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Efecto de la africanizacin sobre la produccin de miel,

comportamiento defensivo y tamao de las abejas melferas


(Apis mellifera L.) en el altiplano mexicano
The effect of africanization on honey production, defensive
behavior and size of honeybees (Apis mellifera L.) in the
mexican high plateau
Jos Luis Uribe Rubio *, ***
Ernesto Guzmn Novoa*, ***
Greg J. Hunt**
Adriana Correa Bentez***
J. Antonio Zozaya Rubio***

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

Recibido el 11 de febrero de 2002 y aceptado el 26 de abril de 2002.


* CENIFMA-Ajuchitln, Romero 107, int. 119, Col. Nios Hroes de Chapultepec, 03440, Mxico, D.F. Correo electrnico:
uribe@cuauhtli.veterin.unam.mx
* * Department of Entomology, Purdue University, West Lafayette, Indiana, 47907, U.S.A.
* * * Departamento Especies Productivas no Tradicionales: Produccin Apcola, Facultad de Medicina Veterinaria y Zootecnia, Universidad
Nacional Autnoma de Mxico, 04510, Mxico, D.F.

Vet. Mx., 34 (1) 2003 47


del altiplano de Mxico, con la finalidad de relacionar las caractersticas anteriores con su tipo de ADN
mitocondrial (ADNmt). Los resultados mostraron que las abejas de colonias con mitotipo africano fueron
menos productivas, tuvieron comportamiento ms defensivo y fueron ms pequeas que las abejas de
colonias con mitotipos europeos (P < 0.01). La produccin de miel por colonia fue de 23.5, 31.5 y 31.8 kg,
para abejas con mitotipo africano, europeo del oeste y europeo del este, respectivamente. El nmero de
aguijones por colonia fue de 101.7, 56.9 y 41.9, para abejas con mitotipo africano, europeo del oeste y
europeo del este, respectivamente. La longitud de ala fue de 8.9, 9.1 y 9.2 mm, para abejas con mitotipo
africano, europeo del oeste y europeo del este, respectivamente. El comportamiento defensivo de las abejas
en general estuvo negativamente correlacionado con el tamao de sus alas (r = 0.51, P < 0.01). La cantidad
de miel producida por las colonias no tuvo correlacin con el comportamiento defensivo ni con el tamao
de las abejas (P > 0.05). Los resultados demuestran que la introgresin de genes africanos en las poblaciones
de abejas disminuye su produccin de miel y el tamao de las abejas y aumenta su comportamiento de
defensa, por lo que la introgresin de genes europeos en estas poblaciones se hace necesario para criar
abejas productivas y manejables. Se proponen alternativas para introducir genes europeos en colonias de
abejas explotadas comercialmente.

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.

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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

