VOL. 33, NO. 4
SOUTHWESTERN ENTOMOLOGIST
DEC. 2008
Population Dynamics of the Agave Scale, Acutaspis agavis (Hemiptera: Diaspididae), on Agave tequilana var. azul (Agavaceae) in Central Mexico
Manuel Darío Salas-Araiza', Robert W, Jones^, Genaro Montesinos-Silva, Eduardo Salazar-Solis, Luis Antonio Parra-Negrete, Oscar Martinez-Jaime, Rafael RamirezMalagón, and Sandra Flores-Mejia Instituto de Ciencias Agricolas, Universidad de Guanajuato, Ex Hacienda El Copal, Km 5 Carretera Irapuato-Silao, A. Postal #311, Irapuato 36500, Guanajuato, Mexico Abstract. The population dynamics of the agave scale, Acutaspis agavis (Townsend and Cockerell), on Agave tequilana Weber var. azul were studied in the state of Guanajuato, Mexico. Weekly samples were taken of plants to monitor for the presence of scales and to quantify the different developmental stages of the diaspid, together with its parasitoids and predators. Results showed some reproductive activity throughout the year, with two peaks in the abundance of eggs and first-instar nymphs in May and September, suggesting two generations annually of scales occur in the study area. First-instar nymphs within scales and "crawlers" increased in abundance from April through May and from August through early October, with these differences generally being significantly greater than during winter and mid-summer months. The predatory coccinellid Chilocorus cacti fed on the scale and increased in abundance from August to December when eggs and young scales were most abundant. Parasitism by Aphytis spp. occurred throughout the year. Data presented here indicate that the stages of the agave scale most susceptible to chemical control (first instars, or crawlers) were significantly more abundant in May (first generation) and September (second generation). This indicates that the development of an integrated pest management program to control A. agavis in tequila agave plantations in the region should focus control tactics on these periods of the year. Resumen. Se investigó la dinámica poblacional de la escama del agave Acutaspis agavis (Townsend y Cockerell) en Agave tequilana Weber var. azul en el estado de Guanajuato, México. Se tomaron muestras semanales de plantas para registrar los diferentes estados de desarrollo del diaspídido. Asi como sus parasitoides y depredadores. Los resultados sugieren que aun cuando hay actividad reproductiva a la largo del año, hay dos incrementos máximos en la densidad de huevo y ninfas de primer instar, lo que supone la presencia de dos generaciones anuales de la escama en la región. Las ninfas de primor instar dentro de la escama y las ninfas caminadoras, incrementaron su población de abril a mayo y de agosto hasta principios de octubre, con diferencias significativas para abril y mayo y para
[email protected] Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Avenida de las Ciencias, s/n, Juriquilla, Delegación Sta. Rosa Jáuregui, C.P. 76230, Queréíaro, México
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caminadoras en septiembre. Los dos picos poblacionales correlacionaron con el incremento de la temperatura durante abril y mayo, y con el incremento de la precipitación en septiembre y octubre. El coccinéllido Chilocorus cacti se observó alimentándose de la escama, con un máximo poblacional de agosto a diciembre, cuando las densidades de huevos y escamas de primeros estadios fueron mayores. El parasitismo por Aphytis spp. se presentó a lo largo del año. Los resultados de este trabajo indican que la etapa más apropiados para un control quimico de la escama del agave (ninfas caminadoras), presentan su abundancia significativamente mayor en mayo (1^' generación) y septiembre (2^° generación). Con estos resultados se contribuirá a desarrollar un programa de manejo integrado de esta plaga enfocada a esos periodos en las plantaciones de agave tequilana en la región. Introduction The agaves (Agavaceae) are aftacked by a diversity of insects and diseases that can cause severe damage, physiological disorders, or even the death of plants (Consejo Regulador del Tequila 2005). One of the most ubiquitous and persistent pests on the tequila agaves, Agave tequilana Weber, are armored scales. The most common and important of these is the agave scale, Acutaspis agavis (Townsend and Cockerell) (Hemiptera: Diaspididae), that attacks agave plants destined for tequila production, as well as those used to produce "pulque" (MacGregor and Gutiérrez 1983, Solis Aguilar et ai. 1999, Consejo Regulador del Tequila 2005). This insect is capable of reaching densities that completely cover the agave plant, affecting photosynthetic activity as a result of physical blockage of sunlight. Symptoms of damage are deformation of the agave leaf ("penca") and greatly weakening of the plant, and at times, plant death (Salas-Araiza et al. 2004, Consejo Regulador del Tequila 2005). Insecticides are generally not used to control armored scales in tequila production areas, although for major infestations, applications of oils and contact insecticides are recommended (Consejo Regulador del Tequila 2005). The annual seasonal dynamics of the various stages of A. agavis and factors affecting these dynamics need to be understood and quantified to optimize management tactics (Wai-Ki et al. 2001). Little information is available concerning seasonal fiuctutions in abundance of the various stages of A. agavis in tequila agave. Equally important, liftle is known of the effect of natural enemies on the dynamics of this pest. Rosen (1990) concluded that species of Chilocorus (Coleóptera: Coccinellidae) were the most important predator of scales in tropical and semitropical regions. The overall purpose of the present study was to generate information and develop tools for improving pest management programs for the armored scale, A. agavis, attacking the tequila agave. Agave tequilana var. azul. The objectives of the study were to characterize the population dynamics of A. agavis, to determine the periods of the year when the most susceptible stages (crawlers and small scales) are present, and investigate the relationship of these variables with weather conditions and abundance of natural enemies of ^. agavis.
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Materials and Methods The study was conducted at the field station at the Institute of Agricultural Sciences of the University of Guanajuato, at the Ex-Hacienda El Copal (101° 01'01" N, 20° 49' 49" W) in the municipality of Irapuato. at 1,750 m above sea level. The region has annual precipitation of 650 mm, a mean average temperature of 18''C, and a mean annual relative humidity of 56%. The study was done using commercial cultivation practices without application of insecticide in a 1-ha field of 3-year-old tequila agave. Samples of scales and natural enemies were collected weekly from 12 December 2002 to 21 November 2003, Daily meteorological data of temperature, relative humidity, and precipitation were recorded at the facility's weather station 200 m from the study site. Samples of scales of A. agavis were collected each week by cutting a 4 x 9 cm portion of agave leaf at random and immediately placing it into a Zip-Loo® plastic bag. This was brought to the laboratory and inspected with the aid of a stereomicroscope. From this sample, five scales were chosen randomly and inspected by using an insect pin to lift the edge of each scale. For each mother scale, the number was recorded of each of the following stages when present; 1) eggs, 2) first instars (crawlers), 3) solitary females, or 4) winged males. To record the number of crawlers outside the mother scale, a circular area 5 cm in diameter (19.6 cm^) was marked with a pencil, and the number of crawlers within this area was counted. Parasitized scales were recognized by a characteristic darkened color and were isolated and kept in 1-cm gelatin capsules until parasitoids emerged. The population dynamics of the coccinellid Chilocorus. cacti (L.) were studied by examining 20 agave plants and recording the presence of small, medium, and large larvae as well as adult beetles. Statistical analysis of data included a correlation analysis comparing different stages of the scale with weather conditions. Dependent variables (each stage of the scale, as well as numbers of the predator C. cacti) were measured in different experimental units (plants) at different time units (sample date). Because all variables were not normally distributed (using Shapiro-Wilks test), the nonparametric procedure, Kruskal Wallis, was used to compare abundance variables grouped by month. All analyses were conducted using SAS statistical software (SAS 1996). Identified specimens of A. agavis. C. cacti, Apttytis spp., and other natural enemies were deposited in the Entomological Collection "Leopoldo Tinoco Corona" of the Institute of Agricultural Sciences of the University of Guanajuato in Irapuato, Guanajuato. Mexico. Results and Discussion Eggs. Eggs of A. agavis were present during all months of the year, with a moderate peak in abundance in January (12.1 eggs per scale) and larger peaks in late August and September (Fig. 1A). A maximum mean of 34,1 eggs per scale was found on 26 September 2006. This peak in the mean abundance of eggs within scales for September was significantly greater than for February, all spring months (March-May), and for Juiy and December, This peak in abundance of eggs was also correlated (r = 0.736; p < 0.05; y = -1.24 + 0,55x) with the heaviest precipitation events of the region from mid-August to early October. Beardsley and
