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Preserved honey bee health in Latin America: a fragile
equilibrium due to low-intensity agriculture and
beekeeping?
Rémy Vandame, María Alejandra Palacio
To cite this version:
Rémy Vandame, María Alejandra Palacio. Preserved honey bee health in Latin America: a fragile
equilibrium due to low-intensity agriculture and beekeeping?. Apidologie, Springer Verlag, 2010, 41
(3), <10.1051/apido/2010025>. <hal-00892093>
Apidologie 41 (2010) 243–255 Available online at:
c
INRA/DIB-AGIB/EDP Sciences, 2010 www.apidologie.org
DOI: 10.1051/apido/2010025 Review article
Preserved honey bee health in Latin America:
a fragile equilibrium due to low-intensity agriculture
and beekeeping?*
Rémy Vandame1, María Alejandra Palacio2
1El Colegio de la Frontera Sur, Carretera Panamericana y Periférico Sur S/N, Barrio María Auxiliadora,
29230 San Cristóbal de las Casas, Chiapas, Mexico
2Unidad Integrada INTA – Facultad de Ciencias Agrarias, Universidad Nacional de Mar del Plata, CC 276,
7600 Balcarce, Argentina
Received 6 October 2009 – Revised 4 February 2010 – Accepted 13 February 2010
Abstract – The Latin American subcontinent contains some of the world’s major honey producing and
exporting countries, but the status of bee health in this part of the world has not been clearly documented.
There have been no reports of massive colony losses in Latin America, at least from the symptoms of CCD
(colony collapse disorder) or in the proportion and extent of the situations in the US and Europe. We exam-
ine possible reasons for the difference, and develop hypotheses that this prevailing good bee health could
be due to: (1) the management of generally unselected bees with a certain natural resistance to diseases
(tropical regions) or the selection of disease resistant bees (temperate regions); (2) a lower proportion of
cropland over the total land area, resulting in more abundant or higher-quality pollen resources for bees;
(3) the generally small-scale, low-income and little subsidized agriculture, and concomitant lower use of
insecticides compared to industrialized countries. These general parameters may act synergistically, result-
ing in a large number of configurations across the tremendous ecological, social and economic diversity of
Latin America. We suggest that the health of honey bees in Latin America may be ultimately due to the
practices of low-income agriculture and beekeeping in the region, leading to more sustainable conditions
for the bees. However the increasing trend of land use intensification in some parts of Latin America could
lead to declines in honey bee health and population size.
honey bee health /colony losses /disease resistance /genetic diversity /pollen nutrition
1. INTRODUCTION
Losses of honey bee (Apis mellifera L.)
colonies have been documented repeatedly
during the last years in Europe (Neumann
and Carreck, 2010) and in the United States
(van Engelsdorp et al. 2008,2009). Colony
mortality characterized by rapid loss of adult
worker bees was named colony collapse disor-
der (CCD) (van Engelsdorp et al., 2009). But
there is little data on similar symptoms of bee
losses outside of these areas, including Latin
Corresponding author: R. Vandame,
remy@ecosur.mx
* Manuscript editor: Marla Spivak
America (LA). Countries like Argentina and
Mexico have a strong beekeeping tradition,
and are among the world’s largest honey pro-
ducers (ranking 2nd and 6th, respectively) and
exporters (1st and 3rd respectively; FAOSTAT,
2009). Therefore it is interesting to focus on
the LA region to determine if colony losses
have been reported.
In this paper we first state that no massive
losses due to symptoms described for CCD
have been documented to date in LA. There-
fore we attempt to determine possible rea-
sons for differences between what is occurring
in the US and bee losses in Europe com-
pared to LA. We structure our observations
Article published by EDP Sciences
244 R. Vandame, M.A. Palacio
by examining the four items considered as
possible factors responsible for colony loss in
the Managed Pollinator Coordinated Agricul-
tural Project (Managed Pollinators CAP, 2008;
Pettis and Delaplane, 2010): disease agents
(pathogens, parasites) and environmental fac-
tors (nutrition, pesticides). We examine if the
conditions in LA ameliorate the impact of
these factors, and if these conditions could ex-
plain the relatively good health of the honey
bees in this region. Finally we speculate on the
risks that might disrupt the fragile equilibrium
of bee health in LA in the future.
