1284 Florida Entomologist 97(4) December 2014

Aphid (: ) diversity in potato production areas in TUCUMÁN, Argentina

1,2,* 1 3 1 1,2 4 A. L. Avila , M. A. Vera , J. Ortego , E. Willink , L. D. Ploper and V. C. Conci 1Estación Experimental Agroindustrial Obispo Colombres (EEAOC), Sección Zoología Agrícola, Las Talitas (T4104AUD), Tucumán, Argentina 2Instituto de Tecnología Agroindustrial del Noroeste Argentino (ITANOA) - Consejo Nacional de Investigaciones Científicas yT écnicas (CONICET) 3Instituto Nacional de Tecnología Agropecuaria (INTA), EEA Junín, Mendoza, Argentina. 4IPAVE, Instituto de Patología Vegetal-CIAP-INTA. Córdoba, Argentina - CONICET *Corresponding author; E-mail: [email protected]

Abstract are recognized as important plant pests worldwide and they are major vectors of viruses. It is necessary to identify the 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 identi- fied, 27 of which were present in all regions surveyed. Differences in species diversity between regions are discussed. Key Words: aphids, biodiversity, , virus vector

Resumen Los áfidos son una importante plaga de plantas en todo el mundo y su importancia radica en ser uno de los principales vectores de virus. Es necesario identificar las especies de áfidos en un agroecosistema con el fin de desarrollar estrategias de manejo adecuadas. El objetivo de este tra- bajo fue determinar la diversidad taxonómica de las especies de áfidos presentes en cultivos de papa en diferentes regiones agrológicas de Tucumán, Argentina. El monitoreo se realizó utilizan- do dos métodos: se utilizaron trampas amarillas de agua Moericke para los alados y los ápteros fueron colectados directamente de las plantas. Un total de 15,169 áfidos alados y 7,455 ápteros colonizando el cultivo fueron capturados. Se identificaron 56 especies y 27 de ellas estuvieron representadas en todas las regiones evaluadas. Se observaron diferencias en la diversidad de especies entre las regiones, las cuales se discuten en el trabajo.

Palabras Clave: pulgones, biodiversidad, taxonomía, vector de virus

The province of Tucumán, Argentina, produces persistent manner and is acquired and inoculated potato for consumption, industrial use and for use during brief probes by aphids, including the alatae as seed potatoes. With regard to potato production of many species that do not colonize potato. PLRV is for consumption and industrial use, Tucumán is transmitted in a persistent manner. It is confined to characterized mainly by its early winter–spring phloem tissues, and only those aphids that feed long production period (Caldiz 2006). Seed potatoes are enough acquire it, and then inoculate potato plants grown during Oct to Mar in the department of Tafí with PLRV (Woodford 1992). del Valle (Fandos et al. 2011). Seed potato produc- Aphids include some of the most important pests tion is not an easy task, as crops are affected by mul- of potato crops mainly because of their role as virus tiple pests and diseases, including several viruses vectors (Adams & Kelley 1950; Kolbe 1970; Shands that contribute to the devaluation and rejection of et al. 1972a). In South America 336 aphid species seed stocks for certification (Carli & Baltaev 2008). have been recorded (Ortego personal communica- The most important virus diseases of potato tion 2013) of which 237 are known to be present in are Potato virus Y (PVY = mosaic, Genus Potyvi- Argentina (Nieto Nafría et al. 1994; Ortego et al. rus, Family Potyviridae) and Potato leafroll virus 2004; Mier Durante et al. 2011; Mier Durante et al. (PLRV, Genus Polerovirus, Family Luteoviridae), 2012; Ortego 2014 in press). Regarding the aphid di- both being aphid (Hemiptera: Aphididae) trans- versity of Tucumán province, there are studies that mitted (Radcliffe & Ragsdale 2002). Differences in date back to 1922 that cite a total of 82 species of transmission characteristics and number of vec- aphids on several host plants (Ovruski de Martínez tor species influence their spread of the virus and & Delfino 1990; Nieto Nafría et al. 1994; Ovruski de methods of control. PVY is transmitted in a non- Martínez et al. 1997; A. L. Avila unpublished data). Avila et al.: Aphid Diversity on Potato in Argentina 1285

