Journal of Arid Environments (1999) 43: 301-317 Article No. jare.1999.0537 Available online at http://www.idealibrary.com on IDE~L\!Y ..

Effects of season and habitat on abundance and diversity in a steppe desert, northern Saudi Arabia

Yolanda van Heezik & Philip J. Seddon

National Wildlife Research Center-, National Commission for Wildlife Conservation and Development-, P.O. Box 1086-, Taij; Saudi Arabia

(Received 17 November 1998, accepted 11 May

Between 1992 and 1996 the avifauna of the harrat (basalt boulder field) biotope was quantitatively surveyed using belt transectsduring all seasonsand in four habitats (wadi, harrat, almost bare, and sparselyvegetated gravel plains) within the Harrat al-Harrah protected area in northern Saudi Arabia. Twenty species,mostly larks and ,are regularly breeding residents, with five speciesbreeding occasionally.Abundance and diversity increasedin spring and late summer, coinciding with the passageof migrants. The total number of speciesrecorded was 131. Most (70%) resident and non-resident were counted in wadis, which contain the greatestdensity of vegetation, but no trees or high shrubs. Speciesrichness (Margalef's index) and diversity (Iog series alpha) were also highest in wadis. During a seasonwhen relatively abundant rainfalls were evenly distributed throughout the season, bird density was marginally higher than in a year of comparatively poor rainfall, although variation around both figures was large. Comparisons with other areas in Saudi Arabia indicate that increased aridity is associatedwith fewer resident species,but that sites are used by similar numbers of migrant species. The structural complexity of vegetation,including the presenceof trees and grasses, is likely to be the principal factor influencing avifaunal abundancewithin arid areas.

1999 Academic Press

Keywords: northern Saudi Arabia; avian abundance; avian diversity; seasonal changes; habitat preferences; steppe deserts; rainfall effects; diversity indices

Introduction

The aridity of Saudi Arabian landscapes, most of which receive less than 200 rnrn of rainfall a year, places constraints on the level of biodiversity that they can support. However, the presence of distinctive biotopes has resulted in the description of charac- teristic avifaunas within those regions that have been systematically surveyed (Newton et at., 1994; Rahmani et at., 1994; Newton & Newton, 1996; Newton & Newton, 1997). Moreover, Saudi Arabia's resident avifauna is augmented each year by large numbers of passage migrants, that may temporarily comprise the majority of birds found in a par- ticular locality . Here we present results from quantitative and systematic surveys of the avifauna of the harrat biotope, represented within the Harrat al-Harrah protected area in the far north-west of Saudi Arabia. Several harrats (black lava boulder fields) exist in Saudi 0140-1963/99/110301+ 17 $30.00/0 (!:;)1999 Academic Press 302 Y. VAN HEEZIK & P. J. SEDDON

Arabia, but the northern-most is the largest, comprising the southern tip of a harrat that extends into Jordan and Syria, covering a total area of 45,000 km2. Our surveys were designed to determine: ( 1) which species were resident in the protected area, and which species used the area only seasonally; (2) differences in species richness and diversity between habitats, and patterns of habitat use by both resident and migrating species;(3) seasonalchanges in biomass and diversity; and (4) possible limiting factors for avian populations and avifaunal diversity within the pro- tected area.

Study area

Harrat al-Harrah (12,000 km2) was declared a protected area in 1987, and is the southern-most portion of a major biotope, harrat, (basalt boulder fields), that extends from northern Saudi Arabia into Jordan and Syria (Child & Grainger, 1990). The reserveis an undulating plain at about 850 m a.s.l., strewn with basalt boulders, patches of sand deposited on the slopes of some hills, dry lakes, and scattered with extinct volcanic cones.Annual rainfall is in the range of 50-100 mrn (a mean of 58.3 mrn for the years 1985-1996; CV = 33%), and although seasonallypredictable, is unreliable in its quantity, and spatial and temporal distribution. Almost all rain falls between October and May, largely due to the influence of the dominant westerly flow. Ambient temper- atures range between -8 and 44°C. The vegetation is open xeromorphic dwarf shrubland intermixed, after rain, with perennials and annuals (Kiirschner, 1998).There are no trees in or near the study area where bird counts were carried out; occasional Tamarix arboreatrees occur along some of the large wadis in the extreme south of the reserve(Fisher et al., 1998).Vegetative cover of perennial plants and shrubs rangesfrom 0.4% in gravel plains to 18% in wadis (van Heezik& Seddon, 1999), however, in spring the presenceof annual plants may increaseground cover to as high as 72% in wadis that have received regular and relatively abundant rainfall throughout winter and spring. Under these conditions, annuals begin to grow as early as October, with peak flowering and fruiting in March and early April. Perennial speciesflower and fruit in summer and autumn. Before protection Harrat al-Harrah was grazed by sheep, camels and goats; since protection only untended camels have been permitted to graze freely.