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Gonzalez (1975) and Liu et al. (1995) reported that scales survive periods of cold, freezing weather or other adverse climatic conditions, in the egg stage. In temperate regions of the US, scales oviposited in September remain in the egg stage in apparent diapause throughout the winter and eclose in May or June. In the present study, temperatures were only moderate, but rainfall was variable. As for many insects in arid zones, reproductive activity displaying this arid-adapted pattern Is usually intimately timed to the occurrence of seasonal rainfall. First-instar Nymphs within Scales. As with the presence of eggs, nymphs of A. agavis within scales were present throughout the year (Fig. IB). However, abundance of first-instar nymphs (crawlers) peaked twice during the year. The first
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peak occurred in April and May when abundance reached 6.9 and 10.6 nymphs per scale, respectively. Mean abundances for these months were significantly different from those of winter and early spring (December-March). The second peak occurred in September, when abundance was 5.3 nymphs per scale. The first peak apparently was the result of an increase in the eclosión of eggs laid during previous months, perhaps even from fall months of the previous year, responding to increasing spring temperatures in April and May. The second peak was associated with the increased egg production in late August and September discussed previously. However, the peak during September was surprisingly low, given the great number of eggs at this time. This less than expected number of nymphs in scales may have been caused by: 1) greater mortality of nymphs at this time, 2) greater tendency of eggs to remain in the egg stage during September, or 3) more rapid dispersal of nymphs from the mother scale when compared with other months. A positive linear correlation (r = 0.74; p < 0.05; y = 15.61 + 0.734x) was found between the presence of nymphs in scales and ambient temperature. These results suggested that A. agavis have at least two generations each year, with peak numbers of nymphs the first generation appearing under scales in April and May and the second in late August and September. First-lnstar Nymphs. First-instar nymphs outside of the mother scale, or crawlers, were scarce from January through March, with small increases during April and May (significantly so in May), decreases in July and August, and a large, significant Increase (13.5 crawlers per 19.6 cm^) in September (Fig. 2A). Crawlers were not observed in November or December. It is possible that even though crawlers within scales were most abundant in May and June, they remained within scales to avoid desiccation until the rain and greater humidity in September. However, because the number of crawlers within mother scales decreased after June, and eggs increased in September, it is more likely that the appearance of crawlers during September was the result of a second generation coinciding with peak rainfall. As for other scales, the crawler period of A. agavis is probably relatively short. For the California red scale. Aonidielta aurantii (Maskell), crawlers attach themselves and begin scale formation within 24 hours after emergence. Crawlers of the San José scale, Quadraspidiotus perniciosus Comstock, are even more rapid in attaching themselves, requiring only 1 to 4 hours after emergence from the mother scale (Beardsley and Gonzalez 1975). In the present study, we found an abundance of small, immature scales often with only partially developed scales, surrounding the mother scale and at times in contact with one another. This suggests that the dispersal distance of crawlers was short and that crawlers rapidly attached to leaves after leaving the mother scale. The crawler stage of the other scales is the most susceptible to insecticide (Burden and Hart 1989). Our results suggest that the month of September, or periods with the greatest rainfall, is the most appropriate time for controlling crawlers. The first author found significant control of scales with the release of larvae of Chrysoperia carnea Stephens (Neuroptera: Chrysopidae) at the time crawlers emerged (unpublished data). Females. The patterns of abundance of female A. agavis scales also suggested two annual generations on tequila agave. Abundance was greatest during two periods, first in December and February and later in July. August and October. Of these months, abundance in Decemtier and February and July was significantly difterent from that in all months except August and October (Fig. 2B).
