Documenti di Didattica
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africanizadas en Mxico
Abstract
This review article describes the colonization process and the replacement of European honey bee populations
by Africanized bees, as well as the biological characteristics that have given Africanized bees advantages for their
colonizing success, and a discussion on their impact, control, and perspectives for the Mexican beekeeping industry,
taking into consideration the beekeepers point of view with regard to their management and culture in comparison
with European bees.
Resumen
En este trabajo recapitulativo se describe el proceso de colonizacin y reemplazo de las poblaciones de abejas
melferas europeas por africanizadas, as como las caractersticas biolgicas que han dado ventajas a las abejas
africanizadas para su xito colonizador y una discusin sobre su impacto, control y perspectivas para la apicultura
mexicana, abordando el punto de vista de los apicultores respecto a su manejo y explotacin en comparacin con
abejas europeas.
F L
rom the biological point of view, the Africanized as abejas melferas africanizadas (descendientes
honey bees (descendants of Apis mellifera scutellata de Apis mellifera scutellata Lepeletier) son insectos
Lepeletier) are very successful insects, because muy exitosos desde el punto de vista biolgico,
they have been able to colonize and prevail in more porque han podido colonizar y prevalecer en ms de
than 20 American countries, replacing European bee 20 pases del continente americano, reemplazando
populations in those nations.1 The high colonizing a las poblaciones de abejas europeas en esos pases.1
ability of these insects constitutes one of the fastest and La enorme capacidad colonizadora de estos insectos
spectacular biological invasions so far known. However, constituye una de las invasiones biolgicas ms rpidas
what Latin American, and particularly Mexican honey y espectaculares de las que se tenga conocimiento.
producers (beekeepers) are more concerned about, is Sin embargo, lo que ms preocupa e interesa a los
not to know if these bees are biologically successful, but productores de miel (apicultores) en Latinoamrica
whether or not they are better than races of European y en Mxico en particular, no es saber si estas abejas
honey bees to maintain a lucrative beekeeping practice son biolgicamente exitosas, sino si son mejores o no
with them. The productivity of the beekeeping industry que las abejas de razas europeas para practicar una
in Mexico has been negatively affected by the presence apicultura lucrativa con ellas. En Mxico, esta actividad
of Africanized bees.2,3 ha sido afectada en su productividad por la presencia
de las abejas africanizadas.2,3
Historical background
Antecedentes
The western honey bee, Apis mellifera, originated in the
old world, but it was introduced into the Americas by La abeja melfera occidental, Apis mellifera, es originaria
European settlers in the XVII century.4 From the XVII del viejo mundo, pero fue trada al continente
century up to 1956, it was believed that only European americano por colonizadores europeos en el siglo
races of honey bees existed in American countries. XVII.4 desde entonces y hasta 1956 se consideraba
However, in that year, Brazilian researchers introduced que slo haba abejas melferas de razas europeas
queens of Apis mellifera scutellata, a race of honey bees en los pases americanos. Sin embargo, en ese ao,
from southern Africa, to the state of So Paulo, Brazil. investigadores brasileos introdujeron al estado de
The south American scientists tried to establish a Sao Paulo en Brasil, reinas de Apis mellifera scutellata,
selective breeding program aimed at developing bees una raza de abejas melferas del sur del continente
that were more productive and better adapted to the africano. Los cientficos sudamericanos intentaron
tropical conditions of Brazil, because they thought it establecer un programa de mejoramiento gentico
would be possible to produce more honey with tropical encaminado a desarrollar abejas ms productivas y
bees than what was being produced with bees from mejor adaptadas a las condiciones tropicales de Brasil,
temperate climates, such as the races of European ya que pensaban que se podra producir ms miel con
bees.5 As a result of this program, colonies of African abejas tropicales que lo que se estaba produciendo con
bees became feral and interbred with local populations abejas de clima templado, como las abejas de razas
of European bees, thereof, originating the so-called europeas.5 El programa dio lugar a que colonias de
Africanized or neo-tropical honey bees, which are abejas africanas se establecieran de manera silvestre
notorious for their high defensive and migratory y se aparearan con abejas europeas locales, lo que
behaviors.6 Because of these behaviors, Africanized origin las llamadas abejas africanizadas o abejas
bees got adapted and spread widely in most American neo-tropicales, que se caracterizan por su elevado
countries, including Mexico, which makes them the comportamiento defensivo y migratorio.6 Por ello, se
most successful invading organism of the last century. adaptaron y distribuyeron ampliamente en la mayora
de los pases americanos, incluido Mxico, lo que las
Evolution of honey bees in constituye en el organismo invasor ms exitoso del
temperate and tropical climates ltimo siglo.
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species that evolved in Europe and Africa, where, due de las que descendieron las que hoy existen en el pas.
to environmental effects and geographic isolation, Apis mellifera es la nica especie de abejas melferas
diversified into several races or subspecies.7 The que evolucion en Europa y frica, donde por efectos
populations of European and African honey bees were ambientales y de aislamiento geogrfico se ramific en
physically separated during more than 70,000 years, varias razas o subespecies.7 Las poblaciones de abejas
time during which they were influenced by different melferas europeas y africanas estuvieron separadas
environments. Mutations and natural selection favored por ms de 70,000 aos, tiempo durante el cual fueron
adaptations to very different conditions, which shaped influidas por distintos ambientes. Las mutaciones y la
them and generated variation in their morphological, seleccin natural propici adaptaciones a condiciones
physiological, and behavioral characteristics. This muy diferentes, lo que molde y origin variacin
isolation and adaptations to different environments en sus caractersticas morfolgicas, fisiolgicas y de
resulted in different honey bee subspecies or ecotypes, comportamiento, dando lugar a distintas subespecies
that is, bees adapted to a particular ecological region. o ecotipos de abejas; es decir, abejas adaptadas a una
It is known that there are 24 A. mellifera subspecies, ten regin ecolgica en particular. Se reconoce la existencia
of which evolved in Africa, eight in Europe and six in de 24 subespecies de la abeja melfera, A. mellifera, diez
the middle east.7 de las cuales evolucionaron en frica, ocho en Europa y
seis en el cercano oriente.7
The European environment
El medio ambiente europeo
European honey bee populations evolved in envi-
ronments characterized by well-defined seasons, Las poblaciones de abejas europeas evolucionaron
with warm summers, rich in extensive monoculture en ambientes caracterizados por estaciones del ao
blossoms that produce large amounts of nectar during bien diferenciadas, con veranos clidos, ricos en
short periods of time, and with cold and long winters.8 extensas floraciones de monocultivos que producen
Consequently, European bee populations evolved cantidades copiosas de nctar por periodos cortos y
through adaptations that favored the collection and con inviernos fros y prolongados.8 En consecuencia,
storage of large quantities of honey and pollen during las poblaciones de abejas europeas evolucionaron
summers, to survive winters, because winters are too mediante adaptaciones que favorecan la recoleccin
cold for the bees to fly out of their nests to collect y almacenamiento de grandes cantidades de miel y
food (to forage). Additionally, colonies that nested in polen durante el verano para sobrevivir el invierno, ya
unprotected sites died, while those that were kept by que en esta poca del ao hace demasiado fro como
beekeepers in man-made hives, survived. Moreover, para que las abejas puedan volar y recolectar alimentos
the colonies that were too defensive were eliminated, (pecorear). Adems, las colonias que anidaban en
while those that were gentle were protected and cared sitios desprotegidos moran, mientras que las que eran
for by beekeepers.9 alojadas en colmenas artificiales construidas por los
apicultores, sobrevivan. Adicionalmente, las colonias
The environment of southern Africa muy defensivas eran eliminadas, mientras que las
dciles eran protegidas y cuidadas por los apicultores.9
The climate of this African region is predominantly
sabana or open forest, hot, with long dearth periods, El medio ambiente del sur de frica
