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Diversity and phenology of epigeal Coleoptera assemblages in lettuce and tomato crops in Northern Buenos Aires province, Argentina

Abstract

Epigeic coleopteran species are linked by complex trophic webs and implicated in several ecosystem services for agriculture. Although there are reports of ground-dwelling Coleopterans inhabiting main extensive agroecosystems, their assemblages in horticultural crops in Argentina have been little explored. We examined the community structure of epigeal Coleoptera assemblages of Curculionidae, Carabidae, Staphylinidae and Coccinellidae species, in lettuce and tomato crops located in Northern Buenos Aires province, over a 3-year sampling period (2010 to 2013) by using pit-fall traps. Crop species and cycles, and phytosanitary measures (conventional and organic farming), were main factors considered as influencing the insect species composition, abundance and seasonal occurrence in the assemblages. Seventy coleopteran species were identified. The curculionids Ceutorhynchini sp. and Phyrdenus muriceus (Germar), the carabid Scarithes anthracinus Dejean, the coccinelid Eriopis connexa (Germar) and the staphylinids Aleochara sp. and Aleochara obscurus Bernhauer are the most common species in lettuce and tomato crops in the region studied. Especially the carabids, staphylinids and E. connexa are known act as natural enemies of several pests in the agroecosystems studied. Coleopteran assemblages found in lettuce differed from those associated to tomato crops, being the cropping season the main factor that influenced the community structure.

Key words
community; diversity; functional group; guild; horticultural crop; coleopterans

INTRODUCTION

Agricultural activities significantly alter soil properties, as well as its biota in terms of their abundance, biomass and diversity (Brown et al. 2001BROWN G, FRAGOSO C, BARROS I, ROJAS P, PATRON J, BUENO J, MORENO A, LAVELLE P, ORDAZ V & RODRÍGUEZ C. 2001. Diversidad y rol funcional de la macrofauna edáfica en los ecosistemas tropicales mexicanos. Acta Zool Mex 1: 79-110.). Among soil macrofauna (organisms with a body size > 2 mm), beetles represent a numerous and diverse group of species. They are linked by complex trophic webs, and engaged either directly or indirectly in several ecosystem processes such as biological control of pests, as phytophagous, decomposition, nutrient cycling, erosion control, genetic resources and pollination. Furthermore, because of the niche breadth associated to their different developmental stages, beetles connect hypogean and epigean trophic webs, facilitating matter and energy transference (Coleman et al. 2017COLEMAN D, CALLAHAM M & CROSSLEY JR D. 2017. Fundamentals of Soil Ecology. Academic Press.).

Species composition and relative abundance of Coleoptera may vary according to crop management systems. Monoculture, tillage, weeds and pest control produce a simplification of community structure, being generalist species less affected by this management practice. Conversely, those heterogeneous systems that provide both shelter and food to them and other invertebrates pose a greater diversity of coleopterans - both taxonomic and functional – especially promoting biological control of pests (Fournier & Loreau 1999FOURNIER E & LOREAU M. 1999. Effects of newly planted hedges on ground-beetles diversity (Coleoptera, Carabidae) in an agricultural landscape. Ecography 22: 87-97., Magura et al. 2001MAGURA T, TÓTHMÉRÉSZ B & MOLNÁR T. 2001. Edge effect on carabid assemblages along forest-grass transects. Web Ecol 2: 7-13., Fernandes et al. 2018FERNANDES FS, GODOY WAC, RAMALHO FS, MALAQUIAS JB & SANTOS BDB. 2018. The behavior of Aphis gossypii and Aphis craccivora (Hemiptera: Aphididae) and of their predator Cycloneda sanguinea (Coleoptera: Coccinellidae) in cotton-cowpea intercropping systems. An Acad Bras Cienc 90: 373-383.). Organic farming relies on cropping practices that keep agricultural systems operating as naturally as possible. Thus, by reducing or banning chemical inputs organic crops show increased levels of species richness and abundance, depending on the taxonomic group (Shah et al. 2003SHAH PA, BROOKS DR, ASHBY JE, PERRY JN & WOIWOD IP. 2003. Diversity and abundance of the coleopteran fauna from organic and conventionally management systems in Southern England. Agric Forest Entomol 5: 51-60., Hole et al. 2005HOLE DG, PERKINS AJ, WILSON JD, ALEXANDER IH, GRICE PV & EVANS AD. 2005. Does organic farming benefit biodiversity? Biol Conserv 122: 113-130., Zalazar & Salvo 2007ZALAZAR L & SALVO A. 2007. Entomofauna asociada a cultivods hortícolas orgánicos y convencionales en Córdoba, Argentina. Neotrop Entomol 36: 765-773.). For example, Puech et al. (2014)PUECH C, BAUDRY J, JOANNON A, POGGI S & AVIRON S. 2014. Organic vs. conventional farming dichotomy: does it make sense for natural enemies? Agric Ecosyst Environ 194: 48-57. showed that abundances of ladybirds and carabid beetles were higher in organic fields.

Arthropods commonly show associations with plant species, and their populations are subject to variations as vegetation changes over time. Intensive agriculture in temperate regions is practiced in crop cycles, following the seasons. Typically, a short-term replacement of plant species occurs which leads to changes in the arthropod community structure throughout the growing period. Understanding seasonal patterns of biodiversity in agroecosystems may help to enhance management strategies based on ecological processes such as biological control, nutrient cycling, soil formation, etc., and ultimately to increase crop production (Altieri 1999ALTIERI MA. 1999. The ecological role of biodiversity in agroecosystems. Agr Ecosyst Environ 74: 19-31.).

In community ecology, identification of species is a key step to further analyzing patterns of their abundance, seasonal occurrence, feeding habits, etc. in a given place (Morin 1999MORIN PJ. 1999. Community ecology. Blackwell Science, J Wiley & Sons, Malden, Massachusetts., Gotelli 2004GOTELLI NJ. 2004. A taxonomic wish-list for community ecology. Philos T R Soc B 359: 585-597.). In hyperdiverse faunistic groups, such as Coleoptera, this task may be limited by the lack of taxonomic specialists and/or taxonomic keys, as well as reference specimens in local collections. Therefore, there are restrictions at identifying all the species in a community, and, in general, the emphasis is placed on the most predominant groups.

