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Abstract
This study was conducted to determine the effect of african genes on the production of honey, stinging
behavior and size of honeybees (Apis mellifera L.) from colonies commercially exploited in an africanized
area of the mexican high plateau. Data on honey production, stinging behavior and size of workers from
416 colonies having european or african mitochondrial DNA (mtDNA) were analyzed. Bees from colonies
with african mitotype were significantly less productive, more defensive and smaller than the bees from
colonies with european mitotypes (P < 0.01). The honey yield per colony was 23.5, 31.5 and 31.8 kg, for bees
with african, western european and eastern european mitotype, respectively. The number of stings per
colony was 101.7, 56.9 and 41.9, for bees with african, western european, and Eastern European mitotype,
respectively. The wing length was 8.9, 9.1 and 9.2 mm for bees with african, western european, and eastern
european mitotype, respectively. The defensiveness of the experimental colonies was negatively correlated
with the size of the bees (r = 0.51, P < 0.01). Honey yield did not show correlation neither with stinging
behavior, nor with bee size (P > 0.05). Results mentioned demonstrate that the introgression of african
genes into honeybee populations decreases the size of the bees and their honey production, as well as
increasing their defensiveness. Thus, the introgression of european genes into these populations is
advisable to keep productive and manageable bees. Several alternatives for achieving this goal are
discussed.
Key words: A PIS MELLIFERA L., DEFENSIVE BEHAVIOR, AFRICANIZED BEES, HONEY PRODUCTION,
STINGING.
Resumen
Este trabajo se llev a cabo con el objetivo de establecer el efecto de la introgresin de genes africanos en
poblaciones de abejas (Apis mellifera L.) sobre la produccin de miel, comportamiento defensivo y tamao
de stas. Con ese propsito se estudiaron abejas de 416 colonias explotadas comercialmente en una regin
Palabras clave: APIS MELLIFERA L., COMPORTAMIENTO DEFENSIVO, ABEJAS AFRICANIZADAS, PRO-
DUCCIN DE MIEL, AGUIJONEO.
Introduction Introduccin
fricanized honeybees are a major problem for n problema prioritario para la industria apcola
the Mexican beekeeping industry. Africanized mexicana es la africanizacin de las poblaciones
bees are hybrids of European and African races de abejas. Las abejas africanizadas son hbridos de
of honeybees introduced in Brazil in 1957 with the aim razas de abejas europeas y africanas que se crearon en
of developing a selective breeding program.1 The first Brasil en 1957 con la finalidad de desarrollar un programa
swarms of Africanized bees became established in Mex- de mejoramiento gentico.1 Llegaron a Mxico desde
ico at the end of 1986, after crossing the border with finales de 1986, cuando entraron los primeros enjambres
Guatemala, as a result of 29 years of migration from a travs de la frontera con Guatemala, despus de 29 aos
Brazil.2 High defensiveness, absconding and migratory de migracin desde Brasil.2 Entre los principales efectos
behaviors are among the most undesirable characteris- indeseables de las abejas africanizadas estn su compor-
tics of Africanized bees.3 tamiento altamente defensivo y migratorio, as como su
Africanized bees have existed for more than 44 tendencia a abandonar o evadirse de las colmenas.3
years in the Americas, causing a decrease in honey Las abejas africanizadas han existido durante ms de
production in all countries where they have become 44 aos en el continente americano, causando una dismi-
established, Brazil being the only exception.3,4 This nucin de la produccin de miel en todos los pases en que
is one of the reasons why there is controversy about se han establecido, con excepcin de Brasil.3,4 sta es una
whether or not these bees are more efficient for de las razones por las que existe controversia respecto a s
honey production than European bees; but the most estas abejas son o no ms eficientes en la produccin de
important reason for this controversy is the fact that miel comparadas con abejas de razas europeas; pero la
very few comparative experiments between these razn ms importante de esta controversia se sustenta en
two eco-types of bees have been conducted; and, in que se han hecho muy pocos experimentos comparativos
those that have been conducted, no more than 17 entre abejas europeas y africanizadas,1,5,6 en los que nunca
colonies per treatment were used,1,5,6 which is a very se utiliz un nmero mayor de 17 colonias por tratamien-
small sample size to draw general conclusions, giv- to, lo cual es un tamao de muestra insuficiente que no
en that the variation for honey production among permite obtener resultados concluyentes porque la varia-
colonies is very high.3 Additionally, results of these cin entre colonias para la produccin de miel es muy
experiments have been inconsistent. For example, alta.3 Adems, los resultados de estos experimentos han
Kerr 1 found that Africanized bees were more pro- sido diferentes. Por ejemplo, Kerr1 encontr que las abejas
ductive than European bees, Rinderer et al.5 con- africanizadas son ms productivas que las de razas euro-
cluded that European bees produce more honey peas, en tanto que Rinderer et al.5 concluyeron que las
than Africanized bees, while Spivak et al.6 did not abejas de razas europeas producen ms miel que las
find differences. africanizadas, y Spivak et al.6 no encontraron diferencias.
