1
2
Figure S1. PRISMA flow diagram for identification and exclusion criteria of studies in included
3
in this review on shrub facilitation, other plant species, and animals. For additional information
4
see www.prisma-statement.org.
5
6
Identification
7
Records identified through
database searching
(n = 89)
Additional records identified
through other sources (grazing)
(n = 2)
Eligibility
Screening
Records after duplicates removed
(n = 79 )
Records screened
(n = 79 )
Records excluded
(n = 42 )
Full-text articles assessed
for eligibility
(n = 79 )
Full-text articles excluded,
with reasons
(n = 42 )
Included
Studies included in
qualitative synthesis
(n = 36 )
Studies included in
quantitative synthesis
(meta-analysis)
(n = NA )
2
1
Appendix S1. The full list of studies used in systematic review on shrub facilitation, other
2
plants, and animal complexes.
3
4
5
Aragon, S. & Woodcock, D.W. (2010) Plant Community Structure and Conservation of a
Northern Peru Sclerophyllous Forest. Biotropica, 42, 262-270.
6
Battaglia, L.L., Denslow, J.S., Inczauskis, J.R. & Baer, S.G. (2009) Effects of native vegetation
7
on invasion success of Chinese tallow in a floating marsh ecosystem. Journal of
8
Ecology, 97, 239-246.
9
10
11
Carlo, T.A. & Tewksbury, J.J. (2014) Directness and tempo of avian seed dispersal increases
emergence of wild chiltepins in desert grasslands. Journal of Ecology, 102, 248-255.
Carmona-Diaz, G. & Garcia-Franco, J.G. (2009) Reproductive success in the Mexican
12
rewardless Oncidium cosymbephorum (Orchidaceae) facilitated by the oil-rewarding
13
Malpighia glabra (Malpighiaceae). Plant Ecology, 203, 253-261.
14
Catorci, A., Tardella, F.M., Cesaretti, S., Bertellotti, M. & Santolini, R. (2012) The interplay
15
among grazing history, plant-plant spatial interactions and species traits affects
16
vegetation recovery processes in Patagonian steppe. Community Ecology, 13, 253-263.
17
Chambers, J.C. (2001) Pinus monophylla establishment in an expanding Pinus-Juniperus
18
woodland: Environmental conditions, facilitation and interacting factors. Journal of
19
Vegetation Science, 12, 27-40.
20
Chaneton, E.J., Mazia, C.N. & Kitzberger, T. (2010) Facilitation vs. apparent competition: insect
21
herbivory alters tree seedling recruitment under nurse shrubs in a steppe-woodland
22
ecotone. Journal of Ecology, 98, 488-497.
23
24
DeWalt, S.J., Denslow, J.S. & Ickes, K. (2004) Natural-enemy release facilitates habitat
expansion of the invasive tropical shrub Clidemia hirta. Ecology, 85, 471-483.
3
1
Duarte, L.D.S., Dos-Santos, M.M.G., Hartz, S.M. & Pillar, V.D. (2006) Role of nurse plants in
2
Araucaria Forest expansion over grassland in south Brazil. Austral Ecology, 31, 520-
3
528.
4
Farris, E. & Filigheddu, R. (2008) Effects of browsing in relation to vegetation cover on common
5
yew (Taxus baccata L.) recruitment in Mediterranean environments. Plant Ecology, 199,
6
309-318.
7
Garcia, D. & Obeso, J.R. (2003) Facilitation by herbivore-mediated nurse plants in a threatened
8
tree, Taxus baccata: local effects and landscape level consistency. Ecography, 26, 739-
9
750.
10
11
12
Gill, D.S. & Marks, P.L. (1991) Tree and shrub seedling colonization of old fields in central New
York. Ecological Monographs, 61, 183-205.