Knowing the aphid species present in potato the world as vectors of PVY and PLRV virus (Völk agroecosystems of Argentina is important in under- 1959; Van Hoof 1980; Piron 1986; Blackman & Ea- standing the epidemiology of aphid-borne viruses stop 2000) (Table 1). of potato and the development of appropriate man- All the aphids collected belonged to the Aphidi- agement strategies. Therefore, the present study dae family and within it, to 6 subfamilies: Aphidi- aims to establish the aphid species composition in nae, Calaphidinae, Chaitophorinae, Eriosomatinae, Tucumán Province, one of the potato production ar- Saltusaphidinae and Lachninae. In all 3 regions eas in Argentina. sampled, more than 95% of the species belonged to the . Regarding the aphids collected in Materials and Methods both seasons, Tafí del Valle accounted for the great- The following 3 agroecological regions of est number of species, although Las Talitas had the Tucumán were chosen from the “Agrologic outline largest number of individuals captured. Twenty- of the Province of Tucumán” of Zuccardi & Fadda seven species appeared in the 3 regions, and within (1985), i.e., these, the genus Aphis was the most abundant. 1. Alto Verde, in the southwest, department of Furthermore, the following species were the most Chicligasta (S 27° 21’-W 65° 40'; 390 m asl) is prominent in each region: lactucae the principal production site of potatoes for con- (Linnaeus) at Las Talitas, kondoi sumption. Shinjiat Alto Verde and Pemphigus sp. at Tafí del 2. Tafí del Valle, in the northwest, department of Valle (Table 1). Tafí del Valle (S 26° 54’-W 65° 45'; 2,000 m asl) Among known vectors of PVY and PLRV, the is a significant production site of seed potatoes. green peach aphid, persicae (Sulzer), was the most abundant in the 3 regions, while 3. Las Talitas, in the northeast, department of elaeagni (Del Guercio) was quite evenly abundant Tafí Viejo, located (S 26° 48'-W 65° 12'; 481 m among all 3 regions (Table 1). Main differences were asl) is a production site of potatoes for consump- observed for alates both of brassicae tion and industrial use. (Linnaeus) and erysimi (Davis). Brevico- Every week during 2 cropping seasons, winged ryne brassicae was much more abundant at Tafí del forms of aphids were collected in the 3 regions with Valle than in the other 2 regions. Lipaphis erysimi modified yellow Moericke water pan traps (Moer- was most prominent at Las Talitas, where it consti- icke 1955). Each pan was made of plastic and it tuted more than 16% of the catches in contrast to was a little smaller than the original (53 × 35 × 11 representing less than 1% of the catches at Tafí del cm). To determine which species colonized the crop, Valle. The total number of specimens of known vec- apterae aphids were collected weekly from plants tors was 8,898 winged individuals (Table 1), which evenly distributed throughout each plot. Potato represented 58.66% of the total, with the higher plants were gently beaten against a vertical beat quantity collected in Las Talitas (5,470 individuals, sheet used for sampling soybeans (Drees & 60.6%), followed by Alto Verde (2,291 individuals, Rice 1985). Specimens were preserved in 70% etha- 59%) and Tafí del Valle (1,137 individuals, 50.2%). nol until identification. In each region, during 2 po- It is worth noting that several species within the tato seasons, monitoring was conducted for various Aphis genus are known as virus vectors, and that numbers of weeks because of weather conditions, the identities of species of the alatae captured in the the duration of the crop, etc. flight phase cannot be reliably determined, except In Alto Verde alatae were collected during 27 for a few species whose alatae are highly distinc- weeks and wingless aphids during 16 weeks. In Las tive (Stroyan 1984). Since in this work we did not Talitas, alatae individuals were monitored during identify the species belonging to this genus, further 26 weeks and apterae during 15 weeks. Finally, in studies could modify these results. Tafí del Valle alatae were collected during 37 weeks With regard to apterous aphids (Table 2), a to- and wingless individuals during 12 weeks. tal of 7,455 individuals of 9 different species were Several keys were used to identify the species, collected, all of which belonged to the Aphididae. i.e., Remaudière & Seco Fernandez (1990), Black- Two subfamilies were found within this family, i.e., man & Eastop (2000), and Taylor & Robert (1984). Aphidinae and its (97.2%) and Aphi- Sometimes identifications could be done only to the dini tribes (2.7%), and Eriosomatinae and its Pem- genus. Aphid classification of Blackman & Eastop phigini tribe (< 0.01%) (Table 2). In Alto Verde and (2000) was followed in this work. Literature was Tafí del Valle the preponderance of M. persicae was consulted to highlight which of the species collected very clear, different from what occurred in Las Tali- had been cited previously as a vector of an impor- tas, where the dominance was shared by M. persi- tant potato virus. cae and euphorbiae (Thomas).

