SUPPORTING INFORMATION
Habitat fragmentation and the species–area relationship: a focus on total species richness
obscures the impact of habitat loss on habitat specialists
Thomas J. Matthews, H. Eden W. Cottee‐Jones, Robert J. Whittaker
Diversity and Distributions
Appendix S1 Source paper information and species classification methodology
Table S1 Description of the source papers. The habitat island type in each case was forest.
The full references follow the table.
Study
Location
Brazil
No. of
hab. isl.
7
No. of
sp.
100
Area range
(Ha)
15-350
1. Anciães & Marini
(2000)
2. Blake & Karr(1984)
3. Castelletta et al. (2005)
USA
Singapore
12
10
26
132
1.8-600
7-935
4-24
49-98
Poland
50
50
0.04-15.44
0-37
Brazil
12
119
0.5-10
45-92
UK
USA
Costa Rica
20
10
7
48
31
69
0.14-18
0.01-24
420-16804
13-35
0-31
20-45
Australia
13
127
24-73
Ghana
15
147
Madagascar
Brazil
France
Norway
Spain
UK
UK
Peru
Finland
8
6
40
41
42
37
16
5
35
51
145
47
55
47
43
49
52
45
0.00020.2044
236058790
0.64-1250
7.5-230
0.11-150
0.2-150
0.06-110
0.5-172
0.74-14.51
4.3-82
0.4-101
Mexico
South Africa
17
9
129
55
22. Wethered & Lawes
(2005) - Gilgoa
South Africa
9
23. Willson et al. (1994)
Chile
10
4. Cieślak &
Dombrowski (1993)
5. dos Anjos & Boçon
(1999)
6. Ford (1987)
7. Forman (1976)
8. Gillespie & Walter
(2001)
9. Hannah et al.(2007)
10. Holbech (1995)
11. Langrand (1995)
12. Marini (2001)
13. This study
14. This study
15. This study
16. This study
17. McCollin (1993)
18. Ríos et al. (2011)
19. Simberloff & Martin
(1991)
20. Watson (2003)
21. Wethered & Lawes
(2005) - Balgowan
Richness Matrix type
range
17-25
Agriculture
80-117
Agriculture
Urban &
Grassland
Agriculture
Grassland
Agriculture
Agriculture
Agriculture
Agriculture
Savannah
15-51
46-103
5-40
2-32
6-34
4-32
12-32
15-28
0-30
Grassland
Agriculture
Agriculture
Agriculture
Agriculture
Agriculture
Agriculture
Grassland
2-159242
0.5-215
4-78
23-49
52
0.5-273
28-39
25
0.5-350
8-20
Scrub
Grassland
&
Plantation
Grassland
&
Plantation
Agriculture
Agriculture
Source papers:
Anciães, M. & Marini, M.Â. (2000) The effects of fragmentation on fluctuating asymmetry in
passerine birds of Brazilian tropical forests. Journal of Applied Ecology, 37, 1013–1028.
Blake, J.G. & Karr, J.R. (1984) Species composition of bird communities and the conservation
benefit of large versus small forests. Biological Conservation, 30, 173–187.
Castelletta, M., Thiollay, J.-M. & Sodhi, N.S. (2005) The effects of extreme forest
fragmentation on the bird community of Singapore Island. Biological Conservation, 121,
135–155.
Cieślak, M. & Dombrowski, A. (1993) The effect of forest size on breeding bird communities.
Acta Ornithologica, 27, 97–111.
dos Anjos, L. & Boçon, R. (1999) Bird communities in natural forest patches in Southern
Brazil. The Wilson Bulletin, 111, 397–414.
Ford, H.A. (1987) Bird communities on habitat islands in England. Bird Study, 34, 205–218.
Forman, R.T.T., Galli, A.E. & Leck, C.F. (1976) Forest size and avian diversity in New Jersey
woodlots with some land use implications. Oecologia, 26, 1–8.
Gillespie, T.W. & Walter, H. (2001) Distribution of bird species richness at a regional scale in
tropical dry forest of Central America. Journal of Biogeography, 28, 651–662.
Hannah, D., Woinarski, J.C.Z., Catterall, C.P., McCosker, J.C., Thurgate, N.Y. & Fensham,
R.J. (2007) Impacts of clearing, fragmentation and disturbance on the bird fauna of Eucalypt
savanna woodlands in central Queensland, Australia. Austral Ecology, 32, 261–276.