2. PRESENT SITUATION:
NO MASSIVE LOSSES
OF COLONIES IN LA
Evaluating the health of honey bees in LA
is a difficult task for two reasons. First, this
region is large and highly diverse, with bee-
keeping being practiced over a wide range of
climates (from tropical to temperate) and alti-
tudes (from sea level to around 2000 m alti-
tude), by very different beekeepers (who have
from 15 colonies each in Mesoamerica up to
15 000 in northern Mexico or the Pampas re-
gion of Argentina). Hence it is hard to draw a
general picture that can take into account all of
this diversity. Second, there is little synthetic
information published on honey bee health in
different parts of the region.
However, to date, from Mexico to Ar-
gentina, there have been no reports of mas-
sive colony losses or weakening of colonies
due to adult bees losses, such as described
by CCD, by official institutions, researchers,
or beekeepers professional beekeeping organi-
zations. This situation is the same in Africa,
southern Asia and Australia (Neumann and
Carreck, 2010). Local problems in various re-
gions of LA are commonly reported however
and we will mention some of them here.
For example, for several years beekeep-
ers of southeastern Guatemala have reported
significant losses in the months from Febru-
ary to April (flowering season). They place
the responsibility on an international con-
trol program for the Mediterranean fruit fly
(Ceratitis capitata), in which the insecticide
Spinosad is commonly used on a large scale.
Edwards et al. (2003) demonstrated toxicity
of this compound to honeybees under labora-
tory conditions, though Mangan and Moreno
(2009) showed that honey bees are repelled
by the fruit fly attractant components of the
commercial product that is used in the field.
However, field observations show that api-
aries are regularly sprayed with this insecti-
cide, and it appears to be a toxicological prob-
lem as reported by beekeepers for many years
(Vandame et al., 1995). In the northern state
of Chihuahua, Mexico, recurrent losses are de-
scribed (Arnulfo Ordoñez, unpubl. data) and
are still unexplained, but are limited to a local
scale.
Beekeepers of Uruguay report frequent de-
clines in honey bee populations in spring,
called “Mal de Santa Lucia”. Though no fac-
tor has been clearly identified (Harriet et al.,
2009), this decline seems to be an effect of
food shortage in spring, apparently increasing
in recent years due to loss of natural vegeta-
tion. Losses related to Va r roa also have been
reported in recent years in Argentina, in par-
ticular due to the lack of a generalized Var-
roa control strategy (Emilio Figini, pers. com-
mun.), mite resistance to coumaphos (Maggi
et al., 2009), and in Chile, due to the ap-
plication of mite control too late in the sea-
son (Miguel A. Neira, Universidad Austral de
Chile, pers. commun.) or because of nutri-
tional problems. It is also notable that dur-
ing the last summer, in the northern parts of
Chile, where honey bees are used for polli-
nation, thousands of colonies have been lost
(Juanse Barros, unpubl. data). This massive
mortality is a true cause for concern, but seems
to be restricted to areas with intensive agricul-
tural practices, hence generating the suspicion
that the losses may be due to toxic effects of
pesticides.
The situation is also diverse in Brazil
(David de Jong and Dejair Message, unpubl.
data). Periodic large-scale die-offs of bees re-
ported for the last 40 years were originally
blamed on a local type of sacbrood disease,
or some sort of spring dwindle. Now the
losses are known to be caused by toxic pollen
from native trees in the Cerrado (Savanna-like
biome) regions (de Carvalho and Message,
Honey bee health in Latin America 245
2004;deSouzaetal.,2006). Large-scale
losses have become increasingly common in
Brazil. Since these losses have been simulta-
neous to the expansion of crops for agrofuels
and the increased use of pesticides, beekeepers
tend to attribute these losses to insecticides, es-
pecially neonicotinoids, though no evidences
have been given. The pesticides affect both
honey bees and stingless bees, making bee-
keeping inviable in some regions. Moreover,
Var ro a infestation levels are reported to be
alarmingly high in the (cooler) southern states
of Rio Grande do Sul and Santa Catarina in
Brazil, with beekeepers reporting losses. Also
it seems that Nosema and Va r roa are becoming
more problematic than they used to be, though
for unknown reasons (Aaroni Sattler, Univer-
sidade Federal do Rio Grande do Sul, personal
communication), and may be a consequence
of the increased use of pesticides that could
weaken honey bee immunological or behav-
ioral defenses.
These cases of bee losses, which are likely
much more common than what can be found in
published reports, either can be attributed to a
clear cause or are confined to a local level, and
remind us of the problems routinely encoun-
tered by the beekeepers worldwide, rather than
a CCD-like phenomenon. When they occur on
a larger scale, as in Chile or Brazil, they seem
to be geographically correlated with more in-
tensive agriculture. In the following sections,
we therefore examine some situations that may
explain why CCD has not been reported in LA.