48
Several studies have demonstrated that Africanized Varios estudios han demostrado que las abejas afri-
bees are more defensive than European bees,7-14 and canizadas son significativamente ms defensivas que
that this characteristic is highly heritable.8,14-17 las abejas europeas7-14 y que esta caracterstica es alta-
In Mexico, the high defensiveness of Africanized mente heredable 8,14-17.
bees has resulted in more than three thousand sting- En Mxico, el comportamiento altamente defensivo
ing incidents to people, in which more than 300 have de estas abejas ya ha ocasionado ms de tres mil acci-
died.18 There are no statistics regarding stinging dentes por picaduras a personas, de stas ms de 300
incidents to animals, but these probably number in han muerto.18 Por otro lado, aunque no existen estads-
the thousands since it is very common to find ani- ticas sobre el nmero de animales muertos, ste segu-
mals that were stung to death in all beekeeping ramente es de miles a juzgar por lo comn que es
regions of Mexico. One of the direct consequences of escuchar quejas sobre animales picados y muertos en
bees defensive behavior is that beekeepers find todas las regiones apcolas del pas. Una de las conse-
other means of employment or reduce their number cuencias directas de esta agresividad, es que los apicul-
of colonies, given that it has become increasingly tores abandonan la actividad o reducen su nmero de
difficult to find suitable places to establish apiaries.3 colmenas, seguramente por la dificultad para encon-
It is a fact that keeping aggressive bees increases trar sitios apropiados para ubicar sus apiarios.3 Es una
costs of production because beekeepers have to relo- realidad que tener abejas agresivas aumenta los costos
cate their apiaries to more remote areas, increasing de produccin porque obliga a los apicultores a ubicar
the investment in transportation and labor (each sus apiarios en sitios ms remotos, con el consecuente
beekeeper works less colonies per day). Guzmn- aumento en los costos de transportacin y de mano de
Novoa and Page3 reported that costs also increase obra (cada hombre revisa menos colmenas por da).
due to the acquisition of additional safety equip- Guzmn-Novoa y Page3 indican que los costos tam-
ment such as coveralls and gloves. bin aumentan por concepto del uso de equipo de
There is no doubt that the highly defensive be- proteccin adicional como overoles y guantes.
havior of Africanized bees is their most undesirable Sin duda, el comportamiento altamente defensivo
characteristic. However, there are not enough stud- es la caracterstica ms indeseable de las abejas africa-
ies to fully understand the genetic basis of this be- nizadas. A pesar de esto no existen suficientes estudios
havior, in order to find solutions for the beekeeping sobre este comportamiento para entenderlo mejor y
industry. For instance, no studies have been con- para buscar soluciones a mediano y largo plazos. Por
ducted with a high enough number of colonies un- ejemplo, no se han llevado a cabo estudios en un
der commercial conditions, only a few experimental nmero representativo de colonias explotadas comer-
and feral colonies have been used, and there is no cialmente (slo se han hecho estudios en muy pocas
certainty about whether or not it is possible to breed colonias silvestres y experimentales) y persiste la duda
Africanized bees that are relatively gentle and pro- de si es posible seleccionar abejas africanizadas que
ductive. Many beekeepers believe that there are sean relativamente dciles y productivas. Muchos api-
many Africanized colonies with gentle and produc- cultores creen que hay muchas colonias africanizadas
tive bees. mansas y productivas.