and with sporadic rains; this climate favors the
existence of abundant nectar and pollen-producing El clima de esta regin de frica es predominantemente
plants. The honey bee races that have evolved in this de sabana o bosque abierto, es caliente, con largos
region, mainly A. m. scutellata, are well adapted to this periodos de sequa y lluvias espordicas; este clima
habitat.1 These bees tend to swarm (the colony divides da lugar a la existencia de abundantes plantas
itself into two groups of bees, with the queen and the productoras de nctar y polen. Las razas de abejas
oldest workers abandoning their original colony to get que han evolucionado en esta regin, principalmente
established in another dwelling, and with a new queen A. m. scutellata, estn bien adaptadas a este hbitat.1 Estas
remaining with the population of younger workers in abejas enjambran (la colonia se divide en dos, con la
the original dwelling) or abscond (all the bees of a reina y las obreras ms viejas abandonando su colonia
colony abandon the hive to seek a new dwelling where original para establecerse en otro sitio, quedndose
to nest) frequently, and nest in open sites, favored by una reina nueva con la poblacin de obreras ms
the dry and hot environment of the region. Therefore, jvenes) o se evaden (la totalidad de las abejas de una
their swarms, even the smallest, have high probabilities colonia abandona la colmena para buscar un nuevo
of survival, particularly when they migrate to locations lugar donde anidar) con frecuencia, y anidan en sitios
152
Africanized bees.6 There is another version about enjambraron con las reinas africanas originales. Estos
the origin of these bees, in the sense that Brazilian enjambres se establecieron de manera silvestre, se
bee researchers distributed Africanized queens to reprodujeron y se cruzaron con la poblacin local de
beekeepers.13 Regardless of which of these two possible abejas de razas europeas (principalmente A. m. mellifera),
ways these bees originated from, Africanized bees are lo que dio lugar a las hoy llamadas abejas africanizadas.6
the result of the hybridization of African and European Existe otra versin sobre el origen de estas abejas, en
races of honey bees, and thus, their descendants carry el sentido de que los mismos investigadores brasileos
germplasm of both origins.1 distribuyeron reinas africanizadas e hbridas entre los
apicultores.13 De cualquiera de las dos maneras en
Biological characteristics and behavior que se hayan originado, las abejas africanizadas son
el resultado de una hibridacin entre razas de abejas
Characterizing Africanized bees with precision is europeas y africanas y sus descendientes conllevan
complicated because there is high variability among germoplasma de ambos orgenes.1
colonies for many traits due to their hybrid nature. In
spite of this fact, it is possible to make some general Caractersticas biolgicas
distinctions between these bees and European races y comportamiento
of bees for the following characteristics that are
summarized in Tables 1 and 2. Caracterizar de manera precisa a las abejas africanizadas
es complicado porque debido a su naturaleza hbrida
Developmental time existe variabilidad entre sus colonias para muchas
caractersticas. A pesar de ello, pueden hacerse algunas
The development of an adult bee occurs, like in other distinciones generales entre estas abejas y las de razas
holometabolous insects, through a developmental and europeas para las siguientes caractersticas, las cuales
transformation process that begins with an egg laid by se resumen en los Cuadros 1 y 2.
a queen and that ends with the emergence of an adult
bee from a comb cell. In average, it takes 21 days for Tiempo de desarrollo
workers of European honey bee races to develop and
emerge as adults, from the time that a queen lays an La formacin de una abeja adulta ocurre como en
egg, while Africanized workers emerge 18.5 days after otros insectos holometbolos, mediante un proceso
an egg is laid.2 One consequence of these differences de desarrollo y transformacin que inicia con la
in developmental time is that Africanized bee colonies postura de un huevo por una reina y concluye con la
produce workers at a faster rate than do colonies salida de un adulto de una celda del panal. Las abejas
of European bees. Regarding queens and drones obreras de razas europeas tardan, en promedio, 21
(male bees) there are no significant differences in das en desarrollarse y emerger desde que una reina
developmental time between these two types of bees.14 pone un huevo, mientras que las obreras africanizadas
emergen a los 18.5 das a partir de que el huevo es
Size and weight puesto.2 Una consecuencia de estas diferencias en
su tiempo de desarrollo es que las colonias de abejas
Africanized bees are approximately 10% smaller (length africanizadas producen obreras a un ritmo ms rpido
12.7 mm Africanized workers vs 13.9 mm European que las colonias de abejas europeas. Para el caso de
workers) and 33% lighter than European bees (62 mg reinas y znganos (abejas macho) no hay diferencias
Africanized workers vs 93 mg European workers); this significativas en cuanto al tiempo de desarrollo entre
is why they build combs with smaller cells.12 The cell estos dos tipos de abejas.14
dimensions of a European honey bee comb range from
5.2 to 5.5 mm in diameter, while the range for cells of Tamao y peso
Africanized bee combs is 4.6 to 5.0 mm.12
Las abejas africanizadas son aproximadamente 10% ms
Reproduction and swarming pequeas (longitud de 12.7 mm obreras africanizadas
contra 13.9 mm europeas) y 33% menos pesadas que
The populations of Africanized bee colonies grow las europeas (62 mg obreras africanizadas contra 93 mg
much more faster that those of European bees. Among europeas); por ello construyen panales con celdas ms
other factors, this is due to the fact that Africanized pequeas.12 Las dimensiones de las celdas de un panal
queens are exceptionally prolific; they can lay close de abejas europeas van de 5.2 a 5.5 mm de dimetro,
to 3,000 eggs per day, while European queens rarely mientras que las de los panales de abejas africanizadas
lay more than 2,000 eggs in that period of time.15 The miden entre 4.6 y 5.0 mm.12
Cuadro 2
Comparacin relativa entre abejas europeas y africanizadas en cuanto a caractersticas de importancia
econmica que pudieran conferir ventajas de produccin y manejo a los apicultores
Relative comparison between European and Africanized bees for characteristics of economic
importance that could confer advantages in production and management to beekeepers
154
brood combs of Africanized bee colonies are usually Reproduccin y enjambrazn
almost totally occupied by larvae and pupae, even at
their top corners, which is extremely rare to observe Las poblaciones de colonias de abejas africanizadas
on combs of European bees, because this type of bees crecen con mayor rapidez que las europeas. Esto
generally fill those spaces with honey.12 se debe, entre otros factores, a que las reinas son
The swarming process, or the split of the population excepcionalmente prolficas, pudiendo llegar a poner
of individuals of a colony, constitutes a natural form cerca de 3,000 huevos por da, mientras que las reinas
of bee reproduction that yields two or more colonies, europeas raramente exceden de 2,000.15 Los panales
each with its respective queen.8 Africanized bees de una colonia de abejas africanizadas en desarrollo
swarm much more frequently than European bees; se observan casi totalmente cubiertos de cra, incluso
one colony of Africanized bees may originate more en sus esquinas superiores, lo cual es extremadamente
than eight swarms in a single year, while European bee raro de observar en panales de abejas europeas, debido
colonies, only in rare occasions produce more than a que estas abejas generalmente llenan esos espacios
one of them. At the same time, these swarms can also con miel.12
multiply and colonize new areas. Otis15 found that a La enjambrazn, o divisin de la poblacin de
single colony of Africanized bees could yield up to 16 individuos de una colonia, es la forma de reproduccin
colonies in one year. natural de las abejas para formar dos o ms colonias, cada
Some of the reasons why Africanized bee colonies una con su respectiva reina.8 Las abejas africanizadas
swarm more frequently than Europeans, is that son significativamente ms enjambradoras que las
they build smaller nests, and the nectar and pollen europeas; una misma colonia de abejas africanizadas
they gather from flowers are mainly invested in the puede originar ms de ocho enjambres en un solo
production of more bees in lieu of being stored.15 The ao, mientras que una de europeas en raras ocasiones
high reproductive and swarming rates of Africanized produce ms de uno. Estos enjambres, a su vez, tambin
bees are an ideal preadaptation that has favored their pueden multiplicarse y colonizar nuevas reas. Otis15
successful colonization of tropical regions in the encontr que de una colonia de abejas africanizadas
Americas. podran formarse hasta 16 de ellas en un ao.
