Status of Breeding Seabirds on the Northern Islands of the Red Sea, Saudi Arabia

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,*, Abdulhadi A. Alouﬁ b a Biology Department, Faculty of Science, Taif University, P.O. Box 888, Zip Code 21974 Taif, Saudi Arabia b 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 Abstract We undertook breeding surveys between 2010 and 2011 to assess the status of breeding Seabirds; birds on 16 islands in the northern Saudi Arabia. Sixteen bird species were found breeding at three Breeding season; different seasons; i.e. winter (Osprey), spring (Caspian and Saunder’s Terns), and summer (Lesser Northern Red Sea; Crested, White-cheeked, Bridled Terns). It is postulated that food availability is an important factor Saudi Arabia 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 tem-

peratures (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 the importance of Saudi Arabia for breeding terns and gulls (Evans, 1987). In 1996, the Saudi Wildlife Authority (SWA) Despite its importance as a breeding area for seabirds, few sur- (previously the National Commission for Wildlife Conserva- veys have been carried out in the northern part of Saudi Ara- tion and Development: NCWCD) carried out aerial and bian Red Sea (Shobrak et al., 2002a; PERSGA, 2003). The first ground surveys to identify the important islands for breeding systematic survey of seabirds was carried out by IUCN and seabirds (Newton and As-Suhaibani, 1996). After that no sea- MEPA during the summers of 1982 and 1983, and highlighted bird 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 sur- * Corresponding author. Tel.: +966 2 7241880; fax: +966 2 veys of the island north of Yanbu (Meadows, 1993), the Umm 7241880. al Qamari islands protected area survey (Symens, 1988a), sev- E-mail addresses: [email protected] (M.Y. Shobrak), aloufi@u- eral surveys of Kutambil Island between April and July (Stagg, t.edu.sa (A.A. Aloufi). 1984); and two surveys of the Farasan Islands during spring Peer review under responsibility of King Saud University. 1988 (Jennings, 1988; Symens, 1988b). In 1993 a joint expedition involving Manchester Metropol- itan University (MMU) and the SWA undertook an aerial sur- Production and hosting by Elsevier vey 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

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 ttso reigsaid nteNrhr sad fteRdSa ad rba3 Arabia Saudi Sea, Red the of Islands Northern the on seabirds breeding of Status laect hsatcei rs s hba,MY,Aofi ..Sau fbedn ebrso h otenIlnso h Red the of Islands Northern the on seabirds breeding of (2013), Status Sciences A.A. Biological Aloufi, of M.Y., Journal Shobrak, Saudi as: Arabia. press Saudi in Sea, article this cite Please

Table 1 Location and description of the islands visited. Island Location Size (Km2)# Island discretion Al Nabageyah N 26 44.427 E 36 02.579 0.02 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 Al Uwandiyah N 26 35.920 E 36 06.608 0.015 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 Riykhah N 26 11.068 E 36 21.696 1.2 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 Mardunah N 26 03.940 E 36 28.888 0.06 A sandy flat surface in the north with high coral rocky area in the south (10-13 m) Ad Dahrah N 26 09.165 E 36 26.787 12.5 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 Sheikh Marbat N 25 52.810 E 36 35.955 0.09 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 Mrumah N 25 42.000 E 36 36.104 12.6 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

http://dx.doi.org/10.1016/j.sjbs.2013.11.002 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 Mezabeyah N 25 41.893 E 36 32.637 0.3 A semi-circle island, mostly with a sandy surface except for the western edge of the island which is rocky Harr N 25 40.257 E 36 31.436 0.3 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 Ber-reem N 25 39.550 E 36 30.775 19 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 Attaweel N 25 12.333 E 37 10.629 0.7 Has a sandy surface, with a maximum height of 6 m., with scattered vegetation. The coast is rocky Jazayah N 25 12.945 E 37 10.269 0.1 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 Umm Al Malek N 25 13.829 E 37 08.794 0.02 Has a sandy flat surface. Some of its coasts are rocky. Al-Munqaleb N 25 09.974 E 37 08.987 0.005 A longitudinal atoll that extends from east to west, and has a flat surface with maximum height of 1 m. This surfaceis sandy and bushes. The coasts is rocky except in the east Umm Khadav N 25 09.673 E 37 09.691 0.05 A circular atoll, within a coral barrier with a flat sandy surface Umm Qshaiyat N 25 10.110 E 37 10.170 0.01 It has sandy flat surface, with a mostly rocky coast 4 M.Y. Shobrak, A.A. Aloufi 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 ambi- Rock Dove 25 23 ent air temperature (Ta) from the Al Wajh airport meteoro- logical station were provided by the Presidency of Meteorology and Environment (PME) and used to understand the effect of air temperature on the breeding season. Tern 4 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 relation- White-cheeked Tern Bridled Tern Saunders’s 175 62 ship between breeding and food availability, we used pub- lished 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). Tern 3. Results and discussion

3.1. Breeding season Swift Tern Lesser-Crested Caspian Tern Sixteen species were recorded, eight true seabirds, ﬁve water 3 100 (2010) 0 (2011) 14 (2010) 0 (2011) 185(2011) 147(2010) birds, two birds of prey and the rock dove Columba livia. Ta- ble 2 shows the total number of breeding pairs recorded on

the islands. Fig. 2 shows the breeding periods for all species Gull 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, Sterna saundersi while Caspian Tern and Saunder’s Tern laid Sooty Gull White-eyed 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. Plover 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 (T ) a Crab Plover Kentish to the availability of food (as represented by the timing of breeding of different ﬁsh families) shows that the majority Falcon 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 per- Osprey Sooty iod when food is most plentiful and available. Our results highlight the importance of food availability for seabird Purple Heron breeding at the study area, although other factors also must inﬂuence their reproduction. Several studies have shown that Striated Heron food availability is the main factor affecting the timing of the breeding in the majority of seabird populations (Lack, 1968; Western Reef Heron 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 Brown Booby laying and the number of offspring produced, it seems that The number of breeding pairs estimated on different islands. the majority of colonial species nest when the mean temperature (Ta) is high. Species that nest in summer are potentially Table 2 Al NabageyahAl UwandiyahRiykhahMardunahAd Dahrah 1Sheikh Marbat 84 1MrumahMezabeyah 10Harr 4Ber-reemAttaweelJazayahUmm Al MalekAl-Munq-aleb 1Umm Khadav 1 Umm Qshaiyat PB PB 2 PB 1 2-5 PB PB 2 2-3 2 PB 2 1 1 2 2-3 2 1 1 34(2010) 25(2011) 1 3 2 1 1 1 5 2 26 75 Ind. PB. 80 (2010) 87 3 25 (2011) (2010) 47 (2011) 4 (2010) 0 PB (2011) PB 10-20 PB 3 18 35 4 4 PB 2 150 10 2-3 21 1965 152 134 (2010) PB 790 (2011) 2 804(2010417(2011 2 67(2010) 134(2011) PB 15 PB 13 (2011) 67 (2010) 107 5 (2010) 220 (2011) PB PB 363 134 PB 168 PB 168 168 217 67 PB 51 Ind. PB PB PB stressed by the heat. However, some species nest in the shade Island Breeding Species Recorded (Pairs (Year))

