Aphids are recognized as important plant pests worldwide and they are major vectors of viruses. It is necessary to identify the aphid species in an agroecosystem in order to develop appropriate pest management strategies. The aim of this work was to determine the taxonomic diversity of aphid species present in potato crops in different agroecological regions of Tucumán, Argentina. Monitoring was done by 2 methods: modified Moericke yellow water traps were used for the alatae, while the apterae were collected directly from the plants. A total of 15,169 winged aphids were caught and 7,455 apterae colonizing the crop were collected. Fifty-six species were identified, 27 of which were present in all regions surveyed. Differences in species diversity between regions are discussed.
The province of Tucumán, Argentina, produces potato for consumption, industrial use and for use as seed potatoes. With regard to potato production for consumption and industrial use, Tucumán is characterized mainly by its early winter-spring production period (Caldiz 2006). Seed potatoes are grown during Oct to Mar in the department of Tafí del Valle (Fandos et al. 2011). Seed potato production is not an easy task, as crops are affected by multiple pests and diseases, including several viruses that contribute to the devaluation and rejection of seed stocks for certification (Carli & Baltaev 2008).
The most important virus diseases of potato are Potato virus Y (PVY = mosaic, Genus Potyvirus, Family Potyviridae) and Potato leafroll virus (PLRV , Genus Polerovirus, Family Luteoviridae), both being aphid (Hemiptera: Aphididae) transmitted (Radcliffe & Ragsdale 2002). Differences in transmission characteristics and number of vector species influence their spread of the virus and methods of control. PVY is transmitted in a nonpersistent manner and is acquired and inoculated during brief probes by aphids, including the alatae of many species that do not colonize potato. PLRV is transmitted in a persistent manner. It is confined to phloem tissues, and only those aphids that feed long enough acquire it, and then inoculate potato plants with PLRV (Woodford 1992).
Aphids include some of the most important pests of potato crops mainly because of their role as virus vectors (Adams & Kelley 1950; Kolbe 1970; Shands et al. 1972a). In South America 336 aphid species have been recorded (Ortego personal communication 2013) of which 237 are known to be present in Argentina (Nieto Nafría et al. 1994; Ortego et al. 2004; Mier Durante et al. 2011; Mier Durante et al. 2012; Ortego 2014 in press). Regarding the aphid diversity of Tucumán province, there are studies that date back to 1922 that cite a total of 82 species of aphids on several host plants (Ovruski de Martínez & Delfino 1990; Nieto Nafría et al. 1994; Ovruski de Martínez et al. 1997; A. L. Avila unpublished data).
Knowing the aphid species present in potato agroecosystems of Argentina is important in understanding the epidemiology of aphid-borne viruses of potato and the development of appropriate management strategies. Therefore, the present study aims to establish the aphid species composition in Tucumán Province, one of the potato production areas in Argentina.
Materials and Methods
The following 3 agroecological regions of Tucumán were chosen from the “Agrologic outline of the Province of Tucumán” of Zuccardi & Fadda (1985), i.e.,
Alto Verde, in the southwest, department of Chicligasta (S 27° 21'-W 65° 40′; 390 m asl) is the principal production site of potatoes for consumption.
Tafí del Valle, in the northwest, department of Tafí del Valle (S 26° 54'-W 65° 45′; 2,000 m asl) is a significant production site of seed potatoes.
Las Talitas, in the northeast, department of Tafí Viejo, located (S 26° 48′-W 65° 12′; 481 m asl) is a production site of potatoes for consumption and industrial use.
Every week during 2 cropping seasons, winged forms of aphids were collected in the 3 regions with modified yellow Moericke water pan traps (Moericke 1955). Each pan was made of plastic and it was a little smaller than the original (53 × 35 × 11 cm). To determine which species colonized the crop, apterae aphids were collected weekly from plants evenly distributed throughout each plot. Potato plants were gently beaten against a vertical beat sheet used for sampling soybeans insects (Drees & Rice 1985). Specimens were preserved in 70% ethanol until identification. In each region, during 2 potato seasons, monitoring was conducted for various numbers of weeks because of weather conditions, the duration of the crop, etc.