Vet. Mx., 34 (1) 2003 49


sensitive enough to identify hybrid bees. Recently para la identificacin de abejas hbridas. Recientemente
Nielsen et al.22 proposed a method that combines mor- Nielsen et al.22 propusieron un mtodo combinado de
phometry and mitochondrial DNA ( mtDNA), and which morfometra y ADN mitocondrial (ADNmt) que identifica
correctly identifies more than 95% of the bee samples. correctamente ms de 95% de las muestras de abejas.
When mtDNA is used, it is possible to identify the Cuando se utiliza exclusivamente el ADNmt se puede
maternal lineage of the bees without error, though not determinar sin ninguna probabilidad de error el origen
the paternal lineage, since mitochondrial DNA is only gentico de la lnea materna de las abejas, aunque no el de
inherited through the mother. This technique is very la lnea paterna, porque el ADNmt se hereda nicamente
useful because it allows the discrimination of Eastern a travs de la madre. La identificacin del tipo de ADNmt
European (A. m. ligustica, A.m. carnica, A. m. caucasica), de las abejas (mitotipo) es muy til porque permite dife-
Western European (A. m. mellifera, A. m. iberica), and renciar entre razas de abejas del este de Europa (A. m.
African honeybees (A. m. scutellata). ligustica, A. m. carnica, A. m. caucasica), del oeste de Europa
Based on the above, one can infer the importance of (A. m. mellifera, A. m. iberica) y de frica (A. m. scutellata).
conducting studies that generate reliable information Con base en lo anterior, se infiere la importancia de
about the effect that the introgression of African genes realizar estudios que generen informacin confiable so-
in commercial populations of honeybees has on their bre el efecto de la introgresin de genes africanos en
defensive behavior and honey production capability. poblaciones comerciales que pueden afectar la produc-
Both the defensive behavior and honey production cin de miel y el comportamiento defensivo de las abejas.
of honeybees are highly influenced by genetic ef- Tanto la produccin de miel como el comportamiento
fects.15,23-25 Therefore, this study had the objective of defensivo de las abejas estn altamente influenciados por
determining if the introgression of African genes in efectos genticos.15,23-25 Por ello este trabajo tuvo como
commercially exploited honeybee colonies established objetivo determinar si la introgresin de genes africanos
in two areas of the Mexican high plateau, affected their en abejas melferas explotadas comercialmente en dos
honey production, their defensiveness, and the size of zonas de una regin del altiplano mexicano, afectan su
the bees. The interaction between genotype and loca- produccin de miel, su comportamiento defensivo y su
tion was also analyzed. tamao, as como analizar el grado de interaccin entre el
genotipo de las abejas y la zona de explotacin.
Material and methods
Material y mtodos
This study was conducted in the Mexican high pla-
teau (the second most important beekeeping region Este estudio se llev a cabo en una regin del altiplano
in Mexico for honey production and in number of mexicano (segunda zona apcola en importancia en Mxi-
colonies), in the counties of Coatepec Harinas, Villa co por produccin de miel y nmero de colmenas), en los
Guerrero, Ixtapan de la Sal, and Tonatico, in the State municipios de Coatepec Harinas, Villa Guerrero, Ixtapan
of Mexico, Mexico. Africanized bees were first identi- de la Sal y Tonatico, Estado de Mxico, Mxico. Las abejas
fied in this region in 1990.3 The counties of the study africanizadas fueron identificadas por vez primera en
area are located at 1858north latitude and 9938 esta regin en 1990.3 Los municipios del rea de estudio se
west longitude, at 1,900 m above sea level. These localizan al suroeste del Estado de Mxico, situados a 18
counties have a sub-humid temperate climate (w), 58 de latitud Norte y a 99 38 de longitud Oeste, a 1 900
with rains during the summer and an average tem- msnm. Estos municipios cuentan con un clima templado
perature of 14 C. They have borders with Tenango subhmedo (w), con lluvias en verano y temperatura
del Valle, Temascaltepec, and Calimaya to the north, promedio de 14C. Colindan al norte con Tenango del
Tescaltitlan to the west, and Tenancingo to the east, Valle, Temascaltepec y Calimaya; al oeste con Tescaltit-
all in the State of Mexico, as well as with Pilcaya, state ln; al este con Tenancingo, todas estas poblaciones en el
of Guerrero, to the south.26 Estado de Mxico; y al sur con Pilcaya, Guerrero.26