Since they are hybrids from different races, but Por ser hbridos de razas diferentes, pero de la misma
within the same species (Apis mellifera L.), it is very especie (Apis mellifera L.), las abejas africanizadas son
difficult to discriminate between European and Afri- muy difciles de diferenciar de las abejas europeas a
canized bees with the naked eye. Daly and Balling 19 simple vista. Daly y Balling 19 encontraron que adems
found that besides being defensive, Africanized bees de tener un elevado comportamiento defensivo, estas
are smaller than European bees. Defensiveness and abejas son ms pequeas que las europeas. La defensi-
size of honeybees are correlated characteristics in Afri- vidad y tamao de las abejas son caractersticas altamen-
canized areas. Guzmn-Novoa and Page20 reported a te relacionadas en zonas africanizadas. Guzmn-Novoa
high and negative correlation (r = -0.54) between the y Page20 notificaron una correlacin altamente significa-
bees stinging behavior and their wing length. Wing tiva y negativa (r =0.54) entre el aguijoneo de las abejas
length is a measurement used to estimate the size of y su longitud de ala, la cual constituye una caracterstica
honeybees. importante para determinar el tamao de las abejas.
The only internationally recognized methods used Los mtodos morfomtricos para identificar a las abe-
to identify Africanized bees are morphometric meth- jas africanizadas son los ms usados, pero no son total-
ods, yet these methods are not totally reliable. Guzmn- mente confiables. Guzmn-Novoa et al.21 demostraron
Novoa et al.21 demonstrated that the above methods que los mtodos morfomtricos diagnostican correcta-
correctly diagnose 100% of the bee samples from high- mente el total de las colonias altamente africanizadas o
ly Africanized or European colonies, but they are not europeas, pero que no son lo suficientemente sensibles
Records of honey production and defensive behav- Se tomaron registros sobre produccin de miel y com-
ior, as well as samples of bees from 416 randomly portamiento defensivo, adems de muestras de abejas
chosen commercial colonies, for wing length and obreras para determinar su longitud de ala anterior y
mt
DNA determination, were obtained. These colo- tipo de ADNmt, de 416 colonias comerciales escogidas al
nies were located at two different altitudes (areas), azar en dos zonas, una alta y una baja. La zona alta tiene
one high and one low. The high area had colo- colonias establecidas a 2 200 y 2 600 msnm, mientras
nies established between 2,200 and 2,600 m above que la zona baja tiene colonias a 1 400 y 1 600 msnm.
50
sea level, while the low area had colonies established Produccin de miel
between 1,400 and 1,600 m above sea level.
La produccin de miel se midi durante la floracin de
Honey production otoo (octubre y noviembre), siguiendo la metodolo-
ga de Estrada y Guzmn-Novoa 27 modificada por
Honey production was estimated, using the method- Guzmn-Novoa y Prieto.28
ology described by Estrada and Guzmn-Novoa 27 and
modified by Guzmn-Novoa and Prieto,28 during the Comportamiento defensivo
autumn blossom season (October and November).
Este comportamiento se midi despus de la floracin
Defensive behavior de otoo, mediante dos repeticiones de una prueba
tradicional de campo29 que se basa en el conteo del
The bees defensive behavior was measured after the nmero de aguijones dejados por las abejas en un
blossom season. Two replicates of a traditional field test29 parche de cuero, despus de una exposicin sobre el
were conducted. The test is based on the number of stings nido de cra por un tiempo breve.
embedded by the bees in a leather patch, after exposing
it over the brood nest of colonies for a brief period of time. Mitotipo y tamao
where donde:
Yijk = variable measured (honey production, defen- Yijk = variable medida (produccin, defensa, tama-
siveness, size) in the two areas o) en las zonas.
Data were also subjected to correlation analyses.32 Los datos tambin se sometieron a anlisis de correla-
The European and African mitotypes were compared cin.32 Los mitotipos europeos y africano fueron compa-
for honey production, number of stings, and wing rados en cuanto a su produccin de miel, nmero de
length in both areas (high and low). aguijones y tamao de alas en las dos zonas (alta y baja).
