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249

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Turkish Journal of Zoology Turk J Zool(2013) 37: 249-261© TÜBİTAKdoi:10.3906/zoo-1211-34

Impacts of anthropogenic activities and habitat degradationon breeding waterbirds

Ortaç ONMUŞ*, Mehmet SIKIDepartment of Biology, Faculty of Sciences, Natural History Museum Research and Application Center,

Ege University, Bornova 35100 İzmir, Turkey

* Correspondence: [email protected]

1. IntroductionHuman activities have resulted in the modification of our natural world at an unprecedented scale, resulting in global species extinction rates rising higher than the projected figures (Greuter, 1994; Pimm et al., 1995; Pimm and Raven, 2000; Millennium Ecosystem Assessment, 2005a, 2005b). Therefore, an important step to conserve the world’s biodiversity is the collection of baseline data that can be used to identify key areas for biodiversity conservation (Olson and Dinerstein, 1998; Myers et al., 2000; Olson et al., 2001). Habitat loss and extinctions in biodiversity hotspots are serious problems (Brooks et al., 2002; Venter et al., 2006; Underwood et al., 2009). Therefore, information on population estimates and trends, identification of imperiled species, and factors affecting them are of immense importance for conservation practitioners (Salafsky et al., 2002; Battisti et al., 2008). However, effective conservation can only be achieved by standardizing the methods applied and used in conservation science (Salafsky et al., 2008).

The Gediz Delta is identified as a Key Biodiversity Area (Eken et al., 2006). Furthermore, the delta has been

designated as a wetland of international importance, a “Natural Site” area, and a wildlife protection area under national law. It also satisfies Important Bird Area (IBA) criteria (with IBA designation code of TR016), as it harbors 30 bird species, including populations of globally threatened species such as the Dalmatian Pelican (Pelecanus crispus), Lesser Kestrel (Falco naumanni), and Red-Breasted Goose (Branta ruficollis) (Kılıç and Eken, 2004; Onmuş and Sıkı, 2011). In addition, many of the delta’s breeding birds have “Unfavorable Conservation Status” and therefore qualify as “Species of European Conservation Concern” (BirdLife International, 2004).

Unfortunately, the delta and its biodiversity have been suffering from many threats such as wetland filling and modification of formerly wild areas into urban and industrial areas, illegal dumping, sludge deposition on wetland habitats (approximately 500 t of sludge is produced per day by the sewage treatment plant of the İzmir Metropolitan Municipality, and this sludge has been deposited on the wetland habitats since 2002), poaching, and illegal reed bed cutting and burning (Eken, 1997; Onmuş et al., 2009; Onmuş and Sıkı, 2010, 2011).

Abstract: We investigated the effects of threats on breeding waterbirds in the Gediz Delta, Turkey. Breeding Bird Surveys were conducted in 2002 and 2006. The survey area comprised 305 UTM grids of 1 × 1 km2. Populations and distributions of breeding birds were compared between 2002 and 2006 for the UTM grids under threat and without any threat using paired samples t-test, Wilcoxon signed-rank test, and GIS. Urbanization, industrialization, pollution, overgrazing, disturbance, and illegal reed cutting and burning were identified in 151 (49.5%) of 305 grids in 2002. The mean total number of breeding birds per UTM grid slightly decreased in areas under threat, but significantly increased (P < 0.05) in areas without threat. The mean total number of breeding waterbirds significantly decreased (P < 0.05) in both the grids under and without threat. Out of 30 waterbirds breeding in grids under threat, 23 shifted their breeding locations. The total number of breeding pairs of 9 waterbirds decreased, 7 species increased, and 6 species were stable. The maximum breeding code of 6, maximum number of breeding pairs of 11, total number of observed birds of 11, and frequency of occurrence of 15 species significantly decreased in UTM grids under threat. Threats have significantly affected (P < 0.05) the breeding populations of bird species even in a short period of 4 years.

Key words: Waterbirds, Breeding Bird Survey, threats, urbanization, industrialization, pollution, disturbance, Important Bird Area, Key Biodiversity Area, Gediz Delta

Received: 28.11.2012 Accepted: 08.01.2013 Published Online: 29.04.2013 Printed: 29.05.2013

Research Article

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ONMUŞ and SIKI / Turk J Zool

However, our understanding of which species are affected in what ways due to various factors has been minimal. Therefore, we designed the present study to quantify impacts of threats (urbanization, industrialization, pollution, overgrazing, disturbance, and illegal reed cutting and burning) on breeding waterbirds in the Gediz Delta.

2. Materials and methods2.1. Study areaThe Gediz Delta (38°32.00′N, 26°52.00′E) is located on the west coast of Turkey (Figure 1) and occupies an area of 40,000 ha consisting of approximately 40% wetlands and 60% farmland and hills (Kılıç and Eken, 2004). The delta, besides having Turkey’s largest active marine saline habitat, possesses a myriad of habitats including extensive mud flats, sand beaches with Salicornia vegetation and seashells, coastal marshes, lagoons, extensive salt marshes, agricultural lands (mainly cotton, wheat, and maize farming), pastures, tree plantations (Eucalyptus sp. and Pinus pinea), and urban and industrial areas (Onmuş et al., 2009; Onmuş and Sıkı, 2010).2.2. Breeding Bird Surveys (BBSs)The surveys were conducted in 2002 (15 May to 9 June) and 2006 (15 May to 11 June). The wetland and surrounding

ecosystems, comprising a total of 30,500 ha, were selected for the study. The atlas boundary coordinates are between 480,000 and 509,000 m E and 4,254,000 and 4,279,000 m N in UTM grid zone 35S (WGS84). The area was divided into 305 UTM grids of 1 × 1 km2 in size (Figure 1). To represent each grid, 3 random points separated by at least 300 m of distance were sampled and surveyed only once during the breeding season. The number of point counts applied in a grid was reduced in squares having open-surface water areas or partial sea to secure unbiased sampling. A 2-day pilot study was applied before the BBSs to test the method and to standardize the techniques applied. Point counts with a fixed radius were conducted for 10 min, for a total of 30 min for each grid. The counts were carried out between 0700 and 1100 hours and between 1600 and 1930 hours to reduce bias due to inactivity of the birds around midday (Bibby et al., 2000).

The number of individuals for each bird species observed at each point was counted, and their breeding evidence was quantified using the standard 16 breeding codes presented in the Appendix (Hagemeijer and Blair, 1997; Bibby et al., 2000; Sutherland, 2006). Special field recording forms were designed where UTM coordinates, time of day (to ensure data collection standards), habitat types, threats, and the bird species that were seen and/or

480,000 490,000 500,000 510,000

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Old Rive rbe d

Old Rive rbe d

Old Rive rbe d

Ge diz De lta

İzmir B a y

" Turke yİzmir

Old Rive rbe d

Figure 1. Study area location, 1 × 1 km2 UTM grids, and the major habitats and their distributions.