Grau, O., Ninot, J.M., Blanco-Moreno, J.M., van Logtestijn, R.S.P., Cornelissen, J.H.C. &
13
Callaghan, T.V. (2012) Shrub-tree interactions and environmental changes drive treeline
14
dynamics in the Subarctic. Oikos, 121, 1680-1690.
15
16
17
Holl, K.D. (2002) Effect of shrubs on tree seedling establishment in an abandoned tropical
pasture. Journal of Ecology, 90, 179-187.
Holl, K.D., Loik, M.E., Lin, E.H.V. & Samuels, I.A. (2000) Tropical montane forest restoration in
18
Costa Rica: Overcoming barriers to dispersal and establishment. Restoration Ecology, 8,
19
339-349.
20
Iponga, D.M., Milton, S.J. & Richardson, D.M. (2009) Soil type, microsite, and herbivory
21
influence growth and survival of Schinus molle (Peruvian pepper tree) invading semi-arid
22
African savanna. Biological Invasions, 11, 159-169.
23
Maher, K.A., Hobbs, R.J. & Yates, C.J. (2010) Woody shrubs and herbivory influence tree
24
encroachment in the sandplain heathlands of southwestern Australia. Journal of Applied
25
Ecology, 47, 441-450.
4
1
2
3
4
Maron, J.L. & Connors, P.G. (1996) A native nitrogen-fixing shrub facilitates weed invasion.
Oecologia, 105, 302-312.
Maron, J.L. & Jefferies, R.L. (1999) Bush lupine mortality, altered resource availability, and
alternative vegetation states. Ecology, 80, 443-454.
5
McCusker, C.E., Ward, M.P. & Brawn, J.D. (2010) Seasonal responses of avian communities to
6
invasive bush honeysuckles (Lonicera spp.). Biological Invasions, 12, 2459-2470.
7
Milton, S.J., Wilson, J.R.U., Richardson, D.M., Seymour, C.L., Dean, W.R.J., Iponga, D.M. &
8
Proches, S. (2007) Invasive alien plants infiltrate bird-mediated shrub nucleation
9
processes in arid savanna. Journal of Ecology, 95, 648-661.
10
11
12
13
14
15
16
Rafferty, C. & Lamont, B.B. (2007) Selective herbivory by mammals on 19 species planted at
two densities. Acta Oecologica-International Journal of Ecology, 32, 1-13.
Sasal, Y. & Suarez, M.L. (2011) Insect herbivory in climber-host shrubs associations: Benefit or
detriment? Austral Ecology, 36, 814-820.
Schmidt, K.A. & Whelan, C.J. (1999) Effects of exotic Lonicera and Rhamnus on songbird nest
predation. Conservation Biology, 13, 1502-1506.
Seymour, C.L. (2009) Protege Ziziphus mucronata (Rhamnaceae) show no negative effects of
17
competition with the nurse tree Acacia (Leguminaceae), even as adults. Journal of
18
Vegetation Science, 20, 926-934.
19
Smit, C., Vandenberghe, C., den Ouden, J. & Müller-Schärer, H. (2007) Nurse plants, tree saplings and
20
grazing pressure: changes in facilitation along a biotic environmental gradient. Oecologia, 152,
21
265-273.
22
23
24
Smith, A.D. & McWilliams, S.R. (2014) Fruit removal rate depends on neighborhood fruit
density, frugivore abundance, and spatial context. Oecologia, 174, 931-942.
Soliveres, S. & Eldridge, D.J. (2014) Do changes in grazing pressure and the degree of shrub
25
encroachment alter the effects of individual shrubs on understorey plant communities and soil
26
function? Functional Ecology, 28, 530-537.
5
1
2
Sommaggio, D., Paoletti, M.G. & Ragusa, S. (1995) The effects of microhabitat conditions,
3
nutrients and predators on the abundance of herbivores on stinging nettles (Urtica dioica
4
L). Acta Oecologica-International Journal of Ecology, 16, 671-686.