SF OsP 32 CP KP StH 30 WRH PH ST SLT 28 CT LCT BT 26 WCT WYG SG BB 24 Temperature ( C) Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec 22

20 Figure 2 The estimated range of breeding season of different species recorded during the study. (BB, Brown Booby Sula 18 leucogaster; SG, Sooty Gull Larus hemprichii; WYG, White-eyed Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Gull Larus leucophthalmus; WCT, White-cheeked Tern Sterna Month repressa; BT, Bridled Tern S. anaethetus; LCT, Lesser-crested Tern S. bengalensis; CT, Caspian Tern S. caspia; SLT, Saunders’s Figure 4 Mean Ambient Air Temperature in different months Tern S. saundersi; ST, Swift Tern S. bergii; PH, Purple Heron recorded at Al Wajh town. Ardea purpurea; WRH, Western Reef Heron Egretta gularis; StH, Striated Heron Butorides striatus; KP, Kentish Plover Charadrius of breeding, breeding proportion, breeding success and adult alexandrinus; CP, Crab Plover Dromas ardeola; OsP, Osprey survival (Thompson and Ollason, 2011; Monticelli et al., Pandion haliaetus; SF, Sooty Falcon Falco concolor. 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 of bushes to lessen the effect of the sun. As expected, through- those species that nests in the open. out the day Ta and humidity (Ha) at nests in the shade are significantly different than at nests exposed to sun (T , F = 62.47, a 3.2. Species accounts 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 3.2.1. Brown Booby S. leucogaster to protect eggs from harsh sun rays. The Brown Booby was found breeding only on the coral island The environment (including temperature and exposure to of Riykhah (Table 1). The nests were scattered on the ground, sun) can influence productivity and parental care in birds one placed even on an old Osprey nest! Eggs were oval, pale (Lack, 1968; Perrins, 1970; Williams and Tieleman, 2005; Vinc- blue with a chalky white coating. Mean dimensions (n = 13); ze et al., 2013). Studies of Kentish Plovers on Farasan Island 41.646 + 2.01 mm width and 60.231 + 2.75 mm length. The showed that parents spent more time sitting on eggs in exposed number of nests increased from three in late March, to 84 in nests than those nests that were in the shade (AlRashidi et al. June. By the end of July in 2011 all eggs had hatched and 2011a,c). Other seabird species use ‘‘belly soaking’’ to reduce the majority of chicks had white feathers. By October all the egg and nest temperature. Belly soaking can reduce Ta at the nestlings fledged. These observations suggest that egg laying nest up to 5.13 + 1.9 C(Al Suhaibany, 1995). Although the probably started in late February/early March and continued data are not sufficient to clearly define the actual effect of till May, and chicks fledged by end September or early the exposure to higher temperatures on the breeding species October. Newton and As-Suhaibany (1996) suggested that in the study area, we believe that this factor will probably breeding season of the species probably commenced early act more significantly on species that build their nests in places March in the northern Red Sea. Whereas Ostrowski et al. exposed to sunlight. Studies on effect of the climate on sea- (2005) reported that there were birds incubating eggs through- birds have already been documented especially in the timing out the year at three islands of Umm Al-Qamari located in the

Figure 3 The number of ﬁsh families breeding period in the Red Sea (Abu Shushah et al., 2011).

Under shrubs 55 Open area

50 C) o 45

35 Temperature ( 30

20 012345678910111213141516171819202122232425 Hours

Figure 5 The difference in air temperature in nests exposed to sun light and nests under shade of shrubs.

100

40 Humidity (%) Humidity

20 Under shrubs Open area

0 012345678910111213141516171819202122232425 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 The present study confirmed breeding only on rocky (coral) numbers of nests with eggs were found in May, July and island. Previous studies showed that elsewhere in the Red Sea, October. Although there are observations of chicks in early breeding habitats were varied and included sandy beaches, February in the Farasan Islands, the majority of the nests with open rocky islands and occasionally cliffs (Jennings, 2010; eggs there were noted in early July in the first week of July Newton and As-Suhaibany, 1996; Ostrowski et al., 2005; Sho- (Newton and As-Suhaibany, 1996; Jennings, 2010). The brak, 2007). However, more islands are needed to be surveyed current study suggests that the species probably commences to determine the habitat and to estimate the number of the breeding earlier in the northern part of the Red Sea. Brown Booby 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 spe- 3.2.2. Striated Heron Butorides striatus cies has probably declined or was over estimated by earlier Although the species was found on all islands during the sur- studies. Jennings, 2010 estimated the number of breeding pop- vey, no proper estimate is available of the number of breeding ulation in the Saudi Arabia was 2000 pairs. While, Ormond pairs. However, in this study 15 fledged and unfledged chicks et al. (1984) and Newton and As-Suhaibany (1996)found that were recorded during June in the Al Nabageyah and Al the majority of breeding pairs were located in the central and Uwandiyah islands. These islands were covered by Avicennia southern parts of the Saudi Red Sea and suggested that Fara- marina mangrove bushes. Our observations suggest that the san archipelago and the Al Qunfudah areas are the most breeding season probably commence in April in this area, egg important breeding areas for the species. The current results laying in late April early May. In the southern part of the agree with this finding as Riykhah Island was the only island Red Sea fledged chicks were reported during July and seven ac- where the species was found breeding during this study. tive nests with eggs were found in the end of April in Farasan