Algunas de las razones por las que las colonias de
Absconding abejas africanizadas enjambran con mayor frecuencia
que las europeas es que construyen nidos de menor
Absconding occurs when all of the individuals of a tamao y el nctar y polen que recolectan son recursos
colony abandon the hive and migrate to a new dwelling, que destinan, en mayor medida, a la produccin de
a characteristic frequently expressed by Africanized ms abejas en vez de almacenarlos.15 Las elevadas
bees. Absconding takes place because these insects are tasas de reproduccin y enjambrazn de las abejas
highly susceptible to disturbances caused by predators, africanizadas son una preadaptacin ideal que ha
noise, excessive management, intense heat, and favorecido su exitosa colonizacin en las regiones
shortage of water and feed. Absconding occurs at a tropicales del continente americano.
very low frequency in colonies of European bee races,
but it can be observed in 30 to 100% of Africanized Evasin
bee colonies.13
La evasin o emigracin de la totalidad de los
Nesting individuos de una colonia es una caracterstica que las
abejas africanizadas manifiestan con mucha frecuencia.
Africanized honey bees are less selective than Este comportamiento se debe a que estos insectos
Europeans in choosing sites to establish their nests. son altamente susceptibles a disturbios causados por
For example, they can nest in the open air as well as depredadores, ruido, manejo excesivo, calor intenso,
in cavities, while European bees rarely nest in open y a la escasez de agua y alimentos. La evasin de
spaces. Moreover, Africanized bee nests are often colmenas se presenta con muy poca frecuencia en las
smaller than those of European bees.14 Consequently, abejas de razas europeas, pero en africanizadas puede
they are more adaptable to a wide range of conditions; observarse desde 30 hasta 100% de las colmenas.13
hence it is easier for them to find nesting sites in the
tropics. Anidacin
Thermoregulation Las abejas africanizadas son menos selectivas que
las europeas para establecer sus nidos. Por ejemplo,
Honey bee colonies can thermoregulate their nests. pueden anidar tanto al aire libre como en cavidades,
156
between Africanized and European bees has to do with a la recoleccin de nctar aporta a su colonia.20-22
their foraging force, that is, the proportion of bees that Sin embargo, es claro que las abejas africanizadas se
forage in relation to the total number of individuals especializan ms en la recoleccin de polen que de
present in a colony in a given time. Research has nctar. Danka et al.23 compararon la proporcin de
shown that in general, European bee colonies launch abejas pecoreadoras que se dedicaban a la recoleccin
a larger proportion of individuals to forage than do de polen entre colonias africanizadas y europeas en
Africanized colonies, which gives them an advantage Venezuela, y encontraron que ms de 30% de las abejas
for food collection, particularly for the collection of de colonias africanizadas realizaban viajes de polen,
nectar.18,20 mientras que menos de 15% de las europeas lo hacan.
Worker bees that find nectar or pollen in the field, Fewell y Bertram24 corroboraron estos resultados en
communicate the location of the flowers to their nest Arizona.
mates through dances, with the aim of directing them Otra diferencia importante es en cuanto a la fuerza
to that location. And even though all subspecies of de pecoreo, es decir, la proporcin de abejas que
honey bees use this recruiting mechanism to direct pecorean del total de individuos presentes en una
other workers to flowers, Africanized bees tend to colonia en un momento dado. Las investigaciones
depend less on this mechanism in comparison with han mostrado que en general, las colonias de abejas
European bees. This difference in foraging strategy europeas destinan una mayor proporcin de sus
can be explained by the fact that in the tropics, individuos a pecorear que las de abejas africanizadas, lo
blossoms are more varied and less continuous than in cual les da una ventaja en la recoleccin de alimentos,
temperate zones, where there is less variety of plants particularmente de nctar.18,20
(monocultures), but more density of those existing, Las abejas que encuentran nctar o polen
and therefore, it is more profitable for honey bee comunican a sus compaeras la ubicacin de las flores
colonies to depend on individual foraging.20,22 por medio de danzas para dirigirlas a dicho lugar.
Y aunque todas las subespecies de abejas melferas
Robbing behavior utilizan este mecanismo de reclutamiento hacia las
flores, las abejas africanizadas tienden a depender
Robbing behavior is a type of mistaken foraging menos de l en comparacin con las europeas. Esta
in which bees of one colony steal honey reserves of estrategia de pecoreo es explicable por el hecho
another colony. Africanized bees tend to rob more de que en los trpicos la floracin es ms variada y
intensively than European bees, and this behavior is discontinua que en las zonas templadas, donde hay
acutely expressed, particularly during nectar dearth menos variedad de plantas (monocultivos), pero
periods.1 Robbing behavior is harmful to honey bee mayor densidad de aqullas que existen y por lo tanto,
colonies not only because some of them lose food es ms rentable depender del pecoreo individual.20,22
reserves, but also because this behavior favors the
transmission and spread of diseases in apiaries.2 Pillaje
158
been the characteristic more frequently evidenced in cra de abejas hbridas (africanizada x europea) fue
the scientific literature as well as in the massive media tan susceptible como la cra de abejas europeas, lo
of communication. Some media have coined them the que sugiere un tipo de dominancia gentica para la
title of killer bees, thus, the general public sees them caracterstica de alta atraccin. Otros estudios tambin
as a pest rather than as a beneficial insect. However, even han sugerido que la cra de abejas africanizadas resulta
when it is clear that Africanized bees are more defensive menos atractiva y desfavorable para la reproduccin
than their European counterparts, it is also true that this de varroa en comparacin con la cra de abejas
problem has been exaggerated through terror movies, europeas.37 La razn de esta menor atraccin no
books, documentaries, and articles describing the most est del todo clara, pero parece que puede deberse a
fantastic stories about these insects aggressiveness and diferencias cualitativas y cuantitativas en las feromonas
danger; but these characterizations of Africanized bees de atraccin producidas por las larvas de las abejas.25
lack scientific objectivity. To place things in context,
Africanized bees have caused the death of about Defensa
1 000 people in 30 years according to mortality statistics
in Latin America;38 this is equivalent to an average of El alto comportamiento de defensa ha sido la
slightly over 33 people killed by bees in a year. In this caracterstica ms evidente de las abejas africanizadas
same region of the world, over 900 000 people die as tanto en la literatura cientfica como en los medios
a consequence of cardiovascular diseases every year.39 masivos de comunicacin. Algunos medios les han
While it is regrettable that fatalities due to bee stinging acuado el mote de abejas asesinas y por ello son vistas
incidents occur, it is also true that the number of ms como una plaga que como un insecto benfico, al
deaths due to this cause is relatively insignificant when menos por el pblico en general. Sin embargo, si bien
compared to other causes of mortality. Unfortunately, es cierto que las abejas africanizadas son ms defensivas
this public health problem has created an environment que las europeas, tambin es cierto que se ha exagerado
of fear and antagonism towards bees in the general el problema a travs de pelculas de terror, libros,
public of different countries, without consideration reportajes y artculos que describen las ms fantsticas
that the actual health risks that these insects pose are historias acerca de la agresividad y el peligro de estos
relatively low. insectos, pero estas caracterizaciones de las abejas
When bee types are compared, there is no question africanizadas carecen de objetividad cientfica. Para
that Africanized bees are significantly more defensive poner las cosas en contexto, las abejas africanizadas han
than European bees. Initially, it was thought that when ocasionado la muerte de ms de 1 000 personas en 30
interbreeding with European bees, the descendants aos de estadsticas de mortalidad en Latinoamrica,38
of Africanized bees would reduce their defensive lo que corresponderan a poco ms de 33 personas
behavior. However, multiple studies have repeatedly muertas por ao, en promedio. En esa misma regin del
shown that Africanized bees may sting 5 to 20 times mundo mueren cada ao ms de 900 000 personas por
more than bees of European origin; they also have a enfermedades cardiovasculares.39 Si bien es lamentable
patrolling ratio around their nests that is at least 10 que ocurran decesos por picaduras de abejas, tambin
times wider than that of European bees.40-44 Africanized es cierto que el nmero de muertes por esta causa es
bees respond faster than European bees to defensive relativamente insignificante si se le compara con el
stimuli too.44,45 Africanized bees respond faster and in de otras causas de mortalidad. Desafortunadamente
greater numbers to defensive stimuli than European este problema de salud pblica ha creado un clima de
bees because they have a lower response threshold to miedo y antagonismo hacia las abejas entre el pblico
these stimuli than their European counterparts (they en general en distintos pases, sin considerar que los
are more sensitive). Additionally, Africanized bee riesgos reales a la salud que estos insectos representan
colonies pursue intruders with 10 to 30 times more son relativamente bajos.