5
Tecco, P.A., Gurvich, D.E., Diaz, S., Perez-Harguindeguy, N.P. & Cabido, M. (2006) Positive
6
interaction between invasive plants: The influence of Pyracantha angustifolia on the
7
recruitment of native and exotic woody species. Austral Ecology, 31, 293-300.
8
van Zonneveld, M.J., Gutierrez, J.R. & Holmgren, M. (2012) Shrub facilitation increases plant
9
10
11
12
13
14
15
diversity along an arid scrubland-temperate rain forest boundary in South America.
Journal of Vegetation Science, 23, 541-551.
Verdu, M. & Garcia-Fayos, P. (2003) Frugivorous birds mediate sex-biased facilitation in a
dioecious nurse plant. Journal of Vegetation Science, 14, 35-42.
Verdu, M. & Garcia-Fayos, P. (1996) Nucleation processes in a Mediterranean bird-dispersed
plant. Functional Ecology, 10, 275-280.
Vieira, I.C.G., Uhl, C. & Nepstad, D. (1994) The role of the shrub Cordia multispicata Cham. as
16
a succession facilitator in an abandoned pasture, Paragominas, Amazonia. Vegetatio,
17
115, 91-99.
18
19
20
Watling, J.I. & Orrock, J.L. (2010) Measuring edge contrast using biotic criteria helps define
edge effects on the density of an invasive plant. Landscape Ecology, 25, 69-78.
Woods, T.M., Jonas, J.L. & Ferguson, C.J. (2012) The invasive Lespedeza cuneata attracts
21
more insect pollinators than native congeners in tallgrass prairie with variable impacts.
22
Biological Invasions, 14, 1045-1059.
23
24
6
1
Table S1. A list of the instances from each study testing facilitation with shrubs that included
2
both other plants and animals (see Methods for full list of search terms) summarized here. A
3
total of 79 articles were returned in searches, 36 studies were appropriate, and 53 independent
4
instances reporting plant facilitation including animals were summarized in this review.
5
Study authors
Hypothesis
Shrub functional role
Animal functional role
Carlo & Tewksbury 2014
dispersal
seed trap
disperser
Smith & McWilliams 2014
resources
seed trap
consumer
Catorci et al. 2012
protection
herbivore protection
consumer
Grau et al. 2012
protection
herbivore protection
consumer
van Zonneveld, Gutiérrez &
Holmgren 2012
Woods, Jonas & Ferguson
2012
Sasal & Suarez 2011
protection
herbivore protection
consumer
magnet
floral resource
pollinator
protection
herbivore protection
consumer
Aragon & Woodcock 2010
protection
herbivore protection
consumer
Chaneton, Mazia &
Kitzberger 2010
Maher, Hobbs & Yates
community
herbivore protection
consumer
protection
herbivore protection
consumer
McCusker, Ward & Brawn
2010
Watling & Orrock 2010
community
habitat
consumer
invasion
habitat
disperser
Battaglia et al. 2009
invasion
seed dispersal
disperser
Carmona-Diaz & GarciaFranco 2009
Iponga, Milton & Richardson
2009
Seymour 2009
magnet
floral resource
pollinator
protection
herbivore protection
consumer
protection
herbivore protection
consumer
Farris & Filigheddu 2008
protection
herbivore protection
consumer
Milton et al. 2007
dispersal
seed dispersal
disperser
Rafferty & Lamont 2007
protection
herbivore protection
consumer
Duarte et al. 2006
dispersal
seed dispersal
disperser
Tecco et al. 2006
dispersal
seed dispersal
consumer
DeWalt, Denslow & Ickes
2004
Garcia & Obeso 2003
invasion
herbivore protection
consumer
protection
herbivore protection
consumer
Verdu & Garcia-Fayos 2003
dispersal
seed trap
disperser
Holl 2002
dispersal
seed trap
disperser
Chambers 2001
protection
herbivore protection
consumer
Holl et al. 2000
dispersal
seed trap
disperser
Maron & Jefferies 1999
resources
resource source
decomposer
7
1
2
Schmidt & Whelan 1999
protection
habitat
none
Maron & Connors 1996
resources
resource source
decomposer
Verdu & Garcia-Fayos 1996
dispersal
seed trap
disperser
Sommaggio, Paoletti &
Ragusa 1995
Vieira, Uhl & Nepstad 1994
resources
resource source
consumer
seed trap and herbivore
protection
seed trap
disperser and consumer
Gill & Marks 1991
dispersal and
protection
dispersal
Smit et al. 2007
protection
herbivore protection
consumer
Solvieres & Eldridge 2014
protection
herbivore protection
consumer
disperser
8
1
Table S2. The shrub traits from each study testing facilitation with shrubs that included both
2
other plants and animals (see Methods for full list of search terms) summarized here. A total of
3
79 articles were returned in searches, 36 studies were appropriate, and 53 independent
4
instances reporting plant facilitation including animals were summarized in this review.
