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Revista mexicana de ciencias agrícolas

versión impresa ISSN 2007-0934

Rev. Mex. Cienc. Agríc vol.7 no.8 Texcoco nov./dic. 2016



Defense, hygiene and production behavior of Apis mellifera L. ecotypes in Tabasco, Mexico

Dulce Nayeli Contreras-Ramírez1  § 

María Isabel Pérez León1 

Emeterio Payró-de la Cruz2 

Gerardo Rodríguez-Ortiz1 

Ernesto Castañeda-Hidalgo1 

Rosa María Gómez-Ugalde1 

1Instituto Tecnológico del Valle de Oaxaca. Ex Hacienda de Nazareno, Xoxocotlán, Oaxaca. CP. 71230. Tel. 01 951 51 70 788. (; leonisa70@;;;;

2Instituto Tecnológico de la Zona Olmeca. Ignacio Zaragoza s/n. Villa Ocuitzapotlán, Centro, Tabasco. CP. 86270. (


Africanization, disease, particularly varroosis, the instability of the international honey market and the deterioration of ecological environment, has led to a constant research on how to obtain bees with high performance characteristics, low defensiveness and resistance to disease. The objective was to evaluate the defense, hygiene and productive behavior of Apis mellifera L. and two bee ecotypes (carniolas and Africanized) in Centla, Huimanguillo and Tacotalpa, Tabasco, Mexico; from March to May 2014. The climate is humid with average temperature of 27 °C and annual average rainfall of 2 550 mm. Defense and hygiene behavior was evaluated through the technique from Payró et al. (2010) and varroosis infestation in adult through David de Jong test; honey production was evaluated by weight. A DCA with 10 hives per municipality were used and Tukey tests (p= 0.05) and “t”-Student to separate population means. In Tacotalpa, defensiveness (1.7) and varroosis infestation in adult bee was higher (6.6%). Varroa in larva was very light in Huimanguillo (0.7%) while in Centla and Tacotalpa showed light levels. Preening in Tacotalpa was intermediate (39.8%) and light in Centla and Huimanguillo. Honey production in Huimanguillo was higher (58.44 kg hive). Carniola bees are less defensive (4.4). It is concluded that in the three municipalities had hygiene colonies with removal greater than 86%. In carniolas and africanized bees the incidence of varroosis in adult and larva, hygienic and honey production behavior are similar.

Keywords: preening; hygienic behavior; honey production


La africanización, las enfermedades, especialmente varroasis, la inestabilidad del mercado internacional de la miel y el deterioro del entorno ecológico, ha llevado a una constante investigación sobre como obtener abejas con características de alto rendimiento, baja defensividad y resistencia a enfermedades. El objetivo fue evaluar el comportamiento defensivo, sanitario y productivo de Apis mellifera L. y dos ecotipos de abejas (carniolas y africanizadas) en Centla, Huimanguillo y Tacotalpa, Tabasco, México; durante marzo a mayo de 2014. El clima es húmedo con temperatura media de 27 °C y precipitación media de 2 550 mm anuales. En comportamiento defensivo y sanitario se evaluó mediante la técnica de Payró et al (2010) y la infestación de varroa en adultas mediante la prueba de David de Jong; y se evaluó la producción de miel en peso. Se utilizó un DCA, con 10 colmenas por municipio y se aplicaron las pruebas de Tukey (p= 0.05) y “t”- de Student para separar medias poblacionales. En Tacotalpa, la defensividad (1.7) e infestación de varroa en abeja adulta fue mayor (6.6%). Varroa en cría fue muy ligera en Huimanguillo (0.7%) mientras que en Centla y Tacotalpa se presentaron niveles ligeros. El acicalamiento fue medio en Tacotalpa (39.8%) y ligero en Centla y Huimanguillo. La producción de miel en Huimanguillo fue mayor (58.44 kg colmena). Las abejas carniolas son menos defensivas (4.4). Se concluye que en los tres municipios presentaron colonias higiénicas con remoción mayor a 86%. En abejas carniolas y africanizadas la incidencia de varroa en adultas y en cría, el comportamiento higiénico y la producción de miel son similares.