Islands (Jennings, 2010). Atthe Umm Al Qamari islands un- Although the habitat is suitable for the species, especially fledged chicks were recorded in May 25, 2002 (Ostrowski on the mangrove-covered islands such as Ber-reem, we could et al., 2005). These studies show that the majority of nesting not confirm breeding. Jennings (2010) considered the Purple activities on Saudi Red Sea takes places between April and July. Heron species as a common and widespread migrant with a Jennings (2010) suggests that the breeding habitats were few wintering and breeding birds on Farasan Islands and Al usually in dense vegetated islands and occasionally in holes Lith lagoon, as well as Yanbu. While, Newton and Al-Suhai- and crevices of fossil coral, often among colonies of Western bany, 1996 did not observe any individuals at Farasan Islands, Reef Herons and Eurasian Spoonbills. We also found that they recorded them at the Qishran lagoon near Al Lith and both the islands were covered by A. marina mangrove bushes. thought that they could breed. According to Evans (1987), As we were not able to estimate the number of breeding pairs, up to 15 pairs breed on Farasan Islands. Jennings, 2010) noted actual breeding population in the northern Red Sea of Saudi juveniles in June in Farasan, and suggested that the breeding Arabia is not known. However, Jennings (2010) reported that season commences in spring and sometimes in summer. The it is a widespread species over the whole Red Sea region and species is usually a solitary nester but may nest adjacent to col- the breeding population probably exceeds 1000 pairs with onies of other herons in areas of dense mangroves. majority of colonies at Al Wajh and Farasan archipelagos. 3.2.5. Osprey Pandion haliaetus 3.2.3. Western Reef Heron Egretta gularis The Osprey was the only species which was breeding on all the We located only two empty nests and two nestlings under man- islands visited, with at least one active nest on each island, grove A. marina bushes during April; one at Al Nabageyah Is- sometimes two active nests on the larger islands (e.g. Ber-reem, land and the other at the Al Uwandiyah Island. The behavior Riykhah and Mezabeyah). We recorded eggs about to hatch at of adults nearby suggested that these nests were active. Several the end of March. One egg was measured and the size was L old nests were recorded on other islands with dense vegetation. 63.52 and W 46.36 mm. Jennings (2010) reported the mean This suggests that the Western Reef Heron nests on these is- measurement of 41 clutches of three eggs on Farasan as lands, may be in low numbers. 60.1 mm in length and 43.3 mm in width. We found solitary nests, whereas Jennings (2010) found The result of this work suggested that egg laying probably that the Western Reef Heron sometimes congregate in larger commences late November–early December. Similar observa- numbers, up to 450 pairs. Newton and As-Suhaibany tion was recorded on the Farasan Islands, when 51–65 pairs (1996)noted that the Western Reef Heron nesting is in solitary were found breeding in late autumn in 1993 (Fisher, 2001). pairs and in small colonies with a maximum of eight nests per Jennings (2010) reported that the chicks hatch in as late as colony. The largest known colony on the Red Sea coast was May on Tiran Island. Our study suggests that the species starts recorded in Egypt with 40–60 pairs in mangroves of Manqata breeding a few weeks earlier than was recorded in Tiran Island. north of Nabq (Goodman and Meininger, 1989). Some nesting In the northern Red Sea we suggest that all islands may have pairs were associated with Eurasian Spoonbills (Ormond et al., one pair and large islands could have two nesting pairs. During 1984; Shobrak, 2001). An aerial survey in February 1993 from the mid-winter waterfowl count in Saudi Arabia in 1993, an Jizan to Gulf of Aqaba found 422 birds. Jennings, 2010 sug- estimate of the population was made by Symens and Al Sala- gested that the total number of breeding pairs in Arabia is mah (1993). Although their survey did not include all the is- about 3000 pairs. We believe that the species need more inves- lands in the Red Sea, their results showed that the Red Sea tigation to estimate the actual size of the breeding population holds a substantial proportion (64%) of the total Saudi popu- in Saudi Arabia. lation. The survey carried out by Newton and Al-Suhaibany Although the species is considered as a common breeding (1996) showed that the species was abundant in Al Wajh archi- resident along the Saudi Red Sea coast (Jennings, 2010), the pelago where nest density appeared to be the highest in the Western Reef Heron uses a variety of vegetation types for nest- Saudi Red Sea coast. Jennings (2010) suggested that the high- ing but especially mangroves and Euphorbi afractiflexa in the est breeding concentration is in the Red Sea islands, especially southern Red Sea (Newton and Al-Suhaibany, 1996). While in Farasan and Al Wajh Archipelago with an estimate of 500 to the north of Al Wajh the species was only recorded nesting pairs. on mangrove trees (Ormond et al., 1984; Newton and Al- Suhaibany, 1996). However, nests can be in cliffs and under 3.2.6. Sooty Falcon Falco concolor small bushes (Shobrak et al. 2002a; Jennings, 2010). The breeding season possibly ranges between March and August. Adults were observed during our visit in July 2010 at Ber-reem However, Jennings (2010) found that there is little variation and Mardunah islands. While in 2011 we only saw a fledged on the breeding seasons from different areas in Arabia, with nestling being fed by an adult at Riykhah in October and an earliest egg laying in the first week of October on islands one pair in Mardunah. This suggests that the species probably of Bahrain in the Arabian Gulf. 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. 3.2.4. Purple Heron Ardea purpurea In the present study, adult Sooty Falcons were recorded on We did not observe this species during the survey, but we sus- July at Ber-reem and Mardunah islands whereas fledged nest- pected that it breeds in the mangrove area on Ber-reem Island, ling was observed at Riykhah in October. We suspected that as a pair was seen standing on the mangrove during March the breeding season probably started in July for this species. and April visit. As the species was not observed in June and This probably matches with earlier studies that 90% of later visits the assumption of breeding in the northern Saudi clutches in the Red Sea were laid in the last three weeks of July Arabian Red Sea needs more investigation. and extended to the first 10 days of August in some years