5
Thorniness and height were determined from plant trait databases. Palatability was typically
6
reported in the publications. The heights listed represent the median height.
7
Shrub species
Family
Thorniness
Height (m)
Palatability
Acacia erioloba
Fabaceae
yes
15
Palatable
Acacia pulchella
Fabaceae
yes
0.486
Unpalatable
Acacia tortilis
Fabaceae
yes
10
Unpalatable
Allocasuarina huegeliana
Casuarinaceae
no
7.5
Unknown
Araucaria angustifolia
Araucariaceae
yes
6
Palatable
Artemisia tridentata
Asteraceae
no
1.8
Unpalatable
Baccharis mesoneura
Asteraceae
no
2
Toxic
Baccharis uncinella
Asteraceae
no
1.97
Toxic
Baccharis vernalis
Asteraceae
no
1.35
Toxic
Banksia attenuata
Proteaceae
no
0.161
Palatable
Banksia menziesii
Proteaceae
no
0.197
Palatable
Berberis buxifolia
Berberidaceae
yes
2
Unknown
Bossiaea eriocarpa
Fabaceae
no
0.159
Unknown
Calophyllum brasiliense
Calophyllaceae
no
10.5
Palatable
Celtis pallida
Ulmaceae
yes
3.75
Palatable
Condalia montana
Rhamnaceae
yes
2
Unknown
Cordia multispicata
Boraginaceae
no
2.15
Palatable
Cornus racemosa
Cornaceae
no
4
Unknown
Corymbia calophylla
Myrtaceae
no
0.227
Unknown
Crataegus monogyna
Rosaceae
yes
10
Palatable
Crataegus spp.
Rosaceae
yes
6
Palatable
Discaria articulata
Rhamnaceae
yes
0.9
Palatable
Dodonaea viscosa
Sapindaceae
no
2
Palatable
Eremophila sturtii
Scrophulariaceae
No
2
Unpalatable
9
1
2
Hakea prostrata
Proteaceae
yes
0.133
Palatable
Hardenbergia comptoniana
Fabaceae
no
0.222
Palatable
Ilex aquifolium
Aquifoliaceae
yes
12
Palatable
Juniperus sabina
Cupressaceae
no
2.5
Toxic
Lespedeza cuneata
Fabaceae
no
1.25
Palatable
Lonicera maackii
Caprifoliaceae
no
6
Unpalatable
Lonicera spp.