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These peaks correlated well with the later, sequential appearance of eggs, firstinstar nymphs and crawlers. Males. Males were only found during winter (Fig. 3A). However, results presented here suggest two generations of A. agavis scales on tequila agave. The lack of male scales during summer suggests the second generation is parthenogenetic. Other scales, such as Aspidiotus nerii Bouché. Hemiberlesia lataniae (Signoret), and Lepidosaphes ulmi (L.), reproduce both sexually and asexually {Beardsley and Gonzalez 1975), with production of males and females at
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different times of the year (Gullan and Kosztarab 1997). More study is needed to determine when and how sexual and parthenogenetic reproduction occurs. Natural Enemies. One ofthe most abundant predators in the present study was the coccinellid C. cacti. This beetle was present during all months of the study, although abundance was greatest from August through January (Fig. 3B). The combined densities of all stages of this beetle were significantly different in September, November, and December from the months of February through July,
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Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Fig. 3. A. Mean monthly abundance of males of agave scale of Acutaspis agavis (Townsend and Cockerell) on Agave tequilana Weber in Irapuato, Mexico, during 2003. Means with the same letter (individually or in series) are not significantly different (p > 0.05) using Kruskal-Wallis non-parametric test, {H = 2.07). B. Mean monthly abundance of adults and larvae of Chilocorus cacti L. on Agave tequilana Weber in Irapuato, Mexico, during 2003. Means with the same letter (individually or in series) are not significantly different (p > 0.05) using Kruskal-Wallis nonparametric test (H = 1.98).
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with the exception of April (Kruskal Wallis test, p < 0,05, Fig 3A). For adults, abundance in December was five-fold greater than that in any other month. The peaks in coccinellid abundance began with small larvae appearing in greater numbers in July and August and peaking in September, whereas larger larvae were more common after August, No eggs were found in the present study, although plants and the soil at their base were searched, Rosen (1990) reported that the eggs of this coccinellid species are placed in cracks in the soil and plant. SalasAraiza (2001), found that C. cacti occurs on Opuntia spp., where it feeds on other scales. With the widespread distribution of Opuntia spp., it is possible that this coccinellid moves from cacti species into tequila agave plantations. In the plantations, A. agavis is probably an important prey of C, cacti, because peaks in abundance of the predator were correlated (r = 0.72; p < 0.05; y = 0.065 + 0.138x) with those of the scale. This conclusion is supported by observations of larvae and adult coccinellids opening the upper portion of scales to feed on internal contents. Other predators in the agave plantations were other Coccinellidae: Nephaspis spp., Scymnus spp., Paranaemia vittigera (Mann,), Oiia v-nigrum (Mulsant), and hiippodamia convergens Guerin-Meneville, as well as Coilops femoratus Schaeffer (Coleóptera: Melyridae) and Sinea spp, (Hemiptera: Reduviidae), A larva of the family Nitidulidae was also observed feeding on the interior of a scale. Various fungi were found on the exterior of scales. An unidentified parasitoid of the genus Aphytis (Hymenoptera: Aphelinidae), was reared from scales in January, March, April, September, and December. Cooper and Cranshaw (2004) reported that Aptiytis is a common genus with various species abundant as parasitoids of soft and armored scales. Evaluation of the impact of this parasitoid on abundance of A. agavis was not within the scope of the present study. Conclusions. A. agavis seems to produce two generations on A. tequHana var. azul in the study area of north-central Mexico, The first generation occurs from eggs apparently oviposited in September through December, with greater numbers of nymphs emerging and crawlers appearing from March through June, This peak was correlated with increased temperature. Adult females from this generation peaked in abundance in July and August, and subsequently significantly greater numbers of eggs and crawlers appeared in September, This peak was also correlated