(Gaucher et al. 1995; Jennings, 2010). These observations are birds were observed at Harr Island during April. Adults carry- related to the previous works such as (Ormond et al., 1984; ing food items to burrows in July 2010 indicated nestlings. This PERSGA, 2003; Jennings, 2010). suggests that the species probably commences breeding by late Ormond et al. (1984) recorded significant breeding colonies May–early June in the northern islands. In October fledged on a number of rocky islands in the northern Red Sea. In addi- youngs were seen with adults at the above islands. The present tion PERSGA (2003) and Jennings (2010) suggested that the survey suggests that the species probably commences egg lay- distribution of the species in Red Sea shows concentrations ing early May/June. Al Malki (2011) reported dead chicks in near Al Wajh Bank and Al Lith. early June at Al Natain Island. However, incubating adults Studies carried out in Bahrain and in the United Arab were found in July on Sudanese Islands (Shobrak et al. Emirates and Oman showed that there is a decline in Sooty 2002b; PERSGA, 2003). Falcons populations in these areas (Kavanaugh and King, Before 1996 survey, the species was considered as a breeder 2008; Shah et al., 2008; McGrady et al., 2010). Previously its of south of Al Lith as all nesting colonies at the time were re- population was over estimated, between 4000 and 10,000 pairs corded in Saudi Arabia on Farasan Islands (Ormond et al., (Moreau, 1969; Brown et al., 1982; Cade, 1982). However, 1984; Jennings, 2010). In 1996 a new colony was found in Al Gaucher et al. (1995) estimated that the world population Wajh archipelago with 100 breeding pairs (Newton and Al- was only 1000 breeding pairs and the Saudi population was Suhaibany, 1996). Jennings (2010) estimated the number of 260–381 pairs in the Red Sea. This is far less than the previous breeding pairs was about 250 on three or four islands. A large estimation. Jennings (2010) suggested that there may be more population was later recorded in Al Batain Island at Al Qunfu- breeding pairs in the north of the Red Sea between Al Wajh dah consisting of about 620 burrows (Al Malki, 2011). How- Bank and Tiran Island than has been estimated. Gaucher ever, according to De Marchi et al. (2006) there are larger et al. (1995) suggested that the distribution pattern, density breeding populations on the other side of the Red Sea. He esti- and breeding success of this falcon seemed to be strongly influ- mated the number breeding in the central Eritrea to be 5000– enced by the food availability (autumn migration of small and 6000 pairs, probably representing 50% of the known world medium–size birds) and the deterring presence of terrestrial breeding population. The changed position of the nesting bur- predators. We suggest that northern Red Sea population in rows at Sheikh Marbat Island noted accords with the sugges- Saudi Arabia has probably declined (or has been over esti- tion of Chiozzi et al. (2011), that the species changes colony mated) and that more work is needed to investigate the status location every year even in the same island. of this Near Threatened species. Based on the results, its global status should be reassessed. 3.2.9. Sooty Gull L. hemprichii The species was observed on all islands in the present survey. 3.2.7. Kentish Plovers Charadrius alexandrinus The largest colony was found on the rocky island of Riykhah Kentish plover chicks were seen on Harr and Sheikh Marbat with 80 pairs in 2010 and 87 pairs in 2011. The majority of islands during April and June visits with one fledged chick with nests were in the shade of rocks. Eggs as well as chicks were an adult in July. This suggests that the species probably com- seen in June 2011 on Riykah Island and by the end of July. mence breeding in February/March until late July. It was dif- Moreover, birds with 1–3 eggs were observed in late June ficult to determine the actual population of the islands within 2011 on Harr Island, and we estimated 10–20 pairs probably the time period available but we believe that there are probably nested. The nests on this island were beside or underneath only a few breeding pairs in the islands visited. Present obser- bushes. The species probably commences breeding in late vations showed that the species commences egg laying from May or early June. Eggs measured during the survey showed late February to early March. AlRashdi et al. (2011b) showed that length was 57.95 + 3.03 mm, width was that most of the suitable areas for the Kentish Plover are con- 41.37 + 2.08 mm, (n = 15). centrated from about 100 km south of Jiddah to Yanbu Al This study suggested that egg laying commenced in late Bahr and near the city of Jizan, whereas suitable areas in the May or early June. Newton and Al-Suhaibany, 1996 reported north have relatively small populations. Generally the species the same time of breeding on this island (Riykhah). However, is known to be a widespread breeding bird in the coastal areas in the southern Red Sea, the egg laying commences in June/ and islands of Saudi Arabia (Jennings, 2010). July (Jennings, 2010). Newton and Al-Suhaibany (1996) estimated the population of the species was 200 breeding pairs 3.2.8. Crab Plover D. ardeola on Riykhah Island, which was almost twice the number re- In Saudi Arabia the first confirmed breeding record for the corded in the present survey. This may be due to different sur- species was in May 1983 with 45 burrows (Ormond et al., veys methods, as the earlier survey was carried out by plane 1984). A detailed study on the species was done by Gregory and the present survey used flush counts on the ground. On and Goldspink (1998) in Farasan Islands and provided infor- the other hand, the total number of birds estimated in 1982/ mation on the distribution, status and feeding of this species 83 was 73 breeding pairs in the same island. with particular references to conservation and management. In the northern part of the Red Sea, Saudi Arabia, the first 3.2.10. White-eyed Gull Larus leucophthalmus breeding colony was recorded in 1996 (Newton and Al-Suhai- The breeding of the white-eyed gull was observed at three is- bany, 1996). lands off Umm Lajj town. These islands were sandy with rocky During the present survey, on two islands we recorded habitats. The nests were usually exposed to sunlight. We esti- breeding colonies; Sheikh Marbat had 46 burrows and 85 indi- mated a total of 304 breeding pairs. Whereas, in 1982 (Ormond viduals present, and Attaweel Island had 26 burrows with 35 et al., 1984) found 152–155 pairs at Al Wajh bank (Is this a individuals. In addition, possible nesting areas with nearly 70 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 9 number in