the north west of the island. The sandy area is covered partly with vegetation A sandy flat surface in the north with high coral rocky area in the south (10-13 m) Low sandy island divided into two parts at high tide, (we visited the southern part only). The southern part has a sandy surface covered with A. marina mangrove bushes It longitudinal atoll, with a mix of sandy flat, gravel and rocky coral (2 m high) areas, with vegetation on the sandy southern part of the island A large island (10.9 km in length), the atoll is divided into three parts linked together by the emerging coral reefs. The northern part of the atoll extends south in the form of a long flat strip with a maximum height of 2 m. This strip is covered with sand and has some small scattered bushes. While the eastern coasts of the strip is mostly covered with the thick plants, its western coast has rocky edges A semi-circle island, mostly with a sandy surface except for the western edge of the island which is rocky A semicircular atoll with promontories on its northern, western and southern coasts. It has a sandy flat surface and about 2 m. high. The western coast is rocky It is curved shape with a length of 6.3 km. The bay area and the eastern coast are mostly covered with plants. The majority of the island surface is sandy, the central and western parts have good amounts of guano. The northern, western and southern coasts are rocky Has a sandy surface, with a maximum height of 6 m., with scattered vegetation. The coast is rocky It takes the form of a crescent strip with a sandy quasi-planar surface that gets higher gradually in the direction of the middle until a maximum height of 6 m. The coasts are rocky Has a sandy flat surface. Some of its coasts are rocky. A longitudinal atoll that extends from east to west, and has a flat surface with maximum height of 1 m. This surface is sandy and bushes. The coasts is rocky except in the east A circular atoll, within a coral barrier with a flat sandy surface It has sandy flat surface, with a mostly rocky coast

Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia 3

Please cite this article in press as: Shobrak, M.Y., Aloufi, A.A. Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia. Saudi Journal of Biological Sciences (2013), http://dx.doi.org/10.1016/j.sjbs.2013.11.002

Table 1 Island

M.Y. Shobrak, A.A. Aloufi

Table 2

PB 67 62 363

2 4

2 2-3 2 PB PB

80 (2010) 87 (2011) 25 (2010) 47 (2011) 4 (2010) 0 (2011) 5

3 10-20 PB 18 PB

PB

PB

134 168

168 175

PB PB 168 217

4 PB PB

67(2010) 134(2011) 152 (2010) 790 (2011) 804(2010417(2011

PB

15

5

25 23 107 (2010) 220 (2011) 185(2011) 147(2010) 13 (2011) 67 (2010) 14 (2010) 0 (2011) 1965 100 (2010) 0 (2011)

10 35

2

26

75 Ind. PB.

34(2010) 25(2011) 3 2 1

3 PB PB

150 134 21

4 3 1

2-3 2-5 PB PB PB

1 1 2 1 2 2 1 2 1 2-3 2 1 1 1 1 2 PB PB PB

10 4 84

Kentish Sooty Gull Plover Western Striated Purple Osprey Sooty Crab Plover Reef Heron Heron Falcon Heron Brown Booby

Breeding Species Recorded (Pairs (Year)) Island

Sixteen species were recorded, eight true seabirds, five water birds, two birds of prey and the rock dove Columba livia. Table 2 shows the total number of breeding pairs recorded on the islands. Fig. 2 shows the breeding periods for all species recorded on the surveyed islands, from which three egg laying periods can be distinguished: winter (November–January), spring (February–Mid April) and summer (June–August). Osprey was the only species recorded to lay eggs in winter, while Caspian Tern and Saunder’s Tern Sterna saundersi laid in spring. The majority of colonial species were recorded laying eggs in summer, including Bridled, White-cheeked and Lesser Crested Terns, and White-eyed and Sooty Gulls. Brown Booby S. leucogaster was found at nests with eggs from March to June. Late March to August is probably the period when most species raise their chicks. Relating the mean monthly air ambient temperature (Ta) to the availability of food (as represented by the timing of breeding of different fish families) shows that the majority of seabird species were raising chicks during summer, which is characterized by increase in temperatures (Ta) Figs. 3 and 4. Thus, chick-rearing is probably synchronized with the period when food is most plentiful and available. Our results highlight the importance of food availability for seabird breeding at the study area, although other factors also must influence their reproduction. Several studies have shown that food availability is the main factor affecting the timing of the breeding in the majority of seabird populations (Lack, 1968; Perrins, 1970; Newton, 1998; Le Corre, 2001; Suddaby and Ratcliffe, 1997; Crawford et al., 2006; Vieyra et al., 2009). Although other environmental factors may also affect egg laying and the number of offspring produced, it seems that the majority of colonial species nest when the mean temperature (Ta) is high. Species that nest in summer are potentially stressed by the heat. However, some species nest in the shade

The number of breeding pairs estimated on different islands.