Results Resultados
52
and their bees had the longest wings (Figure 3). The 2) y de mayor longitud de ala (Figura 3). Las abejas
colonies having bees with Western EuropeanmtDNA con mitotipo del oeste de Europa fueron significativa-
were significantly more defensive and their bees mente ms defensivas y de menor longitud de ala que
had smaller wings than those from colonies with las que posean mitotipo del este de Europa, aunque
Eastern European mtDNA, but there were no differ- no hubo diferencias en cuanto a su produccin de
ences between these for honey production (Figures miel (Figuras 1-3). Hubo efecto de los mitotipos de
1-3). There were effects of mitotype, area, as well as abejas, de las zonas, e interaccin entre mitotipos y
interactions between area and mitotype for the vari- zonas para las variables medidas, con excepcin de las
Cuadro 1
CUADRADOS MEDIOS DE UN ANLISIS DE VARIANZA DE TRES MITOTIPOS DE ABEJAS, ZONAS (ALTA Y BAJA) E INTERACCIN
MITOTIPOS POR ZONAS, PARA NMERO DE AGUIJONES DEJADOS POR LAS ABEJAS EN UN PARCHE DE CUERO EN 60 SEG,
PRODUCCIN DE MIEL (KG) Y LONGITUD DE ALA DELANTERA (mm), DE OBRERAS DE COLONIAS DE ABEJAS CON MITOTIPO
DEL ESTE EUROPEO, OESTE EUROPEO Y AFRICANO*
MEAN SQUARES OF AN ANALYSIS OF VARIANCE FROM THREE HONEY BEE MITOTYPES, TWO AREAS (HIGH AND LOW),
AND INTERACTION OF MITOTYPE BY AREA, FOR NUMBER OF STINGS LEFT BY THE BEES IN A LEATHER PATCH IN 60 s,
HONEY YIELD (kg) AND FORE-WING LENGTH (mm), FROM HONEY BEES WITH EASTERN EUROPEAN, WESTERN EUROPEAN
AND AFRICAN MITOTYPES*
*Mean squares were obtained with square-root transformed data because the data were not homoscedastic.
ns
= not significant
*P < 0.05
**P < 0.01
***P < 0.0001
Cuadro 2
COEFICIENTES DE CORRELACIN ENTRE EL NMERO DE AGUIJONES, PRODUCCIN DE MIEL (kg) Y LONGITUD DE ALA DELAN-
TERA (mm), DE OBRERAS DE 416 COLONIAS DE ABEJAS DE UNA ZONA AFRICANIZADA DEL ALTIPLANO MEXICANO
CORRELATION COEFFICIENTS BETWEEN NUMBER OF STINGS, HONEY YIELD (kg), AND FORE-WING LENGTH (mm) OF WORKER
HONEY BEES FROM 416 COLONIES LOCATED IN AN AFRICANIZED REGION OF THE MEXICAN HIGH PLATEAU.
Correlation coefficients were obtained with square-root transformed data because the data were not homoscedastic.
ns
= not significant
*P < 0.0001
54
The defensive behavior was, in general, negative- El comportamiento defensivo en general estuvo
ly correlated with wing length (r = -0.51, n = 416, P negativamente correlacionado con la longitud de ala
< 0.01). Honey production was not correlated nei- de las abejas (r = 0.51, n = 416, P < 0.01). La produc-
ther with defensive behavior, nor with wing length cin de miel, no tuvo correlacin ni con el comporta-
(Table 2). miento defensivo ni con la longitud de ala de las abejas
(Cuadro 2).