Methods

The censustechnique chosenwas the sameas that used by Newton & Newton ( 1997) in a concurrent study of bird diversity in west-central Saudi Arabia, to facilitate direct comparisons. Eight belt transects measuring 1 kIn by 100 m were marked out, two in each of four defined habitat types: wadi, harrat, virtually bare gravel plains and sparsely vegetated gravel plains, that together comprised 77% of the study area (van Heezik & Seddon, 1999). Wadis representedthe most vegetatedhabitat in the reserve,and bare gravel plains and harrat the leastvegetated; bare gravel plains had a few perennial shrubs in low-lying spots, and harrat was crossedby occasionalnarrow drainagelines. Sparsely vegetated gravel plain was crossed with poorly vegetated washes, which ultimately drained into a large low-lying basin. The co-ordinates of the starting points and the end points of the transects were recorded by GPS, and these and the mid-points were marked. Other habitat types were present in the reserve (low ro<;kyhills and outcrops, drainage lines and silty depressions) but were not extensive enough to allow the establishment of a transect. The central portions of some dry lakes were sufficiently extensive,but as they were totally devoid of vegetation, they were not sampled. We surveyed each transect at the beginning and the end of each month when the authors were present in Harrat al-Harrah, beginning in November 1992, and ending in BIRDS IN NORTHERN SAUDI ARABIA 303

November 1997; in this way the set of eight transects were counted on 26 occasions covering all months except May and June. Surveys were always carried out between sunriseand mid-morning. One observerwalked eachtransect, following a straight line in transects lacking much vegetation, but deviating from the centre line in the wadi and intermittent vegetation transects, to locate birds lurking inside and behind bushes. All birds seenon the transect were counted, with the exception of birds flying high abovethe transect. Birds heard calling inside the transect were also counted. Birds were assigned a status following the classification system outlined in Newton & Newton (1997): resident breeders-virtually always present in Harrat al-Harrah, and recorded as breed- ing; local visitors-a species that breeds in northern Saudi Arabia; passage mi- grants-only present during spring and/or autumn; winter visitors-migrants present from November to March (individuals from many species in this category are also passagemigrants); vagrants-migratory speciesout of their normal range; occasional breeders-could be local visitors or passagemigrants that stay to breed when conditions are appropriate. Seasonswere defined as follows: winter (December, January, February), when ambi- ent temperatures remained below 15°C and there was some rain and initial growth of annuals; spring (March and April) , when ambient temperaturesranged between 15 and 25°C, rain fell and plant productivity was highest; summer (July, August, September), when temperatureswere generally above 35°C, there was no rainfall, and only perennial plants reproducing; and autumn (October, November), when temperatures were between 20°C and 30°C, there was some rainfall, and some perennial plants fruiting. We calculated three diversity indices: Margalef's index, which indicates species richness, the Berger-Parker index, which reflects the degree of dominance of species, and a diversity index (Magurran, 1988).Magurran (1988) suggeststhat it is important to couple an estimate of species richness with a measure of dominance, as species richnessindices may fail to discriminate situations where the number of species(s) and the number of individuals (n) are identical, but dominance varies. The diversity index was derived by fitting an abundance model to the data; in this casea log seriesmodel. Log seriesmodels are a way of mathematically describing the relationship between the number of speciesand the number of individuals in those species(Magurran, 1988).In order to be really useful, diversity indices must be able to detect subtle differences betweensites, and the alpha value derived from the log seriesis the best discriminator, as well as being less affected by variations in sample size than other indices (Taylor, 1978, in Magurran, 1988). The log series index alpha, the Berger-Parker dominance index and a measure of speciesrichness (either S or the Margalef index) 'appear to combine most satisfactorily the advantagesof being simple to calculate,easy to interpret and statistically and ecologically sound' (Magurran, 1988: p. 80). Margalef's indices were calculated from each transect walked. When calculating the Berger-Parker index, the low numbers of individuals sighted in three of the habitats resulted in a large number of zero values, or values that were calculated from such a small sample they were meaningless;therefore, one Berger-Parker index value was calculated from all the sightings counted for each habitat in each month. Rank abund- anceplots indicated the log seriesmodel would be appropriate for the data, and this was confirmed by goodness of fit tests (X2 = 14007, df. = 7, NS for wadis; X2 = 3.53, df. = 4, NS for harrat; X2 = 0.26, df. = 4, NS for sparsely vegetated gravel plains; X2 = 1.59, df. = 4, NS for virtually bare gravel plains). The influence of seasonand habitat were tested on log-transformed valuesof numbers of individuals, and numbers of species,using a two-way ANOV A, followed by post hoc contrasts to determine where significant differences layo Sporadic observations of birds encounteredin the protected areawere noted. Densities of birds were calculatedin relation to the proportion of each habitat in the area. Proportions were determined as part of a concurrent study (van Heezik & Seddon, 1999) by flying transects at 130 m altitude, and sampling habitat at 25 s intervals of latitude using a Global Positioning 304 Y. VAN HEEZIK & P. I. SEDDON

40

"' " "["' o 30 t ~ s 120 ] "' ] .0 J ~ 10 ~ z 0 J F M A M J J A S O N D Figure 1. Monthly variation in rainfall (mean values for the period 1992-1996 with S.D.) and the mean number of birds (.) and mean number of species (0) counted per set of four transects (i.e. one in each habitat type), in Harrat al-Harrah. No counts were made in May and June.

System, through a fixed 'quadrat' attached to the aircraft's rear window, equivalent to approximately 3 x 3 m area. Twenty-one transectswere flown, each of 20 min latitude, yielding 1701 data points. Because sparsely vegetated gravel plains were not distin- guished from virtually bare gravel plains when the sampling was carried out, the proportion of this habitat was later estimated at about 2%, from maps of the area. No data on rainfall was available from inside the protected area during the period of the study, and figures given are from the closest meteorological station, 125 kIn to the south-eastof the reserve,in Al Jouf. These data are not accurate for the areascounted, but do reflect seasonaltrends in abundance and timing of rainfall.

