Ecological Modelling 244 (2012) 127–131

Contents lists available at SciVerse ScienceDirect

Ecological Modelling
journal homepage: www.elsevier.com/locate/ecolmodel

Pollination services at risk: Bee habitats will decrease owing to climate change in
Brazil
Tereza C. Giannini a,∗ , André L. Acosta a , Carlos A. Garófalo b , Antonio M. Saraiva c ,
Isabel Alves-dos-Santos a , Vera L. Imperatriz-Fonseca a,d
a
Instituto de Biociências da Universidade de São Paulo, Rua do Matão, 321, 05508-900 São Paulo, São Paulo, Brazil
b
Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Av. Bandeirantes, 3900, 14040-901 Ribeirão Preto, São Paulo, Brazil
c
Escola Politécnica da Universidade de São Paulo, Av. Prof. Luciano Gualberto, 380, 05508-970 São Paulo, São Paulo, Brazil
d
Universidade Federal Rural do Semi-Árido, Av. Francisco Mota, 572, 59625-900 Mossoró, Rio Grande do Norte, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Native bees are important providers of pollination services, but there are cumulative evidences of their
Received 21 March 2012 decline. Global changes such as habitat losses, invasions of exotic species and climate change have been
Received in revised form 28 June 2012 suggested as the main causes of the decline of pollinators. In this study, the influence of climate change
Accepted 30 June 2012
on the distribution of 10 species of Brazilian bees was estimated with species distribution modelling. We
Available online 28 July 2012
used Maxent algorithm (maximum entropy) and two different scenarios, an optimistic and a pessimistic,
to the years 2050 and 2080. We also evaluated the percentage reduction of species habitat based on the
Keywords:
future scenarios of climate change through Geographic Information System (GIS). Results showed that
Species distribution modelling
Regional crops
the total area of suitable habitats decreased for all species but one under the different future scenarios.
Agriculture The greatest reductions in habitat area were found for Melipona bicolor bicolor and Melipona scutellaris,
Pollinators which occur predominantly in areas related originally to Atlantic Moist Forest. The species analysed have
Apidae been reported to be pollinators of some regional crops and the consequence of their decrease for these
crops needs further clarification.
© 2012 Elsevier B.V. All rights reserved.

1. Introduction also demonstrated based on a pool of species (Parmesan and

Pollinators are considered fundamental keys to global biodiver-
sity because they provide vital ecosystem services to agriculture
and natural systems (Daily, 1997). There is evidence of a global
decline in pollinators owing to multiple drivers (Potts et al., 2010).
Habitat fragmentation and loss, land-use changes and aggressive
agricultural practices are considered among the main drivers of
this decline. For example, Girão et al. (2007) reported that habitat
fragmentation in the Brazilian Atlantic Forest resulted in the loss
of three pollination systems (birds, flies and non-flying mammals)
present in control plots. Carvalheiro et al. (2011) also showed the
negative effect of extensive crop fields and of the distance to natural
habitats on the diversity of pollinators.
Climate change also has been considered one of the possible
drivers of the decline in pollinators. Local declines in pollinator
species richness and abundance have been reported in studies
based on historical survey data (Biesmeijer et al., 2006; Dupont
et al., 2011). Geographic shifts in species distribution have been
∗ Corresponding author. Tel.: +55 11 3091 7533; fax: +55 11 3091 7533.
E-mail address: giannini@usp.br (T.C. Giannini).
Yohe, 2003; Tingley et al., 2009; Chen et al., 2011). Recently, it
was also reported that climate change can disrupt flowering phe-
nology, negatively affecting pollinators (Aldridge et al., 2011),
and that it can cause a spatial mismatch between the geo-
graphical areas occupied by interacting species (Schweiger et al.,
2008).
The influence of climatic variables on natural areas may pro-
vide critical insights to help explain the potential effects of climate
change on plant-pollinator interactions. For example, temperature
(Tuell and Isaacs, 2010) and precipitation (Devoto et al., 2009;
González et al., 2009) have been shown to play important roles
in the interactions between plant and pollinator communities.