3. UNSELECTED HONEY BEES
AND RESISTANCE TO DISEASES
There is a general consensus that CCD is
multifactorial, and research indicates that it
may be due to “either increased exposure to
pathogens or a reduced resistance of bees to-
ward pathogens” (van Engelsdorp et al., 2009).
The introduction of new pathogens and their
interaction with already present ones may in-
crease the problems (Eyer et al., 2009). Resis-
tance to pathogens has a strong genetic basis
(Rothenbuhler, 1964), and many studies have
shown that honey bee colonies vary in their re-
sistance to diseases as common as American
foulbrood (AFB; Behrens et al., 2007). How-
ever, it is only in the last 20 years that signif-
icant work has been done to understand and
select for resistance to AFB and chalkbrood
diseases in bees (Spivak and Reuter, 1998;
Palacio et al., 2000)andtoVarroa destructor
(Ibrahim et al., 2007; Harbo and Harris, 2009;
Fries and Bommarco, 2007; Rinderer et al.,
2010).
In turn, very little artificial selection has
been done on honey bees in LA. The intro-
duction of the European bee races at differ-
ent times during the XVIIth century, and of
the African bee race in 1956 has resulted in a
considerable genetic mixture of Apis mellifera
races (Kraus et al., 2007). We now differenti-
ate the situation in tropical and temperate parts
of LA to understand a differential resistance to
diseases.
Africanized honey bees (AHB) have been
successfully established throughout most of
tropical LA. Relatively little effort has been
made to select these bees, so that there has
been little or no reduction in AHB genetic
diversity. Hence they can still be considered
as mainly unselected bees. Beekeepers work-
ing with AHB normally have no AFB prob-
lems, very little chalkbrood, and Varro a mites
populations in untreated colonies always re-
main below a critical level (Vandame et al.,
2002; Mondragón et al., 2005), even though
miticide treatments can help to improve honey
production (Guzmán-Novoa et al., 1999). It is
worth noting that when only EHB was found
in Mexico (i.e. before 1986), AFB and tracheal
mites, Acarapis woodi, were significant prob-
lems. The disease resistance described above
occurred subsequent to AHB invasion (Medina
et al., 2006). The strongest hypothesis to ex-
plain this resistance is that AHB express a
high degree of hygienic behavior, in which the
adult bees are able to detect brood cells in-
vaded by a reproducing Va rr o a mite. We report
here unpublished data demonstrating that EHB
colonies detect only 18% of experimentally
infested pupae, while a higher percentage of
AHB colonies are able to detect mite-infested
pupae, up to a maximum of 64% (Fig. 1).
Africanized bees in Brazil are more resis-
tant to Va r roa than European bees, and mite
infestations were found to be higher in the
246 R. Vandame, M.A. Palacio
Figure 1. Removal of pupae artificially in-
fested with a Varroa destructor mite in colonies
with different Africanization levels. Selection of
colonies. The level of Africanization (morpho-
metric analysis) of 60 colonies of beekeepers
apiaries was determined following the proce-
dure described by Rinderer et al. (1993). Among
them, 25 colonies were chosen for their ho-
mogeneous distribution along an Africanized-
European cline, in groups of 5 colonies. The
Africanization degree (ID) is the projection on
the discriminant function 1 in the multivariate
analysis performed by Rinderer et al. (1993)
and varies from –6 (most Africanized colonies,
top graph) to 4 (most European ones, bottom
graph). Artificial infestation. 30 mites were col-
lected from emerging brood (i.e. at a phase
when they are able to reproduce) and were in-
troduced into 30 cells containing pupae from the
same colonies (to avoid detection for odor of an-
other colony) that had been capped for less than
3 h. Additionally, 30 cells were uncapped and
immediately recapped as controls. Determina-
tion of removal abilities. The cells containing
artificially infested pupae were observed every
2 days over 10 days to determine if the bees
removed the pupae. The 10th day, all remain-
ing cells were uncapped to determine if they
were still infested, and if so, if the mite inside
had reproduced. The figure shows for each 5-
colony group of colonies from most African-
ized (top graph) to least Africanized (bottom
graph), the percent of observed pupal cells in
each of the following categories: cells uncapped
in each 2-day period over 10 days after capping
(“2” to “10”); cells in which mites reproduced
normally (“R”); cells still capped, but in which
mites did not reproduce (“NR”); cells no longer
infested (“NI”); control cells uncapped in the
first 10 days after capping (“C”). Overall, the
more Africanized (i.e. unselected) the colonies,
the more they detected pupae containing repro-
ducing Varro a mites.