Holbech, L.H. (2005) The implications of selective logging and forest fragmentation for the
conservation of avian diversity in evergreen forests of south-west Ghana. Bird Conservation
International, 15, 27–52.
Langrand, O. (1995) The effects of forest fragmentation on bird species in Madagascar: a case
study from Ambohitantely Forest Reserve on the central high plateau. University of Natal,
Pietermaritzburg.
Marini, M.Â. (2001) Effects of forest fragmentation on birds of the cerrado region, Brazil.
Bird Conservation International, 11, 13–25.
McCollin, D. (1993) Avian distribution patterns in a fragmented wooded landscape (North
Humberside, U.K.): the role of between-patch and within-patch structure. Global Ecology
and Biogeography Letters, 3, 48–62.
Ríos, S.S., Lloyd, H. & Valdés-Velásquez, A. (2011) Bird species richness, diversity and
abundance in Polylepis woodlands, Huascaran biosphere reserve, Peru. Studies on
Neotropical Fauna and Environment, 46, 69–76.
Simberloff, D. & Martin, J.L. (1991) Nestedness of insular avifaunas: simple summary
statistics masking complex species patterns. Ornis Fennica, 68, 178–192.
Watson, D.M. (2003) Long-term consequences of habitat fragmentation-highland birds in
Oaxaca, Mexico. Biological Conservation, 111, 283–303.
Wethered, R. & Lawes, M.J. (2005) Nestedness of bird assemblages in fragmented
Afromontane forest: the effect of plantation forestry in the matrix. Biological Conservation,
123, 125–137.
Willson, M.F., De Santo, T.L., Sabag, C. & Armesto, J.J. (1994) Avian communities of
fragmented south-temperate rainforests in Chile. Conservation Biology, 8, 508–520.
Species classification method and references
To classify species into specialists and generalists we used a combination of books, articles,
online reference databases and expert opinion. The books were largely accessed through the
Alexander Library of Ornithology, University of Oxford. Where necessary, articles were
obtained through a literature search using combinations of the following keywords: “birds”,
“habitat specialisation”, “forest specialists”, “habitat specificity” and a given region, for
example “South America”. A number of studies (e.g. Anciães & Marini, 2000; Salisbury et
al., 2012) had already classified a large number of species based on habitat specificity (e.g.
Salisbury et al., 2012, classified 739 species in the Amazon), which provided us with a
resource with which to compare with our own classifications. Finally, we also consulted a
number of ornithological experts for additional opinions on particular species.
The following references relate to the core source material used to classify the species
in our datasets. A large number of additional books, articles (found using the aforementioned
keywords and from the reference lists of sourced papers) and other sources of identification
material from the Alexander Library and the wider literature were referenced for individual
species information and are not included here:
Alonso, J.A. & Whitney, B.M. (2003) New distributional records of birds from white-sand
forests of the northern Peruvian Amazon, with implications for biogeography of
northern South America. The Condor, 105, 552–566.
Anciães, M. & Marini, M.Â. (2000) The effects of fragmentation on fluctuating asymmetry in
passerine birds of Brazilian tropical forests. Journal of Applied Ecology, 37, 1013–
1028.
Birdlife (2011) Birdlife data zone. Available at: http://www.birdlife.org/datazone/home.
Borges, S.H., Cohn-Haft, M., Carvalhaes, A.M.P., Henriques, L.M., Pacheco, J.F. &
Whittaker, A. (2001) Birds of Jaú national park, Brazilian Amazon: Species checklist, biogeography and conservation. Ornitologia Neotropical, 12, 109–140.
Borrow, N. & Demey, D. (2010) Birds of Ghana. Christopher Helm, London.
Brooker, M.G., Braithwaite, R.W. & Estbergs, J.A. (1990) Foraging ecology of some
insectivorous and nectarivorous species of birds in forests and woodlands of the wetdry tropics of Australia. Emu, 90, 215–230.
Christiansen, M.B. & Pitter, E. (1997) Species loss in a forest bird community near Lagoa
Santa in South Eastern Brazil. Biological Conservation, 80, 23–32.
Cohn-Haft, M., Whittaker, A. & Stouffer, P.C. (1997) A new look at the "species-poor"
Central Amazon: the avifauna north of Manaus, Brazil. Ornithological Monographs,
48, 205–235.