Knowledge of ground-dwelling beetles inhabiting horticultural crops in Argentina is scarce. There are studies on extensive crops, especially for Carabidae and Curculionidae (Marasas et al. 1997MARASAS ME, CICCHINO AC & URRUTIA MI. 1997. Variación numérica de los coleópteros del suelo en un cultivo de frutilla sujeto a fertilización orgánica y convencional. Rev Fac Agron UNLP 102: 81-86., Lanteri et al. 2002LANTERI AA, MARVALDI AE & SUÁREZ SM. 2002. Gorgojos de la Argentina y sus plantas huéspedes. Publicación especial de la Sociedad Entomológica Argentina N° 1. San Miguel de Tucumán, Argentina., Marasas 2002MARASAS M. 2002. Efecto de los sistemas de labranza sobre la abundancia y diversidad de la coleopterofauna edáfica, con especial referencia a las especies de Carabidae, en un cultivo de trigo y los ambientes naturales circundantes. Ph.D. thesis dissertation. Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Argentina., Novo et al. 2002NOVO RJ, VIGLIANCO A & VAUDAGNA E. 2002. Efectos de insecticidas sobre el gorgojo de la papa, Phyrdenus muriceus (Germ.) (Coleoptera: Curculionidae). Agriscientia 19: 3-10., Cicchino et al. 2003CICCHINO AC, MARASAS ME & PALEOLOGOS MF. 2003. Características e importancia de la carabidofauna edáfica de un cultivo experimental de trigo y sus bordes con vegetación espontánea en el partido de La Plata, Pcia. de Buenos Aires. Rev C y T UNSdE 8: 41-55., 2005, Paleologos 2012PALEOLOGOS MF. 2012. Los carábidos como componentes clave de la agrobiodiversidad. Su rol en la sustentabilidad de los agroecosistemas de vid de la zona de Berisso, Provincia de Buenos Aires. Ph.D. thesis dissertation, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Argentina.), and other important families have been less studied. Since soil Coleopterans are taxonomically and functionally diverse, knowledge of their assembling in agroecosystems could provide insights to detect micro-environmental heterogeneity and to design tools for preserving them (Agosti & Sciaky 1998AGOSTI M & SCIAKY R. 1998. Carabidocenosi dei vigneti: rapporti con le zone limitrofe ed evoluzione nel tempo. Natura Bresciana, Annali del Museo Cívico di Scienze Naturali. Brescia 31: 69-86., Niemelä et al. 1990NIEMELÄ J, HALME E & HAILA Y. 1990. Balancing sampling effort in pitfall trapping of carabid beetles. Entomol Fen 21: 233-238., Paleologos et al. 2008PALEOLOGOS MF, FLORES CC, SARANDÓN SJ, STUPINO SA & BONICATTO MM. 2008. Abundancia y diversidad de la entomofauna asociada a ambientes semi-naturales en fincas hortícolas de La Plata, Buenos Aires. Argentina. Rev Bras Agroecol 3: 28.).

In this work we examine the assemblage structure of epigeal Coleoptera that inhabits two main horticultural crops of Argentina, lettuce (Lactuca sativa L.) and tomato (Solanum lycopersicon Mill.), cultivated under conventional and organic management. The study was focused on determining the taxonomic composition, abundance, and dominance of the species belonging to the main four families present in these crops: Curculionidae, Carabidae, Staphylinidae and Coccinellidae. Our hypothesis is that given coleopterans are among the most ubiquitous insect groups and perform multiple ecological functions in agroecosystems, their communities will be well represented in horticultural crops and will show different structure according to the crop species, the cropping season and the cultural practices implemented by producers, from conventional to organic farming.

MATERIALS AND METHODS

Study area and sampling

The study was carried out in commercial farms located surrounding La Plata city, Northern Buenos Aires province, Argentina. This area is known as ‘La Plata Horticultural Belt’, and comprises about 4,500 ha of cultivated land, being 70% dedicated to a variety of vegetables, strawberry and blueberry crops (including open and protected fields). Chemical control is the conventional phytosanitary measure to suppress pests and weeds, but organic farming that includes spraying with natural pesticides (purines) and conservation biological control through habitat manipulation is gaining importance (Salas Gervassio et al. 2016).

To evaluate species composition and community structure of epigeic Coleopteran assemblages in L. sativa and S. lycopersicon, open field crops under conventional (CM) or organic (OM) pest management were selected in the localities of Colonia Urquiza (34°56’36.76 “S, 58°05’20.24”W), Los Hornos (34°58’55.77”S, 57°59’02.01”W) and Lisandro Olmos (35°00’20.48”S, 58°01’59.89”W) (La Plata county, Buenos Aires Province, Argentina).

Insects were sampled by means of pitfall trapping, a technique that allows estimating relative abundance. This method has been widely used in other arthropod community studies (Boito et al. 2009BOITO GT, GERARDO UA, GIUGGIA JA, GIOVANINI D & ORNAGHI JA. 2009. Uso de trampas “Barber” para determinar la diversidad de coleópteros epígeos asociados al cultivo de maní (Arachis hypogaea L.). Rev Fac Cienc Agrar UNCuyo 41: 23-31., Cheli & Corley 2010CHELI GH & CORLEY JC. 2010. Efficient sampling of ground-dwelling arthropods using pitfall traps in arid steppes. Neotrop Entomol 39: 912-917.). The trap consisted in a plastic cup (800 ml, 12 cm height, and 10 cm upper diameter), filled with 350 ml of a saturated NaHCl3 water solution, and detergent as tensioactive. In each farm, an area of 150 m2 of each crop was chosen, and 11 traps were installed at about 5-10m distance along cultivated rows (Jones & Eggleton 2000JONES DT & EGGLETON P. 2000. Sampling termite species assemblages in tropical forests: testing a rapid biodiversity assessment protocol. J Appl Ecol 37: 191-203.). The top of the container was covered with a lid.

Open-field lettuce is cultivated almost year-round, in two cycles: fall-winter (May to August) and spring-summer (September to January). Open-field stalked tomato is cultivated during the warmer months, i.e., spring-summer (October to March). Samplings were taken bi-weekly in lettuce crops and monthly in tomato crops, up to the end of the cropping cycle. Once the traps were emptied and the solution transferred into sealed plastic bags (Ziploc®), new clean solution was added accordingly. Bags were labeled and transported to the laboratory. Information regarding in-farm plant diversity, cultural methods practiced by producers, etc. was gathered.