Results

Transects were surveyedfour times eachin November and December, twice in January, five times in February, four times in March, once each in April, July and August, and twice each in September and October. Mean times taken to walk the transects were 20 min (S.D. = 6.5, n = 52) for wadis, and 14 min for virtually bare gravel plains, harrat and sparsely vegetated gravel plains (S.D. = 3.7, n = 52; S.D. = 2.8, n = 50; S.D. = 3.8, n = 49, respectively). All speciesrecorded by the authors in the transects are given in Appendix 1, and all other speciesrecorded in the reserve are given in Appendix 2, classified following the definitions given in Newton & Newton (1997).

Variations with season and habitat

A two-way ANOV A was performed on log-transformed values of the total number of individuals counted, in four habitats and over four seasons:significant differences were found between seasons(F = 4'469, d,f. = 3, n = 206, p = 0-005) and between habitats (F = 56'61, df- = 3, n = 206, p < 0.001). Post hoccontrasts showed that num- bers in spring and summer were higher than those in winter (F = 10'59, p = 0-001, F = 6'47,p = 0'012, respectively,Fig- 1)- Numbers of birds in wadis were higher than in the three other habitats (F= 122'64, p < 0-001, F= 199-9, p < 0-001, F= 91.5, p < 0-001 for wadis vs, bare gravel plains, sparsely vegetated gravel plains and harrat respectively, Table 1) - BIRDS IN NORTHERN SAUDI ARABIA 305

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The number of species also showed significant differences between seasons (F = 4-221, df- = 3, p = 0-006) and habitats (F = 52-28, df- = 3, p < 0.001). Number of species was higher in spring and summer than in winter (F = 10-49, p = 0-001; F = 5.44, p = 0-021 respectively, Fig- I), and more species were recorded in wadis than in the other three habitats (F = 117-4, p < 0.001, F = 110-83, p < 0-001, F = 76.71, p < 0-00 I for bare gravel plains, sparsely vegetated gravel plains and harrat respectively, Table I). More species were counted in harrat than in bare gravel plains (F= 4-31, p = 0-039).

Species richness and dominance

Comparisons between habitats

Speciesrichness, as described by Margalef's index, was greatestin wadis, but not signi- ficantly different among the other three habitats (Kruskal-Wallis test, H = 83.13, df. = 3, n = 205,p < 0.001; Table 1.). Alpha valuesfrom the log-seriesmodel were also highest in wadis, and lowest in sparselyvegetated gravel plains (Table 1) .There were no differences between habitats in Berger-Parker indices (Kruskal-Wallis, H = 2.956, df. = 3, NS, Table 1.). Rank abundance plots, which illustrate patterns of dominance and diversity, are shown for each habitat (Fig. 2).

Comparisons between seasons

No difference was found in species richness (Margalef's index) or dominance (Berger-Parker) between seasons (Kruskal-Wallis, H = 3.26, df. = 3, NS; H = 1.26, df. = 3, NS, respectively) or between months (H = 13.02, df. = 9, NS; H = 14.09, df. = 9, NS, respectively). The mean species richness index, calculated for all habitats and over all months sampled, was 0.511 (S.D. = 0.204, n = 10).

Table 2. Proportions ( %) of resident speciescounted in each habitat (excluding thosespecies for which the total number counted amounted to lessthan 20) and mean number of birds (and standard deviation) counted per pair of transects over all habitats (n = 26). n = total number of birds recorded

Habitat

Wadi Harrat Gravel Sparsely Mean n plain vegetated (S.D.)

Desert 74 8 17 2.77 (2.64) 72 Isabelline wheatear 90 10 O O 0.77 (1.27) 20 Crested lark 96 0 2 2 7.23 (6.82) 188 Hoopoe lark 51 10 26 13 1.50 (1.36) 39 Desert lark 38 53 9 O 2.12 (2.07) 55 Ternrninck's homed lark 54 9 12 25 7-58 (11-6) 197 Bar-tailed desert lark 37 27 18 18 1.96 (2.89) 51 Scrub warbler 100 2.23 (2.61) 58 BIRDS IN NORTHERN SAUDI ARABIA 307

2.5

2.0

" " ~ 1.5 ." .8 os 3 1.0

0.5

0 Speciessequence

Figure 2. Rank abundance plots for birds counted in each habitat in Harrat al-Harrah

Resident speciesonly

A two-way ANOVA on the number of resident individuals counted showed highly significant habitat differences (F = 54.90, df- = 3, p < 0.001), and barely signifi- cant seasonal differences (F = 2-65, df- = 3, p = 0-05)- Post hoc contrasts indicated wadis contained more birds than did the other three habitats (F = 127-5, p < 0-001; F = 111-5, p < 0-001, F = 80.7, p < 0-001 for wadis vs- bare gravel plains, sparsely vegetatedgravel plains and harrat, respectively), and that harrat contained more indi- viduals than did bare gravel plains (F = 5.4, p = 0-022)- Post hoc seasonalcomparisons indicated more resident birds were counted in spring than in winter - The number of species also varied between habitats, but not between seasons (F = 50.9, df- = 3, p < 0-001). More specieswere counted in wadis than in the other three habitats (F = 122.9, p < 0-001; F = 102-3, p < 0-001; F = 64-6, p < 0.001) for bare gravel plains, sparselyvegetated gravel plains and harrat, respectively), and there were more species in harrat than in bare gravel (F = 9-3, p = 0-003) or sparsely vegetatedgravel plains (F = 4-7, p = 0.031) - Resident speciesused eachof the four habitats in the sameproportions as did all other species (X2, df. = 7.78, df- = 3, n = 930, NS). However, use of habitats was not in proportion to their availability (X2 = 83-6, df- = 3, p < 0.001). The proportion that resident speciesand individuals contributed to the total number using the reserve, in each month sampled, is shown in Fig- 3.