Palabras clave: acicalamiento; comportamiento higiénico; producción de miel


Beekeeping is an important activity within Mexican livestock since it has developed successfully and economic relevance. It is the third collecting activity of foreign exchange for the country, and ranks sixth as producer and third as honey exporter worldwide (SAGARPA, 2006). The country is segmented into six apiculture regions; North, Pacific, Altiplano, Central, Gulf and the Yucatán Peninsula. Tabasco belongs to the apiary Gulf region, along with the states of Veracruz and Tamaulipas. Tabasco has seen a dramatic decline in honey production from 1980, ranking 28th nationally and considering their contributions as insignificant (SIAP, 2013). This is paradoxical because Tabasco has a great richness and abundance of native and introduced plant species, making it an important laboratory to research the ecological and economic role of bees in the Mexican humid tropics (Córdova- Córdova et al., 2009).

Low honey production in the state is due to several factors, standing out on importance is Africanization, the presence of the parasite Varroa destructor, responsible for a disease known as varroasis in hives, frequent and intense rainfall during the year and the low level of development of this activity due to poor government support. Also the Africanization bee process, an undesirable trait for beekeepers, as it generates the appearance of ecotypes with high defensiveness, making difficult to handle apiaries and is one of the main causes of the abandonment of this activity. However, not everything regarding to these bee ecotypes is bad, because the queen bees are prolific, have high resistance to disease attacks, more hygienic and more productive than carniolas bees (Payró et al., 2009). Uribe et al. (2003) mention that in Mexico, the defensive behavior of Africanized bees has caused more than three thousand accidents by stings in people, of which more than 300 have died.

However, the factor with the highest direct effect in reducing honey production is the presence of varroa in hives. Varroa mite is an ectoparasite from the the Varroidae family and affects Apis mellifera in all development stages by sucking hemolymph. Furthermore, it is considered to be responsible for malformations in bees, which prevent them from achieving optimum collection and normal movement, and makes them susceptible to diseases related to bacteria and viruses (Ministerio de Agricultura, 2010).

Bees are organisms that by nature are social and highly cooperative, so that this interaction leads to the exposure of pathogens and disease transmission due to factors such as high population density, reduced space and constant physical contact. However, sociability also provides them protection against parasites, by the hygienic behavior that possesses (Baracchi et al., 2012). As a result, mite populations are controlled by bees through the development of a resistance behavior to health problems. These behaviors are invaluable for management and economy of beekeepers. So this study aims to evaluate honey production and hygiene and defensive behavior of bees in the municipalities of Centla, Huimanguillo and Tacotalpa, Tabasco; under the same evaluation traits in two major bee ecotypes (africanized and carniola).

Materials and methods

Study area

The study was conducted in the municipalities of Centla (18° 25’ 30.27” north latitude and 93° 00’ 44.96” west longitude), Tacotalpa (17° 21’ 34.53” north latitude and 92° 43’ 43.28” west longitude) and Huimanguillo (17° 37’ 40.62" north latitude and 93° 35’ 55.11” west longitude), in the state of Tabasco, during the months of March to May 2014. The state has warm- humid climate, the annual average temperature is 27 °C and the state average rainfall is 2 550 mm per year (Figure 1).

Figure 1 Location of apiaries in Tabasco. 

Evaluation of variables

In each of the municipalities an apiary was chosen and in each of these ten hives were chosen, where defensive, hygiene behavior and honey production were evaluated, these same variables were considered to evaluate the behavior of two different bee ecotypes (carniolan and Africanized).

Evaluation of defensive behavior of bees

The defensive behavior was evaluated by applying smoke to the hive; which is recommended to be made by the front of the hive. Smoke application allows observing bee behavior. According to the degree of their defensiveness a value according to the proposals of Payró et al. (2010) and Vandame et al. (2012) is assigned, who use a scale of five levels to determine defensiveness. The value of 1 represents the most aggressive level and is considered intolerable for experienced beekeeper. Can react even when beekeeper is viewing neighboring hives and even their control is very difficult with enough smoke. This causes its aggressiveness and spread to the surroundings, reason why attack people and animals that are present. The value two, the reaction mechanism of bees is immediate from which generate a strong buzz, with which initiates the attack by stinging.