Structure of assemblages

The material collected was rinsed with tap water and filtered using a 1-mm diameter metallic mesh to separate insects from debris. All specimens were assorted firstly according to supra-order taxonomic categories and preserved in 70% ethanol for further examination. Coleopteran species identifications were made at genus and/or species levels, whenever possible, by using taxonomic keys and diagnostic descriptions (Crowson 1981CROWSON RA. 1981. The biology of the Coleoptera. Academic Press. London, UK., Borror et al. 1989BORROR DJ, TRIPLEHORN CA & JOHNSON NF. 1989. An introduction to the study of insects. Sixth Edition. Saunders College Publishing, New York., Britton & Mackerras 1991BRITTON E & MACKERRAS I. 1991. The Insects of Australia: A Textbook for Students and Research Workers, Melbourne, Australia. Melbourne University Press 2: 543-638., Artigas 1994ARTIGAS JN. 1994. Entomología económica. Insectos de interés agrícola, forestal, médico y veterinario (nativos, introducidos y susceptibles de ser introducidos). Vol. I. Ediciones Universidad de Concepción, Concepción, Chile, 493 p., Lawrence & Britton 1994LAWRENCE JF & BRITTON EB. 1994. Australian Beetles. Melbourne University Press, Australia., White 1998WHITE R. 1998. A field guide to the beetles of North America. Houghton, Mifflin, Harcourt. Peterson field Guides. Boston, Massachusetts., Arnett & Thomas 2001ARNETT JR RH & THOMAS MC 2001. American beetles. Vol. 1: Archostemata, Myxophaga, Adephaga, Polyphaga: Staphyliniformia. CRC Press, Boca Raton, 443 p., Arnett et al. 2002ARNETT JR RH, THOMAS MC, SKELLEY PE & FRANK JH. 2002. American beetles. Vol. 2: Polyphaga: Scarabaeoidea through Curculionoidea. CRC Press, Boca Raton, 861 p.), and compared with reference specimens deposited at División Entomología, Museo de La Plata. Consultations were also made to: CARABIDAE: Sergio Roig-Juñent; and CURCULIONIDAE: Analía Lanteri and Guadalupe Del Río (Museo de La Plata, La Plata, Argentina). STAPHYLINIDAE were identified by Mariana Chani Posse. Insects were assigned to six different assemblages: four for lettuce crops (two types of plant protection management) × (two cropping seasons), and two for tomato crops (two types of plant protection management). To analyse spatial (crops, plant protection management) and temporal (cropping seasons) patterns of the six epigeic Coleopteran assemblages, relative abundance per species or morphospecies was calculated as the number of individuals per species/total number of individuals collected, and then each value plotted sequentially taking into account dominance categories, from lowest to greater abundances. The categories were: 1) dominant (≥ 5 %); 2) codominant (4.9 - 2 %), and rare (de 0 - 1.9%) (Pedraza et al. 2010PEDRAZA MC, MÁRQUEZ J & GÓMEZ-ANAYA JA. 2010. Estructura y composición de los ensamblajes estacionales de coleópteros (Insecta: Coleoptera) del bosque mesófilo de montaña en Tlanchinol, Hidalgo, México, recolectados con trampas de intercepción de vuelo. Rev Mex Biodiv 81: 437-456.).

Niche partitioning of species in the six assemblages was explored by adjusting data of their abundances to the Log-normal and Logarithmic series, which show non-interacting, randomly distributed individuals in a community. These models have been reported as common to a large number of different communities (Magurran 1988MAGURRAN AE. 1988. Ecological diversity and its measurement. Princeton University Press, New Jersey., Morin 1999MORIN PJ. 1999. Community ecology. Blackwell Science, J Wiley & Sons, Malden, Massachusetts., Magurran & Henderson 2011MAGURRAN AE & HENDERSON PA. 2011. Commonness and rarity. Biological diversity: frontiers in measurement and assessment, Magurran AE and McGill BJ (Eds), Oxford University Press, UK, p. 97-104.). Species-abundance curves fitting was made by means of PAST software, v. 2.16 (Hammer et al. 2001HAMMER O, HARPER D & RYAN P. 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. (http://palaeo-electronica.org).
http://palaeo-electronica.org...
), and significance of goodness of fitting was evaluated by chi-square tests (P > 0.05).

Finally, to compare the six assemblages with respect to their species overlap a multivariate analyses of hierarchy clustering was carried out (Gotelli 2004GOTELLI NJ. 2004. A taxonomic wish-list for community ecology. Philos T R Soc B 359: 585-597.). The variables considered were: crop (lettuce or tomato), cropping season for lettuce (fall-winter or spring-summer), and plant protection practices (conventional or organic farming). The method consisted in testing three different dissimilarity (1 – similarity) or distance coefficients: qualitative Jaccard and Sørensen, and quantitative Sørensen. Qualitative data were referred as the presence or absence of a given species, and quantitative also included abundance of each species (Gotelli 2004GOTELLI NJ. 2004. A taxonomic wish-list for community ecology. Philos T R Soc B 359: 585-597.). Clustering using the three coefficients was performed but the Sørensen quantitative coefficient was chosen since it described more realistically the structure of Coleopteran assemblages found. The matrix used had 70 species × 6 assemblages.

Sørensen similarity coefficient (CS ) (Magurran 1988MAGURRAN AE. 1988. Ecological diversity and its measurement. Princeton University Press, New Jersey.) between pairs of assemblages was calculated as:

C S = 2 p N / a N + b N

where:

aN = total number of individuals of all species in assemblage A.

bN = total number of individuals of all species in assemblage B.

pN = sum of the lowest abundance of each shared species in A and B.

Results were graphically expressed with a dendrogram plotted using Euclidean distances (Peña 2002PEÑA D. 2002. Análisis de datos multivariantes. S.A. Mc Graw-Hill e Interamericana de España.). Cluster analyses were performed using the Cluster procedure (SAS v. 9.1), and then, a dendrogram was plotted by means of Semi-Partial R Square (SPRQ) that measures the loss of homogeneity when two groups join a new one. A lower SPRQ value shows that two homogeneic groups join a new one meanwhile higher values suggest that two heterogeneous groups were joint.