individuals than do colonies of European bees.46,47 Cuando se compara entre tipos de abejas, no hay
Honey bee defensive behavior is highly herita- duda de que las abejas africanizadas son significati-
ble.40,42,48-50 Additionally, this trait seems to be influenced vamente ms defensivas que las europeas. Inicialmente
by genetic dominance effects40,43,51,52 as well as by se crea que al cruzarse con abejas europeas, los
paternal effects, meaning that the progeny shows a descendientes de las abejas africanas disminuiran su
defensive behavior that more closely resembles that of comportamiento defensivo. Sin embargo, mltiples
the paternal colony rather than that of the maternal estudios han mostrado repetidamente que las abejas
one (Table 3).51,53 de origen africano pueden picar de 5 a 20 veces ms
Most of the people and animals that have died as a que las de origen europeo y que mantienen un radio
consequence of bee stings, have passed away as a result de patrullaje en la periferia de sus nidos de al menos 10
of a toxic or an anaphylactic reaction, after receiving veces mayor distancia que el de abejas europeas.40-44 Las
160
Cuadro 3
Nmero promedio de aguijones clavados por las abejas en un parche de cuero
en un minuto, en pruebas de comportamiento de defensa de colonias de abejas
europeas, africanizadas e hbridas, en estudios llevados a cabo en Mxico*
Mean number of stings left by the bees on a leather patch in one minute, in defensive
behavior tests using European, Africanized, and hybrid bee colonies from studies
conducted in Mexico*
European 31 20
Africanized 32 110
F1 (European mother x Africanized father) 24 121
F1 (Africanized mother x European father) 28 69
*Data of Guzman-Novoa et al.53
in more than 95% of the countrys beekeeping regions; Se cree que los primeros enjambres de abejas
therefore, it can be said that they are an example of a africanizadas entraron a Mxico por Chiapas a finales
very successful invading organism. Morphometric and de 1986, 29 aos despus de su origen y migracin
mitochondrial DNA data suggest that there has been desde Brasil.59 Al principio y por varios aos estuvieron
a greater degree of African gene introgression in the dispersndose en el sureste del pas. En 1987 ya haban
bee populations of the Gulf coast, in comparison with sido localizadas en los tres estados de la pennsula
those of the countrys high plateau, and those of the de Yucatn, adems de Oaxaca, Tabasco y el sur de
pacific coast;60 this pattern of Africanization probably Veracruz. Para 1989, llegaron a Guerrero, Michoacn
occurred because of the more humid conditions y Tamaulipas, y en el altiplano, los primeros enjambres
and higher abundance of blossoms of the Gulf coast de abejas africanizadas se encontraron en 1990.60 Para
relative to the other two regions of the country, which 1993, ya se haban detectado en todo el territorio
favored the colonization of this region. nacional, excepto en Baja California Sur, donde el
The Africanized bees continued spreading desierto sirvi de barrera natural para retrasar su
throughout Mexico reaching the United States of llegada, la cual ocurri hasta 2005.60,61 Las abejas
America (USA) through Texas by 1990.63 During the africanizadas han ido reemplazando a las europeas a
21 years these bees have existed in the USA, their medida que se han expandido por Mxico;62 hoy da
dispersion and colonization speed has slowed down, se encuentran bien establecidas en ms de 95% de las
apparently because of low winter temperatures and regiones apcolas del pas, por lo que se puede decir
differences in photoperiod, conditions to which que son ejemplo de un organismo invasor muy exitoso.
tropical bees do not adapt well.64 However, these bees Datos morfomtricos y de ADN mitocondrial sugieren
are well distributed throughout the southern part of que hubo un mayor grado de introgresin de genes
the country.57 So far they have been found in the states africanos en las poblaciones de abejas de la costa del
of Texas, New Mexico, Arizona, California, Nevada, golfo en comparacin con poblaciones del altiplano
Florida, Louisiana, and Arkansas.13,57 y de la costa del pacfico,60 debido probablemente, a
las condiciones ms hmedas y de mayor floracin
The process of Africanization del golfo, que favorecieron ms su colonizacin, en
relacin con otras regiones del pas.
The Africanized bees have retained a predominantly Las abejas africanizadas continuaron su avance
African genotype because there has been a greater flow y llegaron a los Estados Unidos de Amrica (EUA)
of African genes towards European bee populations por Texas en 1990.63 En los 21 aos que estas abejas
than the other way around.56,65-71 Both, feral and llevan en los EUA, su expansin se ha desacelerado,
managed colonies manifest African bee traits within aparentemente debido a las bajas temperaturas
just a few years of the arrival of the first swarms of invernales y a diferencias en el foto periodo, condicio-
Africanized bees to a region; this process is known as nes a las que no se adaptan bien las abejas tropicales.64
Africanization.72 Sin embargo, estas abejas estn bien distribuidas al sur
The Africanization of honey bee colonies has not del pas.57 En la actualidad, se localizan en los estados
been due to a single factor, but to the interaction of de Texas, Nuevo Mxico, Arizona, California, Nevada,
several mechanisms, that together have caused the Florida, Louisiana y Arkansas.13,57
replacement of populations of European bee races
162
introgression of European genes into Africanized bee Superioridad numrica y comportamiento
populations. de los znganos
Colony usurpation Las colonias africanizadas producen una mayor
cantidad de znganos que las europeas14,66 y stos se
Colony usurpation is a type of reproductive parasitism introducen con frecuencia a las colmenas manejadas
occurring in some species of social insects that is de abejas europeas, donde su alto nmero inhibe
frequently expressed in honey bee populations of la produccin de ms znganos por parte de esas
African descent. Swarms of Africanized bees penetrate colonias, lo que puede considerarse como parasitismo
hives inhabited by European bees, kill the resident de znganos africanizados.66 El nmero de znganos
queens and replace them with their own queens, thus, africanizados en las reas de congregacin (reas en
becoming the new mothers of these colonies. Several el aire donde las abejas se aparean) puede superar el
studies have shown that the percentage of European 80% de la poblacin total de machos.66,78 Los znganos
bee colonies usurped by Africanized bee swarms may africanizados dominan los apareamientos no slo
represent between 5 and 40% of the cases of colony por su mayor nmero, sino tambin porque llegan
Africanization.79-81 The mechanisms that regulate ms temprano y permanecen ms tarde en las reas
colony usurpation are virtually unknown, and thus, it is de congregacin que los znganos europeos.12 Estos
difficult to explain how the bees of invaded colonies do factores favorecen la introgresin paterna de genes
not defend themselves from the invading bees and allow africanos a las poblaciones de abejas europeas, con
them to enter into their hives. It has been proposed muy poca introgresin de genes europeos en sentido
that Africanized bees release pheromones that facilitate inverso.