They seek primarily exposed parts of the beekeeper body or dark areas of clothing. In this state bees can be controlled with the use of a lot of smoke. In the value three, bees react with a strong and constant buzz. Some bees fly out aggressively and collide with the veil and beekeeper protective clothing. In this state the bees are considered manageable, but require a lot of smoke. In level four, bees react with a strong buzz, and after a few seconds, some bees are limited to about flying outside the hive. In general, they can be handled well and with little smoke. Level five is considered the most docile. When opening a hive, bees remain very calm, responding only with a soft hum and its handling is very good.

Evaluation of hygiene behavior

It was assessed through hygienic behavior (CH), the degree of preening and infestation of varroa in pupa and adult. The first test consisted of Hygienic behavior (CH) proposed by Vandema et al. (2012). To perform the test it is recommended to use a brood frame and select 100 pupae that should be killed with an insulin needle through a deep puncture that cross the entire pupa. With indelible ink it is marked the used area. Finally, after 24 hours records the number of brood cells and removed by bees. For the hygienic behavior the removal percentage was considered through the following formula:

Ch=(Total alveolus punctured - Total alveolus non cleanedTotal alveolus punctured * 100

Evaluation of varroa infestation in larva (Ivc)

To assess varroa infestation in bee larva (Ivc) was followed the procedure proposed by Payró et al. (2010). For this purpose a brood frame is chosen, from which a fragment of approximately 100 cells is taken. Required laboratory analysis was performed in the Biotechnology laboratory from the Instituto Tecnologico of the Olmeza Zone (ITZO). For this purpose the brood frame was removed and carefully took the baby bees, detail body and cells were observed to count the number of larvae infested with varroa.

Ivc=Total of varroas foundTotal cells observed*100

Varroa infestation in adult bee (Ivaa)

It was performed through the laboratory test proposed by David de Jong. This test requires a sample of 100 bee maximum in jars with alcohol. This test was also performed in the Biotechnology laboratory from the Instituto Tecnologico of the Olmeca Zone. The test requires the vials to be agitated vigorously, thereby varroa detach from the bee. Finally placed in a mesh above a container to separate bees from varroa, the number of bees and varroa mites are counted. To determine Ivaa the following formula is used:

Ivaa=Total of varroas foundTotal bees in the sample*100

Evaluation of preening

To perform this test it is recommended to pass through the entrance of the hive an oiled card, held there for 24 h. After this time the sheet is removed and the number of varroa stuck to the sheet and the number of injured varroa mites is counted.

Preening=Amount of varroa injured (VL)Total de varroas the sample (VT)*100

Evaluation of honey production

It was performed by counting the number of racks of harvested honey from each hive and apiary under study. After the brood frames were removed with a honey comb, immediately the frame was weighed, extracted honey and weighed the empty frame, being the weight difference the amount of honey contained in a frame.

Statistical analysis

The municipalities evaluated were considered the treatments and beehives replications. All variables were evaluated by analysis of variance, under a completely randomized design and mean separation was performed for treatment through Tukey (α= 0.05). To evaluate defensiveness, hygienic behavior, preening and varroas infestation in pupa and Ivaa and honey production in carniolan and Africanized bees, five hives were considered for each ecotype. These were compared through "t" Student test using the Statistical Analysis System package (SAS) Windows 9.0.

Results and discussion

The defensive behavior of bees in each community showed significant difference (p< 0.001). Being Tacotalpa the municipality with the most defensive hives with a value of 1.7; placing them at level one, although very close to level two; indicating that bees are aggressive and not easy to handle. Centla and Cárdenas commounities showed similarity in reaction to aggression, with a value of 3.5, indicating that these hives bees are less defensive, and that can be handled with little smoke. In case of showing aggressiveness, bees will dissuade of seeking exposed areas from the beekeeper to sting, without looking the dark areas (Table 1).

Table 1 General characteristic of production, hygiene and defensive behavior of apiaries from the municipalities of Tabasco. 