In Alto Verde alatae were collected during 27 weeks and wingless aphids during 16 weeks. In Las Talitas, alatae individuals were monitored during 26 weeks and apterae during 15 weeks. Finally, in Tafí del Valle alatae were collected during 37 weeks and wingless individuals during 12 weeks.
Several keys were used to identify the species, i.e., Remaudière & Seco Fernandez (1990), Blackman & Eastop (2000), and Taylor & Robert (1984). Sometimes identifications could be done only to the genus. Aphid classification of Blackman & Eastop (2000) was followed in this work. Literature was consulted to highlight which of the species collected had been cited previously as a vector of an important potato virus.
A total of 15,169 alatae aphids were caught during this study. Fifty-six species were identified. Twenty-one of these species have been cited around the world as vectors of PVY and PLRV virus (Völk 1959; Van Hoof 1980; Piron 1986; Blackman & Eastop 2000) (Table 1).
All the aphids collected belonged to the Aphididae family and within it, to 6 subfamilies: Aphidinae, Calaphidinae, Chaitophorinae, Eriosomatinae, Saltusaphidinae and Lachninae. In all 3 regions sampled, more than 95% of the species belonged to the Aphidinae. Regarding the aphids collected in both seasons, Tafí del Valle accounted for the greatest number of species, although Las Talitas had the largest number of individuals captured. Twentyseven species appeared in the 3 regions, and within these, the genus Aphis was the most abundant. Furthermore, the following species were the most prominent in each region: Hyperomyzus lactucae (Linnaeus) at Las Talitas, Acyrthosiphon kondoi Shinjiat Alto Verde and Pemphigus sp. at Tafí del Valle (Table 1).
Among known vectors of PVY and PLRV , the green peach aphid, Myzus persicae (Sulzer), was the most abundant in the 3 regions, while Capitophorus elaeagni (Del Guercio) was quite evenly abundant among all 3 regions (Table 1). Main differences were observed for alates both of Brevicoryne brassicae (Linnaeus) and Lipaphis erysimi (Davis). Brevicoryne brassicae was much more abundant at Tafí del Valle than in the other 2 regions. Lipaphis erysimi was most prominent at Las Talitas, where it constituted more than 16% of the catches in contrast to representing less than 1% of the catches at Tafí del Valle. The total number of specimens of known vectors was 8,898 winged individuals (Table 1), which represented 58.66% of the total, with the higher quantity collected in Las Talitas (5,470 individuals, 60.6%), followed by Alto Verde (2,291 individuals, 59%) and Tafí del Valle (1,137 individuals, 50.2%). It is worth noting that several species within the Aphis genus are known as virus vectors, and that the identities of species of the alatae captured in the flight phase cannot be reliably determined, except for a few species whose alatae are highly distinctive (Stroyan 1984). Since in this work we did not identify the species belonging to this genus, further studies could modify these results.
With regard to apterous aphids (Table 2), a total of 7,455 individuals of 9 different species were collected, all of which belonged to the Aphididae. Two subfamilies were found within this family, i.e., Aphidinae and its Macrosiphini (97.2%) and Aphidini tribes (2.7%), and Eriosomatinae and its Pemphigini tribe (< 0.01%) (Table 2). In Alto Verde and Tafí del Valle the preponderance of M. persicae was very clear, different from what occurred in Las Talitas, where the dominance was shared by M. persicae and Macrosiphum euphorbiae (Thomas).