Caprifoliaceae
no
6
Palatable
Lupinus arboreus
Fabaceae
no
1.25
Palatable
Malpighia glabra
Malpighiaceae
no
2.5
Palatable
Mirbelia dilatata
Fabaceae
yes
0.324
Unknown
Morella cerifera
Myricaceae
no
Myrceugenia euosma
Myrtaceae
no
2.17
Unknown
Oxylobium lanceolatum
Fabaceae
yes
0.149
Palatable
Pinus elliotti
Pinaceae
no
3.88
Palatable
Pistacia lentiscus
Anacardiaceae
no
4
Palatable
Porlieria chilensis
Zygophyllaceae
no
1.35
Unknown
Prosopis velutina
Fabaceae
yes
12
Palatable
Prunus annularis
Rosaceae
yes
7.5
Palatable
Pyracantha angustifolia
Rosaceae
yes
1.5
Unpalatable
Quercus oocarpa
Rosaceae
no
6
Unpalatable
Rhamnus cathartica
Rhamnaceae
no
8
Toxic
Rhus typhina
Anacardiaceae
no
5
Palatable
Rosa canina
Rosaceae
yes
3
Palatable
Rosa rubiginosa
Rosaceae
Yes
2
Palatable
Rubus allegheniensis
Rosaceae
yes
1.3
Palatable
Rubus ulmifolius
Rosaceae
no
8
Palatable
Schinus patagonica
Anacardiaceae
no
5
Unknown
Senna artemisioides
Fabaceae
no
3
Unknown
Vaccinium myrtillus
Ericaceae
no
0.25
Palatable
Viburnum dentatum
Caprifoliaceae
no
1.5
Palatable
Viburnum recognitum
Caprifoliaceae
no
3
Palatable
Palatable
10
1
Figure S2. A contrast of studies examining shrub facilitation with other plants and animals by
2
country. The data are from a systematic review (terms described in Methods). Frequency
3
histograms plotted for each independent instance that included facilitation with a shrub, other
4
plant species, and at least one animal species.
5
6
7
11
1
Figure S3. The relative proportion of animal interactors with shrub-plant-animal or shrub-animal
2
plant facilitation nested assemblies. The data are from a systematic review (terms described in
3
Methods). The values plotted denote total number of instances tested across studies with
4
independent shrub species that included another plant species and at least one animal species.
5
Only one animal species was reported/measured per instance.
6
7
8
9
12
1
Figure S4. A phylogeny of shrub species by shrub functional role from the systematic review
2
on shrub facilitation, other plants, and animals. The tree was produced using the Phylomatic
3
software, and the shrub functional role was subsequently assigned to each appropriate node on
4
the tree. Models were run for 999 randomizations using a null model that randomized across all
5
species within the data matrix. The shrub functional roles were identified and coded in this
6
synthesis using the descriptions provided in the primary research publications, and independent
7
instances across all studies are plotted.
8
13
habitat
herbivore protection
floral resource
resource source
seed dispersal
seed trap
1
2
Pinus elliotti
Juniperus sabina
Araucaria angustifolia
Berberis buxifolia
Banksia menziesii
Banksia attenuata
Hakea prostrata
Cornus racemosa
Vaccinium myrtillus
Eremophila sturtii
Cordia multispicata
Ilex aquifolium
Viburnum recognitum
Viburnum dentatum
Lonicera spp.
Lonicera maackii
Baccharis vernalis
Baccharis uncinella
Baccharis mesoneura
Artemisia tridentata
Rhus typhina
Schinus patagonica
Pistacia lentiscus
Dodonaea viscosa
Myrceugenia euosma
Corymbia calophylla
Porlieria chilensis
Malpighia glabra
Calophyllum brasiliense
Rubus ulmifolius
Rubus allegheniensis
Rosa rubiginosa
Rosa canina
Quercus oocarpa
Prunus annularis
Pyracantha angustifolia
Crataegus spp.
Crataegus monogyna
Discaria articulata
Rhamnus cathartica
Condalia montana
Celtis pallida
Morella cerifera
Allocasuarina huegeliana
Lupinus arboreus
Lespedeza cuneata
Hardenbergia comptoniana
Oxylobium lanceolatum
Mirbelia dilatata
Bossiaea eriocarpa
Senna artemisioides
Prosopis velutina
Acacia tortilis
Acacia pulchella
Acacia erioloba