this study with the previous surveys in 1982, we incubating birds were observed in the middle of July (Shobrak found the number of breeding pairs has probably increased. et al., 2002b). These findings suggest that the species com- On the other hand, the aerial survey in 1996 estimated the min- mences breeding by early May in northern Red Sea and later imum breeding population in Saudi Arabian Red Sea was 1500 on the southern islands. Pairs (Newton and Al-Suhaibany, 1996). A survey covering 22 Considering data size of our present survey, it is difficult to islands in the Yemeni Red Sea found 3500–4000 pairs (Al Sag- estimate the population of Swift Tern. An aerial survey in 1996 hier, 2002; Jennings, 2003). However, Jennings (2010) assumed between June and July covering 262 islands found about 2000 that the species was slightly more numerous than the sooty breeding pairs spread from the Farasan Islands to Al Wajh gull, particularly in the extreme north and south, with an esti- bank, most colonies were found near Qunfudhah (Newton mate of 3000 pairs in Saudi Arabia. and Al-Suhaibany, 1996). They recorded the species in most Nests with eggs and chicks were observed on 28 July 2011 of the areas south of Jeddah and only at Al Wajh in the north. and suggested that breeding probably started in the late Nearly 76% of nesting pairs found by Newton and Al-Suhai- May/early June, which is similar to the Sooty Gull. In the bany (1996) were associated with active colonies of Lesser Red Sea area under Yemen, fresh nests were found in July Crested Tern S. bengalensis. Their estimate suggests 4500– (Al Saghier, 2002). Jennings (2010) suggested that there is a 5000 individuals and probably 1845–2000 breeding pairs on slight bias toward earlier nesting in the northern Red Sea, with the Saudi Arabian Red Sea coast. Jennings (2010) reported eggs dated between June and August from Tiran to Farasan that the total Arabian population is probably up to 13,000 and from July to September in Yemen. In Djibouti, adults pairs. However, the species need more investigation to deter- were found incubating in July (Shobrak, 2007). Egg measure- mine its status and the breeding biology. ments were 48.86 + 5.01 mm in length and 34.89 + 4.11 in width (n = 21). 3.2.13. Lesser Crested Tern S. bengalensis The nests of this species were found in dense colonies on open 3.2.11. Caspian Tern Sterna caspia sandy islands. The nests were found at four islands and the A total of 22 breeding pairs were observed on all the sandy is- highest number was observed in Al Nabageyah with 1965 lands visited during this survey. Breeding probably occurred breeding pairs. On 16 July 2010 it was observed that birds were on all islands off Umm Lajj with flat sandy areas. Newly starting to build a colony at Al Nabageyah Island. By end of hatched chicks and nests with eggs were observed in late April July 2011 the colony was completed and the majority of birds and fledged chicks being fed by an adult were seen in late June, were found incubating. In October fledged nestlings with which suggests that the species probably commences breeding adults were observed around the islands. This suggests that in early March. Shobrak (2001) recorded three pairs showing the species commences egg laying by late June or early July. aggressive behavior on a small island near Al Qunfudah in In the Sudanese islands of the Red Sea, incubating adults were early April 2001, but no nest was found. The species was re- seen in the second week of July (Shobrak et al., 2002b). Similar corded nesting in late winter or early spring on the mainland results were found in Umm Al Qamari Island, with 420 pairs coast south of Yanbu and on several sandy islands within incubating in 16 July (Ostrowski et al., 2005). On islands near the Farasan Islands (Newton and Al-Suhaibany, 1996). Dis- Bab Al Mandeb, adult birds were incubating on 17 August persed loose colonies of small size were found near Yanbu (Jennings, 2010). On Djibouti islands courtship behavior was and Jeddah (Gallagher et al., 1984). observed in the first week of July and birds with chicks were Newton and Al-Suhaibany (1996) estimated the breeding seen in September (Shobrak, 2007). These observations suggest population in Saudi Arabian Red Sea to be between 100 and that the Saudi Arabian population in the Red Sea probably 200 pairs, whereas Jennings (2010) estimated the total Arabian commence breeding earlier than the southern population at population to be 500 pairs. In Red Sea population in Yemen the Bab Al Mandeb. The southern population probably was estimated at 20 pairs. This suggests that more breeding oc- started a few weeks later in July or early August. The mean curs in northern parts of the Red Sea. However, most of the length and width of the eggs were 50.44 + 3.25 and earlier surveys were carried out in summer and we believe that 35.17 + 2.67 (n = 49), respectively. the Saudi Arabian population has probably been Ormond et al. (1984) consider it a common bird on the Sau- underestimated. di Arabian Red Sea coast. Comparing the 1982/83 and 1996 estimates of the number of breeding pairs, the 1982/83 survey 3.2.12. Swift Tern Sterna bergii recorded 1,880 breeding pairs, while that of 1996 reported Courtship behavior and birds carrying food were observed at 2000–4000 pairs. The total number estimated for the Saudi Sheik Marbat Island during the April visit, but no nests or Red Sea was between 9000 and 10,000 individuals (PERSGA, chicks were recorded later on the islands. This suggests that 2003). The species seems to be common also in the western the species breeds on nearby islands and egg laying probably part of the Red Sea (Shobrak et al., 2002b). starts in May. However, more islands in the northern Red Sea need to be surveyed to determine the status of this species. 