➢

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251


heard were noted along with their breeding codes for each point separately. All other birds seen and/or heard during passage through a grid were recorded separately as “casual records” for that grid and used for the determination of the maximum breeding codes of each grid. The total number of individuals of a bird species observed in a UTM grid was calculated by adding the total number of individuals observed and/or heard in each point count of that grid. The presence of a species among the 3 different point counts (1, 2, or 3) in each UTM grid was calculated from the raw data and used to derive frequency of occurrence values.2.3. Census of breeding pairsIf point counts established the presence of a breeding waterbird in a certain UTM grid, a census was conducted to determine the maximum and minimum number of breeding pairs of that species. Different census strategies of Gilbert et al. (1998) were used for various dispersed breeding species, while we used direct counts for colonial breeding species since the largest number of breeding pairs in a colony in our study area was less than 200 pairs (Gilbert et al., 1998; Bibby et al., 2000). The number of apparently active or occupied nests counted during the census was accepted as the minimum number of breeding pairs. The maximum number of breeding pairs was calculated by adding possible breeders (old-looking nests that appeared to be active, or nests that could not be definitively identified as actively occupied) to this minimum number (Onmuş et al., 2009; Onmuş and Sıkı, 2010, 2011).2.4. Threat dataDuring 2002, we recorded urbanization, industrialization, pollution, overgrazing, disturbance, and illegal reed cutting and burning as the main threats to waterbirds in our study area. Any point count location having natural habitats was considered under threat if 1 of these threats existed within a distance of approximately 300 m. The number of observed threats in each UTM grid and their frequencies (i.e. the presence of a specific threat at any of the 3 different point counts: 1, 2, or 3) were calculated from the raw data and used to indicate the prevalence of the threats. The UTM grids that were under any of these threats at any observation point in 2002 were classified as grids under threat. Other UTM grids without any of these threats in 2002 were accepted as UTM grids without threat. The threats were classified as follows:– Urbanization or industrialization: any point-count

zone having natural habitats with urban or industrial zone development.

– Pollution: debris of construction, house waste, and sludge dumping.

– Overgrazing: overgrazed pastures around a point-count zone were accepted as an overgrazing threat. Overgrazed pastures were noted in our study area as being dominated by Typha sp., Phragmites sp., and

long-grass species communities; by Scirpus sp. and Juncus sp. communities; and by short-grass species communities, respectively. The soil was frequently visible between plants in the stand.

– Disturbance: existence of hunters, hunting hides and/or cartridges, fishing activities, mussel and bait pickers, or Salicornia pickers (Salicornia leaves are gathered and sold in grocery stores or appear on restaurant menus as “sea beans” or “sea pickle” in the region).

– Reed bed burning and cutting: reed bed burning and cutting are usually extensive and frequently take place around the river banks, irrigation and drainage channels, and zones of freshwater entries. Any point-count zone with signs of recent or actual reed bed burning and cutting activity was considered as being under this threat.

2.5. GIS analysesThe distribution and observation frequency of the threats per UTM grid were presented. The total number of breeding bird and waterbird species and their distributions per UTM grids were calculated and presented using ArcGIS 10.0.2.6. Statistical analysesThe mean total number of breeding birds and breeding waterbird species per UTM grid in 2002 and 2006 were compared with a paired samples t-test, separately for the grids under threat (n = 151) and for the remaining grids without these threats (n = 154) (stratification according to threat status; stratified analysis hereafter). The UTM grids without breeding evidence of any species were excluded from the analyses.

Among the 30 species that were breeding in both years, 22 species continued to breed in 2006 at least in 1 UTM grid that was under threat in 2002 (matching species hereafter). The mean maximum breeding codes, maximum number of breeding pairs, total number of observed individuals, and frequency of occurrence values (BBS parameters hereafter) of matching species per UTM grid were compared with the Wilcoxon signed-rank test or paired samples t-test at P < 0.05. If a species discontinued breeding in 2006 in a specific grid (among the 151 grids under threat in 2002), the relevant variable value was assigned as zero in order to include these grids in the analysis. The remaining 8 bird species that did not breed in 2006 in grids under threat or which bred only in 1 UTM grid under threat were excluded from the analyses. Therefore, only descriptive data are presented for these 8 waterbirds. The statistical analyses were conducted using PASW (Version 18.0, www.spss.com).

3. ResultsWe recorded threats in 151 (49.5%) of the UTM grids in 2002 (Table 1; Figure 2), with no breeding evidence in the

252


Table 1. The observed number of 1 × 1 km2 UTM grids [n (%)] under urbanization, industrialization, pollution, overgrazing, disturbance, and illegal reed cutting and burning threats and their observed frequencies in 2002 during the study.

Urbanization Industrialization Pollution Overgrazing Disturbance Reed cutting and burning

Frequency of observation

1 17 (5.6) 12 (3.9) 63 (20.7) 37 (12.1) 40 (13.1) 5 (1.6)

2 9 (3.0) 13 (4.3) 14 (4.6) 17 (5.6) 8 (2.6) 2 (0.7)

3 2 (0.7) 2 (0.7) 2 (0.7) 4 (1.3) 2 (0.7) 0

Totals 28 (9.3 ) 27 (8.9) 79 (26.0) 58 (19.0) 50 (16.4) 7 (2.3)

UrbanizationFrequency123

UTM Grids

IndustrializationFrequency123

UTM Grids

Pollution/DumpingFrequency

123

UTM Grids

Overgra zingFrequency

123

UTM Grids

Disturba nc eFreque nc y

123

UTM Grids

Reed cutting /burningF re que nc y12

UTM Grids

Figure 2. Distribution and observation frequency of urbanization, industrialization, pollution, overgrazing, disturbance, and illegal reed cutting and burning threats in 2002.

253


2 grids having mainly open-water habitat. The mean total number of all the breeding bird species per UTM grid in 149 grids under threat was 16.3 ± 8.3 in 2002 and 15.8 ± 9.1 in 2006 (P = 0.351), while the same figures in 135 grids (the remaining 19 grids consisted of only open-water habitats) without threat were 12.5 ± 7.8 in 2002 and 14.1 ± 9.7 in 2006 (P = 0.022). On the other hand, the mean total number of breeding waterbird species per UTM grid in 104 grids under threat was 2.8 ± 1.7 in 2002 and 2.3 ± 2.0 in 2006 (P = 0.014), while the same figures in 89 grids without threat were 2.8 ± 1.8 in 2002 and 1.9 ± 2.2 species in 2006 (P = 0.001). Distributions of the total number of breeding birds and waterbirds per UTM grid in 2002 and 2006 are given in Figure 3.