Effect of rainfall

The effect of rainfall in the months preceding and during spring, on numbers of birds counted in the transects, was examined by comparing three springs (February, March and April): (1) in 1996, when little rain fell duringJanuary, February and March, as well as during the preceding September, October and November; (2) in 1995, when rainfall was greater than averagefor all months between September 1994 and February 1995, except during November; and (3) in 1993, when rainfall was abundant during the spring months, and more or less average between September and October of the preceding year. Total rainfall between Septemberand the following April was as follows: 25.9 mm in 1995-1996 (no value availablefor December), 86.3 mm in 1994-1995 and 308 Y. VAN HEEZIK & P. I. SEDDON

(a) 100

80

60

40

20

J F M A M J J A s 0 N D

(b) 100

80

60

40

20

0 J F M A M J J A s 0 N D Month Figure 3. Monthly variation in the proportions of (a) total birds counted, and (b) number of species, that were resident in Harrat al-Harrah. No data (*) were collected in May and june.

43.7 mm in 1992-1993. From 1993 to 1994 there was also an averageseasonal rainfall (50.9 mm), but no bird counts were made during the spring months. Densities of birds in relation to available habitat in the protected area were: 107 birds km-2 (S.D. = 79, n = 6 counts) in the spring of 1996, 184km-2 in 1995 (S.D. = 133, n = 4) and 161 km -2 in 1993 (S.D. = 103, n = 10; Fig. 4).

Discussion

Habitat as a determinant of bird distribution in Harrat al-Harrah

The principal distinction between the perennial vegetation of different habitats within Harrat al-Harrah is its density, rather than its speciesstructure, which changes mainly in the proportions of each dominant species.Even with cover at a modest 18%, wadis contain significantly more speciesat greater densitiesthan all other habitats in the BIRDS IN NORTHERN SAUDI ARABIA 309

50 350

300 40 ° 250 ~ 0--. .~N ~'

200 ~~ 13° .9 '1:) :a '" 0= :g~ 150 e ~ ] 20 0;:= . ~~ 100 .~ ~ -8 .. 10 ~ 50 .I: p. ti)

0 0 SONDJFMA SONDJFMA SONDJFMA

1992-1993 1994-1995 1995 -1996

Months (September-April)

Figure 4. Monthly rainfall from September to April during three seasons (no value available for December 1995) , and corresponding spring densities of birds in relation to proportions of habitat available, counted in Harrat al-Harrah. No values are given for 1993-1994 as no bird counts were carried out in spring 1994. reserve.During most winters and springs, annual plants flourish in all habitats, but wadis support the greatestproliferation of vegetation.The absenceof trees and tall shrubs in all habitats sampled is reflected in the predominance of larks and wheatears among the resident species,which are capable of living constantly on the ground. About 70% of numbers of resident birds were recorded in wadis, and of the eight speciesoccurring in sufficient numbers for analysis, at least half of individuals of six of the specieswere found in wadis. Scrub warblers Scotocercainquieta were only ever counted in wadis, and at least 90% of crested larks Galerida cristata and isabelline wheatearsOenanthe isabellina were recorded in wadis. Presumably,populations of these speciesare likely to be most vulnerable to changesin the quality of wadi vegetation, brought about, for example, by overgrazing. Although commonly seen in this study, scrub warblers were recorded as rare breedersby Symens ( 1998) 1 year after sheepand goats had been excluded from the area. This apparent increase in their numbers may have been in responseto an improvement in vegetation after severalyears of protection from over-grazing. Passagemigrants and winter visitors were also attracted by more densely vegetated habitats, as 70% of thesewere also counted in wadis. Comprising only about 12% of the surface area of the reserve,the amount of wadi availableto birds must constitute one of the main factors limiting the population sizes of resident speciesin Harrat al-Harrah. The small number of relatively abundant speciesand large proportion of less abundant speciespredicted by the log seriesanalysis suggest that this model is most applicable in situations where one or a few factors dominate the ecology of a community (Magurran, 1988).The log series model fitted out data well, and we suggest that the factor dominating the ecology in Harrat al-Harrah is vegetation density, which is in turn determined by patterns of water runoff. Becausethese surveys were always carried out during mornings, when birds were most likely to be active (foraging, courtship displays in some months), recorded habitat preferences reflect the habitats preferred for activities carried out during this time, 310 Y. VAN HEEZIK & P. ]. SEDDON but may not reflect habitats preferred for other activities. For example, hoopoe larks Alaemon alaudipes and black-crowned finch larks Eremopterix nigriceps were observed foraging in the same habitat in west-central Saudi Arabia, but used different habitats for sheltering throughout the middle of the day (M. Shobrak, pers. comm.). Harrat, which comprises about 51% of the surface area of the reserve, was the preferred habitat of desert larks Ammomanesdeserti (the dark race annae, 53% of individuals), which are common in almost all rocky areas in Saudi Arabia (Jennings, 1995).A significant proportion of bar-tailed desert larks Ammomanescincturus (27% ) were also counted on harrat. Both specieswere recorded in rocky habitat virtually devoid of vegetation, but most likely use the small vegetatedrunnels and depressionsthat also make up the harrat mosaic. Virtually bare gravel plains, comprising about 13% of the surface of the reserve, were avoided by most resident and migratory species, except hoopoe larks Alaemonalaudipes (26% of individuals), bar-tailed desert larks (18%) and to some extent Temminck's horned larks Eremophilabilopha (12%). Sparselyvegetated gravel plains were most preferred, after wadis, by desert wheatearsOenanthe deserti and Temminck's horned larks, and were used to a lesser extent by hoopoe larks and bar-tailed desert larks. Desert wheatearsare a common and widespreadwinter visitor to Saudi Arabia (Jennings, 1995), and were absentfrom summer counts made in Mahazat as-Sayd reserve in west-central Saudi Arabia (Newton & Newton, 1997), but were present in significant numbers year-round in Harrat al-Harrah, suggesting they are certainly resident and most likely breed there. The two most abundant speciesin the reserve, occurring at similar densities, dif - fered in their habitat preferences:Temminck's horned larks, a widespread resident in northern Saudi Arabia, usually in stony gravel deserts(Jennings, 1995) were recorded in all habitats in this study, though infrequently in harrat. Crested larks, which are common throughout the Arabian Peninsula,but restricted to relatively vegetatedareas rather than open desert (Jennings, 1995), were almost only ever recorded in wadis. Hoopoe larks appear to be one of the more arid-adapted larks, resident in all sandy/gravel desert areas including the Empty Quarter (Jennings, 1995; Wacher, 1998).