However, additional research is required to better understand the
processes related to the spatiotemporal variation in pollination sys-
tems, and long-term studies are of particular importance (Burkle
and Alarcón, 2011).
As one-third of agricultural production depends on animal polli-
nation (Kremen et al., 2007), the consequences of pollinator decline
for agriculture need to be evaluated (Garibaldi et al., 2011). For
example, Gallai et al. (2009) estimated that the economic value of
pollination corresponds to 9.5% of global agricultural production.
These authors suggested that given a scenario of pollinator loss, the

0304-3800/$ – see front matter © 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.ecolmodel.2012.06.035
128 T.C. Giannini et al. / Ecological Modelling 244 (2012) 127–131
production of some crops will fall below the current consumption
level on a worldwide scale.
Species distribution modelling is a computational technique
that has been applied to investigate the impact of future climate
change on species distribution (Franklin, 2009). This modelling
tool relates species distribution data (occurrence or abundance at
known locations) to information on the environmental and/or spa-
tial characteristics of those locations (Elith and Leathwick, 2009).
According to Lavergne et al. (2010), species distribution modelling
has been largely influenced by Hutchinson’s concept of the ecolog-
ical niche (Hutchinson, 1957). Currently, this type of modelling is
also considered an estimate of habitat suitability since it uses the
reported occurrences to estimate other sites with similar suitable
conditions (Kearney and Porter, 2009).
Species distribution models generate first approximations of
the potential effects of global climate change on different taxa.
Because many species are poorly known and information on rel-
evant non-climatic environmental variables may be unavailable
on the global or continental scales, more detailed models may not
be feasible (Carroll, 2010). Moreover, there is a strong demand for
species distribution maps for conservation and land management
purposes and for forecasting potential spatial shifts due to climate
change (Elith and Leathwick, 2009). Several recent examples in
which species distribution modelling has been applied in forecasts
of climate change effects include Kramer et al. (2010), Loiselle et al.
(2010), Pearman et al. (2010), Saupe et al. (2011), Watt et al. (2011),
and Maiorano et al. (2011).
The aim of this study is to evaluate the potential impact of cli-
mate change on the geographical distribution of 10 Brazilian bee
species. The consequence on regional crops of the loss of areas
suitable for these species is also discussed.
2. Materials and methods
We analysed three species and subspecies of Melipona (Api-
dae) and seven species of Centris (Apidae). These species included
Melipona bicolor bicolor, Melipona bicolor schencki, Melipona scutel-
laris, Centris aenea, Centris analis, Centris fuscata, Centris hyptidis,
Centris sponsa, Centris tarsata and Centris trigonoides. The three
Melipona species are social bees usually associated with sites orig-
inally dominated by Tropical Moist Forests and the seven Centris
are solitary bees associated with different biomes (Moure et al.,
2008).
The occurrence of each species was surveyed using differ-
ent data sources, specially literature and Internet data providers
(Global Information Biodiversity Facility, Discover Life and Species-
Link). The details of these data sources can be found in
Supplementary Material 1.
To characterise species requirements in terms of current
climate, we used a set of 19 bioclimatic layers representing combi-
nations of temperature and precipitation for the past 50 years with
a resolution of 2.5 arc-min (Hijmans et al., 2005). These layers were
obtained in the Worldclim website. The environmental layers con-
sidered the following variables: (1) annual mean temperature; (2)
mean diurnal range; (3) isothermality; (4) temperature seasonality;
(5) maximum temperature of the warmest period; (6) minimum
temperature of the coldest period; (7) temperature annual range;
(8) mean temperature of the wettest quarter; (9) mean tempera-
ture of the driest quarter; (10) mean temperature of the warmest
quarter; (11) mean temperature of the coldest quarter; (12) annual
precipitation; (13) precipitation of the wettest period; (14) pre-
cipitation of the driest period; (15) precipitation seasonality; (16)
precipitation of the wettest quarter; (17) precipitation of the dri-
est quarter; (18) precipitation of the warmest quarter; and (19)
precipitation of coldest quarter.