Thirty waterbirds were found breeding in both study years. Of these, 5 species had left all their breeding grids in 2006 that had been under threat in 2002. Nine species left more than 50% and 3 species left 50% of their breeding grounds in UTM grids that had been under threat in 2002. Similarly, there were reductions in breeding dispersals for 6 species in UTM grids under threat, making a total of 23 species shifting to areas without threat (Table 2).

The comparisons of BBS parameters of 22 matching waterbird species in UTM grids under threat are given in Table 3. Among these waterbird species, significant decreases were observed in the maximum breeding codes of 6 species, the maximum number of breeding pairs of 11 species, the total number of observed individuals of 11 species, and the frequency of occurrence of 15 species.

The comparisons of BBS parameters of 22 matching waterbird species in UTM grids without threat are given in Table 4. Among these species, significant decreases (P < 0.05) were observed in the maximum breeding codes of 9 species, the maximum number of breeding pairs of 6 species, the total number of observed individuals of 5 species, and the frequency of occurrence of 8 species.

The total number of breeding pairs of 22 waterbirds throughout the delta, changes in their populations, and comparisons of this change with the results of the stratified analyses are given in Table 5. The total number of breeding pairs of 3 species severely decreased, 6 species were stable, 6 species moderately increased, and 1 species significantly increased.

Figure 3. Distribution of the total number of breeding bird species and waterbird species per UTM grid in 2002 and 2006.

254


Table 2. The total numbers of UTM grids with observed breeding evidence in 2002, both throughout the delta (n = 305) and in the 151 grids under threat, the UTM grids (under threat in 2002) where breeding was discontinued in 2006, and the number of new UTM grids where species started to breed in 2006.

Species

UTM grids with observedbreeding behavior in 2002*

UTM grids under threat in 2002 and

where breeding was discontinued in 2006

[n (%)]

# of new UTM grids where species were

found breeding in 2006 (n)

Total[n (%)]

Under threat [n (%)]

Podiceps ruficollis 16 (5.2) 10 (62.5) 6 (60.0) 8

Pelecanus crispus 4 (1.3) 2 (50.0) 2 (100.0) 1

Ixobrychus minutus 9 (3.0) 6 (66.7) 3 (50.0) 14

Ardeola ralloides 2 (0.7) 1 (50.0) 0 2

Egretta garzetta 1 (0.3) 0 NA 0

Ardea purpurea 1 (0.3) 1 (100.0) 0 0

Ciconia ciconia 9 (3.0) 8 (88.9) 6 (75.0) 3

Platalea leucorodia 1 (0.3) 0 NA 1

Phoenicopterus roseus 1 (0.3) 0 NA 0

Tadorna ferruginea 20 (6.6) 7 (35.0) 2 (28.6) 9

Tadorna tadorna 27 (8.9) 10 (37.0) 7 (70.0) 12

Anas querquedula 1 (0.3) 1 (100.0) 1 (100.0) 1

Gallinula chloropus 22 (7.2) 14 (63.6) 7 (50.0) 37

Fulica atra 20 (6.6) 10 (50.0) 6 (60.0) 7

Haematopus ostralegus 26 (8.5) 17 (65.4) 11 (64.7) 12

Himantopus himantopus 28 (9.2) 11 (39.3) 6 (54.5) 16

Recurvirostra avosetta 8 (2.6) 2 (25.0) 2 (100.0) 6

Burhinus oedicnemus 28 (9.2) 18 (64.3) 10 (55.6) 27

Glareola pratincola 12 (3.9) 10 (83.3) 9 (90.0) 9

Charadrius alexandrinus 90 (29.5) 51 (56.7) 18 (35.3) 15

Vanellus spinosus 23 (7.5) 16 (50.0) 9 (56.3) 12

Tringa totanus 15 (4.9) 12 (80.0) 4 (33.3) 10

Larus melanocephalus 6 (2.0) 2 (33.3) 2 (100.0) 3

Larus genei 1 (0.3) 0 NA 1

Larus michahellis 56 (18.4) 25 (44.6) 12 (48.0) 15

Sterna caspia 1 (0.3) 0 NA 1

Sterna sandvicensis 4 (1.3) 2 (50.0) 2 (100.0) 0

Sterna hirundo 49 (16.1) 26 (53.1) 12 (46.1) 18

Sterna albifrons 46 (15.1) 19 (41.3) 9 (47.4) 11

Sterna nilotica 3 (1.0) 2 (66.6) 1 (50.0) 2

Percentages among the number of grids with breeding evidence in 2002. NA: Not applicable.

255

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70.7

44.3

± 1

47.4

0.35

211

1.1

± 30

1.6

63.6

± 2

16.2

0.14

11.

5 ±

0.9

0.7

± 0.

90.

002

Ster

na a

lbifr

ons

↑19

4.8

± 3.

83.

5 ±

5.3

0.23

65.

5 ±

7.7

27.7

± 7

1.7

0.49

28.

4 ±

9.2

50.6

± 1

35.2

0.31

41.

8 ±

0.8

0.6

± 0.

60.

001

Ster

na n

ilotic

a↓

21.

0 ±

0.0

1.0

± 1.

41.

002.

5 ±

2.1

0.5

± 0.

70.

180

2.5

± 2.

10.

5 ±

0.7

0.18

01.

5 ±

0.7

0.5

± 0.

70.

157

*: Pa

ired

sam

ples

t-te

st re

sults

(all

othe

r bird

spec

ies a

naly

zed

with

Wilc

oxon

sign

ed-r

ank

test

).

256


ble 4

. The c

ompa

rison

s of 2

002

and

2006

BBS

par

amet

ers o

f 22

wat

erbi

rd sp

ecie

s in

UTM

grid

s with

out t

hrea

t in

2002

. The s

peci

es h

avin

g sig

nific

ant P

val

ues a

re m

arke

d in

bol

d,

and

the

obse

rved

bre

edin

g po

pula

tion

chan

ges a

re in

dica

ted

(↓: d

ecre

asin

g, ↑

: inc

reas

ing,

@: s

tabl

e, ↓↑

: fluc

tuat

ing,

NA

: not

appl

icab

le).

Spec

ies

Tren

d#

of

grid

s

Max

. bre

edin

g co

deM

ax. #

of b

reed

ing

pair

sTo

tal #

of b

irds

obs

erve

dR

elat

ive

abun

danc

e

2002

2006

P20

0220

06p

2002

2006

p20

0220

06p

Podi

ceps

rufic

ollis

↓6

3.5

± 4.