Discussion
Discusin
The African mitotype frequency in the population of
honeybees sampled was low, which was probably due La frecuencia del mitotipo africano en la poblacin de
to two main reasons. First, there was a sub-detection of abejas muestreada fue bajo, lo cual se debe a dos razones
the percentage of highly Africanized colonies because principales. Primero, hubo una subdeteccin del porcen-
the molecular technique used ( mtDNA) only shows the taje de colonias altamente africanizadas debido a que la
maternal African lineage, but not the paternal one. tcnica molecular utilizada (ADNmt) slo muestra la he-
Second, it may be that the Africanization process in the rencia africana de las madres, pero no la de los padres de
study region has not yet reached equilibrium, and that las abejas. Segundo, puede ser que el proceso de africani-
gene flow is still occurring from the African to the zacin en el rea de estudio no haya an llegado a un
European populations, as has been demonstrated in equilibrio y que exista todava flujo de genes africanos
bee colonies of the Yucatan peninsula in Mexico.33-35 hacia las poblaciones de abejas europeas, como se ha
The fact that the majority of the colonies had bees with demostrado que sucede en la pennsula de Yucatn,
Eastern European mtDNA, demonstrates the influence Mxico.33-35 El hecho de que la mayora de las colonias
of Italian and Carniolan honeybee races in the popula- tuviera mitotipo del este de Europa, demuestra la influen-
tion studied, since these are the two main races of cia de razas de abejas, como la Italiana y la Carniola, en la
Eastern European honeybees that have been intro- poblacin estudiada, ya que stas son las dos principales
duced in Mexico in the past. The Western European razas de abejas del este de Europa que se han introducido
mitotype corresponds to the first bees originally intro- a Mxico. El mitotipo del oeste europeo corresponde a las
duced by the Spaniards, but during the last 50 years primeras razas de abejas introducidas por los espaoles a
Mexican beekeepers have preferred races of honey- Mxico, pero en los ltimos 50 aos los apicultores mexi-
bees from Eastern Europe, such as the Italian,36 which canos han preferido utilizar abejas de razas del este
explains the higher frequency of its mitotype in the europeo como la Italiana,36 lo cual explica su mayor fre-
population surveyed. cuencia en la poblacin estudiada.
The results demonstrate that the introgression of Los resultados demuestran que la introgresin de
African genes into the populations of commercial genes africanos en las poblaciones de abejas explotadas
honeybee colonies in the Mexican high plateau, de- comercialmente en el altiplano mexicano, disminuye de
creases their honey production, and increases their manera significativa la produccin de miel y aumenta
defensiveness. Additionally, it decreases the wing en forma importante la defensa de las colonias. Adicio-
length of their workers. These results suggest that it is nalmente, disminuye la longitud de ala de las abejas
not desirable to have a high degree of Africanization obreras. Estos resultados sugieren que no es deseable
in commercial populations of honeybees, since this tener un alto grado de africanizacin en poblaciones de
will turn beekeeping into a risky, uncomfortable and abejas comerciales, pues esto har de la apicultura una
less profitable activity. actividad riesgosa, incmoda y menos rentable.
Kerr1 found that Africanized bee colonies were Kerr1 encontr que las abejas africanizadas son ms
more productive, whereas Rinderer et al.5 concluded productivas,1 mientras que Rinderer et al.5 concluyeron
that European bee colonies were more productive, que las abejas europeas producen ms miel que las africa-
and Spivak et al.6 found no differences. The results in nizadas, y Spivak et al.6 encontraron que no hay diferen-
this study agree with those of Rinderer et al.5 and cias. Los resultados del presente trabajo concuerdan con
demonstrate, using a greater amount of data than that los de Rinderer et al.5 y demuestran con ms datos que en
of any of the above studies, that the Africanization of todos los estudios anteriores, que la africanizacin dismi-
honeybee colonies decreases their honey production. nuye la produccin de miel. La produccin media de miel
The average yield of honey per colony was not differ- por colonia no fue diferente entre las zonas, independien-
ent between areas, independent of their mitotype. temente del mitotipo de stas. Sin embargo, las colonias
However, the colonies with African mitotype pro- con mitotipo africano produjeron significativamente
duced considerably less honey than those with Euro- menos miel que las colonias con mitotipos europeos en la
pean mitotypes in the high area. It is possible that zona alta. Es posible que por existir condiciones de menor
Africanized bees had foraged for less time in the high temperatura en la zona alta, las abejas africanizadas ha-
56
and to diminish the defensive behavior of honeybee to defensivo y a incrementar la produccin de miel de las
populations in Africanized regions. This goal has al- poblaciones de abejas en reas africanizadas. Esto ya ha
ready been achieved by Guzmn-Novoa and Page,20 sido demostrado por Guzmn-Novoa y Page,20 quienes