Característica evaluada- significancia Municipios
Huimanguillo Centla Tacotalpa
Producción de miel (kg por colmena) (0.7) 58.44 ± 16.079 a 41.33 ±17.15 b 43.1±20.146 b
Comportamiento higiénico (p= 0.245) 0.926 ± 0. 019 a 0.879± 0.096 a 0.938 ±0.048 a
V. destructor en adultas (p= 0.022) 0.034 ± 0.031 ba 0.021± 0.027 b 0.066±0.046 a
V. destructor en cría (p= 0.019) 0.007± 0.008 b 0.038 ±0.029 a 0.027± 0.019 ba
Acicalamiento (p= 0.041) 0.141± 0. 083 b 0.26±0.315 ba 0.398± 0.122 a
Defensividad (p= 0.0001) 3.5 ± 1.08 a 3.5 ± 0.849 a 1.700± 0.674 b
Alzas 1 2 3
Producción de miel kg por colmena (p= <.0001) 23.578 ± 0.925 c 48.815 ±2.585 b 72.738± 2.469 a
Comportamiento higiénico (p= 0.218) 0.874 ± 0.104 a 0. 927 ± 0.067 a 0. 937±0.05 a
V. destructor en adultas (p= 0.504) 0.031 ± 0.034 a 0.046 ±0.047 a 0.041±0.034 a
V. destructor en cría (p= 0.725) 0.032 ± 0.031 a 0.021± 0.022 a 0.019± 0.0161 a
Acicalamiento (p= 0.946) 0.305 ± 0.324 a 0.256 ± 0.166 a 0.239± 0.18 a
Defensividad (p= 0.4) 2.777 ± 0.971 a 3.076± 1.382 a 2.750± 1.281 a

Medias dentro de cada fila con la misma letra no son significativamente diferentes (Tukey, 0.05). La media se acompaña de ± desviación estándar.

Between Africanized and carniolan bees defensiveness was significant (p= 0.0008). The value for canicolan bees was 4.4; while for Africanized was 2.6. This proves that Africanized bees are more defensive than carniola, but with the possibility of controlling them using a lot of smoke. The results agree with Uribe et al. (2003), who indicate that Africanized bees have a higher degree of defensiveness. Thus with Brizuela (2003) who reports that the behavior of defensiveness increases with hybridization of European and Africanized bees (Table 2).

Table 2 General characteristics of production, hygienic and defensive behavior of Africanized bees and carniolan. 

Características a evaluar/significancia Ecotipos de abejas
Africanizada Carniola
Producción de miel ( kg por colmena) (p= 0.4) 62.9 ± 11.31 53.98 ± 20.09
Alzas (p= 0.3) 2.6 ± 0.54 2.2 ± 0.83
Comportamiento higiénico (p= 0.2) 95.6 ± 0.103 89.6 ± 0.036
Varroa en adultas (p= 0.3) 4.37 ± 0.042 2.43 ± 0.012
Varroa en cría (p= 0.1) 0.4 ± 0.004 1.13±0.01
Acicalamiento (p= 0.3) 1.16 ± 0.105 1.65 ± 0.055
Defensividad (p= 0.0008) 2.6 ± 0.054 4.4 ± 0.054

Se utilizó la prueba “t” Student (p= 0.05). La media se acompaña de ± desviación estándar.

As for the analysis of hygienic behavior among municipalities, it was found that there is no significant difference between them (p= 0.09); a variation range between 93.8% and 87.9% in removal of larva sample. So according to Gramacho and Goncanlves (2002) colonies are hygienic. It is considered that a colony is hygienic when it presents a value of larva removal higher than 80%. However, authors like Spivak and Reuter (2001) consider hygiene to those bees that remove 95% of the larva, being a desirable trait (Table 1).

Hygienic behavior between Africanized bees and carniolan was similar (p= 0.2). Vásquez and Tello (1995) indicate that africanized bees have "hygienic genes"; that is, they are capable of uncapping and removing dead brood quickly. This process generates a form of resistance to different diseases. Hygienic behavior is also related to honey production, since confers them disease resistance. Thus, they cut the cycle of bacterial or fungal diseases or well of V. destructor Guzmán-Novoa et al. (2011) (Figure 2).

Figure 2 Uncapping dead larva as hygienic behavior in the apiaries from Huimanguillo, Tabasco. 

Varroa infestation in larva

Proof of varroa in larva (Table 1) showed significant difference (p= 0.03), where Huimanguillo showed a lower rate of varroa infestation in egg laying (0.7%) Tacotalpa and Centla (2.7% and 3.8%, respectively); according to Marcangeli (2001), this explains why the varroa mite has higher affinity for breeding drones, since their life cycle is longer. While Vandame (2000) and Le Conte et al. (1989) consider that chemical attractiveness of larva seems to be the essential factor causing the infestation.