Data collection Registro de datos

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

Mitotype and size De cada una de las mismas colonias de donde se


tomaron registros de produccin de miel y se realiza-
Samples of worker bees were collected from the same ron pruebas de comportamiento defensivo, se toma-
colonies as above for mtDNA and morphometric analy- ron muestras de ms de 30 abejas adultas colectadas
ses. Each sample consisted of 30 workers collected from del nido de cra y se depositaron en frascos que con-
the brood nest and deposited in jars containing 96% tenan etanol al 96%. Estas muestras se utilizaron para
ethanol. To determine the bees mitotype, the samples determinar el tipo de ADNmt, segn la metodologa de
were subjected to the methodology described by Niels- Nielsen et al.22,30 y el tamao de las abejas, a travs de
en et al.,22,30 whereas to determine their size, the bees medir su longitud del ala anterior mediante la prueba
fore-wing length was measured following the Fast rpida de identificacin de abejas africanizadas (FA-
Africanized Bee Identification System (FABIS), using BIS), usando la metodologa de Sylvester y Rinderer.31
the methodology described by Sylvester and Rinder- Tanto la prueba molecular como la morfomtrica,
er.31 Both morphometric and molecular assays were sirvieron para inferir la introgresin de genes africa-
used to show the introgression of African genes into nos en las colonias de abejas comerciales y para clasi-
the experimental population of honeybees, as well as ficarlas. Colonias cuyas obreras resultaron con ADNmt
to classify the colonies according to type. Colonies africano fueron clasificadas como colonias africaniza-
whose bees had African mtDNA were classified as Afri- das, mientras que colonias cuyas obreras tenan ADNmt
canized, whereas colonies whose workers had Europe- europeo fueron clasificadas como colonias con mitoti-
an mtDNA were classified as Eastern or Western Euro- po del este europeo o del oeste europeo, ya que la
pean mtDNA-type, since the technique allows these tcnica permite hacer estas diferenciaciones.
differentiations. Las determinaciones de ADNmt se llevaron a cabo en el
The mtDNA analyses were done in the Honeybee Laboratorio de Gentica Apcola del Departamento de
Genetics Laboratory of the Department of Entomology Entomologa de la Universidad de Purdue, Indiana, Esta-
at Purdue University, Indiana, USA. The morphomet- dos Unidos de Amrica. Las pruebas morfomtricas se
ric studies were carried out at the INIFAP-SAGARPA realizaron en el Centro de Desarrollo Apcola del INIFAP-
Center for Beekeeping Development in Villa Guerre- SAGARPA, en Villa Guerrero, Estado de Mxico, Mxico.
ro, State of Mexico, Mexico. Los datos de produccin de miel, aguijoneo y tama-
Data on honey production, number of stings and size o de alas, se transformaron a raz cuadrada para
of wings, were square-root transformed, and then sub- normalizarlos y luego se sometieron a un anlisis facto-
jected to factorial analyses of variance under a complete- rial de varianza bajo un diseo completamente aleato-
ly randomized design, with the following model: rio con el siguiente modelo:

Yijk = m + aIi + bj + (ab)ij + Eijk Yijk = m + aIi + bj + (ab)ij + Eijk

where donde:
Yijk = variable measured (honey production, defen- Yijk = variable medida (produccin, defensa, tama-
siveness, size) in the two areas o) en las zonas.

Vet. Mx., 34 (1) 2003 51


m= population mean for the variable analyzed m= media de la poblacin para la variable analizada
aIi = mitotype effect (i = 1, 2, 3) aIi = efecto de mitotipo (i = 1, 2, 3)
bj = area effect (j = 1, 2) bj = efecto de zona (j = 1, 2)
(ab)ij = interaction effect for mitotype and area (ab)ij = efecto de interaccin entre mitotipo y zona.
Eijk = error Eijk = error