RESULTS

Species inventory

During the study period, a total of 1,510 adult coleopterans of the main four families were captured. From those, 708 were found in lettuce crops and 802 in tomato crops. Twenty-five taxa (species/morphospecies) were identified as Curculionidae, belonging to five subfamilies. Over 60% of specimens were identified as Phyrdenus muriceus (Germar, 1824) (Table SI - Supplementary Material Table SI. Species of Curculionidae collected by pit-fall trapping in lettuce and tomato crops, conventionally (CM) or organically (OM) managed, in spring-summer (SS) or fall-winter (FW) cycles, in Northern Buenos Aires province. Years: 2010-2013. Table SII. Species of Carabidae collected by pit-fall trapping in lettuce and tomato crops, conventionally (CM) or organically (MO) managed, in spring-summer (SS) or fall-winter (FW) cycles, in Northern Buenos Aires province. Years: 2010-2013. Table SIII. Species of Staphylinidae collected by pit-fall trapping in lettuce and tomato crops, conventionally (MC) or organically (MO) managed, in spring-summer (SS) or fall-winter (FW) cycles, in Northern Buenos Aires province. Years: 2010-2013. ).

Regarding the Carabidae, 17 taxa from three subfamilies and seven tribes were registered. More than a half of individuals belonged to Pachymorphus striatulus (Fabricius, 1792). A new species, Rhytidognathus platensisRoig-Juñent & Rouaux 2012ROIG-JUÑENT S & ROUAUX J. 2012. A new species of Rhytidognathus (Carabidae, Migadopini) from Argentina. ZooKeys 247: 45-60., was described (Roig-Juñent & Rouaux 2012ROIG-JUÑENT S & ROUAUX J. 2012. A new species of Rhytidognathus (Carabidae, Migadopini) from Argentina. ZooKeys 247: 45-60.) (Table SII Table SI. Species of Curculionidae collected by pit-fall trapping in lettuce and tomato crops, conventionally (CM) or organically (OM) managed, in spring-summer (SS) or fall-winter (FW) cycles, in Northern Buenos Aires province. Years: 2010-2013. Table SII. Species of Carabidae collected by pit-fall trapping in lettuce and tomato crops, conventionally (CM) or organically (MO) managed, in spring-summer (SS) or fall-winter (FW) cycles, in Northern Buenos Aires province. Years: 2010-2013. Table SIII. Species of Staphylinidae collected by pit-fall trapping in lettuce and tomato crops, conventionally (MC) or organically (MO) managed, in spring-summer (SS) or fall-winter (FW) cycles, in Northern Buenos Aires province. Years: 2010-2013. )

A total of 27 taxa were identified as Staphylinidae, representing five subfamilies and eight tribes (Table SIII Table SI. Species of Curculionidae collected by pit-fall trapping in lettuce and tomato crops, conventionally (CM) or organically (OM) managed, in spring-summer (SS) or fall-winter (FW) cycles, in Northern Buenos Aires province. Years: 2010-2013. Table SII. Species of Carabidae collected by pit-fall trapping in lettuce and tomato crops, conventionally (CM) or organically (MO) managed, in spring-summer (SS) or fall-winter (FW) cycles, in Northern Buenos Aires province. Years: 2010-2013. Table SIII. Species of Staphylinidae collected by pit-fall trapping in lettuce and tomato crops, conventionally (MC) or organically (MO) managed, in spring-summer (SS) or fall-winter (FW) cycles, in Northern Buenos Aires province. Years: 2010-2013. ). Apocellus obscurus Bernhauer, 1908 (32%), Aleochara sp2 (19%) and Aleochara sp7 (10%) were the most abundant species.

The family Coccinellidae was represented by only one species, Eriopis connexa Germar 1924 which reached 17% of the total of individuals trapped.

Structure of assemblages

For the four epigean Coleoptera assemblages in lettuce crops, five to eight species were dominant, four to eight co-dominant, and a variable number of species were rare (Fig. 1a, b, c and d). The species P. striatulus, P. cordicollis and E. connexa were found in general as dominant or co-dominant species, although the latter was not registered in late crops sprayed with insecticides. Scarites anthracinus Dejean and P. muriceus were dominant in early crops, independently whether they were managed conventionally or organically. Besides, some species, as P. cordicollis, were dominant in warmer months (spring-summer). Interestingly, rare species in organic sites doubled those found in conventionally managed farms.

Figure 1
Relative abundance and dominance structure of Curculionidae, Carabidae, Staphylinidae and Coccinellidae species, collected in conventionally (CM) and organic (OM) managed lettuce crops, during different cropping seasons: (a) Fall-winter, CM; (b) Fall-winter, OM; (c) Spring-summer, CM, and (d) Spring-summer, OM. Dominance categories (from Pedraza et al. 2010PEDRAZA MC, MÁRQUEZ J & GÓMEZ-ANAYA JA. 2010. Estructura y composición de los ensamblajes estacionales de coleópteros (Insecta: Coleoptera) del bosque mesófilo de montaña en Tlanchinol, Hidalgo, México, recolectados con trampas de intercepción de vuelo. Rev Mex Biodiv 81: 437-456.): highly dominant: > 5%, co-dominant: 4.9 - 2%, and rare: 0 - 1.9%.

In tomato crops, six species were found dominant, meanwhile other three species were co-dominant in organic farms and seven in conventionally managed crops (Fig. 2a, b). Dominant species were P. muriceus, Baridinae sp6, E. connexa, A. obscurus, Aleochara sp7 and S. anthracinus. As in lettuce crops, a greater number of rare species were found in organic sites.

Figure 2
Relative abundance and dominance structure of Curculionidae, Carabidae, Staphylinidae and Coccinellidae species, collected in conventionally (CM), and organic (OM) managed tomato crops, during different cropping seasons: (a) Fall-winter, CM; (b) Fall-winter, OM; (c) Spring-summer, CM, and (d) Spring-summer, OM. Dominance categories (from Pedraza et al. 2010PEDRAZA MC, MÁRQUEZ J & GÓMEZ-ANAYA JA. 2010. Estructura y composición de los ensamblajes estacionales de coleópteros (Insecta: Coleoptera) del bosque mesófilo de montaña en Tlanchinol, Hidalgo, México, recolectados con trampas de intercepción de vuelo. Rev Mex Biodiv 81: 437-456.): highly dominant: > 5%, co-dominant: 4.9 - 2%, and rare: 0 - 1.9%.