23.

5 ±

6.3

1.00

01.

7 ±

1.6

1.0

± 1.

30.

157

2.7

± 3.

11.

7 ±

2.3

0.34

31.

5 ±

0.8

0.7

± 0.

80.

129

Pelec

anus

crisp

us↑↑

214

.5 ±

2.1

16.0

± 0

.00.

317

3.5

± 2.

136

.0 ±

11.

30.

180

5.5

± 5.

037

.5 ±

13.

40.

180

1.5

± 0.

71.

0 ±

0.0

0.31

7

Ixob

rych

us m

inut

us↓

32.

0 ±

1.0

0.0

± 0.

00.

109

2.0

± 1.

00.

0 ±

0.0

0.10

93.

0 ±

2.0

0.0

± 0.

00.

109

1.4

± 0.

60.

0 ±

0.0

0.10

2

Cico

nia

cicon

iaN

A1

NA

NA

NA

NA

NA

NA

NA

NA

NA

NA

NA

NA

Tado

rna

ferr

ugin

ea↓

135.

7 ±

4.8

1.8

± 4.

60.

015

2.4

± 1.

80.

7 ±

1.7

0.00

721

.8 ±

49.

19.

1 ±

28.6

0.00

91.

4 ±

0.8

0.4

± 0.

50.

005

Tado

rna

tado

rna

↓17

4.1

± 3.

62.

9 ±

5.7

0.20

01.

4 ±

0.8

0.5

± 0.

90.

001

3.4

± 2.

03.

4 ±

7.2

0.10

51.

2 ±

0.4

0.5

± 0.

60.

002

Gal

linul

a ch

loro

pus

↓8

2.3

± 2.

80.

5 ±

1.1

0.01

41.

5 ±

0.8

0.5

± 1.

10.

054

2.1

± 1.

51.

1 ±

2.2

0.22

21.

3 ±

0.5

0.6

± 1.

20.

132

Fulic

a at

ra↓

104.

3 ±

5.3

0.2

± 0.

60.

005

1.4

± 1.

00.

2 ±

0.6

0.01

33.

2 ±

4.3

0.4

± 1.

30.

004

1.0

± 0.

00.

3 ±

1.0

0.05

2

Hae

mat

opus

ostr

aleg

us↑

92.

6 ±

4.0

5.4

± 6.

90.

592

1.2

± 0.

41.

2 ±

1.7

0.94

32.

0 ±

1.5

2.4

± 3.

40.

858

1.0

± 0.

00.

7 ±

0.9

0.25

7

Him

anto

pus h

iman

topu

s↓

177.

2 ±

5.5

1.1

± 2.

90.

005

19.2

± 2

8.1

0.8

± 2.

10.

002

33.6

± 4

6.9

1.1

± 3.

90.

002

1.7

± 0.

90.

2 ±

0.4

0.00

1

Recu

rviro

stra

avos

etta

↓6

8.0

± 5.

92.

2 ±

5.3

0.04

119

.8 ±

20.

50.

7 ±

1.6

0.02

729

.0 ±

20.

21.

3 ±

3.3

0.02

81.

8 ±

1.0

0.2

± 0.

40.

041

Burh

inus

oed

icnem

us@

104.

7 ±

4.9

1.0

± 2.

00.

027

1.1

± 0.

30.

5 ±

0.9

0.08

31.

7 ±

0.7

0.9

± 1.

70.

194

1.0

± 0.

00.

5 ±

0.9

0.09

6

Gla

reol

a pr

atin

cola

↓↑

24.

0 ±

4.2

8.0

± 7.

10.

180

4.5

± 6.

33.

0 ±

2.8

0.65

535

.0 ±

24.

05.

5 ±

6.4

0.18

01.

0 ±

0.0

1.5

± 0.

70.

317

Char

adriu

s alex

andr

inus

*@

392.

7 ±

3.1

3.3

± 5.

10.

547

2.7

± 3.

32.

0 ±

3.3

0.19

65.

1 ±

4.6

3.8

± 5.

70.

159

1.6

± 0.

91.

0 ±

1.4

0.01

3

Vane

llus s

pino

sus

@7

2.0

± 1.

31.

4 ±

2.7

0.22

71.

7 ±

0.8

0.7

± 1.

50.

200

3.4

± 2.

81.

4 ±

3.0

0.17

51.

3 ±

0.5

0.4

± 0.

80.

058

Trin

ga te

tanu

s↑

34.

7 ±

2.5

7.0

± 6.

00.

285

1.3

± 0.

61.

7 ±

1.5

0.65

52.

7 ±

1.2

3.7

± 1.

50.

317

1.3

± 0.

61.

0 ±

0.0

0.31

7

Laru

s mela

noce

phal

us↓

44.

0 ±

6.0

0.0

± 0.

00.

059

9.5

± 15

.70.

0 ±

0.0

0.06

69.

5 ±

15.7

0.0

± 0.

00.

066

NA

NA

NA

Laru

s mich

ahell

is*↓↑

317.

7 ±

5.9

4.4

± 6.

70.

007

24.6

± 4

6.7

21.9

± 5

1.4

0.63

359

.6 ±

101

.747

.9 ±

121

.20.

433

1.5

± 0.

70.

5 ±

0.7

<0.0

01

Ster

na sa

ndvi

cens

is↑↑

28.

0 ±

7.1

6.5

± 9.

20.

317

21.0

± 2

1.2

33.0

± 4

6.7

0.65

541

.0 ±

42.

465

.5 ±

92.

60.

655

1.0

± 0.

00.

5 ±

0.7

0.31

7

Ster

na h

irund

o↓↑

235.

7 ±

5.6

3.1

± 5.

40.

002

30.9

± 8

0.5

22.3

± 7

4.6

0.05

966

.3 ±

155

.739

.3 ±

135

.90.

051

1.3

± 0.

60.

5 ±

1.0

0.00

5

Ster

na a

lbifr

ons

↓27

5.7

± 5.

81.

7 ±

4.2

<0.0

0112

.4 ±

32.

72.

5 ±

9.9

<0.0

0120

.2 ±

53.

64.

0 ±

14.9

<0.0

011.

8 ±

0.9

0.3

± 0.

6<0

.001

Ster

na n

ilotic

aN

A1

NA

NA

NA

NA

NA

NA

NA

NA

NA

NA

NA

NA

*: Pa

ired

sam

ples

t-te

st re

sults

(all

othe

r bird

spec

ies a

naly

zed

with

Wilc

oxon

sign

ed-r

ank

test

).