Results Discussion A total of 15,169 alatae aphids were caught dur- Our trapping data demonstrate that there are ing this study. Fifty-six species were identified. numerous species of winged aphids visiting potato Twenty-one of these species have been cited around fields that do not colonize the crop. Information on 1286 Florida Entomologist 97(4) December 2014

al % t o

0.11 2.23 0.09 0.01 0.22 0.74 2.00 0.02 3.60 0.01 0.28 0.01 6.51 3.78 0.20 0.33 0.09 0.01 0.12 0.05 1.92 0.20 0.05 0.03 6.14 0.03 11.53 30.58 17 56 the

otal T 8,898 o f 1 3 2 2 1 8 8 5 5

15,169 14 34 42 30 50 13 18 30 16 112 338 304 546 988 573 291 932 N° 4,639 1,749 p er c ent

a n d

% — — — — 0.75 0.04 0.84 1.63 0.18 0.13 1.94 0.09 0.40 5.57 0.35 2.21 0.04 0.80 0.18 0.84 0.22 0.13 0.09 0.27 0.97 0.31 alle 30.87 14.84 6 45 2,264 1,137 nu m ber

1 4 3 2 9 8 1 4 5 3 2 6 7 2010/2011 afí del V — — — — 17 19 37 44 50 18 22 19 N° T 699 336 126 a re

al ues V . % — — — — — — — — 0.11 1.62 0.43 3.27 5.53 0.32 6.70 3.27 0.04 0.04 0.06 0.03 0.04 0.01 0.03 1.93 0.06 9.65 31.18 16.20 6 40 alitas 9,024 5,470 e c t o rs 4 4 5 3 4 1 3 5 10 39 29 V 2011/2012 Las T — — — — — — — — 146 295 499 605 295 174 871 N° 2,814 1,462 **PL RV — % a n d — — — — — — — —

4.51 0.10 0.39 0.93 0.13 0.08 0.10 0.05 1.21 3.92 0.23 0.03 6.83 0.21 0.49 2.53 0.52 1.42 29.01 5 erde 37 3,881 2,291 4 5 3 4 2 9 1 8 — 15 36 47 19 98 20 55 2010/2011 ve c t o rs Alto V — — — — — — — — 175 152 265 N° 1,126 .*P V Y rgentin a , A , u c m án T

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a e t la s p e c i m ens 1. A 1. a b l e ectors of PVY and P L RV raps otal number of specimens otal number of species T R egion S eason T T V Acyrthosiphon ( ) kondoi S hinji Acyrthosiphon ( ) pisum H arris)* Aphis spp. Aploneura lentisci P asserini ( ) solani (Kaltenbach)** ( ) helichrysi (Kaltenbach)* T Taxa Brachycaudus ( Mordvilkomemor ) rumexicolens P atch) Brevicoryne brassicae (Linnaeus)* ( ) tapuskae H ottes & Frison) Macrosiphum ( ) euphorbiae T homas)** Macrosiphum ( ) rosae (Linnaeus) ( ) dirhodum (Walker)* rosarum (Kaltenbach)* (Del G uercio)* Capitophorus hippophaes (Walker)* Capitophorus sp. Cavariella ( ) aegopodii S copoli)* sp. Chaitophorus leucomelas Koch Cinara sp. ( ) ballotae H ille Lis Lambers* acupariae (Buckton) Eucarazzia elegans (Ferrari) foeniculi ( P asserini)* Hyperomyzus ( ) lactucae (Linnaeus)* Illinoia sp. Lipaphis ( ) erysimi (Kaltenbach)* Macrosiphoniella ( ) artemisiae (Boyer de Fonscolombe) Avila et al.: Aphid Diversity on Potato in Argentina 1287