Honey bee health in Latin America 247
Figure 2. Selection of hygienic colonies for disease resistance in Argentina (adapted from Bedascarrasbure
et al., 2009). (a) Percentage of colonies expressing a high or low AFB prevalence in the population in
1997 (2935 colonies observed) and 2008 (9971 colonies observed). (b) Percentage of hygienic and non-
hygienic colonies in the population, before the start of the ProApi national selection program and 5 years
later. (c) Percentage of colonies with brood diseases in populations of hygienic and non-hygienic colonies.
(d) Percentage of colonies with AFB symptoms in populations of hygienic and non-hygienic colonies.
cooler regions when compared to the more
tropical parts of Brazil (De Jong et al., 1984).
This adaptation is probably a consequence
of the bees being infested by the less viru-
lent Japanese type Varroa destructor.How-
ever, the Korean mitotype of Varroa destruc-
tor was identified in Brazil in the 1990s and
it currently is the only type identified through-
out the continent. One of the changesin Brazil
since the Korean mitotype of Va r ro a destruc-
tor took over has been increased reproduction
by the mites. Apparently because of the new
type of Varro a , the percentage of female mites
that reproduced shifted from about the half
(de Jong et al., 1984) to over 80% (Carneiro
et al., 2007).
In temperate LA, where only EHB have es-
tablished, as in Chile and most areas in Ar-
gentina or Uruguay, diseases are more often
a problem. This situation is possibly ampli-
fied because the populations historically in-
troduced may have been more susceptible to
diseases like chalkbrood (Jensen et al., 2009).
However in Argentina, brood diseases are less
of a problem than they used to be, due to
human intervention (Bedascarrasbure, 2009).
AFB was first detected in this country in
1989, and the genetic selection of local eco-
types with high hygienic behavior was started
some years after. Importance was given to dis-
ease tolerance, resulting in a bee strain that is
now mainly resistant to AFB (Palacio et al.,
2000,2005, in press). We report a synthesis of
these results (Fig. 2). Va r r o a is still a signifi-
cant problem in most temperate regions in Ar-
gentina. Although some alternative and effec-
tive acaricides have been developed locally, it
is still necessary to use synthetic acaricides but
the efficiency of these acaricides is now known
to be decreasing (Maggi et al., 2009).
A rare situation is found in the Dominican
Republic, where AHB have not invaded, so
that it is possible to observe EHB in a tropi-
cal climate. Here the population dynamics of
Var ro a shows patterns similar to the one in
Mexico with AHB (Castillo, 2009); i.e., with
248 R. Vandame, M.A. Palacio
a population increase during most of the year,
and a natural decline at the end of the floral
bloom period. Since these bees have been es-
tablished for a long time with very few subse-
quent introductions, their apparent resistance
to Var ro a,incommonwithAHB,seemstobe
that they have gone through very little selec-
tion by the beekeeping industry.
Special mention should be made here to
two other types of diseases. One is the mi-
crosporidium Nosema ceranae, suspected to
be responsible for colony losses in different
parts of the world (Paxton et al., 2007;Higes
et al., 2010) whose biology is currently be-
ing investigated (Naug and Gibbs, 2009;Chen
and Huang, 2010). In Brazil, Nosema had not
been a problem since the 1960s, after African-
ized honey bees took over. However, during
the last years, large numbers of Nosema spores
have been found in adult bees from colonies
that were reported by beekeepers to be weak
and dying. N. ceranae (and not N. apis)was
first confirmed to be present in Brazil in 2006
(Klee et al., 2007) and was recently shown
to have been present in Uruguay for nearly
20 years, without causing particular damages
(Invernizzi et al., 2009), a situation likely to
be similar in all LA. The reason for this low
pathogenicity can be either the presence of a
less virulent strain of the parasite or some re-
sistance trait of the bees.
Other important diseases are the viruses,
still relatively unstudied in honey bees
(Gauthier et al., 2007). Their prevalence has
been shown to be significantly higher in
CCD than in control colonies in the US
(van Engelsdorp, 2009), though it is still hard
to say if such prevalence is a cause or a conse-
quence for CCD. Though little is known about
viruses in LA, the few existing studies show
that most known viruses are present (Antúnez
et al., 2005,2006), even if it has also been
demonstrated that the prevalence of viruses as
a whole is lower in Brazil than in the rest of
the world (Teixeira et al., 2008). It is therefore
possible that the low prevalence of viruses is
part of the reason for the preserved health of
Latin-American bees.
