1. Efectos directos e indirectos de la invasión de arbustos en los
prados alpinos mediados por las interacciones planta-polinizador
Carlos Lara Romero
UTPL – Loja 2016

3. Alpine tundra occurs at high enough altitude at any latitude.
Map of arctic and antarctic tundraMap of alpine tundra
alpinetundrabiome.weebly.com; www.blueplanetbiomes.org

4. o Alpine tundra vulnerability to global change
Nogues-Bravo, 2007 Glob Env Chang

5. o Alpine tundra vulnerability to global change
Ellis, 2011 Proc Royal Soc A

6. o Regime shift on the roof of the world
Comte et al 2014 Nature communications

7. o Regime shift on the roof of the world
Gottfried et al 2012 Climate change, Paulí et al 2012 Science, Barrio et al 2013 MRD,
http://www.illustrationsof.com/

8. o Regime shift on the roof of the world
http://www.grida.no

9. The three general categories of woody plants increase including
(a) infilling of existing patches, (b) increase in growth and (c) an
advancing shrubline.
Myers-Smith et al. 2001. Environmetnal Research Letters
o Shrub encroachment.
Increase in the density, cover and biomass of native woody plants to the
detriment of herbaceous flowering plants

10. o Shrub encroachment.

11. Myers-Smith et al. 2001. Env Reser Let; Wookey et al 2009, Glob Chang Biol
Numerous studies document the effect of shrub encroachment on the structure
of tundra ecosystems
• Soil–atmosphere exchange of water, carbon and nutrients.
• Plant-plant interactions and vegetation composition.
• Energy fluxes
• Regional climate
o Shrub encroachment

12. We lack empirical data showing how shrub encroachment modifies
plant–animal interactions at community scale.
thetechjournal.com
orkin.com
o Shrub encroachment and biotic interactions

13. Difficulties in quantifying changes in interactions compared with
changes in biodiversity
thetechjournal.com
orkin.com
Inouye & Pyke 1988, Tylianakis et al 2008 Ecology Letters, Tylianakis et al 2010 Biological Conservation
o Shrub encroachment and biotic interactions

14. o Shrub encroachment and biotic interactions
Biotic interactions play an important role in the maintenance of biodiversity
and the stability and resistance of ecosystems !!!!!!
Inouye & Pyke 1988; Tylianakis et al 2008 Ecology Letters, Tylianakis et al 2010 Biological Conservation

15. o Shrub encroachment and biotic interactions
Images downloaded from es.dreamstime.com Inouye & Pyke 1988; Kearns & Inouye 1994; Dupont, Hansen & Olesen 2003
The harsh environmental conditions of high-mountain
ecosystems limit pollinator richness and pollination services for plant reproduction
Biotic interactions play an important role in the maintenance of biodiversity
and the stability and resistance of ecosystems !!!!!!

16. o Shrub encroachment and biotic interactions

17. o In this context of limited resources, shrub encroachment increases nutritional resources
for pollinators.
o Positive feedback at both trophic levels
Van valen 1965 Amer Nat, Bolnick et al 2007 PNAS, Hegland et al 2009 Ecol Lett, Blüthgen & Klein 2011 Basic Appl Ecol
Diversity
(e.g.plants)
Diversity
(e.g. flower visitors)
Functional Biodiversity Hypothesis
FBH
Niche width
Niche Variation Hypothesis
NHV
o Shrub encroachment and biotic interactions

18. Capítulo I Capítulo II Capítulo III Capítulo IV
o Research questions
o 1. Does higher diversity at the producer trophic level (plants) result in increased
diversity at the consumers (pollinators) trophic level, as predicted by FBH?
o 2. Does shrub encroachment reduce the specific niche breadth of pollinators?
o 3. Do shared pollinators mediate competitive indirect interactions between shrubs
and forbs?
We expected shrub encroachment to increase pollinator species richness and
simultaneously to reduce the niche breadth of each pollinator species, ultimately
affecting plant–plant interactions through competition for shared pollinators.
o Predictions

19. Objetivos Capítulos Conclusiones
o Study System: Mediterranean alpine communities of Iberian Peninsula

20. Objetivos Capítulos Conclusiones
o Study System: Mediterranean alpine communities of Iberian Peninsula
Silene
ciliata
Armeria
caespitosaFestuca
curvifolia
Cytisus
oromediterraneus

21. Laguna de los Pájaros
Macizo de Peñalara
Año 1.956

22. Año 1.976
Laguna de los Pájaros
Macizo de Peñalara

23. Año 2009
Laguna de los Pájaros
Macizo de Peñalara

24. Año 2009
Laguna de los Pájaros
Macizo de Peñalara

25. Objetivos Capítulos Conclusiones
Adenocarpus hispanicus Lam (DC)
(Fabaceae)
Cytisus oromediterraneus Rivas Mart. & Al.
(Fabaceae)
o Study System: Mediterranean alpine communities of Iberian Peninsula
Sanz-Elorza et al 2003 Annals of Botany; Garcia-Romero et al 2010 Climatic Change

26. 10 km
Nevero
Peñalara
Objetivos Capítulos Conclusiones
o Sampling design and field survey
PA EP