Cramp, S. (ed.) (1980) Handbook of the birds of Europe, the Middle East, and North Africa:
the birds of the Western Palearctic. Vol. 2, Hawks to bustards. Oxford University
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Cramp, S. (ed.) (1985) Handbook of the birds of Europe, the Middle East, and North Africa:
the birds of the Western Palearctic. Vol. 4 Terns to woodpeckers. Oxford University
Press, Oxford.
Cramp, S. (ed.) (1988) Handbook of the birds of Europe, the Middle East, and North Africa:
the birds of the Western Palearctic. Vol. 5 Tyrant flycatchers to thrushes. Oxford
University Press, Oxford.
Cramp, S. & Brooks, D.J. (eds.) (1992) Handbook of the birds of Europe, the Middle East,
and North Africa: the birds of the Western Palearctic. Vol. 6 Warblers. Oxford
University Press, Oxford.
Cramp, S. & Perrins, C.M. (eds.) (1993) Handbook of the birds of Europe, the Middle East,
and North Africa: the birds of the Western Palearctic. Vol. 7 Flycatchers to shrikes.
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Cramp, S. & Perrins, C.M. (eds.) (1994b) Handbook of the birds of Europe, the Middle East
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del Hoyo, J. Elliott, A. & Christie, D.A. (eds.) (2004) Handbook of the birds of the world.
Vol. 9. Cotingas to pipits and wagtails. Lynx Edicions, Barcelona.
del Hoyo, J. Elliott, A. & Christie, D.A. (eds.) (2005) Handbook of the birds of the world.
Vol. 10. Cuckoo-shrikes to thrushes. Lynx Edicions, Barcelona.
del Hoyo, J. Elliott, A. & Christie, D.A. (eds.) (2006) Handbook of the birds of the world.
Vol. 11. Old World flycatchers to Old World warblers. Lynx Edicions, Barcelona.
del Hoyo, J. Elliott, A. & Christie, D.A. (eds.) (2007) Handbook of the birds of the world.
Vol. 12. Picathartes to tits and chickadees. Lynx Edicions, Barcelona.
del Hoyo, J. Elliott, A. & Christie, D.A. (eds.) (2008) Handbook of the birds of the world.
Vol. 13. Penduline-tits to shrikes. Lynx Edicions, Barcelona.
del Hoyo, J. Elliott, A. & Christie, D.A. eds. (2009) Handbook of the birds of the world. Vol.
14. Bush-shrikes to Old World sparrows. Lynx Edicions, Barcelona.
del Hoyo, J. Elliott, A. & Christie, D.A. (eds.) (2010) Handbook of the birds of the world.
Vol. 15. Weavers to New World warblers. Lynx Edicions, Barcelona.
del Hoyo, J. Elliott, A. & Christie, D.A. (eds.) (2011) Handbook of the birds of the world.
Vol. 16. Tanagers to New World blackbirds. Lynx Edicions, Barcelona.
Dorst, J. (1972) The evolution and affinities of the birds of Madagascar. Biogeography and
ecology in Madagascar (ed. by R. Battistini and G. Richard-Vindard), pp. 615–627.
Springer, Netherlands.
dos Anjos, L. (2001) Bird communities in five Atlantic forest fragments in southern Brazil.
Ornitologia Neotropical, 12, 11–27.
dos Anjos, L. & Boçon, R. (1999) Bird communities in natural forest patches in Southern
Brazil. The Wilson Bulletin, 111, 397–414.
Dunn, J. & Garrett, K. (1997) A field guide to warblers of North America. Houghton Mifflin,
Boston.
Edwards, E.P. (1998) A field guide to the birds of México and adjacent Areas: Belize,
Guatemala, and El Salvador. University of Texas Press, Austin.
Erize, F., Rodriguez Mata, J.R. & Rumboll, M. (2006) Birds of South America: NonPasserines: rheas to woodpeckers. Princeton University Press, Princeton.
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Ford, H.A. (1987) Bird communities on habitat islands in England. Bird Study, 34, 205–218.
Garrigues, R. & Dean, R. (2007) The birds of Costa Rica. Cornell University Press, New
York.
Grimmett, R., Inskipp, C. & Inskipp, T. (1999) Guide to the birds of India, Pakistan, Nepal,
Bangladesh, Bhutan, Sri Lanka, and the Maldives. Princeton University Press,
Princeton.
Griscom, L. & Greenway, J.C. (1941) Birds of lower Amazonia. Bulletin of the Museum of
Comparative Zoology, 88, 283–344.