Overall, honey bee strains managed in LA
are either nearly unselected (AHB, EHB in
Dominican Republic) or selected for disease
resistance (EHB in Argentina), and in most of
the countries, especially under temperate cli-
mate, there is little use of synthetic treatments
to control diseases and mites. Even if there is
lower prevalence of diseases in LA compared
to the rest of the world, it appears that there
also has been natural selection for a certain
level of resistance to diseases. This general
picture leads us to hypothesize that CCD, or
high colony losses, have not been found in LA
because the higher level of defense of the bees
against diseases reduces at least one of the
major risk factors involved in CCD. Such an
advantage is threatened however by the com-
mon beekeeping practice of illegally introduc-
ing queens from foreign countries, instead of
promoting selection on local stocks, as is done
for example in Europe (de la Rúa et al., 2009;
Buechler et al., 2010).
4. PRESERVED NATURAL
VEGETATION AND POLLEN
DIVERSITY
Environmental factors may be responsi-
ble for CCD, and in particular deficien-
cies in pollen nutrition (Brodschneider and
Crailsheim, 2010). It has been shown that the
quality of spring-reared workers is strongly
influenced by the availability of pollen in
colonies during larval development (Mattila
and Otis, 2006). Furthermore, “pollen nutri-
tion can play an important role in the develop-
ment of disease because poor nutrition may re-
sult in a less robust defense system” (Managed
Pollinator CAP, 2008). Fries (1993)showed
that good pollen supply reduced infection lev-
els in colonies.
This importance of pollen nutrition may im-
ply that heavily managed landscapes are poor
for the sustainability of honey bee colonies, a
hypothesis that to be tested requires the devel-
opment of a specific methodology to qualify
landscapes. Some data in the US seem to vali-
date this idea (Naug, 2009), but for LA coun-
tries there are no such data published. Thus,
we use indirect parameters to compare differ-
ent regions of the world.
The first parameter is the percentage of
original forest remaining, as determined for
Honey bee health in Latin America 249
Figure 3. Extract of the Water Resources eAtlas published by the World Resources Institute (2003) (http://
earthtrends.wri.org/maps_spatial/watersheds/global.php) showing the original forest remaining in the main
basins in Europe and the Americas.
the main watersheds of the world by the World
Research Institute (2003). The quantified (col-
ored) watersheds in the US and Europe are
heavily influenced by human management and
consequently the forested areas within them
occupy less than 50% and often less than 25%
of their surface (Fig. 3). Though few water-
sheds are quantified in LA, they appear com-
monly covered by more than 50% and some-
times more than 75% with original forest.
Though this is still a very raw analysis, it sup-
ports the observation that forest and by ex-
tension, natural resources, may be better pre-
served in LA than in US and Europe. However
the percentage of forested areas may not be
the best indicator of bee nutrition since forests
offer limited resources for bees; a further un-
derstanding would require the development of
indicators more fitted to honey bee natural his-
tory.
The previous consideration is supported by
data extracted from EarthTrends (2003) coun-
try profiles, synthesized in Table I, showing
the fraction of cropland within total land area.
In western European countries with strong
agriculture, croplands represent around 35%
of the total area. In the US, cropland represents
only 19% of the total area (value lowered by
extended uncultivated areas). This percent de-
creases to 14% in Mexico, and varies between
3% and 10% in South America. Such national
level data do not represent the diversity at re-
gional levels, like in the US or in Argentina.
However it is clear that land use is much more
intense in the US and Europe that in LA, and
it is possible that the pollen nutrition in LA is
more abundant throughout the year, or of bet-
ter quality, than in more industrialized coun-
tries.
Another indirect factor that could influence
bee health is the size of farms. In northern
countries, farms tend to be much bigger and
are cultivated from end to end, while the situa-
tion is reversed throughout most of LA. Small
scale farming results in more fragmented land-
scapes, thus helping to preserve the diversity
250 R. Vandame, M.A. Palacio
Tabl e I . Summary of statistics on land and pesticide use in some countries of Europe and the Americas,
extracted from EarthTrends, the environmental information portal of the World Resources Institute (http://
earthtrends.wri.org) and FAOSTAT of the Food and Agriculture Organization of the United Nations (http://
faostat.fao.org) from September 2009. The insecticide use value is the average of the 1990-2001 data on
FAOSTAT. The last column was calculated based on the previous data.