Relative abundances of the 70 species of epigeic Coleoptera conforming the six assemblages fit to logarithmic (fall-winter CM lettuce crop) and log-normal (two OM lettuce crops and two tomato crops, CM and OM) distributions, with the exception of the spring-summer CM lettuce crop that fitted to both distributions (Table IV and Fig. 3a, b, c, c`, d, e, f).

Table IV
Values of probability and goodness of fit tests to distribution models of abundance logarithmic and log-normal for the species of Curculionidae, Carabidae, Staphylinidae and Coccinellidae conforming epigeic coleopteran assemblages in lettuce and tomato crops, in Northern Buenos Aires province, Argentina. Years: 2010-2013.
Figure 3
Rank-abundance curves plotted for logarithmic and log-normal series: (a) Lettuce, fall-winter, conventional management (CM); (b) Lettuce, fall-winter, organic management (OM); (c and c’) Lettuce, spring-summer, conventional management (CM); (d) Lettuce, spring-summer, organic management (OM); (e) Tomato, conventional management (CM), and (f) Tomato, organic management (OM).

Similarity analysis showed that lettuce crops resembled more in composition and abundance of epigeic Curculionidae, Carabidae, Staphylinidae and Coccinellidae than in tomato crops (Table V).

Table V
Similarity Sørensen quantitative indexes, calculated using specific composition and abundance of epigeic coleopteran species belonging to Carabidae, Curculionidae, Staphylinidae and Coccinellidae families (see also Fig. 4). Years: 2010-2013. LT: lettuce; TOM: tomato; FW: fall-winter; SS: spring-summer; CM: conventional use of pesticides; OM: organic farming.

Furthermore, coleopteran assemblages slightly showed greater distance between lettuce and tomato crops. Species in lettuce crops were split based in the cropping season (lowest SPRQ values for late crops, both plant protection management practices), being early crops segregated in a second group. Crop management in lettuce had less impact on epigeic coleopteran structure than seasonality (Fig. 4).

Figure 4
Cluster analysis for epigeic coleopteran assemblages conformed by the species of the dominant families Curculionidae, Carabidae Staphylinidae and Coccinellidae, inhabiting lettuce and tomato crops under different pest protection management (conventional use of insecticides –CM- and organic –OM- practices) in Northern Buenos Aires province, Argentina. Cropping seasons for lettuce: fall-winter and spring-summer. Years 2010-2013. Similarity index: Sørensen quantitative (CS) (Magurran 1988MAGURRAN AE. 1988. Ecological diversity and its measurement. Princeton University Press, New Jersey.).

DISCUSSION

We report novel information on the coleopteran assemblages that inhabit soils of L. sativa and S. lycopersicon crops in northern Buenos Aires province, Argentina. They were composed of 70 species or morphospecies of Curculionidae (26), Carabidae (16), Staphylinidae (27) and Coccinellidae (1). The curculionids Ceutorhynchini sp. and P. muriceus, the carabid S. anthracinus, the coccinelid E. connexa and the staphylinids Aleochara sp. 2, and A. obscurus were the most common species recorded in lettuce and tomato crops in the region studied. Besides, a great number of new Coleopteran species are expected to be described, as it was the case of the carabid weevil R. platensis (Roig-Juñent & Rouaux 2012ROIG-JUÑENT S & ROUAUX J. 2012. A new species of Rhytidognathus (Carabidae, Migadopini) from Argentina. ZooKeys 247: 45-60.). Changes in assemblage structure in relation to the crop species, cultural practices and seasonality were observed. In general, organic crops showed greater species richness of epigeic coleopterans, with few dominant and co-dominant species and plenty of rare species. The cropping season affected the presence and abundance of coleopterans, probably because of their life histories and life cycles, being aestival species predominant. Overall, the four families have members that belong to different functional groups (phytophages, predators, parasitoids and saprophages), i.e., exploiting diverse vegetation conditions (monoculture or diversified orchards) and cultural practices (fertilizing, pest control).