257


ble

5. T

otal

num

ber

of b

reed

ing

pairs

of 2

2 w

ater

bird

s thr

ough

out t

he d

elta

, cha

nge

in th

e to

tal b

reed

ing

popu

latio

n, a

nd c

onco

rdan

ce (C

on.)

of th

is ch

ange

with

the

resu

lts

give

n in

Tab

les 3

and

4 (↓

: dec

reas

ing,

↑: i

ncre

asin

g, @

: sta

ble, ↓↑

: fluc

tuat

ing,

NA

: not

app

licab

le).

The

obse

rved

or e

stim

ated

reas

ons f

or c

hang

e or

disc

repa

ncy

of th

e re

sults

ar

e al

so e

xpla

ined

.

Spec

ies

Tota

l # o

f br

eedi

ng p

airs

(min

–max

)

Obs

erve

dch

ange

s in

bree

ding

pai

rs

Obs

erve

d ch

ange

s in

bree

ding

pai

rsC

on.

Reas

on fo

r cha

nge

or d

iscre

panc

y

2002

2006

Tota

l bre

ed.

pop.

Und

er

thre

atW

ithou

t th

reat

Podi

ceps

rufic

ollis

13–2

412

–23

@↓

↓N

oA

shift

is o

bser

ved

in b

reed

ing

loca

tions

.

Pelec

anus

crisp

us23

–23

75–7

5↑

↓↑↑

Yes

Succ

essf

ul co

loni

zatio

n in

grid

s with

out t

hrea

t.

Ixob

rych

us m

inut

us5–

157–

19@

↓↓

No

A sh

ift is

obs

erve

d in

bre

edin

g lo

catio

ns.

Cico

nia

cicon

ia16

9↓

↓N

AYe

sLo

ss o

f sui

tabl

e for

agin

g an

d br

eedi

ng h

abita

ts d

ue to

the t

hrea

ts; s

topp

ed b

reed

ing

in U

TM g

rids u

nder

thre

at.

Tado

rna

ferr

ugin

ea31

–40

27–3

9@

@↓

Yes

Spec

ies s

eem

s not

to b

e aff

ecte

d by

the

thre

ats b

ut a

shift

is o

bser

ved

in b

reed

ing

loca

tions

out

of t

hrea

t.

Tado

rna

tado

rna

30–3

426

–34

@↓

↓N

oA

shift

is o

bser

ved

in b

reed

ing

loca

tions

.

Gal

linul

a ch

loro

pus

16–3

050

–62

↑↑

↓↑

↓N

oIn

crea

se in

suita

ble f

orag

ing-

bree

ding

hab

itats

due

to eu

troph

icat

ion

in b

reed

ing

loca

tions

.

Fulic

a at

ra27

–39

15–2

1↓

↓↓

Yes

Loss

of s

uita

ble

fora

ging

and

bre

edin

g ha

bita

ts.

Hae

mat

opus

ostr

aleg

us19

–28

25–3

1@

↓↑

Yes

A sh

ift is

obs

erve

d in

bre

edin

g lo

catio

ns d

ue to

disc

harg

es o

f sew

age

trea

tmen

t pla

nt.

Him

anto

pus h

iman

topu

s34

0–42

013

0–15

2↓↓

↓↓

Yes

Loss

of s

uita

ble

fora

ging

and

bre

edin

g ha

bita

ts d

ue to

thre

ats.

Recu

rviro

stra

avos

etta

107–

121

24–2

8↓↓

↓↓

Yes

Stro

ngly

affe

cted

by

wat

er-le

vel c

hang

e in

salte

rns.

Burh

inus

oed

icnem

us20

–32

31–4

5↑

↓@

No

A sh

ift is

obs

erve

d in

bre

edin

g lo

catio

ns.

Gla

reol

a pr

atin

cola

54–6

236

–42

↓↓

↓↑

Yes

Loss

of s

uita

ble

bree

ding

hab

itats

due

to th

reat

s.

Char

adriu

s alex

andr

inus

220–

300

214–

253

↓↓

@Ye

sC

ore

bree

ding

hab

itat i

s los

t due

to se

wag

e du

mpi

ng; s

topp

ed b

reed

ing

in U

TM g

rids u

nder

thre

at.

Vane

llus s

pino

sus

41–4

943

–48

@↓

@N

oA

shift

is o

bser

ved

in b

reed

ing

loca

tions

due

to u

rban

izat

ion.

Trin

ga to

tanu

s17

–26

30–3

7↑

↓↑

No

Poss

ible

obs

erve

r bia

s due

to m

ore

expe

rienc

e w

ith th

e sp

ecie

s.

Laru

s mela

noce

phal

us79

4–83

010

30–1

100

↑↓

↓N

oA

shift

is o

bser

ved

in b

reed

ing

loca

tions

, and

sew

age

trea

tmen

t fac

ility

crea

ted

new

fora

ging

site

s.

Laru

s mich

ahell

is16

10–1

920

1253

–150

2↓↓

↓↓

Yes

Loss

of b

reed

ing

habi

tats

due

to th

reat

s; st

oppe

d br

eedi

ng in

UTM

grid

s und

er th

reat

.

Ster

na sa

ndvi

cens

is51

–53

63–6

6↑

↓↑↑

Yes

Succ

essf

ul co

loni

zatio

n in

grid

s with

out t

hrea

t.

Ster

na h

irund

o18

00–2

040

1660

–192

0↓

↓↓↑

Yes

Loss

of s

uita

ble

fora

ging

and

bre

edin

g ha

bita

ts d

ue to

thre

ats;

stop

ped

bree

ding

in U

TM g

rids u

nder

thre

at.

Ster

na a

lbifr

ons

386–

438

669–

776

↑↑

↓N

oA

shift

is o

bser

ved

in b

reed

ing

loca

tions

due

to m

anag

emen

t of b

reed

ing

sites

.

Ster

na n

ilotic

a20

–22

0–10

↓↓

NA

Yes

Cor

e br

eedi

ng h

abita

t is l

ost d

ue to

sew

age

dum

ping

; sto

pped

bre

edin

g in

UTM

grid

s und

er th

reat

.