Total cropland Cropland per 1000 Cropland as % Fertilizer Insecticide Insecticide
(1000 ha) population of total land area use (kg/ha) use (T) use (g/ha)
Source EarthTrends EarthTrends EarthTrends EarthTrends FAOSTAT Calculated
Date 1999 1999 1998 1999 1990-2001
World 1 501 452 251 11.3 94 388 743 259
Europe 307 286
Netherlands 949 60 23.0 501 488 514
Germany 12 038 147 33.9 252 1 426 118
France 19 515 331 35.4 244 6 109 313
Italy 11 422 199 37.0 155 25 215 2208
Spain 18 530 464 36.6 125 9 345 504
North America 224 703
USA 179 000 638 19.1 111 102 682 574
Central America 43 426
Mexico 27 300 280 13.9 66 na
Guatemala 1 905 172 17.5 95 234 123
Cuba 4 465 400 40. 3 33 na
South America 116 131
Brazil 65 200 388 7.6 90 15 076 231
Chile 2294 153 3.0 207 2 893 1261
Argentina 27 200 744 9.8 30 7 422 273
Uruguay 1 307 394 7.4 103 222 170
na: not available data.
of plants (i.e. diversity of food for bees) and
the abundance of nesting places.
However, in southern countries like Ar-
gentina, Brazil and Uruguay, yield-intensive
crops have increased in recent years (partic-
ularly soy) and this has negatively affected
beekeeping through lower pollen availabil-
ity. Beekeepers and scientists report that the
strength of colonies at the end of wintering
(early spring) tend to decrease in many areas,
and proteins have to be supplied to colonies
in some areas with intensive, commercial bee-
keeping.
We hypothesize that generally smaller scale
of agriculture in LA permits a higher diversity
of pollen, and thus better pollen nutrition and
a lower susceptibility to diseases for the bees.
This hypothesis could explain why CCD has
not been reported in LA. But if true, then the
risks to bee health are slowly increasing due to
agricultural intensification.
5. SMALL SCALE AGRICULTURE,
LOW USE OF PESTICIDES AND
GMOS
Another permanent threat for the bees com-
ing from human manipulated environments is
the exposure to pesticides used in crop pro-
duction. For a long time this topic has been
a source of conflict between beekeepers and
the pesticide industry. There is actually a large
amount of data showing that certain pesticides
that have no demonstrated lethal effects on
honey bees in laboratory conditions do in fact
have sublethal (Vandame et al., 1995; Desneux
et al., 2007) or synergistic effects (Vandame
and Belzunces, 1997). Since they may alter
Honey bee health in Latin America 251
bees development, adult longevity, mobility,
navigation, orientation, feeding behavior or
learning, they could explain the common CCD
observation that affected foragers fail to return
to their nest (Managed Pollinator CAP, 2008).
In general, intensive crops are less abun-
dant in LA, but again, it is rather difficult
to compare pesticide use in Europe, US and
LA. We have reported that croplands repre-
sent a much higher proportion of the total land
area in industrialized countries compared to in
LA (as a whole) (Tab. I). Furthermore, Earth-
Trends (2003) data show that fertilizer use is
about twice as high in western Europe com-
pared to the US or LA. The pesticide statistics
are more interesting since these compounds
may affect bees more directly. According to
FAOSTAT (2009) data, the insecticide use per
unit of area is roughly twice as high in the US
and in Europe than in LA (except in Chile,
where data are probably influenced by vine-
yard data), a situation derived from the high
level of subsidized agriculture by the EU and
the US (Mayrand et al., 2003; Pearce, 2002).
Unfortunately, since these statistics are based
on voluntary information provided to FAO by
the countries, the data are not completely reli-
able or comparable, nor are they detailed about
compounds used such as imidacloprid (Guez
et al., 2001). However, the data do show a clear
trend of lower use of insecticides in LA. Even
a locally intensive insecticide use would have
a rather local effect, thus having no general im-
pact.
The effect of genetically modified (GM)
crops on honey bees is a controversial but little
studied topic. Though one study and a recent
meta-analysis showed that Bt crops had no ef-
fect on honey bee survival (Rose et al., 2007;
Duan et al., 2008), a different study showed
some impact on feeding behavior and learn-
ing performances of worker bees (Ramirez-
Romero et al., 2008).