3.1. Breeding season

1 1

3. Results and discussion

Al Nabageyah Al Uwandiyah Riykhah Mardunah Ad Dahrah Sheikh Marbat Mrumah Mezabeyah Harr Ber-reem Attaweel Jazayah Umm Al Malek Al-Munq-aleb Umm Khadav Umm Qshaiyat

White-eyed Caspian Swift Tern Lesser-Crested Gull Tern Tern

White-cheeked Tern Bridled Tern

Saunders’s Rock Dove Tern

were made for some species using a digital caliper, and the location of each island was recorded using a Garmin 12, GPS (Garmin, Olathe, KS, USA). Values for monthly ambient air temperature (Ta) from the Al Wajh airport meteorological station were provided by the Presidency of Meteorology and Environment (PME) and used to understand the effect of air temperature on the breeding season. Air temperatures (Ta) and humidity (Ha) at the nest were measured to understand the effect of these variables on the nesting of colonial species, whose nests were in shaded places and also in the open. Temperature (Ta) at the nest was recorded during egg incubation at the beginning of the summer breeding season of 2011 from 24 June to 28 July. HOBO U10 temperature and humidity data loggers (ONSET Computer Corporation, USA) were used. In addition, four of these data loggers were placed in the burrows of Crab Plover Dromas ardeola on 24 June, but unfortunately the loggers were not recovered in time to download data. For our initial examination of the relationship between breeding and food availability, we used published fisheries data (Abu Shusha et al., 2011). The scientific names of birds used are as per Dickinson (2003), whereas the English names are as per Gill and Wright (2006).

51 Ind. PB

4

Please cite this article in press as: Shobrak, M.Y., Aloufi, A.A. Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia. Saudi Journal of Biological Sciences (2013), http://dx.doi.org/10.1016/j.sjbs.2013.11.002

Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia

5

34

SF

OsP

SLT CT

BB Jan

30

WRH

Temperature ( C)

KP StH PH

32

CP ST

WYG SG

LCT BT WCT

Feb Mar Apr May Jun

Jul

Aug Sep Oct Nov Dec

Figure 2 The estimated range of breeding season of different species recorded during the study. (BB, Brown Booby Sula leucogaster; SG, Sooty Gull Larus hemprichii; WYG, White-eyed Gull Larus leucophthalmus; WCT, White-cheeked Tern Sterna repressa; BT, Bridled Tern S. anaethetus; LCT, Lesser-crested Tern S. bengalensis; CT, Caspian Tern S. caspia; SLT, Saunders’s Tern S. saundersi; ST, Swift Tern S. bergii; PH, Purple Heron Ardea purpurea; WRH, Western Reef Heron Egretta gularis; StH, Striated Heron Butorides striatus; KP, Kentish Plover Charadrius alexandrinus; CP, Crab Plover Dromas ardeola; OsP, Osprey Pandion haliaetus; SF, Sooty Falcon Falco concolor.

of bushes to lessen the effect of the sun. As expected, throughout the day Ta and humidity (Ha) at nests in the shade are significantly different than at nests exposed to sun (Ta, F = 62.47, P < 0.0001, Fig. 2; Ha, F = 45, 79, P < 0.0001, Figs. 5 and 6). This could explain why birds with nests exposed directly to the sun return quickly to their nests after been disturbed in order to protect eggs from harsh sun rays. The environment (including temperature and exposure to sun) can influence productivity and parental care in birds (Lack, 1968; Perrins, 1970; Williams and Tieleman, 2005; Vincze et al., 2013). Studies of Kentish Plovers on Farasan Island showed that parents spent more time sitting on eggs in exposed nests than those nests that were in the shade (AlRashidi et al. 2011a,c). Other seabird species use ‘‘belly soaking’’ to reduce egg and nest temperature. Belly soaking can reduce Ta at the nest up to 5.13 + 1.9 C (Al Suhaibany, 1995). Although the data are not sufficient to clearly define the actual effect of the exposure to higher temperatures on the breeding species in the study area, we believe that this factor will probably act more significantly on species that build their nests in places exposed to sunlight. Studies on effect of the climate on seabirds have already been documented especially in the timing

Figure 3

28 26 24 22 20 18 Jan

Feb

Mar

Apr

May

Jun

Jul

Aug

Sep

Oct

Nov

Dec

Month

Figure 4 Mean Ambient Air Temperature in different months recorded at Al Wajh town.

of breeding, breeding proportion, breeding success and adult survival (Thompson and Ollason, 2011; Monticelli et al., 2007; Gaston et al., 2009; Sandvik et al., 2005, 2012). In addition, an increase of air temperature (Ta) from 3 to 5 C is predicted over the next century (Thompson, 2010; Thompson et al., 2009) and could affect seabird populations, especially those species that nests in the open. 3.2. Species accounts 3.2.1. Brown Booby S. leucogaster The Brown Booby was found breeding only on the coral island of Riykhah (Table 1). The nests were scattered on the ground, one placed even on an old Osprey nest! Eggs were oval, pale blue with a chalky white coating. Mean dimensions (n = 13); 41.646 + 2.01 mm width and 60.231 + 2.75 mm length. The number of nests increased from three in late March, to 84 in June. By the end of July in 2011 all eggs had hatched and the majority of chicks had white feathers. By October all the nestlings fledged. These observations suggest that egg laying probably started in late February/early March and continued till May, and chicks fledged by end September or early October. Newton and As-Suhaibany (1996) suggested that breeding season of the species probably commenced early March in the northern Red Sea. Whereas Ostrowski et al. (2005) reported that there were birds incubating eggs throughout the year at three islands of Umm Al-Qamari located in the

The number of fish families breeding period in the Red Sea (Abu Shushah et al., 2011).

