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Taxonomic and Functional Structure of Phytophagous Insect Communities Associated with Grain Amaranth

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Taxonomic and Functional Structure of Phytophagous Insect Communities Associated with Grain Amaranth Taxonomic and Functional Structure of Phytophagous Insect Communities Associated with Grain Amaranth S Niveyro & A Salvo Neotropical Entomology ISSN 1519-566X Volume 43 Number 6 Neotrop Entomol (2014) 43:532-540 DOI 10.1007/s13744-014-0248-3 1 23 Your article is protected by copyright and all rights are held exclusively by Sociedade Entomológica do Brasil. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Neotrop Entomol (2014) 43:532–540 DOI 10.1007/s13744-014-0248-3 ECOLOGY, BEHAVIOR AND BIONOMICS Taxonomic and Functional Structure of Phytophagous Insect Communities Associated with Grain Amaranth 1 2 SNIVEYRO ,ASALVO 1Fac de Agronomía, Univ Nacional de La Pampa, Santa Rosa, La Pampa, Argentina 2Centro de Investigaciones Entomológicas de Córdoba, Instituto Multidisciplinario de Biología Vegetal, CONICET, Fac de Ciencias Exactas Físicas y Naturales, Univ Nacional de Córdoba, Córdoba, Argentina Keywords Abstract Amaranthus, herbivory, insect guilds, stem Amaranthus are worldwide attacked mainly by leaf chewers and sucker borer insects. Stem borers and leaf miners follow in importance, while minor Correspondence herbivores are leaf rollers, folders, and rasping-sucking insects. The her- SNiveyro,Fac de Agronomía, Univ Nacional de bivorous community observed on Amaranthus spp. in Argentina was La Pampa, Santa Rosa, La Pampa, Argentina; [email protected] consistent with the information reported worldwide both in guild compo- sition and order proportion. Amaranth plants had a higher number of Edited by Antônio R Panizzi – Embrapa/Trigo phytophagous species in their native rather than in its introduced range. Received 8 April 2014 and accepted Occurrence of insect guilds differed in space and time. The highest density 6 October 2014 of leaf chewers was observed shortly after the emergence of plants, while Published online: 13 November 2014 higher density of borer and sucker insects coincided with reproductive stages of the crop. The sucking guild was observed mainly at panicles, * Sociedade Entomológica do Brasil 2014 while the insects within the leaf chewer group were registered in both leaves (92.6%, n=746 adults) and inflorescences (7.4%). The borer guild was also recorded in stems and inflorescences; however, the density of larvae in stems was about four times as high as the density observed in panicles (n=137 larvae). Introduction crops are not able to grow (Brenner et al 2000,Johnson &Henderson2002). In the last decades, amaranth has received renewed Numerous herbivorous insects have been reported to interested as a food crop. This is largely due to the high affect the Amaranthus genus worldwide (El-Aydam & Bürki amounts of good quality proteins for human consumption 1997). Among them, species of leaf chewers and sucking contained in its grains (Downton 1973, Teutonico & Knorr insects are known to feed heavily on leaves and floral buds 1985). Its amino acid profile, and in particular the high (Bürki et al 1997,Olson&Wilson1990), whereas the stem levels of lysine, makes amaranth grains an attractive borer guild is mentioned as the prevalent group at global protein source, very similar to the recommended amino scale (Louw et al 1995). Leaf miners, leaf rollers, and leaf acid pattern required for human nutrition, as established folders are also mentioned as amaranth insect feeders. For by FAO and the World Health Organization (Becker et al the first group, species are usually reported in Amaranthus 1981,Pedersenet al 1990). Moreover, being a pseudo- wild plants rather than in crops (Stegmaier 1950,Spencer cereal, grains of amaranths lack gluten, thus being a 1973, Mujica & Berti 1997, Carrasco 1987), while little is suitable food for people with gluten intolerance (Zannini known about the species in the leaf roller and folder guilds et al 2012). But Amaranthus plants are not only recog- (Jena et al 2000, Waterhouse 1994). Although Amaranthus is nized for their nutritional features but also due to their a genus that is widely distributed around the world, most of ability to thrive in many environments and tolerate ad- the species (including those cultivated for grain purpose) versities such as low water regime (Liu & Stützel 2002), have originated in the Americas (Sauer 1950, 1967,Coons poor soils, and moderate salinity levels (Omami & 1982), while only a few of them are native to Europe, Asia, Hammes 2006), conditions on which other commercial and Africa (Sauer 1967, Robertson 1981, Costea et al 2001). Author's personal copy Phytophagous Insect Communities Associated with Grain Amaranth 533 For it being an introduced crop in many non-American