Speciesrecorded

A total of 35 species were counted in the transects (Appendix 1), 15 of which were resident breeders. Five other species of resident breeders have been recorded in the reserve,but thesetend to be rare, or they typically breed in areasthat were not covered in the transects, e.g., golden eaglesAquila chrysaetos,brown-necked ravens Corvus ruficol- lis, little owls Athene noctua and eagle owls Bubo bubo breed on rocky jabals, house sparrows Passerdomesticus bred only where human habitation is continuous (the main ranger camp) .Pin-tailed sandgrouse Pteroclesalchata and pale rock sparrows Petronia brachydactylawere recorded breeding in small numbers by Symensin 1988, which was a particularly good year for rainfall and plant growth (Symens, 1988), but have not been recorded by any other observers,therefore, these specieswere designatedas occasional breedersin Appendix 2, together with cream-coloured coursers Cursoriuscursor, Dunn's lark Eremalauda dunni and great grey shrikes Lanius excubitor, from Appendix 1. Although we did not record many Dunn's larks, Green (1984) saw them frequently during mid-May, early June and late October, and Symens (1988) described them as common breedersin the more sandier parts of the reserveduring March 1988. Goriup et al. (1989) listed them as one of the commonest larks in the study area during the period April-June of 1989, and flushed one from a nest in April, but then saw them only infrequently during severalvisits in spring, summer and autumn of 1990, and amended their status to that of a nomadic breeder, or perhaps a summer breeding visitor, present mainly in May and June (Goriup et al., 1992). Most of the remaining speciescounted in BIRDS IN NORTHERN SAUDI ARABIA transects were passagemigrants (10) and winter visitors (7), although the long-billed pipit was probably a local visitor. When records from all sources are combined, 131 species have been recorded in Harrat al-Harrah (Appendices 1 & 2). Resident breeders account for 15% (n = 20) of the total, migrants 58% (n = 76), winter visitors (which may also be passage migrants) 15% (n = 20), local visitors 5% (n = 6), occasional breeders 3% (n = 4) and vagrants 4% (n = 5). Occasional breeders may use the reserve during years of abundance,when frequent and plentiful rainfall results in a tremendous variety and biomass of annual plants. Winter and local visitors may be attracted to flourishing patches of annual plants present in most years, that are not subjected to the high level of grazing pressureexperienced outside protected areas.'Dry lakes' that fill from runoff to form temporary large 'wet lakes' may also provide a haven from hunters for migrating waders and water-fowl. Green (1984) observed hunting of waders, coots and ducks at a lake and marsh system immediately to the south of Harrat al-Harrah.

Seasonal changes in numbers of birds and species

Higher numbers of species and individuals found in the reserve during spring and summer reflected the passageof migrants. Transect counts showed that the proportions of speciesthat were resident were greatest in January and July, but less than 55% in February, March, September, October and November. However, residents comprised the greatestproportion of individuals counted during all months with the lowest value of 61 % occurring in March. As would be expected, the number of resident speciesdid not vary throughout the year. However, significantly higher numbers of individuals in spring compared to winter may be the result of an increase in visibility due to courtship and breeding behaviour, and in late spring, the presenceof that year's offspring.

Effect of rainfall The amount and timing of rainfall has been shown in west-central Saudi Arabia to have a considerableinfluence on numbers of both breeding, granivorous species,and passage migrants due to the subsequentflush of plant growth and seedproduction, although it did not appear to attract greater speciesdiversity (Newton & Newton, 1997).Densities in individual months increasedbetween eight- and 16-fold between years of poor and good rainfall (Newton & Newton, 1997). In Harrat al-Harrah, although good rainfall throughout autumn, winter and spring resulted in a remarkable proliferation of annual species, the density of birds recorded in relation to habitat available during such a good year (1995) was not much greater than during a particularly poor year for rainfall (182 km-2 cf. 107 km2), especially when the amount of variation is taken into consideration.