their entrance into European bee colonies.13
Usurpacin de colonias
Dominance of African genes
La usurpacin de colonias es una forma de parasitismo
Honey bees start showing African-like behaviors, reproductivo que ocurre en algunos insectos sociales
even in areas with high numbers of European bee y que est altamente acentuado en las poblaciones
colonies that have been recently colonized by swarms de abejas de origen africano. Enjambres de abejas
of Africanized bees.66,67,69 Thus, it is inferred that africanizadas penetran en las colmenas habitadas
some of these behaviors are influenced by genetic por abejas europeas, matan a las reinas residentes y
dominance, and even though this dominance may las reemplazan por sus propias reinas, las cuales se
not necessarily lead to the loss of European genetic convierten en las nuevas madres de esas colonias. Varios
markers, it contributes to the preservation of the estudios han demostrado que la africanizacin de
African phenotype. colonias por medio de la usurpacin puede representar
It has been found that there are genetic dominant entre 5 y 40% de los casos.79-81 Los mecanismos que
effects of African origin for certain components of regulan la usurpacin de colonias son virtualmente
the foraging behavior of honey bees,24,76 as well as for desconocidos y por ello es difcil explicar cmo las
behaviors that confer resistance to bees against the abejas de las colonias invadidas no se defienden
parasitic mite Varroa destructor.36,72 However, most of the de las abejas invasoras y permiten su entrada. Se ha
studies conducted on genetic dominance have been especulado que la liberacin de feromonas por parte
focused on the defensive behavior of bees. Hybrid de las abejas africanizadas les facilita su entrada a las
colonies of European mother and Africanized father colonias de abejas europeas.13
show defense levels similar to those of Africanized
bee colonies.43,51,52,82 Conversely, hybrid colonies of Dominancia de genes africanos
Africanized mother and European father are less
defensive than Africanized colonies, but significantly Las colonias de abejas empiezan a mostrar compor-
more aggressive than European colonies.51,53 These tamientos de origen africano, aun en reas recientemente
results suggest that defense traits of African origin are colonizadas y con alto nmero de colonias de origen
genetically dominant and that the defensive responses europeo.66,67,69 Por ello se deduce que algunas de
of colonies are mainly affected by paternal effects estas caractersticas exhiben dominancia gentica, y
rather than by maternal effects. aunque esta dominancia no necesariamente conduce
Considering all of the above, it can be concluded a la prdida de marcadores genticos europeos, s
that Africanized bees have spread, colonized, and contribuye a la preservacin del fenotipo africano.
prevailed in the new world, because they are better Se ha encontrado que hay efectos de dominancia
adapted to the tropical environment of the majority de genes de origen africano para ciertos aspectos del
164
Relocation of apiaries est hoy en da afectada por una variedad de problemas,
siendo las abejas africanizadas uno de los factores que
Most of the apiaries have been relocated to distances ms daa a esta actividad. El tener que trabajar con
of at least 200 m from houses, farms, animal pens, and abejas africanizadas ha forzado una serie de cambios
other locations where animals are kept captive. The en el manejo de las colonias.
number of hives per apiary has been reduced too, and
hives are installed on individual bases to prevent that Cambios en el manejo de las colonias
aggressive colonies alter the behavior of the rest of
the colonies in an apiary. The relocation of apiaries La mayora de los cambios de manejo que se han
has not been uniform across the country and has establecido en la prctica apcola mexicana se
been difficult to achieve in locations where not many han implementado con base en la experiencia e
secondary roads exist.87 investigacin que sobre estas abejas se ha obtenido
en Sudamrica, particularmente en Brasil.3,85,86 Entre
Protection and management equipment los principales cambios en el manejo de las abejas se
pueden mencionar los siguientes:
When beekeeping was practiced with European races
of bees, Mexican beekeepers used to manage them Reubicacin de apiarios
wearing light clothes such as cotton pants and t-shirts;
they even used sandals and a simple veil. Managing La mayora de los apiarios han sido alejados al menos
Africanized bees wearing such clothes and protective 200 metros de casas, granjas, establos y otros sitios
equipment could be fatal. Therefore, beekeepers have donde se mantienen animales cautivos. Tambin el
invested in better protection equipment, such as thick nmero de colmenas por apiario se ha reducido y las
coveralls, boots, gloves, and square-framed veils (veils colmenas se instalan en bases individuales para evitar
that do not touch the beekeepers face). Additionally, que colonias agresivas alteren el comportamiento de
larger smokers have been built to produce more smoke las dems colonias en el apiario. La reubicacin de
for longer time, to pacify the bees.87 apiarios no ha sido uniforme en todo el pas y se ha
dificultado en sitios donde no hay muchos caminos
Requeening secundarios.87
166
colonies in most countries where Africanized bees abejas africanizadas. Veinte aos despus de su arribo,
have become established, in Brazil, it has increased en 2006, la produccin super las 56 000 ton y la
to levels well above what was produced prior to the exportacin alcanz las 29 000,83 lo que refleja un ligero
Africanization of bee colonies in that country. Thus, incremento con respecto a diez aos antes (Figuras
there is controversy with respect to whether or not 1 y 2). El rendimiento medio de miel por colmena
Africanized bees are more productive than European tambin disminuy en aproximadamente 25% luego
bees.1,20,86 However, the main reason behind this de la llegada de las abejas africanizadas. Sin embargo,
controversy is the fact that there have been very few la productividad por colmena se ha recuperado
studies comparing honey production between these parcialmente en la ltima dcada (Figura 3). Este patrn
two types of bees. Additionally, the majority of these de decremento en la produccin de miel, seguido de
studies were conducted with an insufficient number un incremento posterior, es consistente con lo que
of colonies (small sample size), which does not allow ha ocurrido en Brasil y Venezuela. Inicialmente, los
to draw valid conclusions, because between colony apicultores experimentaron una prdida de colmenas
variation for this trait is very high.45 In addition to all y de produccin y conforme adoptaron nuevos
of the above, the results of these studies have been mtodos de manejo y repusieron o incrementaron el
inconsistent. For example, Kerr,5 using ten colonies nmero de colonias perdidas, la produccin de miel
per treatment, found that Africanized bees were fue aumentando gradualmente.
more productive than Europeans. Rinderer et al.,22 Aunque la produccin de miel no se ha recuperado
also with ten colonies per treatment, concluded that a niveles previos a la africanizacin en la mayora de los
European bees were more productive than Africanized pases donde las abejas africanizadas se han establecido,
bees. Finally, Spivak et al.,94 using seven colonies en Brasil la produccin ha aumentado muy por encima
per treatment, did not find differences in honey de lo que se produca antes de la africanizacin de
production between these two bee types. Then, who las colonias de abejas en ese pas, razn por la cual
to believe? existe controversia respecto a si estas abejas son o no
Actually, when Brazils information is analyzed ms productivas que las europeas.1,20,86 Sin embargo,
in more detail, it can be found that during the first la principal razn de la controversia es el hecho de
15 years after the introduction of African bees into que se han realizado muy pocos estudios comparativos
that country, honey production decreased from over entre estos dos ecotipos de abejas. Adems, los pocos
7 000 ton a year to less than 5 000, a reduction of estudios realizados se llevaron a cabo con un nmero
about 35%.86 However, Brazils honey production reducido de colmenas (bajo tamao de muestra), lo
has increased considerably during the last 30 years, cual no permite obtener conclusiones vlidas, porque
more as a consequence of the colonization and la variacin para esta caracterstica entre colonias es
establishment of large citrus and eucalyptus plantations muy alta.45 Encima de todo ello, los resultados de esos
in the Amazon region (these plantations yield large estudios han sido inconsistentes. Por ejemplo, Kerr,5
quantities of nectar), which allowed the establishment con diez colonias por tratamiento, encontr que las
abejas africanizadas eran ms productivas que las
80000 74613
60000
70000
49178
Tons of honey
50000 40000
40000
30000 27419
25470
30000
20000
20000
10000 10000
0 0
1986 1996 2006
1986 1996 2006
Year Year
Figura 1. Produccin de miel en Mxico el ao de la llegada de Figura 2. Exportacin de miel en Mxico el ao de la llegada de
las abejas africanizadas (1986), 10 aos despus (1996) y 20 aos las abejas africanizadas (1986), 10 aos despus (1996) y 20 aos
despus (2006) de ese hecho (Sagarpa 2009).83 despus (2006) de ese hecho (Sagarpa 2009).83
Figure 1. Honey production in Mexico the year of the arrival of Figure 2. Honey exports in Mexico the year of the arrival of
Africanized bees (1986), 10 years later (1996), and 20 years later Africanized bees (1986), 10 years later (1996), and 20 years later
(2006) (Sagarpa 200983). (2006) (Sagarpa 200983).