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

Los resultados muestran que 57 (13.7%) de las 416


Results show that 57 (13.7%) out of 416 experimental colonias experimentales result con mitotipo africa-
colonies had an African mitotypes, while the rest had no y el resto con mitotipos europeos, aunque la mayo-
European mitotypes, though most of the colonies ra de las colonias (295 o 70.91%) tuvo mitotipo del
(295 or 70.91%) had Eastern European mitotype. De- este de Europa. A pesar de que ms de la mitad de las
spite the fact that more than half of the samples were muestras (228 o 55%) provinieron de la zona alta, esta
from the high area (228 or 55%), only 31.6% of all ltima contribuy con solamente 31.6% del total de
colonies with African mitotype came from this area. las muestras que resultaron con mitotipo africano. Un
Chi-square analyses showed that the proportion of anlisis de Ji-cuadrada demostr que la proporcin de
bee colonies having African mtDNA was significantly colonias de abejas con mitotipo africano fue significa-
greater in the low area than in the high area (X2 = tivamente mayor en la zona baja que en la alta (X2 =
10.84, n = 57, P < 0.01). 10.84, n = 57, P < 0.01).
The colonies having bees with African mtDNA Las abejas de colonias con mitotipo africano fueron
were significantly less productive (Figure 1), more significativamente menos productoras de miel (Figu-
defensive (Figure 2), and their bees had shorter ra 1), ms defensivas (Figura 2) y de menor longitud
wings (Figure 3) than the colonies having bees with de ala (Figura 3) que las abejas de colonias con mito-
European mtDNA. The colonies having bees with tipo europeo. Las abejas de colonias con mitotipo
Eastern mtDNA were the least defensive (Figure 2) europeo del este fueron las menos defensivas (Figura

Figura 1. Media error estndar


para la produccin de miel (kg) en
416 colonias ubicadas en dos zonas
y clasificadas de acuerdo con su
tipo de ADN mitocondrial en colo-
nias del este europeo (EE), del oeste
europeo (OE) y africano (A).*
Mean standard error for honey
yield (kg) from 416 honeybee colonies
located in two areas, and classified
according to their mtDNA as eastern
european (EE), western european
(OE), and african colonies (A).*
*Different superscripts within the
same area indicate significant
differences between means. Data
were subjected to analyses of
variance and LSD tests (P <0.01).
Statistical tests were performed
with square-root transformed data
because the data were not
homoscedastic. Means and SE are
actual non-transformed values.

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

Figura 2. Media error estndar


para el nmero de aguijones deja-
dos por las abejas en un parche de
cuero en 60 seg. Se probaron 416
colonias ubicadas en dos zonas y
clasificadas de acuerdo con su tipo
de ADN mitocondrial en colonias
del este europeo (EE), del oeste eu-
ropeo (OE) y africano (A).*
Mean standard error for the
number of stings left by the bees in
a leather patch in 60 seconds. 416
colonies located in two areas and
classified according to theirmtDNA
as eastern european (EE), western
european (OE), and african colonies
(A) were tested.*
*Different superscripts within the
same area indicate significant
differences between means. Data
weresubjectedtoanalysesofvariance
and LSD tests (P <0.01). Statistical
tests were performed with square-
root transformed data because the
data were not homoscedastic. Means
and SE are actual non-transformed
values.

Figura 3. Media error estndar


para la longitud de ala delantera
(mm) de abejas obreras de 416 colo-
nias ubicadas en dos zonas y clasi-
ficadas de acuerdo con su tipo de
ADN mitocondrial en colonias del
este europeo (EE), del oeste euro-
peo (OE) y africano (A).*
Mean standard error for fore-
wing length (mm) of worker bees
from 416 colonies located in two
areas and classified according to
their mtDNA as eastern european
(EE), western european (OE), and
african colonies (A).*
*Different superscripts within the
same area indicate significant
differences between means. Data
were subjected to analyses of
variance and LSD tests (P <0.01).
Statistical tests were performed
with square-root transformed data
because the data were not
homoscedastic. Means and SE are
actual non-transformed values.

Vet. Mx., 34 (1) 2003 53


ables measured, except for area effect on honey zonas sobre la produccin, la cual no fue diferente
production, which was no different in either the low entre las zonas baja y alta (Cuadro 1). Las abejas en
or high area (Table 1). The experimental bees, in general picaron significativamente ms y fueron de
general, stung more and were smaller in the low area menor tamao en la zona baja, aunque la produccin
than in the high area, although honey production media de miel no fue diferente entre la zona baja y la
was not different between areas. However, the colo- zona alta. Sin embargo, las abejas con mitotipo africa-
nies having bees with African mitotype produced no produjeron significativamente menos miel en la
significantly less honey in the high area than in the zona alta que en la baja y su longitud de ala tambin
low area, and their wing length was also significant- fue significativamente mayor en la zona alta que en la
ly greater (Figures 1-3, Table 1). baja (Figuras 1-3, Cuadro 1).