There are few data on the extent of GMO
crops. They are permitted only at very small
scale in Europe but are exceptionally common
in the US, in particular GM-corn, but their
use seems to be very limited in LA, except
for the notable exception of GM-soy in Ar-
gentina, Brazil and Uruguay. Though they are
also banned in Mexico, the presence of trans-
genes in the Mexican maize (Piñeyro-Nelson
et al., 2009) has been reported. This is a type
of genetic pollution that clearly affects biodi-
versity, but probably has no direct effect on bee
health.
Overall, it seems that small scale agricul-
ture has protected honey bees, due to low
exposure to chemical contaminants, which
could be a third reason why CCD has not
been reported in LA. There are however some
changes in the practices that could convert to
threats, like the continuous extension of GM
crops in Argentina and Brazil, or the increas-
ing use of insecticides in all countries. Cur-
rently in Argentina, the strength of honey bee
colonies in spring is decreasing each year, thus
requiring more intensive feeding. This occur-
rence could be a signal of forthcoming prob-
lems.
6. A FRAGILE EQUILIBRIUM
Overall, the factors most often consid-
ered responsible for CCD in the US or for
colony losses in Europe, the disease agents
(pathogens, parasites) and the environmental
factors (nutrition, pesticides), are found in LA,
but under different conditions or intensities.
Diseases are not a major problem, probably
due to the genetic background of a little man-
aged bee population and the consequent resis-
tance of the bees, or to the selection of disease
resistant bees. Nutrition and pesticides are not
a big problem, probably due to a less intensive
and less subsidized agriculture in LA com-
pared to industrialized countries. If the colony
losses in industrialized countries are the result
of a multifactorial effect, then the lack of sub-
stantial colony losses in LA may be due to the
non-occurrence of this complex effect. In other
words, the small scale that characterizes most
of agriculture and beekeeping in LA may ex-
plain how and why the conditions in the region
lead to more sustainable honey bee health.
We consider the situation in LA as a frag-
ile equilibrium because different kinds of risks
are becoming more extended. Examples of the
risks are: (1) a higher frequency of beekeep-
ers do work with selected queens, but knowl-
edge about disease and mite (mainly Var r o a )
252 R. Vandame, M.A. Palacio
resistance is still insufficient to include desir-
able traits in queen selection; (2) agriculture
is covering more land, pesticides use is in-
creasing and GMOs are becoming more com-
mon; (3) natural vegetation is being lost to
urban development and increasing crop ar-
eas. This situation is particularly true in Ar-
gentina, Uruguay and Chile, which seem to
be already in an intermediate state of risk for
all of the factors, particularly with increas-
ing crop expansion, pesticide and GMO use.
As a specific example, in the region of Mi-
siones in northern Argentina, beekeeping is
practiced at low scale and Va r roa treatments
are unneeded. In contrast, in the nearby region
of NOA, where beekeeping is more intensive
(large scale, introduction of queens, intensive
crops surrounding), Va r ro a is more problem-
atic and has to be controlled.
Though speculative, it is possible that a
CCD-like phenomenon could happen in LA
if principles of sustainability are not imme-
diately included in beekeeping and agricul-
ture development projects. For this reason, the
authors of this paper have initiated an infor-
mal coordination of research on honey bee
genetic diversity and its importance in dis-
eases resistance Latin American (Palacio and
Vandame, 2008). Furthermore it would make
sense to develop a honey bee health surveil-
lance project together with FAO statisticians,
to collect statistics on land use and bee colony
losses in LA, to validate the hypotheses sug-
gested in this paper. This project would be
important for pollinator diversity conservation
and crop production in LA, and more gener-
ally for understanding the conditions leading
to sustainability.
ACKNOWLEDGEMENTS
The authors are most grateful to all the persons
who gave opinions, ideas, data or papers, and in par-
ticular: Emilio Figini, Martín Eguaras and Mariano
Bacci (Argentina), Aaroni Sattler, David de Jong,
Dejair Message, Erica Weinstein, Katia Peres
Gramacho, Lionel Segui Goncalves and Osmar
Malaspina (Brazil), Ernesto Guzmán (Canada),
Juanse Barros, Misael Cuevas and Miguel A. Neira
(Chile), Ana Cubero (Costa Rica), José Ramírez
(Ecuador), Niyra Castillo (Dominican Republic),
Roberto Perdomo (El Salvador), Alejandro Nicol
(Guatemala), Ernesto Tanús, Luis Medina and
Arnulfo Ordoñez (Mexico), Andrés Llaxacondor
(Peru) and finally Jorge Harriet, Juan Pablo Campa,
Yamandú Mendoza, Karina Antúnez, Pablo Zunino
and Ciro Invernizzi (Uruguay). Some of the ideas
have been developed as part of the Mexican-
European FONCICYT 94293 grant “MUTUAL –
Mutualisms with bees in tropical landscapes: risks
and rescue for biodiversity and crop production”,
which is acknowledged here.