168
Cuadro 4
Produccin promedio de miel por colmena de colonias de abejas europeas,
africanizadas e hbridas, en estudios llevados a cabo en Mxico*
Average honey production per hive of European, Africanized, and hybrid bee colonies
from studies conducted in Mexico*
40
the company lost most of its colonies and sold others.
Acapulco Miel and Veramiel, companies that managed 30
more than 15 000 hives each, totally disappeared from
the market.87 Contrary to these losses, there has been 20
a notable resurgence of small scale beekeepers and
sideliners, that is, beekeepers owning between 20 and
10
500 hives.93 These beekeepers adapted themselves
from the beginning of their activities, to work with
0
management techniques more suitable to the behavior 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001
of Africanized bees.
Year
170
considering that complaints about animals being por ao entre 1996 y 2002 (1.7 personas muertas por
stung and killed by bees in all beekeeping regions of cada milln de habitantes).96 De las cifras anteriores se
Mexico are very common.93 The direct consequence desprende que es al menos cinco veces ms probable
of the aggressive behavior of bees on the beekeeping morir por picadura de alacrn que por picaduras de
industry is that some beekeepers abandon the activity abejas en Mxico. Asimismo, la probabilidad de morir
or reduce their colony numbers, because finding en un accidente automovilstico o de una enfermedad
locations suitable for bee yards has become increasingly cardiaca es 375 y 5,500 veces ms alta en comparacin
more difficult. Land-owners who have fields suitable con la posibilidad de morir por picaduras de abejas
for apicultural practices do not easily accept the melferas.
placement of hives within their property because they Por otro lado, aunque no existen estadsticas sobre
want to avoid the problems that bee stinging incidents el nmero de animales muertos, ste seguramente
could cause them. Furthermore, if locations are found es de miles, a juzgar por lo comn que es escuchar
that do not pose this type of risk, they usually are not quejas sobre animales picados y muertos en todas las
easily accessible, which does not allow to provide a regiones apcolas de Mxico.93 La consecuencia directa
good management to the bees.93 de esta agresividad de las abejas en la apicultura, es
When cases of stinging incidents involving humans que los apicultores abandonan la actividad o reducen
or animals happen, the beekeeper normally pays for su nmero de colmenas, pues el encontrar sitios
medical expenses and for the animals killed by the apropiados para establecer apiarios se ha dificultado.
bees, when it can be demonstrated that the beekeepers Los propietarios que cuentan con terrenos aptos para
bees were responsible of the attack. The affected party desarrollar actividades apcolas no aceptan fcilmente
contacts the beekeeper and in most cases they settle la instalacin de colmenas, ello, para evitar los
out of court.87 problemas que les pudieran ocasionar los accidentes
provocados por piquetes de abejas. Por otro lado,
Impact on crop pollination los lugares que no presentan este tipo de riesgo, por
lo general son poco accesibles como para dar una
Africanized bees are as efficient as European bees as atencin adecuada a las abejas.93
pollinators of crops.97 However, it is more complicated Cuando se presentan casos de picaduras de personas
to manage and transport bees that are highly o animales, los apicultores normalmente pagan los
Africanized, because apparently they get more stressed gastos mdicos y el valor de los animales cuando se
than European bees when transported.98 This response demuestra que las abejas del productor fueron las
leads to higher absconding and mortality rates, which responsables de un ataque. La parte afectada contacta
results in weaker colonies and in less hives available al apicultor y se arreglan fuera de foros judiciales en
for rental purposes. Furthermore, stinging incidents casi todos los casos.87
involving agricultural workers increase when dealing
with Africanized bees; this problem difficults their Impacto en la polinizacin
management and compromise future hive rentals de cultivos agrcolas
for the beekeeper. Javier Pompa, the beekeeper who
owns and rents more colonies for crop pollination in Las abejas africanizadas son polinizadoras tan eficientes
Mexico, experienced a dramatic impact in his business como las europeas.97 Sin embargo, resulta ms compli-
of almost 10 000 hives, when as a consequence of the cado manejar y transportar abejas altamente africani-
Africanization of his colonies he lost around 7 000 of zadas, porque aparentemente se estresan ms que las
them due to absconding in a single year. Mr. Pompa europeas durante las movilizaciones.98 Esto conduce
made changes in the way he managed his colonies and a una mayor evasin y mortalidad de colonias, lo que
requeened them with European, imported queens, deja al apicultor con colonias dbiles y con menos
on an annual basis; thanks to these measures, he was colmenas para rentar. Adems, los accidentes de
able to recover and exceed his original number of picaduras a trabajadores agrcolas se incrementan
colonies.99 con abejas africanizadas, lo que hace difcil su manejo
Africanized bees tend to collect more pollen and y compromete futuras rentas para el apicultor. Javier
propolis than European bees;23 this tendency could Pompa, el apicultor con mayor nmero de colmenas
be an advantage for beekeepers who harvest these dedicadas a la polinizacin de cultivos en Mxico,
products. However, it is necessary that the market experiment un dramtico impacto en su negocio
and the price for pollen and propolis grow (they are de casi 10 000 colmenas, cuando perdi alrededor de
currently low) to incentive more beekeepers to collect 7 000 de ellas en un solo ao debido a la evasin de las
these hive products, so that keeping Africanized bees abejas de las colmenas por efecto de la africanizacin.
becomes an advantage of economic importance. Javier Pompa hizo cambios en el manejo de sus colonias
172
of these colonies are as manageable as European Control
bees.42,48,49,78 Therefore, for most Mexican beekeepers,
it is important to identify and discriminate bees with De lo arriba mencionado puede concluirse que la
African characteristics from those showing European apicultura en Mxico es hoy da menos productiva, ms
characteristics, to select the most productive and mana- compleja y ms costosa que antes de la africanizacin.