3.2.14. White-cheeked Tern S. repressa Ostrowski et al. (2005) recorded active nests of about 270 pairs The species was observed nesting on the majority of sandy is- on a sand bank at Umm Al Qamari Island Protected area on lands that we surveyed. Although the species was recorded in 25 May 2002. By 29 July few adults were still incubating and high numbers, it was more common in the southern islands, the majority of the eggs had hatched. On the islands of Dji- especially in Sheik Marbat. The locations of colonies on these bouti, at the southern border of the Red Sea, birds commence islands were different in 2010 and 2011. There were more breeding by early July and chicks were observed in September breeding pairs in 2011. A few eggs were recorded in late June, (Shobrak, 2007). In the Red Sea area under Sudan jurisdiction, 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 M.Y. Shobrak, A.A. Aloufi newly hatched chicks. Thus, the breeding season probably June (Newton and Al-Suhaibany, 1996). Moreover, Jennings commenced by the middle of June. The mean length and width (2010) suggested that breeding in the southern part of Red of the eggs were 38.92 + 1.37 and 27.84 + 1.37 mm (n = 21), Sea, is April to June. The habitat of nests was flat sandy gravel. respectively. According to the present study the species commenced 4. Threats on the Seabirds breeding in late June. Newton and Al-Suhaibany, 1996 found no changes in the time of breeding in Red Sea as they found During our studies we identified several factors that affect the nests with eggs in the third week of June. The species was ob- breeding population of seabirds, such as human disturbance, served nesting in the majority of sandy islands (Shobrak et al., predation, egg collecting. Tracks of humans were found at all 2002a). Several authors suggest that the White-cheeked Tern is islands we visited. Although access to islands is under the a widespread species in the Saudi Arabian Red Sea (Ormond control of the Coast Guards and landing is forbidden except et al., 1984; PERSGA, 2003; Jennings, 2010). Although the on designated islands where overnight shelter and temporary species was recorded in the majority of islands visited, it was camps are sometimes established. One to three fishing boats more numerous in the southern islands, especially Sheik Mar- were observed at all sandy islands during the breeding season. bat. The species was also recorded more numerously in the Casual human visits to breeding islands, whether by fisher- southern islands in the Saudi Arabian Red Sea, especially on men or for recreational purposes, can cause significant distur- Farasan Islands; 70% of the total Saudi Red Sea population bance to nesting birds even if there is no deliberate was recorded (Newton and Al-Suhaibany, 1996). Comparing interference. The high ambient temperature in summer means the earlier information we found a significant increase in the that eggs and chicks suffer heat stress through solar radiation number of breeding pairs between 1982/83 and 1996 surveys, if a sitting bird is disturbed. This factor could be vital in the 1254 to 1264 breeding pairs in the earlier survey and 7500 future; with increased tourism and the predicted increase of breeding pairs in 1996 survey. The species has been targeted air temperature. by egg collectors in most parts of the Saudi Arabian Red Other threats on these islands include the human exploita- Sea (PERSGA, 2003). This probably had an adverse effect tion, pollution and predation. According to local people, many on the population as recorded by Simmons (1994) in Farasan fishermen collect eggs for consumption. Although this is no Islands. longer a common practice in the area, it is still continuing in a smaller scale. We observed tracks of rats on all the islands 3.2.15. Bridled Tern S. anaethetus we visited which probably are predators of seabird eggs and The Bridled Tern was recorded on all sandy islands with veg- nestlings. Several authors discussed the threats on the seabirds etation. Nests with eggs were found in late June when one new- of the Red Sea coast (Gallagher et al., 1984; Evans 1987, 1989; ly hatched chick was present. Nests were under mangrove A. Sweet, 1994; Simmons, 1994; Newton and Al-Suhaibany, 1996; marina bushes. Egg laying probably commences in early June. Shobrak, 2007; Jennings, 2010). The mean length and width of eggs were 46.01 + 3.16 mm and Disturbance is likely to increase the natural predation ef- 32.72 + 2.97 mm (n = 23) respectively. fects on those seabirds whose nests are exposed to the solar Ormond et al., 1984 counted between 4,030 and 5,080 pairs radiation. During our survey, Sooty Gulls were seen to take in the area in 1982/83 while the 1996 survey in the Saudi Ara- eggs of Saunders’s Tern and White-cheeked Tern. In a study bian Red Sea estimated 60,000 breeding pairs. Both the Fara- in 1993 on Sumair island, located in southern part of the san and Al Wajh archipelagoes hold large populations of this Red Sea, up to 30% of all Bridle Tern eggs had disappeared species (Shobrak et al. 2002a). We believe that the species may by the next visit, and all marked White-cheeked Terns’ eggs have been over estimated in the earlier survey of the Al Wajh at other islands in the archipelago were disappeared (Sweet, population. In addition, during 1993, six colonies on different 1994; Simmons, 1994). Therefore, we highly recommend that islands of Farasan archipelago were recorded with a total pop- disturbance to the nesting birds should be strictly avoided, ulation estimate of 37,000 individuals (Sweet 1994; Tatwany especially in the hottest part of day. et al. 1995). We suspect that Farasan Islands has probably a Finally, seabirds could be affected by oil pollution as the higher breeding population than the Al Wajh Bank islands. Red Sea is known to receive 6836 metric tons or 14.61 kilograms per square kilometer per year of oil from shipping 3.2.16. Saunders’s Tern S. saundersi (Awad, 1995). The global refinery input is 0.56 kilograms per We observed eggs and newly hatched chicks during April. The square kilometer per year, whereas the Red Sea receives 6.64 mean length and width of the eggs was 31.21 + 0.53 and kilograms per square kilometer per year: nearly 11 times more. 22.68 + 0.31 mm (n = 3) respectively. Nearly 15 breeding Although oil pollution affects diving birds more, such as cor- pairs in two small colonies were recorded on Sheik Marbart Is- morants, boobies and divers, it can also cause damage to land. In addition, four pairs with pre-fledged chicks were ob- breeding seabirds during the various stages of their life cycle. served on Mezabeyah Island during the same survey period. Large numbers of adults can be killed by oil-fouling. Oiling These observations suggest that breeding season probably of eggs by contaminated incubating birds can also cause seri- starts in late March and continues to late June. Sooty Gull ous problems (Freedman, 1989). Furthermore, beached oil tracks were observed in all colonies of the Saunders’s Tern that can have a severe impact on flightless chicks on beaches near suggests the Sooty Gull could be preying on chicks of Saun- colonies. Oil spills can also affect seabirds indirectly through der’s Tern. the food chain, as toxic hydrocarbons may damage the ecosys- Our study suggests that egg laying probably start in late tems within which the birds’ food resources are produced and March. On the Farasan Islands in the southern part of the the disruption of the breeding cycle of prey fish species could Saudi Arabian Red Sea a fledged juvenile was recorded in early cause a drastic decline in seabirds’ breeding success.