Please cite this article in press as: Shobrak, M.Y., Aloufi, A.A. Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia. Saudi Journal of Biological Sciences (2013), http://dx.doi.org/10.1016/j.sjbs.2013.11.002

6

M.Y. Shobrak, A.A. Aloufi 60 Under shrubs Open area

55

o

Temperature ( C)

50 45 40 35 30 25 20 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

Hours

Figure 5

The difference in air temperature in nests exposed to sun light and nests under shade of shrubs.

100

Humidity (%)

80

60

40

20 Under shrubs Open area 0 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

Hours

Figure 6

The difference in humidity in nests exposed to sun light and nests under shade of shrubs.

central part of the Saudi Arabian Red Sea where the highest numbers of nests with eggs were found in May, July and October. Although there are observations of chicks in early February in the Farasan Islands, the majority of the nests with eggs there were noted in early July in the first week of July (Newton and As-Suhaibany, 1996; Jennings, 2010). The current study suggests that the species probably commences breeding earlier in the northern part of the Red Sea. We were not able to estimate the actual number of breeding pairs in all northern Red Sea islands because of the limited number of islands surveyed. However, we believe that the species has probably declined or was over estimated by earlier studies. Jennings, 2010 estimated the number of breeding population in the Saudi Arabia was 2000 pairs. While, Ormond et al. (1984) and Newton and As-Suhaibany (1996)found that the majority of breeding pairs were located in the central and southern parts of the Saudi Red Sea and suggested that Farasan archipelago and the Al Qunfudah areas are the most important breeding areas for the species. The current results agree with this finding as Riykhah Island was the only island where the species was found breeding during this study.

The present study confirmed breeding only on rocky (coral) island. Previous studies showed that elsewhere in the Red Sea, breeding habitats were varied and included sandy beaches, open rocky islands and occasionally cliffs (Jennings, 2010; Newton and As-Suhaibany, 1996; Ostrowski et al., 2005; Shobrak, 2007). However, more islands are needed to be surveyed to determine the habitat and to estimate the number of the Brown Booby in the northern part of the Red Sea. 3.2.2. Striated Heron Butorides striatus Although the species was found on all islands during the survey, no proper estimate is available of the number of breeding pairs. However, in this study 15 fledged and unfledged chicks were recorded during June in the Al Nabageyah and Al Uwandiyah islands. These islands were covered by Avicennia marina mangrove bushes. Our observations suggest that the breeding season probably commence in April in this area, egg laying in late April early May. In the southern part of the Red Sea fledged chicks were reported during July and seven active nests with eggs were found in the end of April in Farasan

Please cite this article in press as: Shobrak, M.Y., Aloufi, A.A. Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia. Saudi Journal of Biological Sciences (2013), http://dx.doi.org/10.1016/j.sjbs.2013.11.002

Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia Islands (Jennings, 2010). Atthe Umm Al Qamari islands unfledged chicks were recorded in May 25, 2002 (Ostrowski et al., 2005). These studies show that the majority of nesting activities on Saudi Red Sea takes places between April and July. Jennings (2010) suggests that the breeding habitats were usually in dense vegetated islands and occasionally in holes and crevices of fossil coral, often among colonies of Western Reef Herons and Eurasian Spoonbills. We also found that both the islands were covered by A. marina mangrove bushes. As we were not able to estimate the number of breeding pairs, actual breeding population in the northern Red Sea of Saudi Arabia is not known. However, Jennings (2010) reported that it is a widespread species over the whole Red Sea region and the breeding population probably exceeds 1000 pairs with majority of colonies at Al Wajh and Farasan archipelagos.

7

Although the habitat is suitable for the species, especially on the mangrove-covered islands such as Ber-reem, we could not confirm breeding. Jennings (2010) considered the Purple Heron species as a common and widespread migrant with a few wintering and breeding birds on Farasan Islands and Al Lith lagoon, as well as Yanbu. While, Newton and Al-Suhaibany, 1996 did not observe any individuals at Farasan Islands, they recorded them at the Qishran lagoon near Al Lith and thought that they could breed. According to Evans (1987), up to 15 pairs breed on Farasan Islands. Jennings, 2010) noted juveniles in June in Farasan, and suggested that the breeding season commences in spring and sometimes in summer. The species is usually a solitary nester but may nest adjacent to colonies of other herons in areas of dense mangroves. 3.2.5. Osprey Pandion haliaetus

3.2.3. Western Reef Heron Egretta gularis We located only two empty nests and two nestlings under mangrove A. marina bushes during April; one at Al Nabageyah Island and the other at the Al Uwandiyah Island. The behavior of adults nearby suggested that these nests were active. Several old nests were recorded on other islands with dense vegetation. This suggests that the Western Reef Heron nests on these islands, may be in low numbers. We found solitary nests, whereas Jennings (2010) found that the Western Reef Heron sometimes congregate in larger numbers, up to 450 pairs. Newton and As-Suhaibany (1996)noted that the Western Reef Heron nesting is in solitary pairs and in small colonies with a maximum of eight nests per colony. The largest known colony on the Red Sea coast was recorded in Egypt with 40–60 pairs in mangroves of Manqata north of Nabq (Goodman and Meininger, 1989). Some nesting pairs were associated with Eurasian Spoonbills (Ormond et al., 1984; Shobrak, 2001). An aerial survey in February 1993 from Jizan to Gulf of Aqaba found 422 birds. Jennings, 2010 suggested that the total number of breeding pairs in Arabia is about 3000 pairs. We believe that the species need more investigation to estimate the actual size of the breeding population in Saudi Arabia. Although the species is considered as a common breeding resident along the Saudi Red Sea coast (Jennings, 2010), the Western Reef Heron uses a variety of vegetation types for nesting but especially mangroves and Euphorbi afractiflexa in the southern Red Sea (Newton and Al-Suhaibany, 1996). While to the north of Al Wajh the species was only recorded nesting on mangrove trees (Ormond et al., 1984; Newton and AlSuhaibany, 1996). However, nests can be in cliffs and under small bushes (Shobrak et al. 2002a; Jennings, 2010). The breeding season possibly ranges between March and August. However, Jennings (2010) found that there is little variation on the breeding seasons from different areas in Arabia, with an earliest egg laying in the first week of October on islands of Bahrain in the Arabian Gulf. 3.2.4. Purple Heron Ardea purpurea We did not observe this species during the survey, but we suspected that it breeds in the mangrove area on Ber-reem Island, as a pair was seen standing on the mangrove during March and April visit. As the species was not observed in June and later visits the assumption of breeding in the northern Saudi Arabian Red Sea needs more investigation.