258


4. Discussion Despite Gediz Delta’s significance for biodiversity, particularly for waterbirds, 151 (49.5%) UTM grids out of 305 surveyed were under various threats, mainly due to the lack of appropriate protection statuses, measures, and management activities, as in many other IBAs in the world (Long et al., 2007; Buchanan et al., 2009; Ma et al., 2009; Mwangi et al., 2010). Our findings that 28 (9.3%), 27 (8.9%), and 79 (26.0%) of the grids surveyed were under urbanization, industrialization, and pollution threats, respectively, support previous studies that found that the urban development of the İzmir metropolitan area was a major threat (Eken, 1997; Onmuş et al., 2002, 2009; Dogru et al., 2009; Onmuş and Sıkı, 2010, 2011). Urban development threatens biodiversity in many countries (McKinney, 2002; Pauchard et al., 2006). In our study area, urban development was observed to concentrate around the urban core and transform the adjacent lands, as in other developing countries (Lambin et al., 2001; McGranahan and Satterthwaite, 2003). The urban development in our study area that resulted in the disappearance or deterioration of natural ecosystems including coastal and salty marshes, sand, and mud flats seemed to have the greatest effect on the abundance and distribution of the waterbirds analyzed (Eken, 1997; Adam, 2002; Onmuş et al., 2002, 2009; Onmuş and Sıkı, 2010, 2011; this study).

It is generally accepted that bird atlas studies repeated in several-year intervals are very effective tools to indicate the change in distributions and levels of abundance of bird communities (Gibbons et al., 2007; Pomeroy et al., 2008). In both the areas under threat and the areas without threat, the mean total number of breeding waterbirds has significantly decreased, while the total number of breeding bird species overall stayed constant or increased. This might be attributed to the replacement of native species with nonnative species, which could be regarded as a consequence of urban development causing biological homogenization (Blair and Launer, 1997; Blair, 2001). It has been underlined by several researchers that habitat loss has been the main factor causing bird extinction in recent years (Sisk et al., 1994; Bibby, 1995; Fahrig, 2001). However, breeding waterbirds are more affected by habitat change and fragmentation than many other bird species, and are therefore regarded as sentinel species for detecting these changes (Ma et al., 2009; Rais et al., 2010).

Out of 30 waterbirds, 23 shifted their breeding locations from the UTM grids under threat into the grids without threat. Decisions made by the species that shifted their breeding grounds and preserved their populations might be interpreted as a success; nevertheless, those species that change their breeding distributions and colonize in new areas could pose competitive risks for the already resident species in locations that show more or less stable

distributions. These threats not only may deteriorate the optimal breeding habitats of those species, but also possibly decrease the biomass of the natural habitats, resulting in decreasing food availability. Birds are known to react to habitat degradation and food limitation in 2 ways: “(i) birds remaining in their usual areas have decreased breeding success; and (ii) those shifting to new breeding areas could show higher rates of growth and survival if those areas are optimal for breeding” (Williams et al., 1993). As a result, sensitive species would possibly be affected negatively, while dominant and expanding species are likely to benefit from these new conditions. In addition, the observed shifts occurring in the populations of breeding waterbirds would have further negative impacts on the deserted wetland and its aquatic plants, since metapopulations of wetland organisms and dispersal of aquatic plants are known to be highly dependent on transport by wetland animals (Gibbs, 1993, 2000; Semlitsch and Body, 1998). Comparisons of the total breeding populations of waterbirds throughout the delta with the stratified analyses are in agreement that 13 waterbird species have decreased. By contrast, the total numbers of breeding pairs of 9 waterbird species throughout the delta are not in concordance with the stratified analyses, although part of their breeding area was under threat in 2002. Among these species, the total breeding populations of 4 (Little Grebe Podiceps ruficollis, Little Bittern Ixobrycus minutus, Ruddy Shelduck Tadorna tadorna, and Spur-winged Lapwing Vanellus spinosus) were stable, but their breeding locations inside the delta shifted. Six species moderately increased their breeding population. Among these, Moorhen Gallinula cloropus, Stone Curlew Burhinus oedicnemus, and Little Tern Sterna albifrons changed their breeding locations from grids under threat in 2002 to other grids without threat and successfully recolonized in those new areas. Finally, the observed increase in the total breeding population is possibly due to observer bias (due to increased knowledge about breeding biology) for Common Redshank Tringa totanus. As for Dalmatian Pelican Pelecanus crispus, our special conservation efforts were the underlying reasons for its significant increase (Onmuş et al., 2011). Urbanization, industrialization, pollution, overgrazing, and disturbance are rapidly growing causes of many environmental problems in the delta, as in many other wetlands in the Mediterranean (Battisti et al., 2008). The results of the analyses indicated that total breeding populations of 8 species out of 22 were influenced by the threats. Moreover, these threats not only affected the populations of species breeding in grids under threat, but also the remaining populations of breeding species in other grids.

The populations of some of those waterbird species might also be partially affected by other factors independent of the local threat context that might have caused

259


significant fluctuations in numbers. These independent factors may be either local or not local. Local factors that could play a part are possible changes in management practices (Wilson et al., 2004), the water level of both salt pans (Onmuş and Sıkı, 2011), and decreased water levels due to climatic conditions (De Zan et al., 2011). Nonlocal factors that could be responsible are other threats possibly affecting some of those species in their wintering sites (Durell et al., 1997), in their migration routes (Piersma and Lindstrom, 2004), and/or climate change (Hughes, 2000; McCarty, 2002; Walther et al., 2002; Root et al., 2003; Chen et al., 2011).

In this study we investigated BBS results from 2 different years and quantified species richness and distribution to identify the effects of threats on breeding waterbirds. Our findings indicated strong evidence that the threats have significantly affected the breeding populations of waterbird species in a short period of 4 years. Our results demonstrated that these threats did not affect every species in the same way. The observed reductions in the ranges of some of the breeding species have put them under the risk of local extinction, whereas some others are possibly increasing their distributional areas. However, population-level effects should also be investigated to further support these findings.

Many local people and conservationists perceive the existence of the city of İzmir next to the Gediz Delta as a threat, while many of the managers and key

stakeholders in the city perceive the existence of the delta as a threat against the economic development of the city. If the sustainable use of Gediz Delta is achieved through conservation of its existing wetland habitats and their ecological characters, it will not only be beneficial for the existing biodiversity, but also will offer more socially and environmentally sustainable urban development for the metropolitan area as well, since the wetland and the range of services it provides (such as flood control, shoreline stabilization, storm protection, water purification, groundwater replenishment, and recreation and tourism) are essential elements of the supporting infrastructure of urban settlements. As conservation measures, we propose to stop further development and sludge and house-waste dumping on the natural habitats, and to regulate human activities in the delta. The restoration of habitats that have been damaged due to sludge and house-waste dumping would also be beneficial. We suggest that the results of this study will help managers to set priorities, to allocate their resources, and to determine appropriate actions during wetland management planning.

AcknowledgmentsWe thank Dr Raika Durusoy for her advice on statistical matters. We also wish to acknowledge the many helpful comments and suggestions that we received from 2 anonymous reviewers.