Hawkins, A.F.A. (1999) Altitudinal and latitudinal distribution of east Malagasy forest bird
communities. Journal of Biogeography, 26, 447–458.
Holbech, L.H. (2005) The implications of selective logging and forest fragmentation for the
conservation of avian diversity in evergreen forests of south-west Ghana. Bird
Conservation International, 15, 27–52.
Howell, S.N.G. & Webb, S. (1995) A guide to the birds of Mexico and northern central
America. Oxford, Oxford University Press.
Jaramillo, A. (2003) Birds of Chile. Princeton University Press, Princeton.
Jeyarajasingam, A. & Pearson, A. (1999) A field guide to the birds of west Malaysia and
Singapore. Oxford University Press, Oxford.
Krügel, M.M. & dos Anjos, L. (2000) Bird communities in forest remnants in the city of
Maringá, Paraná State, Southern Brazil. Ornitologia Neotropical, 11, 315–330.
Langrand, O. (1990) Guide to the birds of Madagascar. Yale University Press, New Haven.
Langrand, O. (1995) The effects of forest fragmentation on bird species in Madagascar: a
case study from Ambohitantely Forest Reserve on the central high plateau.
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fragmentation: evaluation of species-specific predictions of the impact of habitat
fragmentation on birds in the box–ironbark forests of central Victoria, Australia.
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bird functional diversity in a traditional agroecosystem of Madagascar. Agriculture,
Ecosystems & Environment, 149, 1–9.
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dispersal constraints: ecological specialisation drives diversification in tropical birds.
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Appendix S2 Supplementary Results
Table S2 The c parameter and R2 values of the power ISAR function for 23 bird habitat
island datasets. For each dataset both values are given for the model when fitted to the total
compliment of species, and for specialist and generalist species separately. Dataset
information is presented in Table S1 in Appendix S1.
R2
C
Dataset
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
All
species
18.53
5.29
44.53
9.55
52.75
21.49
17.66
6.95
64.17
47.02
21.08
30.57
9.99
6.60
9.54
8.75
16.52
12.98
6.54
7.27
27.22
30.09
9.01
Specialists Generalists
9.15
2.46
5.41
2.42
19.23
1.76
3.62
0.35
13.66
20.70
7.95
5.89
1.29
1.12
0.62
0.87
2.09
1.94
1.65
2.82
8.59
11.73
3.71
7.25
2.48
41.59
7.18
37.80
19.70
13.87
8.74
36.38
26.9
13.18
25.81
9.14
5.57
9.11
8.04
14.50
16.18
4.94
5.32
18.65
18.36
5.34
All
species
0.28
0.89
0.68
0.95
0.76
0.52
0.90
0.64
0.27
0.54
0.93
0.92
0.77
0.82
0.63
0.74
0.46
0.74
0.81
0.84
0.55
0.41
0.92
Specialists Generalists
0.58
0.88
0.64
0.89
0.78
0.53
0.87
0.88
0.16
0.58
0.90
0.90
0.68
0.79
0.58
0.68
0.32
0.92
0.72
0.86
0.71
0.18
0.82
0.01
0.83
0.41
0.92
0.10
0.45
0.78
0.38
0.21
0.36
0.84
0.93
0.67
0.77
0.48
0.67
0.36
0.08
0.81
0.74
0.40
0.45
0.70
Table S3 Model selection results for all 23 bird–habitat island datasets (generalists and
specialists presented separately). The data presented are the delta (Δ) AICc values. A value of
0 indicates a model provided the best fit accroding to AICc and all models within Δ 2 of the
best model are considered to be in the best model set (i.e. they are argued to have similar
support). Eight models were fit using the ‘mmSAR’ R package (Guilhamon et al., 2010).
‘Expo’ refers to the exponential model, and ‘Neg Expo’ to the negative exponential model.
The Weibull model is the three parameter version. NA refers to cases in which the fitting
process failed to converge.