Acknowledgments Dickinson, E.C., (Ed.), 2003. The Haward and Moore Complete checklist of the Birds of the World, third ed. London; Christopher We are thankful to the Dean of Scientific Research at Tabuk Helm, p. 1039. Evans, P.G.H., 1987. Seabirds of the Red Sea. In Edwards, A.J., Head, University for supporting this project No 23/21/1432. We are S.M. (Eds.), Key Environment: Red Sea, Oxford, Pergamon Press, grateful to Mr. Ali Al Faqeih, Abdullah Alrabdi, Saud Aljethli pp. 315–338. and Mohamed Al Rashedi for their assistance during the field Evans, M., 1989. Breeding birds on some Red Sea islands of North work. Finally, we wish to thank Border Guard Foundation in Yemen. Ornithological Society of the Middle East Bulletin 23, 14– Tabuk region for their help by allowing us to reach the islands 20. in Alwajh and Umluj. We also want to thank Dr. Asad R. Fisher, P.R., 2001. Ecology and behaviour of Osprey Pandion haliaetus Rahmani, the Director of Bombay Natural History Society, of Farasan Islands, Red Sea, Saudi Arabia. PhD thesis, Manchester Dr. Michael J. McGrady and Michael Jennings for their com- Metropolitan University, UK. ments on the draft of this paper. Freedman, B., 1989. Environmental Ecology, the Impacts of pollution and Other Stresses on Ecosystem Structure and Function. Aca- demic Press, San Diego. References Gallagher, M.D., Scott, D.A., Ormond, R.F., Connor, R.J., Jennings, M.C., 1984. The distribution and conservation of seabirds breeding Abu Shusha, T.L., Kalantan, M.Z., Al-Nazry, H.H., Al-Ghamdi, on coasts and islands of Iran and Arabia. ICBP Technical Y.A., 2011. Fishes from Territorial Saudi Arabian Red Sea Water. Publication 2, 421–456. Marian Research Center-Jeddah, 225. Gaston, A.J., Gilchrist, H.G., Mallory, M.L., Smith, P.A., 2009. Al Ghazzawy, A.M., Al-Rashed, M.A., Al-enayzan, A.S., 2007. The Changes in seasonal events, peak food availability, and consequent Atolls of Saudi Arabia in the Red Sea & the Arabian Gulf. Saudi breeding adjustment in a marine bird: a case of progressive Geological Survey, Jeddah, 452. mismatching. Condor 111, 111–119. Al Malki, M., 2011, Breeding ecology and conservation of Kentish Gaucher, P., Thiollay, J.-M., Eichaker, X., 1995. The Sooty Falcon Plover Charadrius alexandrinus, and Crab Plover Dromas ardeola in Falco concolor on the Red Sea coast of Saudi Arabia: Distribution the Red Sea of Saudi. Unpublished report, Bath University. numbers and conservation. Ibis 137, 29–34. Al Saghier, O., 2002. Survey of theBreeding Seabirds in Red Sea of the Gill, F., Wright, M., 2006. Birds of the World: Recommended English Republic of Yemen. PERSGA, Jeddah. Names. Princeton University Press, Princeton NJ. Al Suhaibany, A., 1995. The White Cheeked Tern Sterna repressa: egg Goldspink, C.R., Morgan, D.H., Simmons, D., Sweet, G., Tatwany, temperature and behavioural thermoregulation during incubation H., 1995. The distribution and status of seabirds on Farasan in hot environment. Unpublished MSc Thesis, University of Wales. Isalnds, Red Sea, Saudi Arabia with a note on the possible effect of AlRashidi, M., Kosztolańyi, A., Shobrak, M., Ku¨pper, C., Sze´kely, T., egg predation, NCWCD/Manchester Metropolitan University 2011a. Parental cooperation in an extreme hot environment: Report. natural behaviour and experimental evidence. Animal Behaviour Goodman, S.M., Meininger, P.L. (Eds.), 1989. The Birds of Egypt. 82 (par 2 ‘‘August’’), 235–243. Oxford University Press, Oxford. AlRashidi, M., Kosztolańyi, A., Shobrak, M., Sze´kely, T., 2011c. Gregory, M., Goldspink, C., 1998. Thedistribution, status and feeding Breeding ecology of the Kentish plover Charadrius alexandrinus in behaviour ofthe crab plover Droma sardeola on Farasanislands, Farasan Islands, Saudi Arabia (Aves: Charadriiformes). Zoology Saudi Arabia, with particularreference to conservation and man- of the Middle East 53, 15–24. agement, NCWCD/Manchester Metropolitan University, Report AlRashidi, M., Long, P.R., O’Connell, M., Shobrak, M., Sze´kely, T., NCWCD, Riyadh. 2011b. Use of remote sensing to identify suitable breeding habitat Jennings, M.C., 1988. A note on the birds of the Farasan islands, Red for the Kentish Plover and estimate population size along the Sea, SaudiArabia. Fauna of Saudi Arabia 9, 457–467. western coast of Saudi Arabia. Wader Study Group Bulletin 118 Jennings, M.C., 2003. ABBA survey 31: Bir Ali and Red Sea islands, (1), 32–39. Yemen. Pheoenix 19, 2. Awad, H., 1995. Oil Pollution in the Red Sea: A State of the Art Jennings, M.C., 2010. Atlas of the breeding birds in the Arabia Assessment. PERSGA/IOC/UNEP Workshop on Oceanographic Peninsula. Fauna of Arabia 25, 751. Inputs into Coastal Zone Management in the Red Sea and Gulf of Kavanaugh, B., King, H., 2008. Observations from 1998–2006 on the Aden. Oct. 12, 1995. Jeddah. breeding population of Sooty Falcons Falco concolor on the Brown, L.H., Urban, E.K., Newman, K., 1982. In: The Birds of Hawar Islands, Kingdom of Bahrain. Sandgrouse 30 (1), 70–76. Africa, 1. Academic Press, London. Lack, D., 1968. Ecological adaptations for breeding in birds. Methuen, Bullock, I.D., Gomersall, C.H., 1981. The breeding population of tern London. on Orkney Shetland in 1980. Bird Study 28, 187–200. Le Corre, M., 2001. Breeding seasons of seabirds at Europa Island Cade, T.J., 1982. The Falcons of the World. Collins, London. (southern Mozambique Channel) in relation to seasonal changes in Chiozzi, G., De Marchi, G., Semere, D., 2011. Coloniality in the Crab the marine environment. Journal of Zoological Society of London Plover Dromas ardeola does not depend on Nest. Site Limitation. 254, 239–249. Waterbirds 34 (1), 77–81. McGrady, M.J., Gschweng, M., Al-Fazari, W.A., 2010. Report on Crawford, R.J.M., Barham, P.J., Underhill, Les.G., Shannon, L.J., fieldwork to study the status and distribution of breeding Sooty Coetzee, J.C., Dyer, B.M., Leshoro, T.M., Upfold, L., 2006. The Falcons (Falco concolor) on the northern islands of Oman –2010. influence of food availability on breeding success of African Natural Research Ltd.. penguins Spheniscusdemersus at Robben Island, South Africa. Meadows, B., 1993. Islets near Yanbu alBahar, Red Sea. Phoenix 10, Biological Conservation 132, 119–125. 7–8. De Marchi, G., Chiozzi, G., Semere, D., Galeotti, P., Boncompagni, Monticelli, D., Ramos, J.A., Quartly, G.D., 2007. Effects of annual E., Fasola, M., 2006. Nesting, overwintering, and conservation of changes in primary productivity and ocean indices on breeding the Crab Plover Dromas ardeola in central Eritrea. Ibis 148, 753– performance of tropical roseate terns in the western Indian Ocean. 764. Marin Ecology Progress Series 351, 273–286. Del Hoyo, J., Elliott, A., Sargatal, J., 1996. In: Handbook of the Birds Moreau, R.E., 1969. The Sooty Falcon Falco concolor, Temminck. of the World: Hoatzin to Auks, vol. 3. Lynx Edicions, Barcelona. Bulletin of the British Ornithological Club 89, 62–67.