The family Curculionidae - with ≈ 964 species described for Argentina (Morrone & Posadas 1998MORRONE JJ & POSADAS PE. 1998 Curculionoidea. Biodiversidad de Artrópodos Argentinos. Una perspectiva biotaxonómica, Morrone JJ and Coscarón S (Eds), Ediciones Sur. La Plata, Argentina, 258-278.) - was well represented in both crops, although it was more abundant in tomato. They are all polyphagous phytophagous species that feed upon almost all plant tissues and organs. Phyrdenus muriceus was a dominant species in OM and co-dominant in CM tomato crops, respectively, and interestingly it was also found as dominant and codominant in soils of lettuce crops year-round. This weevil is considered of economic importance as a pest of tomato and eggplant, affecting the seedlings, roots, leaves and flowers (Cordo et al. 2004CORDO HA, LOGARZO G, BRAUN K & DI IORIO O (Eds). 2004. Catálogo de insectos fitófagos de la Argentina y sus plantas asociadas. Sociedad Entomológica Argentina Ediciones, Buenos Aires, Argentina, 734 p.), and can cause up to 80% of crop losses few days after transplanting (Novo et al. 2002NOVO RJ, VIGLIANCO A & VAUDAGNA E. 2002. Efectos de insecticidas sobre el gorgojo de la papa, Phyrdenus muriceus (Germ.) (Coleoptera: Curculionidae). Agriscientia 19: 3-10.). It probably uses crops and non-cultivated solanaceous plants as shelter or for living, and switches to tomato crops from there (Artigas 1994ARTIGAS JN. 1994. Entomología económica. Insectos de interés agrícola, forestal, médico y veterinario (nativos, introducidos y susceptibles de ser introducidos). Vol. I. Ediciones Universidad de Concepción, Concepción, Chile, 493 p., Lanteri et al. 2002LANTERI AA, MARVALDI AE & SUÁREZ SM. 2002. Gorgojos de la Argentina y sus plantas huéspedes. Publicación especial de la Sociedad Entomológica Argentina N° 1. San Miguel de Tucumán, Argentina., Novo et al. 2002NOVO RJ, VIGLIANCO A & VAUDAGNA E. 2002. Efectos de insecticidas sobre el gorgojo de la papa, Phyrdenus muriceus (Germ.) (Coleoptera: Curculionidae). Agriscientia 19: 3-10.). Curculionids are in general active in warmer months -when open-field tomato cropping is typical in the region- and populations peak at the end of crop´s cycle, making their control difficult (Lanteri 1994LANTERI AA. 1994. Bases para el control integrado de los gorgojos de la alfalfa. De la Campana Ediciones, Buenos Aires, Argentina.). Regarding the diverse family of Carabidae, with ≈ 679 species reported for Argentina (Roig-Juñent 1998ROIG-JUÑENT S. 1998. Carabidae. Biodiversidad de artrópodos argentinos. Una perspectiva biotaxonómica, Morrone JJ and Coscarón S (Eds), Ediciones Sur. La Plata, Argentina, p. 194-208.), most of the species found in this study were predators, a common feeding habit of this group. However, few herbivorous were detected. The dominant carnivorous P. striatulus, P. cordicollis, P. bonariensis and S. anthracinus ground beetles have been reported as abundant in other agroecosystems in Argentina (Marasas 2002MARASAS M. 2002. Efecto de los sistemas de labranza sobre la abundancia y diversidad de la coleopterofauna edáfica, con especial referencia a las especies de Carabidae, en un cultivo de trigo y los ambientes naturales circundantes. Ph.D. thesis dissertation. Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Argentina., Paleologos 2012PALEOLOGOS MF. 2012. Los carábidos como componentes clave de la agrobiodiversidad. Su rol en la sustentabilidad de los agroecosistemas de vid de la zona de Berisso, Provincia de Buenos Aires. Ph.D. thesis dissertation, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Argentina.). Vegetation structure is a main factor affecting the distribution of Carabidae (Andow 1991ANDOW D. 1991. Vegetational diversity and arthropod population response. Ann Rev Entomol 36: 561-586., Carmona & Landis 1999CARMONA D & LANDIS D. 1999. Influence of refuge habitats and cover crops on seasonal activity-density of ground beetles (Coleoptera: Carabidae) in field crops. Environ Entomol 28: 1145-1153.) since it modifies microhabitats and alters insect displacement and prey searching. Thus, in L. sativa crops, where soils are bare of non-crop vegetation, cursorial forms were dominant, as P. striatulus and P. cordicollis. In general, carabids are active species during spring-summer months, and reduce their activity or enter in diapause in winter as larvae or pupae (Cepeda-Pizarro 1989CEPEDA-PIZARRO J. 1989. Actividad temporal de tenebriónidos epígeos (Coleoptera) y su relación con la vegetación arbustiva en un ecosistema árido de Chile. Rev Chi Hist Nat 62: 115-125., Grez et al. 2003GREZ AA, MORENO P & ELGUETA M. 2003. Coleópteros (Insecta, Coleóptera) epigeos asociados al bosque maulino y plantaciones de pino aledañas. Rev Chil Entomol 29: 9-18.). Exceptions in this study were the presence of the species P. cordicollis and L. simplex, both abundant and active in fall-winter lettuce assemblages during colder months (June - July). Similar findings were reported by Cicchino et al. (2005)CICCHINO AC, MARASAS ME & PALEOLOGOS MF. 2005. Fenología y densidad-actividad de cinco especies de Carabidae (Coleoptera) edáficas en un cultivo experimental de trigo y su entorno en el Partido de La Plata, Provincia de Buenos Aires. Actas de la V Reunión Científico Técnica de Biología del Suelo y V Encuentro sobre Fijación Biológica de Nitrógeno, Área Temática I, Comunidades Terrestres I: 1-14. and Castro et al. (2012CASTRO A, PORRINI DP & CICCHINO AC. 2017. Diversidad de Carabidae (Insecta: Coleoptera) en distintos ambientes de un agroecosistema del sudeste bonaerense, Argentina. Ecol Aust 27: 252-265., 2017CASTRO AV, PORRINI DP & CICCHINO AC. 2012. Ensamble peridomiciliario de carábidos (Coleoptera: Carabidae) en un talar del sudeste bonaerense, Argentina. Rev Soc Entomol Arg 71: 231-247.) in other agroecosystems. The fossorial species S. anthracinus was dominant in tomato crops, majorly active from August to May. The Staphylinidae is a highly diverse family, with more than 1,017 species reported from Argentina (Chani Posse & Thayer 2008CHANI POSSE M & THAYER MK. 2008. Staphylinidae. Biodiversidad de Artrópodos Argentinos, Debandi GO, Claps LE and Roig-Juñent SA (Eds), Mendoza, Argentina. Ediciones SEA 2: 471-494.). They show varied feeding habits, such as predators, parasitoids, saprophagous, etc. In this study, parasitoids belonging to Aleocharinae (for example Aleochara spp.) and saprophagous to Oxytelinae (A. obscurus and A. opacus) were dominant. Species of Aleochara are known as parasites of dipteran eggs and larvae (Chani Posse 2002CHANI POSSE M. 2002. Contribución al estudio de los Staphylinidae asociados a la bosta vacuna potenciales predadores de Haematobia irritans irritans (L). (Insecta: Diptera). Tesis Doctoral, Universidad Nacional de Tucumán, Facultad de Ciencias Naturales e Instituto Miguel Lillo, Argentina.), which probably develop in manure-fertilized soils, a common and cheap organic amendment used by farmers in the region studied. Adults prey upon eggs, larvae and pupae of Diptera (Cyclorrapha). Species can be either quite polyphagous or strict specialists. In North America, Aleochara bilineata Gyllenhal has been employed to control the cabbage root fly Delia radicum L. and the onion maggot D. antiqua Meigen (Diptera: Anthomyiidae) (Maus 1998MAUS C. 1998. Taxonomical contributions to the subgenus Coprochara Mulsant & Rey, 1874 of the genus Aleochara Gravenhorst, 1802 (Coleoptera: Staphylinidae). Koleopterol Rund 68: 81-100., Chani Posse & Thayer 2008CHANI POSSE M & THAYER MK. 2008. Staphylinidae. Biodiversidad de Artrópodos Argentinos, Debandi GO, Claps LE and Roig-Juñent SA (Eds), Mendoza, Argentina. Ediciones SEA 2: 471-494., Van Driesche et al. 2008VAN DRIESCHE RG, HODDLE MS & CENTER TD. 2008. Control de plagas e malezas por enemigos naturales. Forest Health Technology Enterprise Team, USDA (http://www.fs.fed.us/foresthealth/technology).
http://www.fs.fed.us/foresthealth/techno...
). Generalist predators among paederines and staphylinines (for example: Pinophilus sp. and Philonthus longicornis) prey upon a variety of edaphic arthropods (acari, collembolan, larvae of dipterans, coleopterans and lepidopterans), and other invertebrates (oligochaete and nematode worms) (Marchiori & Linhares 1999MARCHIORI CH & LINHARES AX. 1999. Constância, dominância e freqüência mensal de dípteros muscóides e seus parasitóides (Hymenoptera e Coleoptera), associados a fezes frescas de bovinos, em Uberlândia, MG. Anais Soc Entomol Bras 28: 375-387., Monzó et al. 2005MONZÓ C, VANACLOCHA P, OUTERELO R, RUIZ-TAPIADOR I, TORTOSA D, PINA T, CASTAÑERA P & URBANEJA A. 2005. Catalogación de especies de las familias Carabidae, Cicindelidae y Staphylinidae en el suelo de los cítricos de la provincia de Valencia, España. Bol San Veg Plagas 31: 483-492.). They were codominant or rare species, presumably due to competitive interactions with Carabidae (Hole et al. 2005HOLE DG, PERKINS AJ, WILSON JD, ALEXANDER IH, GRICE PV & EVANS AD. 2005. Does organic farming benefit biodiversity? Biol Conserv 122: 113-130.). The family Coccinelidae is represented by ca. 150 species in Argentina (González 2014GONZÁLEZ G. 2014. Coccinellidae. Biodiversidad de Artrópodos Argentinos. Roig-Juñent S, Claps LE and Morrone JJ (Eds), San Miguel de Tucumán, Argentina. Editorial INSUE-UNT 3: 509-530.). In this study only E. connexa was caught in soils of lettuce and tomato crops and it behaved as a dominant species in five out of six assemblages. This is a common ladybird in many other horticultural crops in the region (Fogel et al. 2016FOGEL MN, SCHNEIDER MI, RIMOLDI F, LADUX LS, DESNEUX N & RONCO AE. 2016. Toxicity assessment of four insecticides with different modes of action on pupae and adults of Eriopis connexa (Coleoptera: Coccinellidae), a relevant predator of the Neotropical Region. Environ Sci Pollut R 23: 14918-14926.). Its abundance is associated to aphids -its main prey- but also to sheltering and alternative food offered by other resources, such as non-crop plants (Bentancourt & Scatoni 2001BENTANCOURT CM & SCATONI IB. 2001. Enemigos naturales. Manual ilustrado para la agricultura y la forestación. Ed. Agropecuaria Hemisferio Sur, Facultad de Agronomía, Montevideo, Uruguay., Dode & Romero Sueldo 2013DODE M & ROMERO SUELDO M. 2013. Coccinélidos (Coleoptera: Coccinellidae) asociados a Brassica rapa (Brassicaceae), en invierno y primavera en Tucumán, Argentina. Acta Zool Lil 57: 217-220.). Eriopis connexa was collected year-round, with the exception of fall-winter lettuce crops, a result that could be explained by the characteristic overwintering aggregation habits of coccinelids (Koch 2003KOCH RL. 2003. The multicolored Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non-target impacts. J Ins Sci 3: 16., Saini 2004SAINI ED. 2004. Insectos y ácaros perjudiciales al cultivo del girasol y sus enemigos naturales. Publicación del Instituto de Microbiología y Zoología Agrícola Nº 8. INTA. Buenos Aires, Argentina.). Among preys reported, Aphis gossypii, Hyperomyzus lactucae, Macrosiphum euphorbiae and Myzus persicae are common pests of horticultural crops (Molinari 2005MOLINARI A. 2005 Control Biológico. Especies entomófagas en cultivos agrícolas. INTA Ediciones, Buenos Aires, Argentina., Fogel et al. 2016FOGEL MN, SCHNEIDER MI, RIMOLDI F, LADUX LS, DESNEUX N & RONCO AE. 2016. Toxicity assessment of four insecticides with different modes of action on pupae and adults of Eriopis connexa (Coleoptera: Coccinellidae), a relevant predator of the Neotropical Region. Environ Sci Pollut R 23: 14918-14926.).