who were able to decrease the defensive responses of despus de cinco aos de seleccin en una poblacin de
their experimental population of honeybees by 50%, as ms de tres mil colonias, lograron disminuir la respuesta
well as increase the honey production of these bees by defensiva de las abejas en ms de 50% y lograron aumen-
16%, in a five year period, using selective breeding. tar la produccin de miel en 16%. Asimismo, el tamao de
These researchers worked with a population of more las abejas aument con el tiempo, as como la frecuencia
than 3,000 colonies and were also able to increase the de colonias con ADNmt europeo, lo que indica que el
size of the bees and the proportion of colonies whose proceso de africanizacin de la poblacin seleccionada
bees had European mtDNA over time. The above results pudo revertirse en cierto grado. Sin embargo, Guzmn-
suggest that the process of Africanization was reversed, Novoa y Page20 trabajaron en una regin recientemente
to some degree, through selective breeding. However, africanizada, por lo que es factible que la frecuencia de
Guzmn-Novoa and Page20 worked in a region that genes europeos en la poblacin de abejas seleccionadas
had been recently Africanized, thus, it is possible that haya sido alta, lo que permiti revertir parcialmente el
the frequency of European genes in the population proceso de africanizacin y disminuir el comportamiento
under selection had been high, which permitted a de defensa de las colonias bajo seleccin. Sin embargo,
partial reversal of the Africanization process in the bees como lo demuestran varios estudios,10,14,17,41 el comporta-
being selected. However, as has been demonstrated in miento defensivo elevado de las abejas africanizadas se
several studies,10,14,17,41 the highly defensive behavior of hereda de manera dominante, lo cual podra causar un
Africanized bees is inherited in a dominant fashion. lento progreso gentico hacia una menor agresividad, si
This fact could slow down the genetic progress to los programas de seleccin se llevaran a cabo en poblacio-
generate gentle genotypes of honeybees, if these pro- nes de abejas en zonas altamente africanizadas. En este
grams area carried out in highly Africanized regions. In caso, la mejor alternativa sera la introduccin de germo-
this case, the best alternative would be the introduc- plasma de razas de abejas del este de Europa.
tion of genotypes of Eastern European bees. Para entender mejor cmo funcionan los comporta-
To better understand how the bees honey produc- mientos de defensa y productivo de las abejas, se requie-
tion and defensive behaviors work, additional studies re de estudios adicionales sobre los efectos y las interac-
on genotype and genotype-environment interactions ciones genotpicas y gentico-ambientales de las pobla-
must be conducted in populations from different bee- ciones de abejas de diferentes zonas apcolas. Estos
keeping regions. These studies will broaden the knowl- estudios ampliarn el conocimiento sobre el porqu las
edge about why Africanized bees have been so success- abejas africanizadas han sido tan exitosas en la coloniza-
ful at colonizing new regions, as well as about how to cin de nuevas reas, sobre cmo criar abejas ms dci-
breed gentle and productive honeybee stocks, which les y productivas y sobre cmo reducir el nmero de
would reduce the number of people and animals killed personas y animales muertos por picaduras de abejas.
in stinging incidents.
Conclusiones
Conclusions
Se encontr que la mayora de las colonias comerciales
It was found that the majority of the commercial muestreadas tenan ADNmt del este de Europa, lo que
colonies sampled had Eastern European mtDNA, demuestra la influencia de razas de abejas como la Italiana
which shows the influence of Italian (Apis mellifera (Apis melifera ligustica) y la Carniola (Apis mellifera carnica).
ligustica) and Carniolan (Apis mellifera carnica) races La introgresin de genes africanos a las poblaciones
of honeybees. de abejas comerciales en el altiplano mexicano dismi-
The introgression of African genes into commercial nuye significativamente su produccin de miel y su
populations of honeybees in the Mexican high plateau tamao y aumenta significativamente su respuesta
decreases their honey production and their body size, defensiva (aguijoneo).
and increases their defensive responses (stinging). La produccin de miel no estuvo relacionada ni con el
Honey production was not correlated with the size of tamao de las abejas ni con su comportamiento defensi-
the bees or with their defensiveness. This means that it is vo. Esto significa que se pueden encontrar colonias muy
possible to find very defensive but productive colonies, as defensivas y productivas y colonias muy defensivas y
well as very defensive but unproductive colonies and poco productivas y viceversa. Esto es bueno para el
vice versa. This is good for breeding, since, if the charac- mejoramiento gentico, ya que al no estar ligadas estas
teristics are not linked, it is possible to generate produc- caractersticas, es posible seleccionar abejas productivas y
tive bees with low defensive responses. con baja respuesta defensiva.
58
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