Our trapping data demonstrate that there are numerous species of winged aphids visiting potato fields that do not colonize the crop. Information on aphids of Tucumán is sparse, and the few available sources of literature indicate that 82 species have been cited in Tucumán province (Ovruski de Martinez & Delfino 1990; Nieto Nafría et al. 1994; Ovruski de Martinez et al. 1997; A. L. Avila, unpublished data)
Alatae aphids collected in potato crops in Tucumán, Argentina.*PVY vectors and **PLRV Vectors. Values are number and percent of the total specimens for each location.
The discovery of apterous individuals in the crop belonging to 3 taxa that normally do not colonize potato plants (Pemphigus sp., H. lactucae and C. fragaefolii) may be due to the presence of nearby strawberry plants from some previous crop and weeds growing between the potato plants, such as Cruciferae and Sonchus spp. (Asterales: Asteraceae), that are hosts of these species.
Virus transmission rate depends on many factors such as the vector abundance and vector population dynamics, the efficiency of transmission, and environmental factors (Boukhris-Bouhachem et al. 2013). During this study, only species diversity and abundance were surveyed. Each region presented its own epidemiological characteristics but they all harbor PVY and PLRV vectors in abundance. In this regard, Tafí del Valle seems different because it had the lowest number of aphids and the greater diversity. This could be because of certain characteristics of the valley such as altitude and climatic conditions, mainly temperature and rainfall that allow the expression of a different vegetation composition (Meyer & Weyrauch 1966).
It has been reported that any aphid visiting the potato plant is a potential vector of non-persistent viruses (Harrewijn et al. 1981). However, only 47 species of aphids including many species that do not colonize potato crop, have been proven capable of transmitting PVY with varying efficiencies (Völk 1959; Van Hoof 1980; Piron 1986; Ortego 1991; Pérez et al. 1995; Kerlan 2006) and only 30 of them are cited in Argentina (Ortego & Mier Durante 2010). Twenty-one of the species collected in this work were previously cited as capable of transmitting PVY and/or PLRV (Table 1). Of these, M. persicae is known to be a major vector of these 2 viruses and merits special attention because of its importance as a crop pest. For example, M. persicae can transmit more than 100 viruses (Kennedy et al. 1962). Additionally, M. persicae stands out from the rest of the aphid species because of its wide geographic distribution and its wide host range (Van Emden et al. 1969). More than 400 of plant species belonging to 50 families are hosts of M. persicae (Ossianilsson 1966). It is possible that secondary hosts of M. persicae are allowed to grow in the 3 regions evaluated. Therefore, if the abundance of secondary host species could be drastically reduced, then the incidence of potato plants infected with these viruses would be greatly reduced as well.
Apterae aphids collected on potato crops in the three major potato production regions of Tucumán province, Argentina. *pvy vectors and **plrv vectors.values are number and percentof the total specimens for each location.
PLRV is mainly transmitted by aphids colonizing potato crops but not by all colonizing aphid species (Harrewijn et al. 1981). The literature mentions the existence of 10 aphid species as vectors of PLRV , 9 of which are present in Argentina (Kennedy et al. 1962; Ortego & Mier Durante 2010) and 5 of them were collected in Tucumán province during this survey (Table 2). A remarkable number of apterae of M. persicae was found colonizing the crop, and this species is well known as an efficient virus vector in several crops including potato. Results have shown that the number of green peach aphids in the crop had reached remarkably great densities, being present throughout the crop cycle, and representing more than 97% of the whole in Tafi del Valle (the region dedicated to seed potato production) and Alto Verde, but being much less abundant in Las Talitas. These findings must be considered only as a first step of a more complete epidemiological study and the development of an effective strategy to minimize virus transmission.
We thank to all the members of Horticulture Department of EEAOC, especially to Ing. Agr. Ramiro Lobo and Ing. Agr. Alicia Forns. Also to Dra. Gabriela Murua and Ing. Agr. Gerardo Gastaminza for excellent technical support. Thanks to Ing. Zoot. Lorena Soulé Gómez for the climatic information. This study was supported by EEAOC and CONICET and it is part of the first author's doctoral thesis.