Diversity indices

Speciesrichness (Margalef's index), and diversity (log seriesalpha value) were greatest in wadis, but more or less the same in the other three habitats. Dominance (Berger- Parker index) was generally low ( < 0.5): the highest value was for sparsely vegetated gravel plains, where Temminck's homed larks comprised 51% of the total number of individuals counted. Rank abundance plots show that wadis have more abundant and 312 y, VAN HEEZIK & p, SEDDON rare speciesthan the other three habitats, and confirm that dominance was highest in sparselyvegetated gravel plains. We did not find a significant difference when comparing Margalef's and Berger- Parker indices between months, and between seasons.However, we did find signi- ficant differences between seasons in the number of individuals and species (Fig. 1).High variability between index values may have precluded a significant result. Newton & Newton (1997) found that with habitats combined, the seasonalpattern of speciesdiversity of birds in central Saudi Arabia closely mirrored that of numbers of species,with peaksoccurring during winter and spring migration, however they did not carry out a statistical analysis.The mean diversity index calculated over all months for all habitats combined was considerably lower in Harrat al-Harrah (0.511) than in Mahazat as-Sayd reserve in west-central Saudi Arabia (4.35; Newton & Newton, 1997).

Comparison between Harrat al-Harrah and other regions in Saudi Arabia

As might be expected, arid regions appear to support few resident species: 20 in Harrat al-Harrah, and 13 in the Mahazat as-Sayd reserve in west-central Saudi Arabia, a flat gravel area of shrub-steppe grassland, with some areas of dry savanna, and an annual rainfall of 102 mm (1992-1994, Newton & Newton, 1997), that has been protected from grazing since 1989. In contrast, in the southern Asir mountains in juniper forest habitat, 56 species (53% of the total) were recorded as resident breeders (Newton & Newton, 1996), and in a wadi with perennially flowing water in western Saudi Arabia (Wadi Turabah), 54 (44% of the total) species were recorded as resident breeders (Newton et at., 1994). Observations made during monthly visits over 3 years to the 'Uruq Bani Ma' arid protected area on the western margin of the higWy arid Rub' al Khali (average rainfall < 50 mm, with dews and fogs) yielded a total of 104 species, of which 16, including local nomadic opportunists, were considered resident (Wacher, 1998) .A very pronounced seasonality in species abundance reflected a high proportion of passage migrants (Wacher, 1998). While the number of resident species varies between biotopes, total species counts in areas that have been surveyed fairly thorougWy do not vary greatly: 133 and 131 in Mahazat as-Sayd and Harrat al-Harrah, respectively (Newton & Newton, 1997; this study), 123 at Wadi Turabah (Newton et at., 1994), 98 in the southern Asir (Newton & Newton, 1996) and 104 at the western margin of the Rub' Al Khali (Wacher, 1998). In the more arid areas, passage migrants comprised 58% (in Mahazat as-Sayd), 59% (in Harrat al-Harrah) and about 75% (in 'Uruq Bani Ma'arid) of the total species counted. The principal difference in the avifauna between Harrat al-Harrah and Mahazat as-Sayd was in the numbers of individuals, which were considerably higher in Mahazat as-Sayd. Monthly densities in Mahazat as-Sayd ranged from between 15 and 180 birds km -2 in seasons following poor rainfall, to between 242 and 1070 km -2 in seasons following good rainfall (Newton & Newton, 1997). In contrast, monthly densities averaged over good and poor seasons in Harrat al-Harrah ranged between a minimum of 15 km -2 in January to a maximum of 280 km -2 in September. Vegetation in Mahazat as-Sayd is structurally more complex than in Harrat al-Harrah, in that three of the five habitats sampled contained trees, grasses, and had estimated ground covers ranging from 20-50% when sampled in September 1992, when vegetation cover was at a peak following heavy rainfalls in the preceding month. In dry seasons many grasses and herbs die back, reducing the cover substantially. Over 85% of all birds and 89% of species were recorded in the two most heavily vegetated sites (Newton & Newton, 1997). Margalef's indices of species richness calculated for four of five defined habitats in Mahazat as-Sayd were greater than in Harrat al-Harrah (except bare gravel, 0.76). BIRDS IN NORTHERN SAUDI ARABIA 313

Rocky jabal (1'86) in Mahazat as-Sayd,with an estimatedcover of < 5%, scoredhigher in species richness than wadis in Harrat al-Harrah (1'258), Indeed, bare gravel in Mahazat as-Sayd (0'76) scored higher than all habitats except wadis in Harrat al- Harrah. The absenceof trees, virtual absenceof grassesoutside of spring, and relatively sparsecovering of perennial shrubs in Harrat al-Harrah is probably the principal factor limiting numbers and diversity of birds in the harrat biotope.

We thank His Royal Highness Prince Saud Al Faisal, the General Manager, and Dr Abdulaziz H. Abuzinada, the Secretary General of the National Commission for Wildlife Conservation and Development, for their support of this work. Much appreciatedassistance in the field was given by Hans Hemmingsen, (Chief Pilot) and other members of the NCWCD flight crew, and by Ali Hamad Al Murri (Head Ranger) and his staff. The manuscript was improved by the comments of Mohammed Y. Shobrak and W.R.]. Dean.