27. 11 census days for each sampling site (PA & EP)
o 10 Linear transects at each site.
o Number flowering plant of each species
o Identity and number of contacts between plants and flower
visitors
o Sites simultaneously surveyed
Animal
Planta
A B C D
A 7 2 12 2
B 0 8 34 8
C 4 9 4 0
D 2 0 23 0
Quantitative bipartite networks for full-season
data for each habitat type.
o Sampling design and field survey
Jordano 1987 Amer Nat

28. Metrics
Effect of shrubs on
metrics
Network-level metrics
Number of plants (P)
Number of animals (A)
Number of interactions (I)
Number of visits (V)
Connectance (C)
Weighted Linkage (lw)
Modularity (Q)
Species-level metrics
Linkage (L)
Species Specialization (d’)
Species strength (S)

29. Metrics
Effect of shrubs on
metrics
Network-level metrics
Number of plants (P) +
Number of animals (A) +
Number of interactions (I) +
Number of visits (V) +
Connectance (C) -
Weighted Linkage (lw) -
Modularity (Q) +
Species-level metrics
Linkage (L) -
Species Specialization (d’) +
Species strength (S) +

30. Capítulo I Capítulo II Capítulo III Capítulo IV
o Results & discussion: species assemblages and visitation patterns

31. Capítulo I Capítulo II Capítulo III Capítulo IV
o Results & discussion: species assemblages and visitation patterns
Blüthgen & Klein 2011 Basic Appl Ecol
o Flower visitor richness was higher in EP than in PA in all functional groups of pollinators
o Result confirmed by sample-based rarefied estimates

32. Capítulo I Capítulo II Capítulo III Capítulo IV
o Results & discussion: species assemblages and visitation patterns
Blüthgen & Klein 2011 Basic Appl Ecol
Mixed lineal models (LMMs) fitted for flower visitors
Number of
interactions
Number of visits
F value Pr(>|F|) F value Pr(>|F|)
Intercept 1109.51 <0.001 773.74 <0.001
Habitat type 20.75 <0.001 14.16 <0.001
Functional group 34.96 <0.001 25.40 <0.001
Plants abundance 0.07 0.78 0.10 0.76
Habitat type: F. group 1.42 0.17 1.34 0.21
Increased number of interactions and visits for each functional
group of flower visitors

33. Capítulo I Capítulo II Capítulo III Capítulo IV
o Results & discussion: species assemblages and visitation patterns
Diversity
(e.g.plants)
Diversity
(e.g. flower visitors)
FBH
Blüthgen & Klein 2011 Basic Appl Ecol
The integration of shrubs into the network increased richness and visitation
rates of all functional groups of flower visitors.

34. Flower visitors did not vary their niche breadth (d’a , La, Lwa)
Niche width
Increased generalization
at EP (H’2)
Bolnick et al 2007 PNAS, Blüthgen & Klein 2011 Basic Appl Ecol, Seifan et al 2014, J Ecol
Both habitat types displayed a
similar modular structure (Q)
o Results & discussion: specific niche breadth of pollinators

35. Number of
interactions
Number of visits
Visits per flowering
plant
F value Pr(>|F|) F value Pr(>|F|) F value Pr(>|F|)
a) Species that occurred at encroached pastures
Intercept 356.87 <0.001 423.69 <0.001 140.69 <0.001
Life form 3.91 0.05 1.12 0.29 12.26 <0.001
Plants abundance 10.88 <0.01 19.46 <0.001 53.28 < 0.001
b) Species that occurred at both habitat types
Intercept 580.23 <0.001 645.22 <0.001 359.16 <0.001
Habitat type 0.019 0.89 0.12 0.73 25.40 <0.001
Plant species 4.64 <0.001 4.70 <0.001 22.00 <0.001
Plants abundance 26.98 <0.001 37.84 <0.001 47.71 <0.001
H. Type:P. Species 0.52 0.87 0.45 0.92 2.36 0.01
o Results & discussion: plant-plant interactions mediated by shared pollinators
LMMs fitted for plants
o Shrubs had more interactions with flower visitors and recevied more visits per plant than
forb species.
o Forb species received fewer visits per plant in EP than in PA

36. Capítulo I Capítulo II Capítulo III Capítulo IV
Shrub encroachment increased plant linkage (Lp y Lwp) while reducing the number
of visits per plant of forb species without affecting their specialization (d’p).
Bolnick et al 2007 PNAS, Morales & Traveset 2009 Ecol Lett, Seifan et al 2014, J Ecol
o Results & discussion: plant-plant interactions mediated by shared pollinators
Niche width
These findings suggest the
existence of competition among
plant species mediated by
pollinator sharing

37. o Research questions and conclusions
o 1. Does higher diversity at the producer trophic level (plants) result in increased
diversity at the consumers (pollinators) trophic level, as predicted by FBH?
o 2. Does shrub encroachment reduce the specific niche breadth of pollinators?
o 3. Do shared pollinators mediate competitive indirect interactions between shrubs
and forbs?

38. Introducción Objetivoso Acknowledgements