To predict future conditions, we used the same 19 layers
projected onto the years 2050 and 2080. Both projections were pro-
vided by the Canadian Centre for Climate Modelling and Analysis
(CCCMA; Ramirez and Jarvis, 2008) and are based on the projec-
tions developed by the Intergovernmental Panel on Climate Change
(IPCC). Two scenarios were applied. One scenario is more opti-
mistic (B2), whereas the other is more pessimistic (A2). These
frameworks are based on contrasting storylines and emission sce-
narios. The optimistic scenario (B2) assumes an increasing level of
CO2 emissions, reaching approximately 10 Gtonnes of carbon per
year in 2100. The pessimistic scenario (A2) assumes emissions of
30 Gtonnes per year in 2100 (IPCC, 2001).
Species distribution modelling furnishes insights about the
relationship between species records and the environmental char-
acteristics of the sites where those records were found (Franklin,
2009). To achieve this end, we used the Maxent algorithm that
estimates a target probability distribution by finding the proba-
bility distribution with maximum entropy or closest to a uniform
distribution (Phillips et al., 2006). The Maxent approach is espe-
cially useful because it can be applied to analyse small and
presence-only data sets (Wisz et al., 2008), a form of data that is
frequent on tropical regions (Feeley and Siman, 2011). We used
the Maxent software package that is available on the Internet
(http://www.cs.princeton.edu/∼schapire/maxent/) and its default
settings, with 500 iterations. The original databases of each species
were randomly split in calibration (80%) and evaluation subsets
(20%) (Fielding and Bell, 1997).
The area under the curve (AUC) of the receiver operating charac-
teristic graph (ROC graph) has been applied to estimate the quality
of the models (Fielding and Bell, 1997). In general terms, ROC curves
deal with classification problems, where each instance is either pos-
itive or negative (Phillips et al., 2006). A classifier can be used to
assign a real value to each instance, and standard methods can be
applied to distinguish between the predictive power of different
classifiers. The AUC of ROC curves determines the probability that
a random positive instance and a random negative instance are cor-
rectly ordered by the classifier. Because the AUC is a region within
the unit square, its value will always be between 0.5 and 1. A model
whose performance does not exceed chance has an AUC of 0.5. As
the value of the AUC increases, it indicates increasingly good model
performance.
The output of Maxent represents the occurrence probability for
each grid cell used in the model. We classified these probabil-
ities into three categories: maximum probability, corresponding
to the cells that show a predicted probability of the presence of
more than 75%; medium probability, corresponding to a range of
probabilities of 50–75%; and minimum probability, representing
probabilities less than 50%. We classified all models using these
three classes. We then compared the total amount of pixels with
maximum occurrence probability obtained to current, 2050 and
2080 scenarios per each species. Based on this information, we eval-
uated the percentage reduction of species suitable area based on
the future scenarios of climate change. All these procedures were
performed with ArcGIS 10 (Esri Inc.).
3. Results
A total of 648 occurrence points were obtained from different
sources (see Supplementary Material 1 for details). The models
obtained to all species exhibited AUC values greater than 0.9 and
can be considered accurate (details about all species models and
their values of AUC can be found in Supplementary Material 2).
According to our results, all but one species will find a reduction
of suitable occurrence areas in the future (Fig. 1 and Table 1). The
greatest reductions in area were found for M. bicolor bicolor under
 T.C. Giannini et al. / Ecological Modelling 244 (2012) 127–131 129

Fig. 1. Reduction in suitable habitat areas of 10 Brazilian bees, given an optimistic (B2) and a pessimistic (A2) scenario of future climate change for the years (a) 2050 and
(b) 2080 (details about all species models can be found in Supplementary Material 2).