The Coleopteran assemblages displayed a lognormal distribution (Morin 1999MORIN PJ. 1999. Community ecology. Blackwell Science, J Wiley & Sons, Malden, Massachusetts.) in conventional and organic tomato, and mostly in organic lettuce and conventional spring-summer lettuce crops, commonly found in rich communities (23 to 44 species). These communities are typically influenced by independent environmental factors, such as spatial and temporal patterns of plant and insect species, as in horticultural crops (Magurran 1988MAGURRAN AE. 1988. Ecological diversity and its measurement. Princeton University Press, New Jersey.). Assemblages found in conventional lettuce crops adjusted to a log-series distribution. They were composed by 10 to 23 species, with common species having intermediate values of abundances. This species distribution model is common for small, stressed or pioneer communities (Morin 1999MORIN PJ. 1999. Community ecology. Blackwell Science, J Wiley & Sons, Malden, Massachusetts., Magurran 1988MAGURRAN AE. 1988. Ecological diversity and its measurement. Princeton University Press, New Jersey.). The lettuce is cultivated throughout the year in the region. It has a productive cycle of approximately four months, after which it is removed, and the soil is carved again to start a new sowing period. This tillage activity certainly affects the edaphic fauna, promoting constant processes of colonization and replacement of species. In relation to similarity analyses, this study evidenced that epigeic coleopteran assemblages associated to L. sativa were clustered and differed from those registered in S. lycopersicon. Organic tomato crops were by far more diverse. In lettuce crops, species were markedly grouped according to cropping seasons (fall-winter and spring-summer), and cultural practices had less influence on the community structure. This result is coincident with Pedraza et al. (2010)PEDRAZA MC, MÁRQUEZ J & GÓMEZ-ANAYA JA. 2010. Estructura y composición de los ensamblajes estacionales de coleópteros (Insecta: Coleoptera) del bosque mesófilo de montaña en Tlanchinol, Hidalgo, México, recolectados con trampas de intercepción de vuelo. Rev Mex Biodiv 81: 437-456., who pointed out that seasonal patterns in life cycles can help reducing competence for food resources. In warmer months, assemblages were in general richer (37 vs. 23 species, Tables S1 to S3). Carabids were less abundant meanwhile curculionids were common in spring-summer months. Notably, E. conexa, which is dominant in most of assemblages, was absent in fall-winter conventional lettuce crops. This coccinelid can show resistance to widely used insecticides (Ferreira et al. 2013FERREIRA ES, RODRIGUES ARS, SILVA-TORRES CSA & TORRES JB. 2013. Life-history costs associated with resistance to lambda-cyhalothrin in the predatory ladybird beetle Eriopis connexa. Agric Forest Entomol 15: 168-177., Fogel et al. 2016FOGEL MN, SCHNEIDER MI, RIMOLDI F, LADUX LS, DESNEUX N & RONCO AE. 2016. Toxicity assessment of four insecticides with different modes of action on pupae and adults of Eriopis connexa (Coleoptera: Coccinellidae), a relevant predator of the Neotropical Region. Environ Sci Pollut R 23: 14918-14926., Santos et al. 2016SANTOS DS, RODRIGUES RS, TORRES JB & LIRA R. 2016. Performance of Eriopis connexa (Coleoptera: Coccinellidae) resistant to lambda-cyhalothrin after extended recovery from knockdown. Neotrop Entomol 45: 718-724., Spíndola et al. 2013SPÍNDOLA AF, SILVA-TORRES CSA, RODRIGUES ARS & TORRES JB. 2013. Survival and behavioural responses of the predatory ladybird beetle, Eriopis connexa, populations susceptible and resistant to a pyrethroid insecticide. Bull Entomol Res 103: 485-494.). However, even when it has a polyphagous feeding habit, a decline in food availability in colder months can lead to overwintering behavior.