References

Child, G. & Grainger, ]. (1990). A systemplan for protectedareas for wildlife conservationand sustainabledevelopment in Saudi Arabia. Riyadh: National Commission for Wildlife Conserva- tion and Development. 335 pp. Fisher, M., Ghazanfar, S.A., Chaudhary, S.A., Seddon, PJ., Robertson, E.F., Omar, S., Abbas, ].A. & Boer, B. (1998). Diversity and conservation. In: Ghazanfar, S.A. & Fisher, M. (Eds), Vegetationof the Arabian Peninsula,pp. 265-303. The Netherlands: Kluwer Academic Pub- lishers. Goriup, P.D. & at-Toraif, M. (1988). Houbara bustardfield researchproject. Report on activities March-April1988. Unpublished Report, NCWCD, Riyadh. 23 pp. Goriup, P.D., Norton, ].A. & al Salamah, M. (1989). Houbara bustard field research project. Report on activities April-June 1989. Unpublished Report, NCWCD, Riyadh. 42 pp. Goriup, P., Norton,]. & al Salamah,M. (1992). Houbara bustardfield researchproject. Reportfor 1990. Unpublished report, NCWCD, Riyadh. 56 pp. Green, A.A. ( 1984).The avifauna of the Al ]awf region, north-west Saudi Arabia. Sandgrouse, 6: 48-58. ]ennings, M.C. (1995). An Interim Atlas of the Breeding Birds of Arabia. Riyadh: National Commission for Wildlife Conservation and Development. 134 pp. Kiirschner, H. 1998. Biogeography and introduction to vegetation. In: Ghazanfar, S.A. & Fisher, M. (Eds), Vegetationof the Arabian Peninsula,pp. 63-69. The Netherlands: Kluwer Academic Publishers. Magurran, A.E. ( 1988).Ecological diversity and its measurement.London: Chapman and Hall. 170 pp. Newton, S.F. & Newton,A.V. (1996). Seasonalchanges in the abundanceand diversity of birds in threatened juniper forest in the southern Asir mountains, Saudi Arabia. Bird Conservation International, 6: 371-392. Newton, S.F. & Newton, A.V. (1997). The effect of rainfall and habitat on abundance and diversity of birds in a fenced protected area in the central Saudi Arabian desert.Journal of Arid Environments,35: 715-735. Newton, S.F., Newton, A.V. & Winkler, H. (1994). The avifauna of Wadi Turabah: status, distribution and habitats associations.Fauna of Saudi Arabia, 14: 442-454. Rahmani, A.R., Shobrak, M.Y. & Newton, S.F. (1994). Birds of the Tihama coastal plains of Saudi Arabia. OSME,32: 1-19. Symens, P. (1988). Houbara bustard survey in Harrat al-Harrah March 1988. In: NWRC Quarterly Report No.8. 1988, pp. 31-49. Riyadh: NCWCD. van Heezik, Y. & Seddon, PJ. (1999). Seasonalchanges in habitat use by Houbara Bustards Chlamydotis[undulataJ macqueeniiin northern Saudi Arabia. Ibis, 141: 208-215. Wacher, T. (1998). Ornithology of 'Uruq Bani Ma' arid Protected Area: a preliminary description. In: Annual Report 1997, KKWRC, pp. 74-77. Riyadh, Saudi Arabia unpublished reoort. 314 Y. VAN HEEZIK & P. I. SEDDON

Appendix 1

List and status of species counted in the transects, and months when they were observedin the Harrat al-Harrah protected area. a = absentfrom the reserveand no counts made. Numbers in boxes indicate observations recorded prior to this study

I Species I StatUsITIFIMIAj a I ~j~IAI s lolNID Hen harrier Circus cxaneus

Pallid harrier Circus macrourus w m i Step~-~ Buteo buteo

i Kestrel Falco tinn~n-c~!us rb ~artridge Ammo12erdixh~v~ rb I Quail Cotumix coturnix m

Houbara bustard Chlam~dotis macQueenii rb/wv ~ Cream coloured courser Cursorius cursor ob

Dotterel Charadrius morinellus wv

Rock dove Colomba livia rb Hoopoe Ul2ul2aeI!°I!s m Dunn's lark Eremalauda dunni ob2.4

I Bar-tailed desert l~k Ammomane~ cincturus rb

I Desert lark Ammomanes~~s~ rb I~laemon alaudi12es rb Thick-billed lark Rarn~hocorisclotbe~ rb4

Bi~aculated l~k Melanocor~l2habimaculata om Short-toed lark Calandrella brachvdactvla --r:essershort-toed lark Calandrella m~l~v/rb4 I ~ --- Crested lark -Galerida cristata rb Skylark Alauda arvensis wv LTemminck's horned lark-E~a-bilol2ha rb

I Sand martin RiI2aria riI2aria ~ I Barn swallow Hirundo rustica ~ Tawny pipit Anthus cam~estris ~ Long-billed pipit Anthus similis iv? Isabelline wheatear Oenantheisabellina rb Oenantheoenanthe ~ I Desert wheatear Oenanthe deserti rb I Finsch;s wheateir Oenanthe-fi-n;;Chii wv

I Mourning wheatear Oenanthe lugens wv I White-crowned black wheatear 0. leucol1~ga rb Scrub warbler Scotocercainguieta rb Great grey shrike Lanius excubitor Trumpeter finch Bucanetesgithagineus rb

1: Goriup et at. (1992); 2: Goriup & at-Toraif (1988); 3: Goriup et at. (1989); 4: Symens (1988). Codes: rb = resident breeder; ob = occasional breeder; pm = passage migrant; v = vagrant; Iv = local visitor; wv = winter visitor. BIRDS IN NORTHERN SAUDI ARABIA 315

Appendix 2

list and status of speciesrecorded outside the transects by the authors, and by other observers (as indicated by numbers} in each month