Generalists
Dataset
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
Power
0.00
3.36
1.15
4.95
1.09
3.75
17.57
0.18
0.00
0.02
1.23
0.00
4.23
8.96
6.43
1.54
1.19
0.00
25.31
0.00
0.00
0.00
0.00
Expo Neg Expo
0.28
5.86
0.00
13.15
0.84
1.14
32.36
14.43
0.95
8.44
2.23
10.49
7.57
21.39
0.08
0.38
0.35
24.99
0.00
6.18
0.00
11.22
1.78
11.80
16.49
33.58
9.32
13.35
15.28
42.28
0.00
13.79
0.73
1.21
0.01
0.18
10.66
4.73
3.16
13.63
0.34
7.43
0.32
14.02
1.74
16.55
Monod
5.86
6.80
0.00
5.45
0.00
0.47
0.00
0.00
2.37
1.93
8.86
8.11
25.92
7.16
33.69
6.16
0.00
0.14
1.03
11.54
3.39
4.55
10.68
Ratio Logistic Weibull Lomolino
5.11
10.57
10.57
8.18
3.71
4.00
3.83
5.59
5.92
5.81
6.00
6.65
0.86
0.04
0.00
3.96
3.16
4.02
3.62
7.12
2.65
3.20
2.13
0.00
22.51
5.53
10.25
12.75
13.93 13.92
13.90
15.25
4.99
4.34
3.79
3.19
5.72
3.80
3.77
6.02
12.17
9.55
9.64
13.87
28.10 30.00
30.00
28.34
0.00
6.70
6.70
0.81
1.37
4.64
3.50
0.00
0.90
8.88
8.88
0.00
3.46
2.54
2.87
5.83
3.61
3.63
3.53
3.47
NA
NA
NA
NA
2.64
3.43
0.90
0.00
0.39
3.49
3.49
12.39
2.31
7.20
7.20
2.35
4.12
7.20
7.20
3.35
2.08
6.00
6.00
2.09
Specialists
Dataset
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
Power
0.14
7.92
9.79
1.53
8.76
0.48
9.62
0.00
0.98
0.00
5.8
0.00
15.78
1.93
0.33
1.31
3.10
0.94
23.12
4.72
0.36
0.00
0.00
Expo Neg Expo
0.00
7.70
2.36
6.15
6.91
0.00
26.03
4.43
7.79
0.00
0.00
2.95
15.22
0.00
1.89
4.22
0.51
13.22
0.07
9.64
0.00
17.18
2.79
7.94
25.9
1.83
14.6
2.34
5.88
0.25
6.67
1.14
1.81
0.00
0.00
3.45
10.13
0.00
10.94
3.29
0.00
7.10
0.05
17.28
0.63
11.14
Monod
6.05
0.76
2.87
0.00
1.08
1.39
1.62
2.91
0.00
3.47
12.99
5.47
2.41
0.00
0.00
0.00
0.88
1.12
4.05
4.25
2.60
1.74
7.93
Ratio Logistic Weibull Lomolino
1.73
4.48
4.29
10.83
0.00
1.88
1.08
1.96
8.83
8.38
5.99
5.24
2.35
0.47
1.00
5.97
4.04
5.77
3.96
0.70
4.54
3.65
3.65
6.21
7.54
5.64
5.68
6.00
13.68 14.00
14.00
13.89
7.20
4.23
3.82
4.62
2.74
3.82
3.81
6.13
13.09
9.00
8.71
14.93
26.22 30.00
30.00
26.26
4.81
0.90
0.00
4.29
1.26
1.45
1.67
2.24
1.82
2.15
2.12
1.82
1.70
2.11
2.22
2.10
3.99
3.38
3.30
3.35
NA
NA
NA
NA
4.46
2.40
1.35
1.78
2.68
5.30
4.41
0.00
6.40
6.85
6.89
6.23
6.11
7.20
7.20
5.90
6.90
6.00
6.00
7.03
Figure S1 The derivative plots for all 23 bird–habitat island datasets. In each plot the rate of
change in species richness predicted by a multi-model SAR, in respect to patch area (dY) is
plotted against patch area for habitat specialists (black line) and habitat generalists (red line).
Eight SAR models were used to construct the multi-model SAR (power, exponential,
negative exponential, Monod, ratio, logistic, Weibull-3) using the ‘mmSAR’ R package
(Guilhaumon et al., 2010). The relative position of the curves indicates the rate at which
species richness varies with area. A number of plots have been truncated at the right hand
side to enable easier interpretation. The order of the datasets (a-w) follows the order (1-23) in
Table S1 in Appendix S1. See Appendix S1 for full details for each of the datasets. All areas
are in hectares.
Figure S2 The plots of the ratio of specialist species to generalist species (S:G) plotted
against habitat island area for all 23 bird habitat island datasets. The order of the datasets (aw) follows the order (1-23) in Table S1 in Appendix S1. See Table S1 in Appendix S1 for
full dataset information.