The Osprey was the only species which was breeding on all the islands visited, with at least one active nest on each island, sometimes two active nests on the larger islands (e.g. Ber-reem, Riykhah and Mezabeyah). We recorded eggs about to hatch at the end of March. One egg was measured and the size was L 63.52 and W 46.36 mm. Jennings (2010) reported the mean measurement of 41 clutches of three eggs on Farasan as 60.1 mm in length and 43.3 mm in width. The result of this work suggested that egg laying probably commences late November–early December. Similar observation was recorded on the Farasan Islands, when 51–65 pairs were found breeding in late autumn in 1993 (Fisher, 2001). Jennings (2010) reported that the chicks hatch in as late as May on Tiran Island. Our study suggests that the species starts breeding a few weeks earlier than was recorded in Tiran Island. In the northern Red Sea we suggest that all islands may have one pair and large islands could have two nesting pairs. During the mid-winter waterfowl count in Saudi Arabia in 1993, an estimate of the population was made by Symens and Al Salamah (1993). Although their survey did not include all the islands in the Red Sea, their results showed that the Red Sea holds a substantial proportion (64%) of the total Saudi population. The survey carried out by Newton and Al-Suhaibany (1996) showed that the species was abundant in Al Wajh archipelago where nest density appeared to be the highest in the Saudi Red Sea coast. Jennings (2010) suggested that the highest breeding concentration is in the Red Sea islands, especially in Farasan and Al Wajh Archipelago with an estimate of 500 pairs. 3.2.6. Sooty Falcon Falco concolor Adults were observed during our visit in July 2010 at Ber-reem and Mardunah islands. While in 2011 we only saw a fledged nestling being fed by an adult at Riykhah in October and one pair in Mardunah. This suggests that the species probably arrives in June–July to the coral islands for nesting. However, more investigation is needed to determine the numbers of breeding pairs in the north of the Red Sea. In the present study, adult Sooty Falcons were recorded on July at Ber-reem and Mardunah islands whereas fledged nestling was observed at Riykhah in October. We suspected that the breeding season probably started in July for this species. This probably matches with earlier studies that 90% of clutches in the Red Sea were laid in the last three weeks of July and extended to the first 10 days of August in some years

Please cite this article in press as: Shobrak, M.Y., Aloufi, A.A. Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia. Saudi Journal of Biological Sciences (2013), http://dx.doi.org/10.1016/j.sjbs.2013.11.002

8 (Gaucher et al. 1995; Jennings, 2010). These observations are related to the previous works such as (Ormond et al., 1984; PERSGA, 2003; Jennings, 2010). Ormond et al. (1984) recorded significant breeding colonies on a number of rocky islands in the northern Red Sea. In addition PERSGA (2003) and Jennings (2010) suggested that the distribution of the species in Red Sea shows concentrations near Al Wajh Bank and Al Lith. Studies carried out in Bahrain and in the United Arab Emirates and Oman showed that there is a decline in Sooty Falcons populations in these areas (Kavanaugh and King, 2008; Shah et al., 2008; McGrady et al., 2010). Previously its population was over estimated, between 4000 and 10,000 pairs (Moreau, 1969; Brown et al., 1982; Cade, 1982). However, Gaucher et al. (1995) estimated that the world population was only 1000 breeding pairs and the Saudi population was 260–381 pairs in the Red Sea. This is far less than the previous estimation. Jennings (2010) suggested that there may be more breeding pairs in the north of the Red Sea between Al Wajh Bank and Tiran Island than has been estimated. Gaucher et al. (1995) suggested that the distribution pattern, density and breeding success of this falcon seemed to be strongly influenced by the food availability (autumn migration of small and medium–size birds) and the deterring presence of terrestrial predators. We suggest that northern Red Sea population in Saudi Arabia has probably declined (or has been over estimated) and that more work is needed to investigate the status of this Near Threatened species. Based on the results, its global status should be reassessed. 3.2.7. Kentish Plovers Charadrius alexandrinus Kentish plover chicks were seen on Harr and Sheikh Marbat islands during April and June visits with one fledged chick with an adult in July. This suggests that the species probably commence breeding in February/March until late July. It was difficult to determine the actual population of the islands within the time period available but we believe that there are probably only a few breeding pairs in the islands visited. Present observations showed that the species commences egg laying from late February to early March. AlRashdi et al. (2011b) showed that most of the suitable areas for the Kentish Plover are concentrated from about 100 km south of Jiddah to Yanbu Al Bahr and near the city of Jizan, whereas suitable areas in the north have relatively small populations. Generally the species is known to be a widespread breeding bird in the coastal areas and islands of Saudi Arabia (Jennings, 2010). 3.2.8. Crab Plover D. ardeola In Saudi Arabia the first confirmed breeding record for the species was in May 1983 with 45 burrows (Ormond et al., 1984). A detailed study on the species was done by Gregory and Goldspink (1998) in Farasan Islands and provided information on the distribution, status and feeding of this species with particular references to conservation and management. In the northern part of the Red Sea, Saudi Arabia, the first breeding colony was recorded in 1996 (Newton and Al-Suhaibany, 1996). During the present survey, on two islands we recorded breeding colonies; Sheikh Marbat had 46 burrows and 85 individuals present, and Attaweel Island had 26 burrows with 35 individuals. In addition, possible nesting areas with nearly 70