Species I Status! J I F I M I A I M I j -1-J-IAI-s r 0 I N I~ Cormorant1 Phalacrocorax carbo v ~~lican Pelecanusonocrotalus ~ ~ ~!!:~ Ixob~chus minutus ~ L~q~ heron" Ardeola ralloides ~ 1 ~~ttle egret B~cu~ .l?!!!- I Mallard Anas l2lat~rh~nchos wv Shoveler Anas cl~~eata wv Black kite Milvus migrans .l?!!!- Egyptian vulture Neol!hron I!ercn°l!terus -- ~ Griffon vulture' G~l2S fulvus v Lappet-faced vulture Torgos tracheliotos Iv ! Marsh harrier Circus aeruginosus ~ I Montagu's harrier" Circus l2~gargus ~ I Sparrowhawk' Acci~iter nisus ~ Long-legged buzzard Buteo rufinus .E!!!.. Lesserspotted eagle AQuila 12omarina .E!!!.. Steppeeagle Aguila ni~alensis .E!!!.. Imperial eagle' AQuila heliaca .E!!!.. Golden eagle AQuila ch!:ysaetos rb Honey buzzard" Pemis a!,ivorus v Short-toedeagle' Circaetus gallicus wv i Lessefkesu:eI' Fi11co naumanni ..E!!!. ~ .-P81cocolumbarius wv I Eleonora's falcon" Falco eleonorae v I Chukar partridge Alectoris chukar Iv Stone curlew! Burhinus oedicnemus ..E!!!. Collared pratincole' Glareola pratincola ..E!!!. Little ringed plover Charadriusdubius wv Ringed plover Charadrius hiaticula ~ Grey plover Pluvialis sQuatarola .2!E.. , White-tailed plover Chettusia leucura .2!E.. ILi~e8tlnt calidrisminu~ .2!E.. rTemminck's Siinfcaiidfis temmilickii .2!E.. I Curlews~dpiJ;ercalidris-ferrugTnea ~ Dunlin Calidris all2ina ~ Common snipe Gallinago gallinago ~ Curlew" Numenius arQuata pm 316 Y. VAN HEEZIK & P. ]. SEDDON

Appendix 2-continued

I Species StatUs rJ IF I Mj-~L~LJ-I~jA~I~J QI-N-IJ21 I Ruff Philo~hus ~ugnax

I~dsha~k Tringa totanus Green sandpiper Tringa ochro~us Wood sandpiper Tringa glareola - Black-headed gull Larus ridibundus Black-bellied sandgrouse Pteroclesorientalis Pin-tailed sandgrouse" Pteroclesalchata -~ Palm dove StreQtoQelia senagalensis - Common cuckoo Cuculus canorus Little owl Athene noctua ,- .- Eagle owl Bubo bubo -. ! Hume's tawny owl Strix butleri Common swift AQus 3QUS

I con;mo~tl~lcedoatthis

I EUropean~te? -Mero;;sal!iaster

I European roller- Coracias garrulus Crag martin' Pt~ono12rogne ru12estris Red-throated pipit Anthus cervinus Yellow wagtail Motacilla flava Grey wagtail Motacilla cinerea White wagtail Motacilla alba Rufous bush robin:' Cercotrichas galactotoes nightingale" Luscinia Iuscinia - ! Black redstart Phoenicurus ochrurus ~~I I Common redstart Phoenicurus I1hoenicurus I Blackstart Cercomela melanura tWhiDChatSaxicola rubetra I Stonechat Saxicola torguata 1- Pied wheatear Oenanthe Qleschanka E!!!:. Black-eared wheatear Oenanthe his~anica -E!!!- Blue rock thrushl Monticola solitarius -E!!!- Fieldfare' Turdus Qilaris wv Song thrush' Turdus Qhilomelos wv Olivaceous warbler HiDDolaisQallida -E!!!- Upcher's warbler.. Hi~Dolais languida ~ -siJectacled warbler! Sylvia consQicillata v I Desert warbler1 Sylvia DaDa ~ IGarden warblerl S~lyia borin ~ Lesserwhitethroati Sylvia carruca ~ Whitethroat Svlvia communis ~ Blackcap' Sylvia atricaRilla Dm Chiffchaff PhylloscoQus collybita

~ BIRDS IN NORTHERN SAUDI ARABIA 317

Appendix l-continued

, Species I Status I J Willow warbler' Phyllosco12UStrochilus ~ Spotted flycatcher' Muscica12astriata ~ Golden oriole Oriolus oriolus ~ I Red-backed shrike~ Lanius collurio ~ Lessergrey shrike' Lanius minor ~ I woodchatshfike" La~nator ~ l Masked shrike Lanius nubicus £]]];.

Brown-necked raven Corvus ruficollis rb4

Rose-colouredstarling" Sturnusroseus V

House sparrow Passerdomesticus rb

Spanishsparrow Passerhisl2aniolensis ob4 Pale rock sparrow Petronia brach~dact~la pmlrb4 Siskin 1 Carduelis sl2inus wv

Desert finch' Rhodos~izaobsoleta iv Ortolan bunting Emberiza hortulana P.!!! Black-headed bunting" Emberiza P.!!! Corn bunting. Miliara calandra wv

1: Goriup et al. (1992); 2: Goriup & at-Toraif (1988); 3: Goriup et al. (1989); 4: Symens (1988). Codes: rb = resident breeder; ob = occasional breeder; pm = passagemigrant; v = vagrant; Iv = local visitor; wv = winter visitor.