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*

Variation origin gl Honey Yield Stings Fore-wing length

Mitotypes 2 30.65** 274.57** 0.01***


Area 1 4.93ns 118.14** 0.02***
Mitotypes*Area 2 16.05* 41.42ns 0.04**
Error 410 4.55 17.13 0.005

*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.

Stings Honey yield

Honey yield 0.01ns


Fore-wing length 0.51* 0.06ns

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-

Vet. Mx., 34 (1) 2003 55


area because these bees are less adapted to the colder yan pecoreado menos tiempo durante el da que las
conditions of the high area than European bees, which abejas europeas, que estn mejor adaptadas para volar a
are better suited to fly at lower environmental tem- temperaturas ms bajas.37
peratures.37 Los resultados tambin apoyan a los encontrados por
The results also support the findings of different diversos investigadores, quienes concluyen que las abe-
researchers who conclude that Africanized bees are jas africanizadas son altamente defensivas7-14 y de menor
highly defensive7-14 and smaller than European bees. 19,38 tamao que las europeas.19,38 Las colonias con abejas de
The colonies having bees with shorter wings were menor longitud de ala fueron ms defensivas, hecho que
more defensive, which may be a result of a higher seguramente responde a un mayor grado de africaniza-
degree of Africanization. Several studies conducted in cin. Varios trabajos han descrito una correlacin negati-
Africanized regions have reported a negative correla- va entre el tamao de las abejas y su defensividad en
tion between the size of the bees and their degree of estudios realizados en zonas africanizadas. 3,20,21,39 Sin
defensiveness.3,20,21,39 However, these correlations are embargo, estas correlaciones son fenotpicas y obedecen
phenotypic and are a consequence of selection for a una seleccin de caractersticas mltiples en abejas
multiple characteristics, and not to pleiotropic effects, africanizadas y no a efectos de pleiotropa, como lo de-
as was demonstrated by Hunt et al.40 and Guzmn- mostraron Huntet al.40y Guzmn-Novoaetal.25 A pesar de
Novoa et al.25 In spite of this, selecting bees with longer lo anterior, seleccionar abejas con alas de mayor longitud
wings may result in less defensive genotypes in Afri- puede generar genotipos menos defensivos en reas
canized areas, since there is a loss of equilibrium for africanizadas, ya que existe desequilibrio en el ligamento
African characteristics, caused by the high probability de caractersticas africanizadas, causado por la alta proba-
that virgin queens will mate with Africanized drones. bilidad de que las reinas vrgenes se apareen con znga-
Low areas apparently favor the process of African- nos africanizados.
ization, based upon the higher number of colonies Las zonas bajas aparentemente favorecen ms el pro-
having bees with African mitotype from the low area, ceso de africanizacin, lo cual se infiere del mayor nme-
as well as their shorter wings and greater defensive- ro de colonias con mitotipo africano, de la menor longitud
ness, as compared to those from the high area. It is de ala de las abejas, as como de su mayor defensividad.
possible that in high areas the cooler climate does not Esto ltimo pudiera deberse a que en las zonas altas, el
greatly favor the establishment of Africanized feral clima ms templado no favorece tanto el establecimiento
colonies, because these bees are better adapted to warm- de colonias de origen africano, pues stas se adaptan
er climates.37 This lower adaptability to high areas mejor a zonas ms clidas que a las templadas. 37 Esta
could be taken advantage of in order to install queen menor adaptabilidad a zonas altas pudiera aprovecharse
mating yards in such areas. This strategy presumably para establecer criaderos de abejas reinas en dichas zonas,
para llevar a cabo los apareamientos en vuelo libre de las
would lead to the breeding of queen bees with a higher
reinas y de esta manera criar abejas con mayor propor-
proportion of European genes.
cin de genes europeos que de africanos.
Honey production was not correlated with the size
La produccin de miel no estuvo relacionada ni con
of the bees or with their defensiveness. This means that
el tamao de las abejas ni con su comportamiento defen-
it is possible to find very defensive and productive
sivo. Esto significa que se pueden encontrar colonias
colonies, as well as very defensive and unproductive
muy defensivas y productivas y colonias muy defensi-
colonies, and vice versa. The present study is the first
vas y poco productivas y viceversa. El presente estudio
to estimate correlations between these two characteris- es el primero en estimar correlaciones entre estas dos
tics. This result is desirable for selective breeding if it is caractersticas. Este resultado es deseable para el mejo-
also true for other honeybee populations, given that if ramiento gentico, si es comn para otras poblaciones
the characteristics are not linked, it should be possible de abejas, ya que de no estar ligadas estas caractersticas,
to breed productive and manageable bees. ser posible seleccionar abejas productivas y con bajo
This study provides strong evidence that the Afri- comportamiento de defensa.
canization of commercially exploited honeybee colo- Este trabajo proporciona fuertes evidencias de que la
nies increases their defensiveness and decreases their africanizacin de colonias de abejas explotadas comer-
honey production, particularly in temperate low areas. cialmente incrementa su defensa y disminuye su produc-
The artificial introduction of European genes into the cin de miel, especialmente en las zonas bajas de regiones
populations of honeybees through the immigration of templadas. La introduccin artificial de genes europeos
Eastern European bee stocks (by regular queen re- en las poblaciones mediante la inmigracin de genotipos
placement), or through selective breeding programs de abejas de razas del este de Europa (por medio del
with the aim of increasing the frequency of European cambio frecuente de reinas), o mediante la seleccin de
characteristics while decreasing African characteris- abejas con caractersticas europeas en las poblaciones
tics, could contribute to augment honey production, locales, pudiera contribuir a disminuir el comportamien-