geable ones for queen breeding purposes. Requeening Debido a ello, es convieniente buscar soluciones para
hives with genetically improved queens is the most controlar o aminorar los efectos nocivos de la africani-
important measure to control Africanized bees; therefore, zacin de las colonias de abejas. Entre estas medidas se
beekeepers need selective breeding methods that are han sugerido las siguientes como las ms importantes:
both, reliable and practical. Unfortunately, there are
less than 50 queen breeders in the country, producing Mejoramiento gentico, cra
less than 300 000 queens annually, which does not satisfy y cambio de reinas
the 1.8 million queens a year that are needed (equal to
the number of hives). Moreover, only four or five queen Estudios previos han demostrado que si las colonias de
breeders follow some sort of selection methodology.93 abejas tienen un grado de africanizacin de alrededor
Scientists from the Instituto Nacional de Investi- de 25% o menor, stas son tan manejables como las
gaciones Forestales, Agricolas y Pecuarias (INIFAP) abejas europeas.42,48,49,78 Por ello, para la mayora
in association with researchers from the University de los apicultores mexicanos resulta importante
of Davis, California, developed a genetic breeding identificar y discriminar las abejas con caractersticas
program with which they demonstrated that it is africanas de las que poseen caractersticas europeas,
possible to increase the production of honey and to para seleccionar las ms productivas y manejables
decrease the defensive behavior of colonies without para la crianza de reinas. El cambio de abejas reinas
using instrumental insemination of queens to control mejoradas es la principal medida para el control de
mating.48,49,100 This program started in 1992 and was abejas africanizadas; por esa razn, los apicultores
based on data collection of honey production from necesitan mtodos confiables y prcticos para la
over 3 000 hives, as well as on evaluations of defensive seleccin y produccin de reinas. Desgraciadamente,
behavior of the group of colonies selected from existen menos de 50 criadores de abejas reinas en el
the honey production assessments. Additionally, pas, los cuales producen menos de 300 mil de ellas
worker samples of the colonies under selection were anualmente, por lo que no se satisface la necesidad
collected each year, to measure their wing length de 1.8 millones de reinas necesarias cada ao (igual
and to determine their type of mitochondrial DNA. al nmero de colmenas). Adems, slo cuatro o cinco
After five years of selection, the honey production criadores de reinas realizan algn tipo de seleccin.93
of the selected population increased 16%, whereas Investigadores del Instituto Nacional de Investi-
that of the unselected population decreased 34%. gaciones Forestales Agrcolas y Pecuarias (INIFAP) y
The number of stings deposited by the bees on a de la Universidad de Davis, California, desarrollaron
leather patch of the population under selection, un programa de mejoramiento gentico con el cual se
decreased 54%, while the wing length of selected ha demostrado que es posible aumentar la produccin
bees increased 1.1%. Additionally, the percentage of de miel y disminuir el comportamiento defensivo
colonies having bees with African mitochondrial DNA de las colonias de abejas, sin necesidad de recurrir
went from 28% before initiating the program, to only a la inseminacin instrumental de reinas.48,49,100 Este
7% after five years of selection.48,49 These results show programa se inici en 1992 y consisti en la toma de datos
that the Africanization process was reversed, at least de produccin de miel de ms de 3,000 colmenas, as
partially, and they also show that it is possible to breed como de evaluaciones del comportamiento defensivo
productive and manageable bees in Africanized areas. de las abejas del grupo de colonias preseleccionadas
por su alta productividad de miel. Adems, cada ao
Management efficiency se tomaron muestras de obreras de las colonias bajo
seleccin, para medir el tamao de sus alas, y para
In addition to apiary relocation and colony requeening, determinar su tipo de ADN mitocondrial. Despus de
swarm control and artificial feeding of colonies in cinco aos de seleccin, la produccin de miel de las
dearth times are the most important management colonias seleccionadas aument 16%, mientras que la
practices to control the negative effects of Africanized de la poblacin no seleccionada disminuy 34%. La
bees. Moreover, beekeepers must harvest colonies poblacin bajo seleccin disminuy 54% el nmero
several times during blossom seasons, to prevent that de aguijones depositados en un parche de cuero
bees with a higher degree of African ancestry use their por las abejas, mientras que el tamao de las alas de
food reserves to generate swarms.93 las abejas seleccionadas aument 1.1%. Adems, el
174
Referencias sus servicios de polinizacin, a fin de sufragar estos
gastos. Actualmente el precio de la miel y de la renta de
1. CARON DM. Africanized bees in the Americas. Medina colmenas son buenos, lo que podra llevar a la apicultura
OH: The A.I. Root Co., 2001. mexicana a superar la produccin y exportacin de
2. CORREA-BENTEZ A, GUZMN-NOVOA E. Zootec- miel registradas en la dcada de los aos ochenta.
nia apcola. En: TRUJILLO ME, editor. Introduccin a Si otros productos de la colmena como el polen y el
la Zootecnia. Mxico DF:FMVZ-UNAM, 2006:403-433. propleo pudieran comercializarse a mejores precios,
3. GUZMAN-NOVOA E, GOODMAN RD, HUANG ZY, podran tambin aprovecharse algunas de las ventajas
MORSE RA, REID M, YOSHIDA T. Beekeeping in vari-
de las abejas africanizadas y los productores tendran
ous parts of the world. In: SHIMANUKI H, FLOTTUM
K, HARMAN A, editors. The ABC & XYZ of Bee Cul-
mayores recursos para su control y explotacin.
ture. Medina, OH:AI Root Co, 2007:83-99.
4. LABOUGLE JM, ZOZAYA RJA. La apicultura en Agradecimientos
Mxico. Cienc Desarrollo 1986;69:17-36.
5. KERR WE. The history of the introduction of African Se agradece el apoyo financiero brindado por el
bees to Brazil. S Afr Bee J 1967;39:3-5. Consejo de Investigacines en Ingeniera y Ciencias
6. NOGUEIRA-NETO P. The spread of a fierce African Naturales de Canad (NSERC, por sus siglas en
bee in Brazil. Bee World 1964;45:119-121. ingls), a los mdicos veterinarios zootecnistas
7. RUTTNER F. Biogeography and taxonomy of honey Ricardo Anguiano Baez, Marta Silvia Reyes Cuayahuitl
bees. Berlin: Springer-Verlag, 1988. y Anglica G. Gris Valle, quienes contribuyeron con
8. SEELEY TD. Honey bee ecology. Princeton: Princeton
sugerencias valiosas para este trabajo.
University Press, 1985.
9. RINDERER TE. Evolutionary aspects of the African-
ization of honey bee populations in the Americas. In: aging activity: comparison between European and Afri-
NEEDHAM G, PAGE RE, DELFINADO-BAKER M, canized honeybees in Brazil. J Apic Res 1979;18:110-115.
BOWMAN C, editors. Africanized Bees and Bee Mites. 20. RINDERER TE, COLLINS AM. Foraging behavior
New York:John Wiley and Sons, 1988:13-28. and honey production. In: SPIVAK M, FLETCHER
10. MCNALLY LC, SCHNEIDER SS. Seasonal cycles of DJC, BREED MD, editors. The African Honey Bee.
growth, development and movement of the African Boulder Co:Westview, 1991:235-257.
honey bee, Apis mellifera scutellata, in Africa. Insectes 21. PESANTE D, RINDERER TE, COLLINS AM. Differen-
Sociaux 1992;39:167-179. tial nectar foraging by Africanized and European hon-
11. PAGE RE. Neotropical African bees. Nature 1989; eybees in the neotropics. J Apic Res 1987;26:210-216.
339:181-182. 22. RINDERER TE, COLLINS AM, TUCKER KW. Honey
12. WINSTON ML. Killer bees: The Africanized honey production and underlying nectar harvesting activities
bee in the Americas. Cambridge: Harvard University of Africanized and European honeybees. J Apic Res
Press, 1992. 1985;23:161-167.
13. SCHNEIDER SS, DEGRANDI-HOFFMAN G, SMITH 23. DANKA RG, HELLMICH RL II, RINDERER TE,
DR. The African honey bee: factors contributing to COLLINS AM. Diet-selection ecology of tropically
a successful biological invasion. Ann Rev Entomol and temperately adapted honey bees. Anim Behav
2004;49:351-376. 1987a;35:1858-1863.
14. WINSTON ML. The biology and management of Afri- 24. FEWELL JH, BERTRAM SM. Evidence of genetic varia-
canized honey bees. Ann Rev Entomol 1992;37:173-193. tion in worker task performance by African and Euro-
15. OTIS GW. Population biology of the Africanized honey pean honey bees. Behav Ecol Sociobiol 2002;52:318-
bee. In: SPIVAK M, FLETCHER DJC, BREED MD, edi- 325.
tors. The African Honey Bee. Boulder Co:Westview, 25. PAGE RE, GUZMAN-NOVOA E. The Genetic Basis of
1991:213-234. Disease Resistance. In: MORSE RA, FLOTTUM K, edi-
16. SCHNEIDER SS, MCNALLY LC. Factors influenc- tors. Honey Bee Pests, Predators, and Diseases. Medina
ing seasonal absconding in colonies of the African OH:AI Root Co, 1997:469-492.
honey bee, Apis mellifera scutellata. Insectes Sociaux 26. ROTHENBUHLER WC. Behavior genetics of nest
1992;39:403-423. cleaning in honey bees. IV. Responses of F1 and back-
17. GIRAY T, HUANG Z, GUZMAN-NOVOA E, ROBIN- cross generations to disease-killed brood. Am Zool
SON G. Physiological correlates of genetic variation for 1964;4:111-123.
rate of behavioral development in the honey bee, Apis 27. SPIVAK M, GILLIAM M. Facultative expression of
mellifera. Behav Ecol Sociobiol 1999;47:17-28. hygienic behaviour of honey bees in relation to disease
18. BECERRA F, GUZMAN-NOVOA E, CORREA- resistance. J Apic Res 1993;32:147-157.
BENITEZ A, ZOZAYA RJA. Length of life, age at first 28. SPIVAK M. Honey bee hygienic behavior and defense
foraging, and foraging life of Africanized and European against Varroa jacobsoni. Apidologie 1996;27: 245-260.
