Soil insects associated with lucumo ( Pouteria lucuma L . ) trees in La Molina

This study aimed to determine the composition and relative abundance of soil insects associated with lucumo ( Pouteria lucuma L.) trees growing in the agricultural fields of the Universidad Nacional Agraria La Molina in Lima, Peru. In total, 12 pitfall traps were installed in a 5-ha lucumo field and samples were collected on a weekly basis for approximately 4 months (March–June). Insects in each sample were separated into morphotypes, and the number of individuals in each morphotype and date of collection were recorded. The collected insects were then identified at the Entomology Museum laboratory in Lima through comparison with museum samples and with the help of identification keys. Individuals in the orders Orthoptera (families Acrididae and Gryllidae), Dermaptera (Anisolabididae), Coleoptera (Carabidae, Staphylinidae, Tenebrionidae, Scarabaeidae and Elateridae), Blattodea (Blatellidae) and Hymenoptera (Formicidae) were identified. Among the Coleoptera, Tetracha chilensis (Laporte, 1834) (Carabidae) was the most abundant species; furthermore, Staphylinidae of the subfamily Oxytelinae and the families Elateridae ( Conoderus spp.), Tenebrionidae ( Epitragopsis sp.) and Scarabaeidae ( Ataenius sp.) were identified. Additional taxa identified were as follow: Gryllus assimilis (Fabricius, 1775) (Gryllidae) in Orthoptera, Euborellia annulipes (Lucas, 1847) (Anisolabididae) in Dermaptera and Linepithema spp. in Hymenoptera.


Introduction
Various perennial crops, primarily fruit trees, are grown in Peru, particularly along the coast.One such tree is the lucumo (Pouteria lucuma L.), which is very important in this region, although it is not sown at a large scale on the coast.Peru is considered to be the primary producer of lucuma in the international market, with Lima, Piura, Cajamarca, La Libertad, Ica and Ayacucho being the regions with the highest production (Lavado, Yenque, & Robles, 2012).Of these, the valleys of Cañete, Huaral and Huacho of the Lima Region and the Chincha valley of the Ica Region produce higher quality fruits for export purposes (SIICEX 2015).
Studies have been conducted on insects that affect this crop; these insects are mostly found in the canopy of trees.These studies have enabled the determination of many pests that are known today.On the contrary, limited information is available regarding the insects that inhabit the soils in which this crop is grown; Among these, potential pests, or beneficial insects can be found to the crop.
Five orders of insects are believed to use soils as their main habitat: Blattodea, Dermaptera, Orthoptera, Coleoptera and Hymenoptera.
Within the order Blattodea, the families Blattidae, Blatellidae and Blaberidae are found most frequently in soil.
In Dermaptera, members of the families Anisolabididae and Labiduridae inhabit soil.Among these, the species Euborellia annulipes (Lucas, 1847) (Anisolabididae) is considered as a predator species, particularly of eggs and larval stages of some insects.However, Rondón (1999) analysed the stomach content of the aforementioned species and determined that these may primarily be phytophagous species and may secondarily feed on some soil arthropods; these findings suggest that E. annulipes is not a predator species.
Most soil-dwelling Orthoptera belong to the family Acrididae, with approximately 84 species recorded in Peru (Lieberman, 1963, as cited by Beingolea, 1990).However, Gryllidae have been recorded in soil, including Gryllus assimilis (Fabricius, 1775), which is considered to be a potential pest of several crops (Sánchez & Vergara, 2014).
The order Coleoptera includes the family Scarabaeidae, including some species of economic importance because they can cause considerable damage by defoliation as adults or feeding on the roots as larvae (Arnett & Thomas, 2002).Within this family, Anomala testaceipennis (Blanchard, 1850) and Paranomala undulata (Melsheimer, 1845) are particularly important pests of various crops, such as potato, strawberry, cotton, sugar cane, beans, lima beans, asparagus and corn (Alata, 1973, as cited by Gonzales-Bustamente, 1994;Vergara & Amaya de Guerra, 1978;Raven, 1988).Some species in the family Elateridae are pests of crops, with adults feeding on nectar, pollen, floral parts, fungi and extrafloral nectaries, with most insects being diurnal and some, particularly in the neotropics, being crepuscular or nocturnal (Johnson & Quartone, 2004, as cited by Aguirre-Tapiero, 2009).In contrast, members of the family Tenebrionidae are mainly scavengers (Van et al., 2000) that can additionally feed on wood, although they often emerge nocturnally to feed on lichens, fungi or some other plant material.
Finally, in the Hymenoptera, members of the family Formicidae mainly inhabit the soil.
Therefore, the objective of this research was to determine the composition and relative abundance of insects inhabiting the soils in which lucumo trees are grown in La Molina, Lima, Peru.