Newton, I., 1998. Population Limitation in Birds. Academic Press, Sweet, G., 1994. Nest site selection and breeding biology of the Bridled London, p. 597. Tern Sterna anaethetus, on the Farasan Islands, Red Sea, Saudi Newton, S. F., Al-Suhaibany, A.H., 1996. Distribution and abundance Arabia. M.Sc. Dissertation, Manchester Metropolitan University, of summer breeding seabirds in the Saudi Arabian Red Sea 1996. UK. Unpublished report, Riyadh, NCWCD, p. 56. Symens, P., 1988a. Birds of Umm Al Gammari. NWRC Quarterly Ormond, R., Shepherd, A.D., Price, A., 1984. Sea and Shore birds. In: Report Autumn, 38–42. Saudi Arabian Marine Conservation Program Report No. 4. Symens, P., 1988b. Birds of the Farasan Islands. NWRC Quarterly University of York, UK, pp. 124–140. Report Summer, 50–66. Ostrowski, S., Shobrak, M., Bouq, A., Bowden, E., 2005. The breeding Symens, P., Al-Suhaibany A., 1996. Status of the breeding populations birds at Umm Al Qamar protected Area. Sandgrouse 27 (1), 53–62. of tern (Sternidea) along the eastern coast of Saudi Arabia Perrins, C., 1970. The timing of birds’ breeding seasons. Ibis 112, 242– following the 1991 Gulf War. In: A Marine Wildlife Sanctuary 255. for the Arabian Gulf. Environmental Research and Conservation PERSGA, 2003. Status of Breeding Seabirds at the Red Sea and the Following the 1991 Gulf War Oil Spill. F. Krupp, A. H. Abuzinada Gulf of Aden, PERSGA, p. 75. and I. A. Nader (eds) 1996. NCWCD, Riyadh and Senckenberg PERSGA, 2004. Standard Survey Methods for Key Habitats and Key Research Institute. Frankfurt a. M. Species in the Red Sea and Gulf of Aden, PERSGA Technical Symens, P., Al Salamah, M.I., 1993. The impact of the Gulf War oil Series No. 10. spills on wetlands and waterfowl in the Arabian Gulf. IWEB Sandvik, H., Erikstad, K.E., Barrett, R.T., Yoccoz, N.G., 2005. The Special Publication 25, 24–28. effect of climate on adult survival in five species of North Atlantic Tatwany, H., Goldspink, C.R., Morgan, D.H., Simmons, D., Sweet, seabirds. Journal of Animal Ecology 74, 817–831. G., 1995. The distribution and status of seabirdson the Farasan Sandvik, H., Erikstad, K.E., Saether, B.E., 2012. Climate affects Islands, Red Sea, SaudiArabia, with a note on the possible effects Seabirds population dynamics both via reproduction and adult of egg predation, NCWCD, Riyadh and Manchester Metropolitan survival. Marin Ecology Progress Series 454, 273–284. University, UK. Shah, J.N., Khan, S.B., Ahmed, S., Javed, S., Hammadi, A., 2008. Thompson, L.G., 2010. Climate change: the evidence and our options. Sooty falcon in the United Arab Emirates. Falco 32, 16–19. Behavior Analyst 33, 153–170. Shobrak, M., 2001. The breeding birds survey in the south west of Thompson, P.M., Ollason, J.C., 2001. Lagged effects of ocean climate Saudi Arabia. NCWCD, Unpublished report (In Arabic). change on fulmar population dynamics. Nature 413, 417–420. Shobrak, M., 2007. On the nesting status of some seabirds in Djibouti. Thompson, L.G., Brecher, H.H., Mosley-Thompson, E., Hardy, D.R., Journal of Zoology of the Middle East 42, 59–66. Mark, B.G., 2009. Glacier loss on Kilimanjaro continues unabated. Shobrak, M., Alsuhaibany, A., Newton, S., 2002a. Status of breeding PNAS 106, 19770–19775. seabirds at the Red Sea of Saudi Arabia, PERSGA, p. 23. Vieyra, L., Velarde, E., Ezcurra, E., 2009. Effects of parental age and Shobrak, M., El-Jack, A.O., Ash Sheikh, F.H., 2002b. The status of food availability on the reproductive success of Heermann’s Gulls the breeding seabirds in Sudan, PERSGA, p. 24. in the Gulf of California. Ecology 90 (4), 1084–1094. Simmons, D.J., 1994. The White-cheeked Tern (Sterna repressa) in The Vincze, O., Sze´kely, T., Ku¨pper, C., AlRashidi, M., Amat, J.A., Red Sea, Saudi Arabia. MSc Dissertation, Manchester Metropol- Arguëlles, A.T., Burgas, D., Burke, T., Cavitt, J., Figuerola, J., itan University, UK. Shobrak, M., Montalvo, T., Kosztolańyi, A., 2013. Local environ- Stagg, A.J., 1984. A note on the breeding birds of Kutambil Island on ment but not genetic differentiation influences biparental care in the Red Sea coast of Saudi Arabia. Fauna of Saudi Arabia 6, 546– ten plover populations. PLoS One 8 (4), e60998, 10137/ 548. jurnal.pone0060998. Suddaby, D., Ratcliffe, N., 1997. The effects of fluctuating food Williams, J.B., Tieleman, B.I., 2005. Physiological adaptation in desert availability on breeding arctic terns (Sterna paradisaea). The Auk birds. BioScience 55, 416–425. 114 (3), 524–530.