The varroa mite in larva showed no significant difference (p= 0.1) between carniolan and Africanized (1.13% and 0.40%, respectively) (Table 2). Vandame et al. (2000) indicate that varroa mite showed greater preference for Africanized bees and that these are more tolerant to this mite. With the results obtained on the preference of larva, does not to that mentioned by the authors.

Varroa infestation in adult bee

There were significant differences (p= 0.03) in varroa infestation in adult bees, where the apiary from Tacotalpa showed higher infestation rate (6.6%) while between Huimanguillo and Centla the percentage was lower (3.4% and 2.1% respectively) (Table 1).

Comparing with the parameters established by the Norma Oficial Mexicana (NOM-056-ZOO-1995), Tacotalpa is in a middle range of normal infestation (> 5%), Huimanguillo and Centla are in a light range (<0.5%). The population rate of Varroa destructor depends on the season, being higher during peak flowering, this is consistent with that proposed by (Manríque and Soares, 2004).

The incidence of varroa was similar between Africanized and carniolan bees (p= 0.3) showing an average infestation of 3.4%. Anderson and Trueman (2000) indicate that varroa is an ectoparasite, constituted as an own pathogen agent from Apis mellifera scutellata. With the results in this study and according to SAGARPA (2012) infestation is low between the two samples as it is <5 varroas/day.


Preening behavior in different apiaries (Table 1) showed a significant difference (p= 0.02). Showing that an apiary from Tacotalpa the preening index was higher (39.8%) while in Centla preening average was intermediate (26%) and the lowest level was reported in municipality of Huimanguillo (14.1%).

According to the results, Tacotalpa shows an intermediate preening behavior according to SAGARPA (2012). Preening between Africanized and Carniolan bees showed no significant difference; however, SAGARPA (2012) reports africanized bees with the highest level of preening.

Regarding to honey production, Table 1 shows the analysis of variance randomized from the three apiaries under evaluation, significant difference (p= 0.7) was found in honey production, being Huimanguillo the municipality that recorded the apiary with higher volume of honey production (58.4 kg hive). Villegas et al, (2004) mention that Huimanguillo and Tacotalpa belong to two of the three sub-regions from the state that has suitable characteristics for optimal beekeeping development. However Tacotalpa recorded low honey production (43.1 kg hive) while in Centla recorded the lowest production among the municipalities evaluated (41.3 kg hive), this fact is strongly related to the presence of varroa (Figure 3) since this municipality recorded hives with higher incidence of this mite, which is credited to depopulation in hives and conferring them multiple diseases associated with viruses and bacteria (Medina and May, 2005).

Figure 3 Varroa mite that affects adults and larva of bees Apis mellifera

According to Córdova-Sánchez (2009), the average yield of honey per hive in Tabasco is 37 kg hive, thus the value obtained in this study, the municipality of Huimanguillo was higher to the range mentioned

Comparing honey production between africanized and carniolan (Table 2), does not show significant difference (p= 0.4), presenting an average of 58.4 kg hive.

These results agree with Spivak and Reuter (1998), who indicate that there are no differences between them, while Vasquez and Tello (1995) conclude that African bees produce more honey than European. In opposition to Uribe et al. (2003), pointing out that the European races are more productive.


In Tacotalpa, bees were more defensive compared to bees from Centla (3.5) and Huimanguillo (3.5). Carniolan bees were less defensive than africanized.

In the apiaries from Centla and Huimanguillo infestation levels of varroa in adult bee are light, and in Tacotalpa infestation is regular (6.6%).

Varroa infestation in breeding bees from the apiary was very light in the three municipalities (0.7 to 3.8%). In preening, Tacotalpa showed an average behavior (39.8%) Centla and Huimanguillo had a light level (26% and 14.1%). In the three municipalities of Tabasco were hygienic colonies with a removal value greater than 87.9%. In Huimanguillo, Tabasco, the bees showed the best defensive, hygienic and productive behavior (58.4 kg hive). There was not a lot of difference between carniolan and africanized bees, in higyene, preening and varroa infestation in young and adult bee and honey production.

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Received: August 2016; Accepted: November 2016

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