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.

Vet. Mx., 34 (1) 2003 57


Defensiveness and bee size were negatively corre- El comportamiento defensivo y el tamao de las
lated. Colonies whose bees had shorter wings stung in abejas estuvieron negativamente correlacionados. Co-
higher numbers than those having bees with longer lonias con abejas de menor longitud de ala picaron ms
wings. This is why it is recommended to select bees que aquellas que tuvieron abejas con alas de mayor
with long wings to breed colonies with lower defensive tamao. Por eso se recomienda seleccionar abejas con
responses. alas de mayor longitud para criar colonias con una
The degree of Africanization and the defensive re- menor respuesta defensiva.
sponses of the colonies sampled were higher in the low El grado de africanizacin y la respuesta defensiva de
area than in the high area. Therefore, it is recommend- las colonias muestreadas fue mayor en la zona baja que
able to establish queen mating yards in high areas, in en la zona alta, por lo que se recomienda establecer los
order to increase the likelihood of desirable mating. criaderos de abejas reinas en zonas altas para aumentar
la frecuencia de apareamientos deseables de las reinas.
Acknowledgments
Agradecimientos
We thank Guillermo Garca, Froylan Gutirrez, Jos Agradecemos a Guillermo Garca, Froyln Gutirrez,
Calvo, Daniel Prieto, and Ricardo Garca for their assis- Jos Calvo, Daniel Prieto y Ricardo Garca su ayuda. El
tance. This study was partially financed by INIFAP, presente estudio fue parcialmente financiado por el
and by the Supporting Program for Research and Tech- INIFAP y por el proyecto IN-201900 del Programa de
nological Innovation (PAPIIT) of the National Autono- Apoyo a Proyectos de Investigacin e Innovacin Tec-
mous University of Mexico, project IN-201900. Addi- nolgica (PAPIIT) de la Universidad Nacional Autno-
tional support was obtained from the National Insti- ma de Mxico, as como por un apoyo del Instituto
tutes of Health of the United States of America (NIH, Nacional de Salud de los Estados Unidos de Amrica
Grant GM 54850). (NIH, Grant GM 54850).

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