Honeybee (Apis mellifera L.) workers during conditions 29. GUZMAN-NOVOA E, CORREA-BENITEZ A. Honey
of resource abundance. J Apic Res 2005;44:151-156. bee selective breeding for resistance against the mite
19. NUEZ JA. Time spent on various components of for- Varroa jacobsoni O. Vet Mx 1996;27:149-158.
176
expansion of Africanized honeybees in Mexico. J Apic Mexico. II. Morphometric, allozymic and mitochon-
Res 2007;46:295-300. drial DNA variability in feral colonies. Apidologie
61. ZAMORA O, DOMINGUEZ R, ALANIZ-GUTIERREZ 2000;31:443-453.
L, QUEZADA-EUAN JJG. Frequency of European and 76. PAGE RE, FONDRK MK, HUNT GJ, GUZMN-
African-derived morphotypes and haplotypes in colo- NOVOA E, HUMPHRIES MA, NGUYEN K et al.
nies of honey bees (Apis mellifera) from NW Mexico. Genetic dissection of honey bee (Apis mellifera L.) for-
Apidologie 2008;39:388-396. aging behavior. J Heredity 2000;91:474-479.
62. TAYLOR OR, DELGADO A, BRIZUELA F. Rapid loss 77. RUBINK WL, LUEVANO-MARTINEZ P, SUGDEN EA,
of European traits from feral neotropical African honey WILSON WT, COLLINS AM. Subtropical Apis mellifera
bee populations in Mexico. Am Bee J 1991;131:783. (Hymenoptera: Apidae) swarming dynamics and Afri-
63. SUGDEN EA, WILLIAMS KR. October 15: the day the canization rates in Northeastern Mexico and Southern
bee arrived. Glean Bee Cult 1991;119:18-21. Texas. Ann Entomol Soc Am 1996;89:243-251.
64. VISSCHER PK, VETTER RS, BAPTISTA FC. Afri- 78. HELLMICH RL II. Continuing comercial queen pro-
canized bees, 1990-1995: Initial rapid expansion has duction after the arrival of Africanized honey bees. In:
slowed in the U.S. Calif Agric 1997;51:22-25. SPIVAK M, FLETCHER DJC, BREED MD, editors. The
65. LABOUGLE JM, MANCERA M, TAYLOR OR. Mor- African Honey Bee. Boulder Co:Westview, 1991:187-197.
phometric and electrophoretic study of the African 79. VERGARA C, DIETZ A, PEREZ A. Usurpation of man-
honey bee in southern Mexico. Am Bee J 1989;129:817. aged honey bee colonies in Tabasco, Mexico. Am Bee J
66. RINDERER TE, STELZER JA, OLDROYD BP, BUCO 1989;129:824-825.
SM, RUBINK WL. Hybridization between European 80. VERGARA C, DIETZ A, DE LEON AP. Female parasit-
and Africanized honey bees in the Neotropical Yucatan ism of European honey bees by Africanized honey bee
Peninsula. Science 1991;253:309-311. swarms in Mexico. J Apic Res 1993;32:32-40.
67. QUEZADA-EUAN JJG, ECHAZARRETA CM, 81. DANKA RG, HELLMICH RL II, RINDERER TE. Nest
PAXTON RJ. The distribution and range of expansion usurpation, supersedure and colony failure contribute
of Africanized honey bees (Apis mellifera) in the state of to Africanization of commercially managed European
Yucatan, Mexico. J Apic Res 1996;35:85-95. honey bees in Venezuela. J Apic Res 1992;31: 119-123.
68. HALL HG. 1999. Genetic and physiological studies of 82. HUNT GJ, GUZMAN-NOVOA E, URIBE JL, PRIETO
African and European honey bee hybridizations: past, D. Genotype by environmental interactions in guard-
present and into the 21st century. In: HOOPINGAR- ing behavior of European and Africanized honey bees.
NER R, CONNOR L, editors. Apiculture for the 21st In: Proceedings of the Animal Behavior Society; 2002
Century. Cheshire, CT:Wicwas Press, 1999:52-59. July 13-17; Bloomington, Indiana, USA. Bloomington:
69. QUEZADA-EUAN JJG, PAXTON RJ. Rapid intergen- Animal Behavior Society, 2002:45.
erational changes in morphology and behaviour in 83. SECRETARA DE AGRICULTURA, GANADERA,
colonies of Africanized and European honey bees (Apis DESARROLLO RURAL, PESCA Y ALIMENTACIN
mellifera) from tropical Yucatan, Mexico. J Apic Res [base de datos en Internet]. Servicio de informacin
1999;38:93-104. estadstica agroalimentaria (SIAP) [citado 2009 ago 2].
70. NIELSEN DI, EBERT PR, PAGE RE, HUNT GJ, GUZ- Disponible en: http://www.siap.sagarpa.gob.mx.
MAN-NOVOA E. Improved polymerase chain reaction- 84. CORREA-BENTEZ A. Historia de la apicultura en
based mitochondrial genotype assay for identification Mxico. Imagen Vet 2004;4:4-6.
of the Africanized honey bee (Hymenoptera: Apidae). 85. GUZMN-NOVOA E. Apicultura y abejas africanas.
Ann Entomol Soc Am 2000;93:1-6. Mxico DF: Quetzalcoatl, 1986.
71. CLARKE KE, RINDERER TE, FRANCK P, QUEZADA- 86. GONALVES LS, STORT AC, DE JONG D. Beekeep-
EUAN JJG, OLDROYD BP. The Africanization of ing in Brazil. In: Spivak M, FLETCHER DJC, BREED
honey bees (Apis mellifera L.) of the Yucatan: a study MD, editors. The African Honey Bee. Boulder
of a massive hybridization event across time. Evolution Co:Westview, 1991:359-372.
2002;56:1462-1474. 87. GUZMAN-NOVOA E, PAGE RE. The impact of Afri-
72. RINDERER TE, HELLMICH RL. The process of Afri- canized bees on Mexican beekeeping. Am Bee J
canization. In: SPIVAK M, FLETCHER DJC, BREED 1994;134:101-106.
MD, editors. The African Honey Bee. Boulder 88. GUZMAN-NOVOA E, PAGE RE, CORREA-BENITEZ
Co:Westview, 1991:95-117. A. Introduction and acceptance of European Queens
73. NIELSEN DI, EBERT PR, HUNT GJ, GUZMAN- in Africanized and European Honey Bee (Apis mellifera
NOVOA E, KINEE SA, PAGE RE. Identification of Afri- L.) Colonies. Am Bee J 1997;137:667-668.
canized honey bees (Hymenoptera: Apidae) incorpo- 89. GUZMAN-NOVOA E, PAGE RE, PRIETO D. Queen
rating morphometrics and an improved PCR mitotyp- introduction, acceptance, and survival in honey bee
ing procedure. Ann Entomol Soc Am 1999;92:167-174. (Hymenoptera: Apidae) colonies of a tropical, African-
74. SMITH DR. African bees in the Americas: insights ized region. J Econ Entomol 1998;91:1290-1294.
from biogeography and genetics. Trends Ecol Evolu- 90. HELLMICH RL II, RINDERER TE. Beekeeping in
tion 1991;6:17-21. Venezuela. In: SPIVAK M, FLETCHER DJC, BREED
75. QUEZADA-EUAN JJG. Hybridization between Euro- MD, editors. The African Honey Bee. Boulder
pean and Africanized honeybees in tropical Yucatan, Co:Westview, 1991:399-411.
178