the pessimistic scenario (A2): near 25% in 2050 and 35% in 2080. M. 4. Discussion
scutellaris is the second species exhibiting relatively high impact
under the pessimistic scenario. For other species, such as C. hyp- The two species whose habitat areas exhibited the highest
tidis and M. bicolor schencki, the projections of the pessimistic and reduction in suitability (M. bicolor bicolor and M. scutellaris) occur
optimistic scenarios differed, varying from less than 5% reduction predominantly in areas related originally to Atlantic Moist Forest.
in the optimistic scenario to greater than 10% in the pessimistic The habitat areas of M. bicolor schencki, a southeastern Brazilian
scenario. species, are also associated exclusively with Atlantic Moist For-
A marked difference between scenarios was also found for C. est but showed one of the smallest reductions. This species is
sponsa. A smaller reduction (less than 5%) was projected for this frequently found at higher altitudes (Moure et al., 2008), and pre-
species, assuming the optimistic scenario. However, the pessimistic vious analyses suggested that some areas suitable for the species
scenario estimated that habitat suitability would increase, espe- will occur on mountains in the South of Brazil in future climates
cially according to the 2050 projection. (Giannini et al., 2010).
An example of the potential areas predicted under different cli- There is evidence that the flight activity of the Melipona species
mate conditions (current, 2050 and 2080) for the species C. tarsata is related to moderate temperatures, high relative humidity and
can be found in Fig. 2. In this figure, the black areas correspond to the the daily foraging cycle, where most flight activity occurs during
maximum values of the probability of C. tarsata predicted presence the early morning hours (Hilário et al., 2000; Alves and Lorenzon,
(probabilities greater than 75% – see Section 2) (details about the 2001; Pierrot and Schlindwein, 2003; Ferreira et al., 2010; Silva
result of all species models can be found in Supplementary Material et al., 2011). A future increase in temperature and a decrease in
2). In addition to reduction in suitable areas, the model projected a humidity can therefore potentially have a high impact on these
marked fragmentation of the suitable areas for this species. These bees. The forecasts for Centris species included a variety of different
fragments occur in different portions of the geographical distribu- results. Nevertheless, because the climate requirements of these
tion of this species. The two future scenarios showed disjunctions bees are still poorly known, it is difficult to discuss these results.
between the North and the coastal areas and between these areas The species showing the smallest reduction, C. sponsa, occurs
and certain small fragments in areas of the Southeast. In the pes- primarily in the dry and warm Caatinga of the Brazilian North-
simistic model (A2), this last fragmentation is more conspicuous. east. Possibly, future climatic conditions will be suitable for this
The areas between the fragments are associated only with medium species. Marengo et al. (2011) suggested that temperatures will
and minimum probabilities of occurrence (the grey and white areas, increase and precipitation will probably decrease in this area under
respectively, in Fig. 2). future climate scenarios. Species occurring on extreme environ-
mental condition can provide particularly interesting study case,
since the climate change possibly will affect them differently.
The resulted fragmentation of suitable areas, found mostly to
Table 1 C. tarsata, is also important because bees are particularly sensitive
Total amount of pixels (×103 ) representing maximum probability of occurrence
to the effects of small population size (Zayed and Packer, 2005).
(higher than 75%) on the current and future scenarios (each pixel has 2.5 arc-min).
This evaluation was used to estimate the changings in the suitable habitats areas The survival of species requires a minimal population size to avoid
of 10 Brazilian bees (Melipona and Centris genera), given an optimistic (B2) and the loss of genetic variability, which can reduce fitness and limit
a pessimistic (A2) scenario of future climate change for the years 2050 and 2080 the ability to adapt to changing environments. Therefore, small
(details about all species models can be found in Supplementary Material 2). fragmented areas could not support viable populations.