coun- were selected randomly and the whole plants were tries, grain amaranth might experience a reduction of her- inspected. The insects observed were counted and collected bivorous insect richness in introduced ranges according to (at least one sample of each species) for later identification in the “enemy release hypothesis” (ERH) (Keane & Crawley the laboratory. The growing stage of the insects and the 2002). This would represent an advantage for its cultivation location where they were found in the plant were also in non-natural areas. However, comparative studies regard- registered. ing herbivore diversity, load, and herbivory damage on During the second year of the trial (summer 2008/2009), Amaranthus spp. in the Americas and elsewhere are not borer insect occurrence was recorded. For that, a total of available. In turn, few studies concerning phytophagous in- 500 plants were taken at random in two different stages of sects on grain amaranth has been published in South the plant coincident with stages R4 and R6, according a America (Ves Losada & Covas 1987, Guerrero et al 2000,de phenological scale (Mujica & Quillahuamán 1989). The stalks Oliveira et al 2012,Riquelmeet al 2013), which is considered and panicles of these plants were sectioned longitudinally, the original region of two cultivable species Amaranthus and active larvae were counted and preserved in 70% etha- cruentus and Amaranthus mantegazzianus (Sauer 1950, nol for identification. 1967). Therefore, the first aim of this study was to inventory and describe the community of phytophagous insects asso- Literature survey ciated to grain amaranth in Argentina, exploring the occur- rence of insect guilds along the phenological cycle of the A literature survey of phytophagous insects associated to crop. The second aim was to compare the Amaranthus Amaranthus spp. was carried out, including research articles, phytophagous insect fauna in American and non-American reviews, and catalogs mentioning insects on both wild and countries on the basis of a literature survey, focusing the cultivated amaranth plants. Only herbivorous insects that analysis on its taxonomic and guild structure. were reported as effectively feeding on plants were consid- ered, and they were grouped into different guilds mainly following Stork (1987). Material and Methods Field surveys Statistical analysis Field surveys of phytophagous insects were conducted in The chi-square test was performed to compare guild struc- crops of three amaranth species (Amaranthus cruentus cv. ture and abundance between phytophagous communities Don León, Amaranthus hypochondriacus cv. Artasa 9122, observed in the Americas and those recorded in other parts A. hypochondriacus San Antonio, A. hypochondriacus FK of the world. The same analysis was performed to compare 280-FH1, and A. mantegazzianus cv. Don Juan) sowed in herbivore communities in Argentina with the information the north of Santa Rosa, La Pampa, Argentina (36°37′S, recorded worldwide. In all cases, an alpha of 0.05 was used. 64°16′W), during two growing seasons (summer 2007– 2008 and 2008–2009). A field of 156 m2 was sowed with a space of 0.50 m between rows and a density of 3.5 kg of seeds per hectare. The plants did not receive any insecticide Results application and weeding was done manually. The essay was located in a livestock area characterized by grasslands, Seventy previous studies on herbivorous fauna associated to wheat, and alfalfa field crops. During two growing seasons, Amaranthus plants made in 33 countries (42 in America and the essay was performed in a field of 7 ha in which several 28 elsewhere) on the five continents reported 255 species of weeds were present, being Cynodon dactylon, Digitaria phytophagous insects. The guild of leaf chewer was the sanguinalis, Portulaca oleracea, Xanthium cavanillesii, largest and richest group worldwide (El-Aydam & Bürki Salsola kali,andConyza bonariensis the most abundant. 1997, Clarke-Harris et al 2004, Aragón-García et al 2011), Insect sampling was conducted shortly after the plant representing half of the total insect species recorded feeding emergence and through all the crop cycle. Five samples in on amaranth (Fig 1a). The remaining species were distributed the first year and seven in the second year were performed among sucking insects (28%), stem borer (9%), leaf miner during daytime (9:00 AM to 2:00 PM approximately), when (8%), and three minor guilds: rasping-sucking insects (3%), most of the herbivorous insects are active. On three occa- leaf folder, and leaf roller (1% each) (Fig 1a). Species in the sions in summer 2008, observations were made at night leaf chewer guild belonged to 21 families of insects, while the (9:00 PM to 10 PM) to sample phytophagous insect not leaf folder guild was just represented by two species in one observed during daytime.
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