% 0.11 0.05 0.02 1.71 0.01 0.01 0.01 0.02 0.28 0.72 1.06 0.09 0.08 0.14 0.20 0.61 0.07 0.01 0.44 0.22 0.34 0.03 0.03 0.03 0.02 0.18 0.30 0.90 21.45 p er c ent

17 56 otal T 8,898 a n d 8 3 1 1 1 3 1 5 4 4 3

15,169 42 13 12 21 30 93 10 66 34 52 28 46 16 259 109 161 136 N° 3,253 nu m ber

a re

% — — — — — — — 0.09 6.14 0.04 0.04 0.13 1.46 0.44 0.66 0.04 0.09 0.80 0.53 0.13 0.04 1.99 0.53 0.09 0.22 0.04 0.71 2.30 alle 19.79 6 45 al ues V 2,264 1,137 . 2 1 1 3 1 2 3 1 2 5 1 2010/2011 afí del V — — — — — — — 33 10 15 18 12 45 12 16 52 N° T 448 139 ve c t o rs % — — — — — — — — 0.01 0.03 0.80 0.06 0.34 0.54 0.14 0.10 0.12 0.21 0.35 0.21 0.18 0.24 0.06 0.02 0.03 0.16 0.38 0.45 15.02 6 **PL RV 40 alitas 9,024 5,470 1 3 5 9 5 2 3 a n d

11 72 31 49 13 19 32 19 16 22 14 34 41 2011/2012 Las T — — — — — — — — N° 1,355 ve c t o rs % — — — — — — — — — — 1.11 0.13 1.24 0.03 0.10 1.75 2.50 0.05 0.03 1.26 0.18 0.05 0.46 0.46 0.03 0.08 0.23 0.28 .*P V Y 37.36 5 erde 37 3,881 2,291 5 1 4 2 1 7 2 1 3 9 11 48 68 97 49 18 18 43 2010/2011 Alto V — — — — — — — — — — N° rgentin a 1,450 , A , u c m án T