Generalist predators were dominant in all assemblages studied, and they may be playing an important role in reducing pest populations (Ghoneim 2014GHONEIM K. 2014. Predatory insects and arachnids as potential biological control agents against the invasive tomato leafminer, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), in perspective and prospective. J Entomol Zool Studies 2: 52-57.). Conservation and augmentative biological control programs based on the use of E. connexa are currently under study (Rocca et al. 2017ROCCA M, RIZZO E, GRECO N & SÁNCHEZ N. 2017. Intra- and interspecific interactions between aphidophagous ladybirds: the role of prey in predator coexistence. Entomol Exp Appl 162: 284-292., Silva et al. 2013SILVA RB, CRUZ I, ZANUNCIO JC, FIGUEIREDO MLC, CANEVARI GC, PEREIRA AG & SERRÃO JE. 2013. Biological aspects of Eriopis connexa (Germar) (Coleoptera: Coccinellidae) fed on different insect pests of maize (Zea mays L.) and sorghum [Sorghum bicolor L. (Moench.)]. Braz J Biol 73: 419-424.). The Carabidae P. striatulus, S. anthracinus, P. cordicollis, and P. bonariensis, that preferably prey on lepidopteran and curculionid larvae (Bentancourt & Scatoni 2001BENTANCOURT CM & SCATONI IB. 2001. Enemigos naturales. Manual ilustrado para la agricultura y la forestación. Ed. Agropecuaria Hemisferio Sur, Facultad de Agronomía, Montevideo, Uruguay., Cicchino & Farina 2007CICCHINO AC & FARINA JL. 2007. Riqueza, dominancia y fenologia primaveral, estival y otonal de los carabidos edaficos (Insecta, Coleoptera) de los currales serranos y periserranos de las Sierras de Mar del Plata, provincia de Buenos Aires, Argentina. Proceedings of the VI REBIOS, Rio Cuarto, p. 1-14., Paleologos 2012PALEOLOGOS MF. 2012. Los carábidos como componentes clave de la agrobiodiversidad. Su rol en la sustentabilidad de los agroecosistemas de vid de la zona de Berisso, Provincia de Buenos Aires. Ph.D. thesis dissertation, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Argentina.) could also have potential as biocontrol agents. Several carabid species are commercially used, such as Calosoma sycophanta (L.) in North America to control the gypsy moth Lymantria dispar (L.). In Argentina, Tulli et al. (2009)TULLI M, CARMONA DM, LÓPEZ AL, MANETTI PL, VINCINI AM & CENDOYA G. 2009. Predation on the slug Deroceras reticulatum (Pulmonata: Stylommatophora) by Scarites anthracinus (Coleoptera: Carabidae). Ecol Aust 19: 55-61. found that S. anthracinus is a potential natural enemy against the gray field slug Deroceras reticulatum, a pest of lettuce crops, preying on eggs and juveniles. Selenophorus sp. is reported as a predator of Tuta absoluta (Meyrick) larvae, a key pest of tomato crops worldwide (Desneux et al. 2011DESNEUX N, LUNA MG, GUILLEMAUD T & URBANEJA A. 2011. The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84: 403-408., Ghoneim 2014GHONEIM K. 2014. Predatory insects and arachnids as potential biological control agents against the invasive tomato leafminer, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), in perspective and prospective. J Entomol Zool Studies 2: 52-57.).

General knowledge of soil fauna inhabiting horticultural crops, such as the coleopteran assemblages described in this paper, can help understanding the complex interactions they share, the processes in which they are involved, and ultimately be useful to design pest management strategies. Many of the epigeic coleopteran species are able to move vertically, connecting soil and canopy arthropod trophic webs. The potential of cultural practices that conserve soil generalist and oligophagous carabids, staphylinids and coccinelids has yet to be fully explored for pest control in these crops.

ACKNOWLEGMENTS

We thank producers Susana Parrillo, Franco and Francisco Petix, Norma Olivera, Raúl López, Marcelo Maita and the association ´Colectivo Orgánico´ for kindly allowing us to conduct this research at their farms. Sergio Roig-Juñent (Laboratorio de Entomología, IADIZA, CRICYT, Mendoza, Argentina), Analía Lanteri and Guadalupe del Río (Museo de La Plata, FCNyM, UNLP, Argentina) helped with species identification. This study was part of the Ph.D. thesis work done by JR (Facultad de Ciencias Naturales y Museo, UNLP, Argentina). Funding was provided by PI UNLP N660 (2013-2016) and PIP 0112 CONICET (2011-2016).

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Publication Dates

  • Publication in this collection
    03 July 2020
  • Date of issue
    2020

History

  • Received
    8 Jan 2019
  • Accepted
    2 Apr 2019
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