M.Y. Shobrak, A.A. Aloufi birds were observed at Harr Island during April. Adults carrying food items to burrows in July 2010 indicated nestlings. This suggests that the species probably commences breeding by late May–early June in the northern islands. In October fledged youngs were seen with adults at the above islands. The present survey suggests that the species probably commences egg laying early May/June. Al Malki (2011) reported dead chicks in early June at Al Natain Island. However, incubating adults were found in July on Sudanese Islands (Shobrak et al. 2002b; PERSGA, 2003). Before 1996 survey, the species was considered as a breeder of south of Al Lith as all nesting colonies at the time were recorded in Saudi Arabia on Farasan Islands (Ormond et al., 1984; Jennings, 2010). In 1996 a new colony was found in Al Wajh archipelago with 100 breeding pairs (Newton and AlSuhaibany, 1996). Jennings (2010) estimated the number of breeding pairs was about 250 on three or four islands. A large population was later recorded in Al Batain Island at Al Qunfudah consisting of about 620 burrows (Al Malki, 2011). However, according to De Marchi et al. (2006) there are larger breeding populations on the other side of the Red Sea. He estimated the number breeding in the central Eritrea to be 5000– 6000 pairs, probably representing 50% of the known world breeding population. The changed position of the nesting burrows at Sheikh Marbat Island noted accords with the suggestion of Chiozzi et al. (2011), that the species changes colony location every year even in the same island. 3.2.9. Sooty Gull L. hemprichii The species was observed on all islands in the present survey. The largest colony was found on the rocky island of Riykhah with 80 pairs in 2010 and 87 pairs in 2011. The majority of nests were in the shade of rocks. Eggs as well as chicks were seen in June 2011 on Riykah Island and by the end of July. Moreover, birds with 1–3 eggs were observed in late June 2011 on Harr Island, and we estimated 10–20 pairs probably nested. The nests on this island were beside or underneath bushes. The species probably commences breeding in late May or early June. Eggs measured during the survey showed that length was 57.95 + 3.03 mm, width was 41.37 + 2.08 mm, (n = 15). This study suggested that egg laying commenced in late May or early June. Newton and Al-Suhaibany, 1996 reported the same time of breeding on this island (Riykhah). However, in the southern Red Sea, the egg laying commences in June/ July (Jennings, 2010). Newton and Al-Suhaibany (1996) estimated the population of the species was 200 breeding pairs on Riykhah Island, which was almost twice the number recorded in the present survey. This may be due to different surveys methods, as the earlier survey was carried out by plane and the present survey used flush counts on the ground. On the other hand, the total number of birds estimated in 1982/ 83 was 73 breeding pairs in the same island. 3.2.10. White-eyed Gull Larus leucophthalmus The breeding of the white-eyed gull was observed at three islands off Umm Lajj town. These islands were sandy with rocky habitats. The nests were usually exposed to sunlight. We estimated a total of 304 breeding pairs. Whereas, in 1982 (Ormond et al., 1984) found 152–155 pairs at Al Wajh bank (Is this a same area where you also surveyed?), Comparing the estimated

Please cite this article in press as: Shobrak, M.Y., Aloufi, A.A. Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia. Saudi Journal of Biological Sciences (2013), http://dx.doi.org/10.1016/j.sjbs.2013.11.002

Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia number in this study with the previous surveys in 1982, we found the number of breeding pairs has probably increased. On the other hand, the aerial survey in 1996 estimated the minimum breeding population in Saudi Arabian Red Sea was 1500 Pairs (Newton and Al-Suhaibany, 1996). A survey covering 22 islands in the Yemeni Red Sea found 3500–4000 pairs (Al Saghier, 2002; Jennings, 2003). However, Jennings (2010) assumed that the species was slightly more numerous than the sooty gull, particularly in the extreme north and south, with an estimate of 3000 pairs in Saudi Arabia. Nests with eggs and chicks were observed on 28 July 2011 and suggested that breeding probably started in the late May/early June, which is similar to the Sooty Gull. In the Red Sea area under Yemen, fresh nests were found in July (Al Saghier, 2002). Jennings (2010) suggested that there is a slight bias toward earlier nesting in the northern Red Sea, with eggs dated between June and August from Tiran to Farasan and from July to September in Yemen. In Djibouti, adults were found incubating in July (Shobrak, 2007). Egg measurements were 48.86 + 5.01 mm in length and 34.89 + 4.11 in width (n = 21). 3.2.11. Caspian Tern Sterna caspia A total of 22 breeding pairs were observed on all the sandy islands visited during this survey. Breeding probably occurred on all islands off Umm Lajj with flat sandy areas. Newly hatched chicks and nests with eggs were observed in late April and fledged chicks being fed by an adult were seen in late June, which suggests that the species probably commences breeding in early March. Shobrak (2001) recorded three pairs showing aggressive behavior on a small island near Al Qunfudah in early April 2001, but no nest was found. The species was recorded nesting in late winter or early spring on the mainland coast south of Yanbu and on several sandy islands within the Farasan Islands (Newton and Al-Suhaibany, 1996). Dispersed loose colonies of small size were found near Yanbu and Jeddah (Gallagher et al., 1984). Newton and Al-Suhaibany (1996) estimated the breeding population in Saudi Arabian Red Sea to be between 100 and 200 pairs, whereas Jennings (2010) estimated the total Arabian population to be 500 pairs. In Red Sea population in Yemen was estimated at 20 pairs. This suggests that more breeding occurs in northern parts of the Red Sea. However, most of the earlier surveys were carried out in summer and we believe that the Saudi Arabian population has probably been underestimated. 3.2.12. Swift Tern Sterna bergii Courtship behavior and birds carrying food were observed at Sheik Marbat Island during the April visit, but no nests or chicks were recorded later on the islands. This suggests that the species breeds on nearby islands and egg laying probably starts in May. However, more islands in the northern Red Sea need to be surveyed to determine the status of this species. Ostrowski et al. (2005) recorded active nests of about 270 pairs on a sand bank at Umm Al Qamari Island Protected area on 25 May 2002. By 29 July few adults were still incubating and the majority of the eggs had hatched. On the islands of Djibouti, at the southern border of the Red Sea, birds commence breeding by early July and chicks were observed in September (Shobrak, 2007). In the Red Sea area under Sudan jurisdiction,

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incubating birds were observed in the middle of July (Shobrak et al., 2002b). These findings suggest that the species commences breeding by early May in northern Red Sea and later on the southern islands. Considering data size of our present survey, it is difficult to estimate the population of Swift Tern. An aerial survey in 1996 between June and July covering 262 islands found about 2000 breeding pairs spread from the Farasan Islands to Al Wajh bank, most colonies were found near Qunfudhah (Newton and Al-Suhaibany, 1996). They recorded the species in most of the areas south of Jeddah and only at Al Wajh in the north. Nearly 76% of nesting pairs found by Newton and Al-Suhaibany (1996) were associated with active colonies of Lesser Crested Tern S. bengalensis. Their estimate suggests 4500– 5000 individuals and probably 1845–2000 breeding pairs on the Saudi Arabian Red Sea coast. Jennings (2010) reported that the total Arabian population is probably up to 13,000 pairs. However, the species need more investigation to determine its status and the breeding biology. 3.2.13. Lesser Crested Tern S. bengalensis The nests of this species were found in dense colonies on open sandy islands. The nests were found at four islands and the highest number was observed in Al Nabageyah with 1965 breeding pairs. On 16 July 2010 it was observed that birds were starting to build a colony at Al Nabageyah Island. By end of July 2011 the colony was completed and the majority of birds were found incubating. In October fledged nestlings with adults were observed around the islands. This suggests that the species commences egg laying by late June or early July. In the Sudanese islands of the Red Sea, incubating adults were seen in the second week of July (Shobrak et al., 2002b). Similar results were found in Umm Al Qamari Island, with 420 pairs incubating in 16 July (Ostrowski et al., 2005). On islands near Bab Al Mandeb, adult birds were incubating on 17 August (Jennings, 2010). On Djibouti islands courtship behavior was observed in the first week of July and birds with chicks were seen in September (Shobrak, 2007). These observations suggest that the Saudi Arabian population in the Red Sea probably commence breeding earlier than the southern population at the Bab Al Mandeb. The southern population probably started a few weeks later in July or early August. The mean length and width of the eggs were 50.44 + 3.25 and 35.17 + 2.67 (n = 49), respectively. Ormond et al. (1984) consider it a common bird on the Saudi Arabian Red Sea coast. Comparing the 1982/83 and 1996 estimates of the number of breeding pairs, the 1982/83 survey recorded 1,880 breeding pairs, while that of 1996 reported 2000–4000 pairs. The total number estimated for the Saudi Red Sea was between 9000 and 10,000 individuals (PERSGA, 2003). The species seems to be common also in the western part of the Red Sea (Shobrak et al., 2002b). 3.2.14. White-cheeked Tern S. repressa The species was observed nesting on the majority of sandy islands that we surveyed. Although the species was recorded in high numbers, it was more common in the southern islands, especially in Sheik Marbat. The locations of colonies on these islands were different in 2010 and 2011. There were more breeding pairs in 2011. A few eggs were recorded in late June, whereas in July 2011 we found large number of nests with

Please cite this article in press as: Shobrak, M.Y., Aloufi, A.A. Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia. Saudi Journal of Biological Sciences (2013), http://dx.doi.org/10.1016/j.sjbs.2013.11.002