Appendix

A) Possible breeding:1. Species observed in breeding season in suitable

nesting habitat.2. Singing male present (or breeding calls heard) in

breeding season in suitable breeding habitat.B) Probable breeding:3. Pair observed in suitable nesting habitat in breeding

season.4. Permanent territory presumed through registration

of territorial behavior (song, etc.) on at least 2 different days a week or more apart at the same place, or many individuals on 1 day.

5. Courtship and display (judged to be in or near potential breeding habitat; treated cautiously with wildfowl).

6. Visiting probable nest site.7. Agitated behavior or anxiety calls from adults,

suggesting probable presence of nest or young nearby.

8. Brood patch on adult examined in the hand, suggesting incubation.

9. Nest building or excavating nest-hole.C) Confirmed breeding:10. Distraction display or injury-feigning.11. Used nest or eggshells found (occupied or laid within

period of survey).12. Recently fledged young (nidicolous species) or downy

young (nidifugous species). Careful consideration should be given to the likely provenance of any fledged juvenile capable of significant geographical movement. Evidence of dependency on adults (e.g., feeding) is helpful. Be cautious, even if the record comes from suitable habitat.

13. Adults entering or leaving nest site in circumstances indicating occupied nest (including high nests or nest holes, the contents of which cannot be seen) or adults seen incubating.

14. Adult carrying fecal sac or food for young.15. Nest containing eggs.16. Nest with young seen or heard.

260


References

Adam, P. 2002. Saltmarshes in a time of change. Environ. Conserv. 29: 39–61.

Battisti, C.I., Luiselli, L., Pantano, D. and Teofili, C. 2008. On threats analysis approach applied to a Mediterranean remnant wetland: is the assessment of human-induced threats related to different level of expertise of respondents? Biodiv. Conserv. 16: 1529–1542.

Bibby, C.J. 1995. Recent, past, and future extinctions in birds. Philosophical Transactions of the Royal Society of London Series B 344(1307): 35–40.

Bibby, C.J., Burgess, D.N., Hill, A.D. and Mustoe, S. 2000. Bird Census Techniques, 2nd ed., Academic Press, London.

BirdLife International. 2004. Birds in Europe, Population Estimates, Trends, and Conservation Status (BirdLife Conservation Series 12). BirdLife International, Cambridge, UK.

Blair, R.B. and Launer, A.E. 1997. Butterfly diversity and human land use: species assemblages along an urban gradient. Biol. Conserv. 80: 113–125.

Blair, R.B. 2001. Birds and butterflies along urban gradients in two ecoregions of the U.S. In: Biotic Homogenization (Eds. J.L. Lockwood and M.L. McKinney). Kluwer, Norwell, MA, USA, pp. 33–56.

Brooks, T.M., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B., Rylands, A.B., Konstant, W.R., Flick, P., Pilgrim, J., Oldfield, S., Magin, G. and Hilton-Taylor, C. 2002. Habitat loss and extinction in the hotspots of biodiversity. Conserv. Biol. 16: 909–923.

Buchanan, G.M., Donald, P.F., Fishpool, L.D.C., Arinaitwe, J.A., Balman, M. and Mayaux, P. 2009. An assessment of land cover and threats in Important Bird Areas in Africa. Bird Conserv. Int. 19: 49–61.

Chen, I.C., Hill, J.K., Ohlemüller, R., Roy, D.B. and Thomas, C.D. 2011. Rapid range shifts of species associated with high levels of climate warming. Science 333: 1024–1026.

De Zan, L.R., Battisti, C. and Carpaneto, G. 2011. Inter-annual and intra-seasonal patterns of abundance in a set of common waterbirds: a long term study in a Mediterranean wetland. Vie Milieu 61(2): 101–106.

Dogru, A.O., Balcik, F.B., Sanli, F.B., Goksel, C. and Ulugtekin, N. 2009. A change detection analysis in the Izmir Bird Paradise: integration of remote sensing and geographic information system. Fresen. Environ. Bull. 18: 51–56.

Durell, S., Gosscustard, J.D. and Clarke, R.T. 1997. Differential response of migratory subpopulations to winter habitat loss. J. Appl. Ecol. 34: 1155–1164.

Eken, G. 1997. The breeding population of some species of waterbirds at Gediz Delta, western Turkey. Zool. Middle East. 14: 53–68.

Eken, G., Bozdoğan, M., İsfendiyaroğlu, S., Kılıç, D.T. and Lise, Y. (Eds.) 2006. [Key Biodiversity Areas of Turkey]. Doğa Derneği, Ankara, pp. 186–187 (in Turkish).

Fahrig, L. 2001. How much habitat is enough? Biol. Conserv. 100(2001): 65–74.

Gibbons, D.W., Donald, P.F., Bauer, H.G., Fornasari, L. and Dawson, I.K. 2007. Mapping avian distributions: the evolution of bird atlases. Bird Study 54: 324–334.

Gibbs, J.P. 1993. Importance of small wetlands for the persistence of local populations of wetland-associated animals. Wetlands 13: 25–31.

Gibbs, J.P. 2000. Wetland loss and biodiversity conservation. Conserv. Biol. 14: 314–317.

Gilbert, G., Gibbons, D.W. and Evans, J. 1998. Bird Monitoring Methods: A Manual of Techniques for Key UK Species. The Royal Society for the Protection of Birds, Spectrum Flair Press, London.

Greuter, W. 1994. Extinctions in Mediterranean areas. Philos. T. Roy. Soc. B 344: 41–46.

Hagemeijer, E.J.M. and Blair, M.J. (Eds.) 1997. The EBCC Atlas of European Breeding Birds: Their Distribution and Abundance. T. & A.D. Poyser, London.

Hughes, L. 2000. Biological consequences of global warming: is the signal already apparent? Trends Ecol. Evol. 15: 56–61.

Kılıç, D.T. and Eken, G. (Eds.) 2004. [Important Bird Areas of Turkey, 2004 Update]. Doğa Derneği, Ankara (in Turkish).

Lambin, E.F., Turner, B.L., Geist, H.J., Agbola, S., Angelsen, A., Bruce, J.W., Coomes, O., Dirzo, R., Fischer, G., Folke, C., George, P.S., Homewood, K., Imbernon, J., Leemans, R., Li, X., Moran, E.F., Mortimore, M., Ramakrishnan, P.S., Richards, J.F., Skanes, H., Steffen, W., Stone, G.D., Svedin, U., Veldkamp, T., Vogel, C. and Xu, J. 2001. The causes of land-use and land-cover change: moving beyond the myths. Global Environ. Chang. 11: 261–269.

Long, P.R., Szekely, T., Kershaw, M. and O’Connell, M. 2007. Ecological factors and human threats both drive wildfowl population declines. Animal Conserv. 10: 183–191.