Current B2 2050 A2 2050 B2 2080 A2 2080 To our knowledge, no previous study has considered the impact
of future climate change on Brazilian bees. However, other stud-
C. aenea 29.2 26.6 26.6 24.3 22.9
C. analis 34.4 31.8 31.0 30.5 27.2 ies have analysed the impact on other species occurring in the
C. fuscata 36.5 35.0 34.0 32.4 28.3 same habitats analysed here. Two studies analysed the impact of
C. hyptidis 10.0 9.5 9.8 8.9 7.9 such change on trees in the Atlantic Moist Forest (Colombo and
C. sponsa 34.8 34.1 35.7 33.6 35.1
Joly, 2010) and in the Cerrado (Siqueira and Peterson, 2003). Both
C. tarsata 41.9 36.9 36.6 33.9 30.7
C. trigonoides 19.0 17.9 18.0 16.8 15.6 studies found a reduction of 20–50% in the suitable habitat areas,
M. bicolor bicolor 18.4 16.0 13.6 14.9 11.9 depending on the different models used.
M. bicolor schencki 20.9 20.5 20.2 18.9 16.7 Our results are also of particular concern if the plants that
M. scutellaris 12.4 11.6 11.1 9.9 8.2 depend on these bees as pollinators are considered. The species
130 T.C. Giannini et al. / Ecological Modelling 244 (2012) 127–131
Fig. 2. Reduction and fragmentation of suitable habitat areas for Centris tarsata, given optimistic (B2) and pessimistic (A2) scenarios of future climate change for the year
2080 (details about all species models and their values of AUC can be found in Supplementary Material 2).
of Melipona analysed here were reported as pollinators of some
fruit crops, including açai (Euterpe oleracea), avocado (Persea amer-
icana) and guava (Psidium guajava) (Castro, 2002; Venturieri et al.,
2008). The Centris species were reported as pollinators of acerola
(Malphighia punicifolia), murici (Byrsonima crassifolia), cashew
(Anacardium occidentale) and tamarind (Tamarindus indica) (Castro,
2002; Freitas et al., 2002; Vilhena and Augusto, 2007; Rego et al.,
2006; Ribeiro et al., 2008; Siqueira, 2010). Some of these crops are
cultivated regionally, and the loss of native pollinators can have a
potentially high impact on local economies. This scenario is alarm-
ing in the light of the analysis by Pinto et al. (2008) of climate change
in Brazil and its impact on agricultural crops. These authors have
already suggested that global warming can cause a future harvest
loss of almost US$9 billion owing to temperature and precipitation
change. Some other impacts on agriculture were already suggested.
For example, increasing of evapotranspiration in a future scenario
will increase the irrigation water demand (Gondim et al., 2008) and
also, will possibly increase crop plant susceptibility for pests and
diseases (Ghini et al., 2011).
Other studies are necessary to complement the analyses pre-
sented here. It remains difficult to quantify the impact of reductions
in bee species on the production of agricultural crops. Moreover,
the occurrence data for bee species are rare for certain areas of
Brazil (especially the northern and central-western regions), and
bee surveys on these areas are urgently needed. Habitat loss and
fragmentation and the impact of agriculture must be evaluated
along with climate change, since the combination of these drivers
can potentially produce an even more pessimistic scenario.
5. Conclusion
This study indicates that the suitable areas for 10 species but one
of Brazilian bees will decrease, and these decreases are expected
to be especially marked in areas associated primarily with Moist
Forest. The impacts of the projected changes onto the agricultural
crops that are pollinated by these bees require further evaluation,
but the results of this study highlight the urgent need for additional
studies that can develop conservation strategies for native bees.
Acknowledgements
To FAPESP (04/15801-0), CNPq (575069/2008-2) and Research
Center on Biodiversity and Computing (BioComp). Also to Carlos
Alfredo Lopes Carvalho, Murilo Sérgio Drummond and Rogério Mar-
cos de Oliveira Alves.
Appendix A. Supplementary data
Supplementary data associated with this article can be found,
in the online version, at http://dx.doi.org/10.1016/j.ecolmodel.
2012.06.035.
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