10 newly hatched chicks. Thus, the breeding season probably commenced by the middle of June. The mean length and width of the eggs were 38.92 + 1.37 and 27.84 + 1.37 mm (n = 21), respectively. According to the present study the species commenced breeding in late June. Newton and Al-Suhaibany, 1996 found no changes in the time of breeding in Red Sea as they found nests with eggs in the third week of June. The species was observed nesting in the majority of sandy islands (Shobrak et al., 2002a). Several authors suggest that the White-cheeked Tern is a widespread species in the Saudi Arabian Red Sea (Ormond et al., 1984; PERSGA, 2003; Jennings, 2010). Although the species was recorded in the majority of islands visited, it was more numerous in the southern islands, especially Sheik Marbat. The species was also recorded more numerously in the southern islands in the Saudi Arabian Red Sea, especially on Farasan Islands; 70% of the total Saudi Red Sea population was recorded (Newton and Al-Suhaibany, 1996). Comparing the earlier information we found a significant increase in the number of breeding pairs between 1982/83 and 1996 surveys, 1254 to 1264 breeding pairs in the earlier survey and 7500 breeding pairs in 1996 survey. The species has been targeted by egg collectors in most parts of the Saudi Arabian Red Sea (PERSGA, 2003). This probably had an adverse effect on the population as recorded by Simmons (1994) in Farasan Islands. 3.2.15. Bridled Tern S. anaethetus The Bridled Tern was recorded on all sandy islands with vegetation. Nests with eggs were found in late June when one newly hatched chick was present. Nests were under mangrove A. marina bushes. Egg laying probably commences in early June. The mean length and width of eggs were 46.01 + 3.16 mm and 32.72 + 2.97 mm (n = 23) respectively. Ormond et al., 1984 counted between 4,030 and 5,080 pairs in the area in 1982/83 while the 1996 survey in the Saudi Arabian Red Sea estimated 60,000 breeding pairs. Both the Farasan and Al Wajh archipelagoes hold large populations of this species (Shobrak et al. 2002a). We believe that the species may have been over estimated in the earlier survey of the Al Wajh population. In addition, during 1993, six colonies on different islands of Farasan archipelago were recorded with a total population estimate of 37,000 individuals (Sweet 1994; Tatwany et al. 1995). We suspect that Farasan Islands has probably a higher breeding population than the Al Wajh Bank islands. 3.2.16. Saunders’s Tern S. saundersi We observed eggs and newly hatched chicks during April. The mean length and width of the eggs was 31.21 + 0.53 and 22.68 + 0.31 mm (n = 3) respectively. Nearly 15 breeding pairs in two small colonies were recorded on Sheik Marbart Island. In addition, four pairs with pre-fledged chicks were observed on Mezabeyah Island during the same survey period. These observations suggest that breeding season probably starts in late March and continues to late June. Sooty Gull tracks were observed in all colonies of the Saunders’s Tern that suggests the Sooty Gull could be preying on chicks of Saunder’s Tern. Our study suggests that egg laying probably start in late March. On the Farasan Islands in the southern part of the Saudi Arabian Red Sea a fledged juvenile was recorded in early

M.Y. Shobrak, A.A. Aloufi June (Newton and Al-Suhaibany, 1996). Moreover, Jennings (2010) suggested that breeding in the southern part of Red Sea, is April to June. The habitat of nests was flat sandy gravel. 4. Threats on the Seabirds During our studies we identified several factors that affect the breeding population of seabirds, such as human disturbance, predation, egg collecting. Tracks of humans were found at all islands we visited. Although access to islands is under the control of the Coast Guards and landing is forbidden except on designated islands where overnight shelter and temporary camps are sometimes established. One to three fishing boats were observed at all sandy islands during the breeding season. Casual human visits to breeding islands, whether by fishermen or for recreational purposes, can cause significant disturbance to nesting birds even if there is no deliberate interference. The high ambient temperature in summer means that eggs and chicks suffer heat stress through solar radiation if a sitting bird is disturbed. This factor could be vital in the future; with increased tourism and the predicted increase of air temperature. Other threats on these islands include the human exploitation, pollution and predation. According to local people, many fishermen collect eggs for consumption. Although this is no longer a common practice in the area, it is still continuing in a smaller scale. We observed tracks of rats on all the islands we visited which probably are predators of seabird eggs and nestlings. Several authors discussed the threats on the seabirds of the Red Sea coast (Gallagher et al., 1984; Evans 1987, 1989; Sweet, 1994; Simmons, 1994; Newton and Al-Suhaibany, 1996; Shobrak, 2007; Jennings, 2010). Disturbance is likely to increase the natural predation effects on those seabirds whose nests are exposed to the solar radiation. During our survey, Sooty Gulls were seen to take eggs of Saunders’s Tern and White-cheeked Tern. In a study in 1993 on Sumair island, located in southern part of the Red Sea, up to 30% of all Bridle Tern eggs had disappeared by the next visit, and all marked White-cheeked Terns’ eggs at other islands in the archipelago were disappeared (Sweet, 1994; Simmons, 1994). Therefore, we highly recommend that disturbance to the nesting birds should be strictly avoided, especially in the hottest part of day. Finally, seabirds could be affected by oil pollution as the Red Sea is known to receive 6836 metric tons or 14.61 kilograms per square kilometer per year of oil from shipping (Awad, 1995). The global refinery input is 0.56 kilograms per square kilometer per year, whereas the Red Sea receives 6.64 kilograms per square kilometer per year: nearly 11 times more. Although oil pollution affects diving birds more, such as cormorants, boobies and divers, it can also cause damage to breeding seabirds during the various stages of their life cycle. Large numbers of adults can be killed by oil-fouling. Oiling of eggs by contaminated incubating birds can also cause serious problems (Freedman, 1989). Furthermore, beached oil can have a severe impact on flightless chicks on beaches near colonies. Oil spills can also affect seabirds indirectly through the food chain, as toxic hydrocarbons may damage the ecosystems within which the birds’ food resources are produced and the disruption of the breeding cycle of prey fish species could cause a drastic decline in seabirds’ breeding success.