with increased precipitation. During November and December, abundance of all stages decreased. However, despite these clear generational peaks, some reproductive activity apparently continued throughout the year, as evidenced by the presence of crawlers and young scales. The continued reproduction suggests that A. agavis may have a flexible phenological life history pattern, probably linked to changes in humidity, as has been reported for other insects adapted to very seasonal, arid environments (Tauber et al. 1986). Males were only observed in December and January, suggesting an annual alternation of sexual and asexual reproduction, with the former in winter and the latter during months with greatest precipitation in August and September, The most common natural enemies of A. agavis were the coccinellid. Chiiocorus cacti, and the parasitoids Aphytis spp. that were reared from the scale. This study suggests that management eftorts, either chemical or biological tactics, should primarily be directed at scale populations in April and May, and in September and October. when the most susceptible stages, crawlers and early established scales, were most abundant. Further research is needed to determine whether control of the first generational peak in spring is most effective, or whether control measures directed
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at the second peak in September results in more effective reduction in abundance of agave scales. Future studies also need to consider the impact of natural enemies, and in particular, C. cacti, which is more abundant during the second generation of the agave scale. Acknowledgment The Secretaria de Desarrollo Social y Humano, Región III and the Consejo de Desarrollo Social de! Municipio de Silao, Guanajuato, helped in the funding and development of this project. References Cited Beardsley, Jr., W. J., and R. H. Gonzalez. 1975. The biology and ecology of armored scale. Ann. Rev. Entomol. 47-73. Burden D. J., and E. R. Hart. 1989. Degree-day model for egg eclosión ofthe pine needle scale (Hemiptera: Diaspididae). Environ. Entomol. 18: 223-227. Consejo Regulador del Tequila. 2005. Plagas y Enfermedades del Agave tequilana Weber var. azul. Subcomité de Investigación. Comité Técnico Agronómico. Guadalajara. Jal. Cooper, D. D., and W. S. Cranshaw. 2004. Seasonal biology and associated natural enemies of two Toumeyetia spp., in Colorado. Southwest. Entomol. 29: 39-45. Gullan, P. L., and M. Kosztarab. 1997. Adaptations in scale insects. Annu. Rev. Entomol. 42: 23-50. MacGregor, R., and O. Gutiérrez. 1983. Guia de insectos nocivos para la agricultura en México. Ed. Alhambra Mexicana. Liu, S.-S., G.-M. Zhang, and J. Zhu. 1995. Influence of temperature variations on rate of development in insects: analysis of case studies from entomological literature. Ann. Entomol. Soc. Am. 88: 107-119. Rosen, D. [ed.]. 1990. Armored Scale Insects; Their Biology, Natural Enemies and Control, Vol. II. B. Elsevier, Amsterdam. Salas-Araiza, M. D. 2001. Insectos asociados a Opuntia spp., (Cactaceae) en el estado de Guanajuato. XXXVI Congreso Nacional de Entomología. Querétaro, Qro. Salas-Araiza, M. D., L. A. Parra-Negrete, and E. Salazar-Solis. 2004. Insectos asociados a los agaves (AGAVACEAE) en el estado de Guanajuato, pp. 199-203. in Morales-Moreno A., M. Ibarra-G onza lez, A. P. Rivera-González, y S. Stanford-Camargo [eds.] Entomología Mexicana 3. Sociedad Mexicana de Entomología. Montecillo, Méx. SAS. 1996. SAS Users Guide. SAS Institute, Inc., Cary, NC. Solis-Aguilar, J. F., H. Gonzalez H., F. J. Flores M., M. Santos C, Hernández C , A. R. Valle de la Paz, A. Equihua M., J. L. Leyva V., and A, Martinez G. 1999. Insectos asociados con Agave tequitana Weber, var. azul, en cinco localidades de Jalisco, México, pp. 455-457. Memorias del XXXIV Congreso Nacional de Entomología. SME. Aguascalientes. Ags. Tauber, M. J., C. A. Tauber, and S. Masaki. 1986. Seasonal Adaptations of Insects. Oxford University Press, New York.
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Tooker F. J., and L. M. Hanks. 2000. Influence of plant community structure on natural enemies of pine needle scale (Homoptera: Diaspididae) in urban landscapes. Environ. Entomol. 29: 1305-1311. Wai-Ki, F., L. P. Pedigo, and P. N. Hinz. 2001. Population dynamics of bean leaf beetles (Coleoptera:Chrysomelidae) in Central Iowa. Environ. Entomol. 30: 562-567.
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