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akahashi) ) A ) al t o

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o ntinue d o f 1. (C 1. a b l e ectors of PVY and P L RV raps otal number of specimens otal number of species T R egion S eason T T V Myzus ( Nectarosiphon ) persicae S ulzer)** ( ) ribisnigri M osley) Ovatus crataegarius (Walker) Pemphigus sp. T Taxa Pleotricophorus glandulosus (Kaltenbach) porosum ( S anderson) poae ( G illette) ( ) latysiphon (Davidson)** maidis (Fitch)* Rhopalosiphum padi (Linnaeus)* Rhopalosiphum rufiabdominale ( S asaki) Rhopalosiphum sp. Saltusaphis scirpus T heobald ( ) graminum R ondani)* Sipha ( Rungsia ) maydis P asserini ( ) avenae (Fabricius)* Takecallis arundinariae ( E ssig) Takecallis taiwanus ( T Takecallis ) nigriabdominalis ( S asaki) ( Tetraneurella Tetraneura Therioaphis ( Rhizoberlesia ) riehmi (Börner) Therioaphis ( Pterocallidiun ) trifolii M onell) Toxoptera aurantii (Boyer de Fonscolombe) Toxoptera ) annulatus ( H artig) ( Tuberculoides Tuberculatus ) querceus (Kaltenbach) ( Tuberculatus Tuberculatus ( ) spp. Uroleucon ( Uromelan ) spp. Uroleucon ( ) sonchi (Linnaeus)* U nidentified nervata ( G illette) Wahlgreniella 1288 Florida Entomologist 97(4) December 2014 aphids of Tucumán is sparse, and the few avail- persicae is known to be a major vector of these 2 able sources of literature indicate that 82 species viruses and merits special attention because of its have been cited in Tucumán province (Ovruski de importance as a crop pest. For example, M. persicae Martinez & Delfino 1990; Nieto Nafría et al. 1994; can transmit more than 100 viruses (Kennedy et Ovruski de Martinez et al. 1997; A. L. Avila, unpub- al. 1962). Additionally, M. persicae stands out from lished data) the rest of the aphid species because of its wide geo- The discovery of apterous individuals in the crop graphic distribution and its wide host range (Van belonging to 3 taxa that normally do not colonize Emden et al. 1969). More than 400 of plant species potato plants (Pemphigus sp., H. lactucae and C. belonging to 50 families are hosts of M. persicae (Os- fragaefolii) may be due to the presence of nearby sianilsson 1966). It is possible that secondary hosts plants from some previous crop and of M. persicae are allowed to grow in the 3 regions weeds growing between the potato plants, such as evaluated. Therefore, if the abundance of second- Cruciferae and Sonchus spp. (Asterales: Asterace- ary host species could be drastically reduced, then ae), that are hosts of these species. the incidence of potato plants infected with these Virus transmission rate depends on many fac- viruses would be greatly reduced as well. tors such as the vector abundance and vector popu- PLRV is mainly transmitted by aphids colonizing lation dynamics, the efficiency of transmission, and potato crops but not by all colonizing aphid species environmental factors (Boukhris-Bouhachem et al. (Harrewijn et al. 1981). The literature mentions the 2013). During this study, only species diversity and existence of 10 aphid species as vectors of PLRV, 9 abundance were surveyed. Each region presented of which are present in Argentina (Kennedy et al. its own epidemiological characteristics but they all 1962; Ortego & Mier Durante 2010) and 5 of them harbor PVY and PLRV vectors in abundance. In were collected in Tucumán province during this this regard, Tafí del Valle seems different because survey (Table 2). A remarkable number of apterae it had the lowest number of aphids and the greater of M. persicae was found colonizing the crop, and diversity. This could be because of certain charac- this species is well known as an efficient virus vec- teristics of the valley such as altitude and climatic tor in several crops including potato. Results have conditions, mainly temperature and rainfall that shown that the number of green peach aphids in the allow the expression of a different vegetation com- crop had reached remarkably great densities, being position (Meyer & Weyrauch 1966). present throughout the crop cycle, and representing It has been reported that any aphid visiting the more than 97% of the whole in Tafi del Valle (the potato plant is a potential vector of non-persistent region dedicated to seed potato production) and Alto viruses (Harrewijn et al. 1981). However, only 47 Verde, but being much less abundant in Las Talitas. species of aphids including many species that do These findings must be considered only as a first not colonize potato crop, have been proven capa- step of a more complete epidemiological study and ble of transmitting PVY with varying efficiencies the development of an effective strategy to mini- (Völk 1959; Van Hoof 1980; Piron 1986; Ortego mize virus transmission. 1991; Pérez et al. 1995; Kerlan 2006) and only 30 of them are cited in Argentina (Ortego & Mier Du- Acknowledgments rante 2010). Twenty-one of the species collected in We thank to all the members of Horticulture Depart- this work were previously cited as capable of trans- ment of EEAOC, especially to Ing. Agr. Ramiro Lobo and mitting PVY and/or PLRV (Table 1). Of these, M. Ing. Agr. Alicia Forns. Also to Dra. Gabriela Murua and

Table 2. 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 percen- tof the total specimens for each location.

Region Alto Verde Las Talitas. Tafí del Valle Total Total number of specimens 3,927 1,353 2,175 7,455 Total number of species 5 5 7 9 Species N° % N° % N° % N° % Aphis gossypii Glover** 12 0.306 150 11.09 25 1.149 187 2.508 Aphis fabae Scopoli** — — 7 0.517 5 0.23 12 0.161 Aulacorthum solani (Kaltenbach)** 13 0.331 — — 12 0.552 25 0.335 Macrosiphum euphorbiae (Thomas)** 23 0.586 553 40.87 2 0.092 578 7.753 Myzus persicae (Sulzer)** 3,877 98.73 636 47.01 2,121 97.52 6,634 88.99 Rhopalosiphum rufiabdominale (Sasaki) 2 0.051 — — — — 2 0.027 Pemphigus sp. — — — — 4 0.184 4 0.054 (Cockerell) — — — — 6 0.276 6 0.08 Hyperomyzus lactucae (Linnaeus)* — — 7 0.517 — — 7 0.094 Avila et al.: Aphid Diversity on Potato in Argentina 1289

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