La santé de l’abeille préservée en Amérique la-
tine : un fragile équilibre dû à une agriculture et
une apiculture peu intensives ?
santé de l’abeille /perte des colonies /résistance
aux maladies /diversité génétique /nutrition sur
pollen
Zusammenfassung –Gesunde Honigbienen in
Lateinamerika: ein fragiles Gleichgewicht basie-
rend auf der geringen Intensität von Landwirt-
schaft und Imkerei? Während der letzten Jah-
re wurden in Europa und den USA mehrfach
Verluste von Bienenvölkern (Apis mellifera L.)
dokumentiert. Dabei wurden Völkerverluste, die
durch den raschen Verlust der Adultbienen her-
vorgerufen wurden, als „Colony Collapse Disor-
der“ (CCD) bezeichnet. Obwohl sich auf dem
lateinamerikanischen Subkontinent einige der größ-
ten Honigproduktions- und Honigexportländer der
Welt befinden, fehlen bisher klare Dokumentatio-
nen über den Gesundheitsstatus der dortigen Honig-
bienen. Bisher gibt es keine Berichte über massive
Völkerverluste in Lateinamerika, zumindest nicht
mit CCD-Symptomen oder in dem Ausmaß, wie
sie aus Europa und den USA berichtet wurden.
Wir prüfen die möglichen Gründe für diese Unter-
schiede und entwickeln folgende Hypothesen für
die Verbreitung „gesunder Bienen“ in Lateiname-
rika: (1) es wird meist mit unselektierten Bienen
gearbeitet, die über natürliche Krankheitsresisten-
zen verfügen (tropische Regionen) oder es wer-
den krankheitsresistente Bienen selektiert (gemä-
ßigte Regionen); (2) der Anteil der Agrarfläche am
Gesamtgebiet ist relativ gering, wodurch es zu einer
ergiebigeren bzw. qualitativ hochwertigeren Pollen-
versorgung kommt; (3) die allgemein kleinräumig
strukturierte Landwirtschaft mit geringem Einkom-
men und wenig Subventionen führt zu einem gerin-
geren Einsatz von Insektiziden im Vergleich zu den
industrialisierten Ländern.
All diese Parameter könnten synergistisch wirken
und würden dadurch zu einer großen Anzahl an
möglichen Konstellationen innerhalb der enormen
ökologischen, sozialen und wirtschaftlichen Viel-
falt in Lateinamerika führen. Wir vermuten, dass
Honey bee health in Latin America 253
die Gesundheit der Honigbienen in Lateinamerika
letztendlich auf die in diesen Regionen vor-
herrschenden kleinräumigen und wenig intensi-
ven Landwirtschafts- und Imkereistrukturen zu-
rückzuführen ist, da solche Strukturen den Bie-
nen nachhaltigere Lebensbedingungen bieten. Al-
lerdings könnte der Trend zur intensiveren Nutzung
der Kulturlandschaft in einigen Teilen Lateinameri-
kas zu einer Verschlechterung des Gesundheitssta-
tus der Honigbienen und damit zu einem Rückgang
der Bienenpopulation führen. Um diese Hypothe-
se zu überprüfen würde es Sinn machen, zusam-
men mit der FAO ein Projekt zur Überwachung
der Bienengesundheit in Lateinamerika zu etablie-
ren und dabei die für eine statistische Auswertung
notwendigen Daten zur Landnutzung und zu Völ-
kerverlusten zu erfassen. Ein solches Projekt wäre
auch wichtig für den Erhalt von natürlichen Be-
stäuberpopulationen und damit für die Sicherung ei-
ner nachhaltigen landwirtschaftlichen Produktion in
Lateinamerika. Dies würde auch dazu beitragen, die
grundsätzlichen Bedingungen für „Nachhaltigkeit“
in tropischen und subtropischen Ländern besser zu
verstehen.
Honigbienengesundheit /Völkerverluste /
Krankheitsresistenz /genetische Vielfalt /
Pollenernährung
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