Ma, Z.J., Wang, Y., Gan, X.J., Li, B., Cai, Y.T. and Chen, J.K. 2009. Waterbird population changes in the wetlands at Chongming Dongtan in the Yangtze River Estuary, China. J. Environ. Manage. 43: 1187–1200.

McCarty, J.P. 2002. Ecological consequences of recent climate change. Conserv. Biol. 15: 320–331.

McGranahan, G. and Satterthwaite, D. 2003. Urban centres: an assessment of sustainability. Annu. Rev. Env. Resour. 28: 243–274.

McKinney, M.L. 2002. Urbanization, biodiversity, and conservation. Bioscience 52: 883–890.

Millennium Ecosystem Assessment, 2005a. Ecosystems and Human Well-being: Wetlands and Water: Synthesis. World Resources Institute, Washington, DC.

Millennium Ecosystem Assessment, 2005b. Ecosystems and Human Well-being: Synthesis. Island Press, Washington, DC.

261


Mwangi, M.A.K., Butchart, S.H.M., Munyekenye, F.B., Bennun, L.A., Evans, M.I., Fishpool, L.D.C., Kanyanya, E., Madindou, I., Machekele, J., Matiku, P., Mulwa, R., Ngari, A., Siele, J. and Stattersfield, A.J. 2010. Tracking trends in key sites for biodiversity: a case study using Important Bird Areas in Kenya. Bird Conserv. Int. 20: 215–230.

Myers, N., Mittermeier, R.A., Mittermeier, C.G., Da Fonseca, G.A.B. and Kent, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853–858.

Pauchard, A., Aguayo, M., Pena, E. and Urrutia, R. 2006. Multiple effects of urbanization on the biodiversity of developing countries: the case of a fast-growing metropolitan area (Concepcion, Chile). Biol. Conserv. 127: 272–281.

Piersma, T. and Lindstrom, A. 2004. Migrating shorebirds as integrative sentinels of global environmental change. Ibis 146: 61–69.

Olson, D.M. and Dinerstein, E. 1998. The Global 200: a representation approach to conserving the Earth’s most biologically valuable ecoregions. Conserv. Biol. 12: 502–515.

Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N., Underwood, E.C., D’Amico, J.A., Itoua, I., Strand, H.E., Morrison, J.C., Loucks, C.J., Allnutt, T.F., Ricketts, T.H., Kura, Y., Lamoreux, J.F., Wettengel, W.W., Hedao, P. and Kassem, K.R. 2001. Terrestrial ecoregions of the world: a new map of life on Earth. BioScience 51: 933–938.

Onmuş, O., Durusoy, R. and Eken, G. 2009. Distribution of breeding birds in the Gediz Delta, western Turkey. Zool. Middle East. 47: 39–48.

Onmuş, O. and Sıkı, M. 2010. State of the breeding birds in Gediz Delta: distributions, abundances, and changes in bird populations. Bird Census News 23(1–2): 59–69.

Onmuş, O. and Sıkı, M. 2011. Shorebirds in the Gediz Delta (İzmir, Turkey): breeding and wintering abundances, distributions, and seasonal occurrences. Turk. J. Zool. 35(5): 615–629.

Onmuş, O., Sıkı, M., Sarıgül, G. and Crivelli, A. 2011. Status and development of the threatened Dalmatian pelican, Pelecanus crispus, in Turkey. Zool. Middle East. 54: 3–17.

Onmuş, O., Tırıl, A., Durusoy, R., Eken, G., Arsan, Z. and Bilge, O. 2002. [Recommendations for Gediz Delta Management Plan]. In: Proceedings of the 4th National Conference on Coastal and Marine Areas in Turkey, 5–8 November 2002, İzmir (in Turkish).

Pimm, S.L. and Raven, P. 2000. Biodiversity: extinction by numbers. Nature 403: 843–845.

Pimm, S.L., Russell, G.J., Gittleman, J.L. and Brooks, T.M. 1995. The future of biodiversity. Science 269: 347–350.

Pomeroy, D., Tushabe, H. and Cowser, R. 2008. Bird atlases – how useful are they for conservation? Bird Conserv. Int. 18: 211–222.

Rais, M., Kabeer, B., Anwar, M. and Mehmood, T. 2010. Effect of habitat degradation on breeding waterbirds at Kallar Kahar Lake District Chakwal. J. Anim. Plant. 20(4): 318–320.

Root, T.L., Price, J.T., Hall, K.R., Schneider, S.H., Rosenzweigk, C. and Pounds, J.A. 2003. Fingerprints of global warming on wild animals and plants. Nature 421: 57–60.

Salafsky, N., Margoluis, R.I., Redford, K.H. and Robinson, J.G. 2002. Improving the practice of conservation: a conceptual framework and research agenda for conservation science. Conserv. Biol. 16: 1469–1479.

Salafsky, N., Salzer, D., Stattersfield, A.J., Hilton-Taylor, C., Neugarten, R., Butchart, S.H.M., Collen, B., Cox, N., Master, L.L., O’Connor, S. and Wilkie, D. 2008. A standard lexicon for biodiversity conservation: unified classifications of threats and actions. Conserv. Biol. 22(4): 897–911.

Semlitsch, R.D. and Body, J.R. 1998. Are small isolated wetlands expendable? Conserv. Biol. 12: 1113–1119.

Sisk, T.D., Launer, A.E., Switky, K.R. and Ehrlich, P.R. 1994. Identifying extinction threats. BioScience 44(9): 592–604.

Sutherland, W.J. 2006. A Handbook: Ecological Census Techniques. Cambridge University Press, Cambridge.

Underwood, E.C., Viers, J.H., Klausmeyer, K.R., Cox, R.L. and Shaw, M.R. 2009. Threats and biodiversity in the Mediterranean biome. Divers. Distrib. 15: 188–197.

Venter, O., Brodeur, N.N., Nemiroff, L., Belland, B., Dolinsek, I.J. and Grant, J.W.A. 2006. Threats to endangered species in Canada. BioScience 56(11): 903–910.

Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Fromentin, J.M., Hoegh-Guldberg, O. and Bairlein, F. 2002. Ecological responses to recent climate change. Nature 416: 389–395.

Williams, T.D., Cooch, E.G., Jefferies, R.L. and Cooke, F. 1993. Environmental degradation, food limitation and reproductive output: juvenile survival in lesser snow geese. J. Anim. Ecol. 62(4): 766–777.

Wilson, A.M., Ausden, M. and Milsom, T.P. 2004. Changes in breeding wader populations on lowland wet grasslands in England and Wales: causes and potential solutions. Ibis 146: 32–40.

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