Please cite this article in press as: Shobrak, M.Y., Aloufi, A.A. Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia. Saudi Journal of Biological Sciences (2013), http://dx.doi.org/10.1016/j.sjbs.2013.11.002

Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia Acknowledgments We are thankful to the Dean of Scientific Research at Tabuk University for supporting this project No 23/21/1432. We are grateful to Mr. Ali Al Faqeih, Abdullah Alrabdi, Saud Aljethli and Mohamed Al Rashedi for their assistance during the field work. Finally, we wish to thank Border Guard Foundation in Tabuk region for their help by allowing us to reach the islands in Alwajh and Umluj. We also want to thank Dr. Asad R. Rahmani, the Director of Bombay Natural History Society, Dr. Michael J. McGrady and Michael Jennings for their comments on the draft of this paper. References Abu Shusha, T.L., Kalantan, M.Z., Al-Nazry, H.H., Al-Ghamdi, Y.A., 2011. Fishes from Territorial Saudi Arabian Red Sea Water. Marian Research Center-Jeddah, 225. Al Ghazzawy, A.M., Al-Rashed, M.A., Al-enayzan, A.S., 2007. The Atolls of Saudi Arabia in the Red Sea & the Arabian Gulf. Saudi Geological Survey, Jeddah, 452. Al Malki, M., 2011, Breeding ecology and conservation of Kentish Plover Charadrius alexandrinus, and Crab Plover Dromas ardeola in the Red Sea of Saudi. Unpublished report, Bath University. Al Saghier, O., 2002. Survey of theBreeding Seabirds in Red Sea of the Republic of Yemen. PERSGA, Jeddah. Al Suhaibany, A., 1995. The White Cheeked Tern Sterna repressa: egg temperature and behavioural thermoregulation during incubation in hot environment. Unpublished MSc Thesis, University of Wales. AlRashidi, M., Kosztola´nyi, A., Shobrak, M., Ku¨pper, C., Sze´kely, T., 2011a. Parental cooperation in an extreme hot environment: natural behaviour and experimental evidence. Animal Behaviour 82 (par 2 ‘‘August’’), 235–243. AlRashidi, M., Kosztola´nyi, A., Shobrak, M., Sze´kely, T., 2011c. Breeding ecology of the Kentish plover Charadrius alexandrinus in Farasan Islands, Saudi Arabia (Aves: Charadriiformes). Zoology of the Middle East 53, 15–24. AlRashidi, M., Long, P.R., O’Connell, M., Shobrak, M., Sze´kely, T., 2011b. Use of remote sensing to identify suitable breeding habitat for the Kentish Plover and estimate population size along the western coast of Saudi Arabia. Wader Study Group Bulletin 118 (1), 32–39. Awad, H., 1995. Oil Pollution in the Red Sea: A State of the Art Assessment. PERSGA/IOC/UNEP Workshop on Oceanographic Inputs into Coastal Zone Management in the Red Sea and Gulf of Aden. Oct. 12, 1995. Jeddah. Brown, L.H., Urban, E.K., Newman, K., 1982. In: The Birds of Africa, 1. Academic Press, London. Bullock, I.D., Gomersall, C.H., 1981. The breeding population of tern on Orkney Shetland in 1980. Bird Study 28, 187–200. Cade, T.J., 1982. The Falcons of the World. Collins, London. Chiozzi, G., De Marchi, G., Semere, D., 2011. Coloniality in the Crab Plover Dromas ardeola does not depend on Nest. Site Limitation. Waterbirds 34 (1), 77–81. Crawford, R.J.M., Barham, P.J., Underhill, Les.G., Shannon, L.J., Coetzee, J.C., Dyer, B.M., Leshoro, T.M., Upfold, L., 2006. The influence of food availability on breeding success of African penguins Spheniscusdemersus at Robben Island, South Africa. Biological Conservation 132, 119–125. De Marchi, G., Chiozzi, G., Semere, D., Galeotti, P., Boncompagni, E., Fasola, M., 2006. Nesting, overwintering, and conservation of the Crab Plover Dromas ardeola in central Eritrea. Ibis 148, 753– 764. Del Hoyo, J., Elliott, A., Sargatal, J., 1996. In: Handbook of the Birds of the World: Hoatzin to Auks, vol. 3. Lynx Edicions, Barcelona.

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Please cite this article in press as: Shobrak, M.Y., Aloufi, A.A. Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia. Saudi Journal of Biological Sciences (2013), http://dx.doi.org/10.1016/j.sjbs.2013.11.002

Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia.

We undertook breeding surveys between 2010 and 2011 to assess the status of breeding birds on 16 islands in the northern Saudi Arabia. Sixteen bird sp...
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