Materials and Methods
Weekly evaluations of the soil invertebrate fauna in a field of the Germplasm Bank of Lucumo of the Research Program in Fruit Trees at the Universidad Nacional Agraria La Molina in Lima, Peru, were conducted between 9th March and 8th June 2013 (n = 13 samples).Lucumo trees were planted over 5 ha in these fields, and soil insects were collected using pitfall traps.

Installation of pitfall traps
Quadrat sampling was used to distribute the pitfall traps as uniformly as possible across the lucumo field.The field was divided into three sectors, each of which had an irregular shape, rendering it impossible to determine the specific area.Therefore, the relative size of each sector was used to determine the distribution of pitfall traps, resulting in the installation of 3, 4 and 5 pitfall traps in the first, second and third sectors, respectively, with 12 traps installed in total.
The pitfall traps were poly-wrap polyethylene containers that were 15 cm in height and 10 cm in diameter.They were filled with 250 mL of a solution that was approximately 9 parts water to 1 part formaldehyde with 4-5 g of detergent.The formaldehyde was added to prevent the decomposition of the collected insects, whereas the detergent was used to break the surface tension of the solution.
To install the pitfall traps, a hole was dug in the ground using a small hoe such that the mouth of the container was flush with the surface of the soil, and the soil was then flattened to create a uniform surface.The pitfall traps were randomly distributed through the lucumo field to cover the largest possible area.Lucumo trees were planted at a spacing of 4 m × 4 m, and the pitfall traps were placed between the trees at a distance of 2 m from each tree and the edge of the irrigation channel.A brightly coloured stake was then placed alongside each trap to enable easy identification.No pitfall traps were installed within 10 m of the ends of the field to avoid any edge effects.

Sample collection
The pitfall traps were removed on a weekly basis and their contents were poured into hermetically sealed polyethylene cups, 7 cm in height and 5 cm in diameter, marked with the trap number and date of evaluation using indelible ink.The pitfall trap containers were washed, cleaned, refilled with 250 mL of solution (as mentioned above) and reinstalled.

Sample processing in the laboratory
The collected samples were transported to the Research Laboratory of the Entomology Museum of the Universidad Nacional Agraria La Molina for processing.
Each sample was sieved through an organza cloth strainer and rinsed with running water until it was clean and free from formalin odours.The sieved sample was then returned to the original polyethylene cup, which was washed and filled with clean water to facilitate the separation of the captured insects and prevent them from being damaged.
The samples were placed in Petri dishes and separated and grouped into morphotypes based on their morphological characteristics (Oliver & Beattie, 1993, 1996a, b) using knife and fine forceps.Further, the number of individuals in each morphotype was counted, and the invertebrates were placed in small 10-mL bottles containing 70% alcohol.These bottles were labelled with a code that consisted of the first letter of the crop, the first three letters of the order to which the invertebrates belonged and the morphotype number, for example, lucumo and order Hymenoptera samples were coded as 'LHYM1', 'LHYM2' and 'LHYM3'.
A sample of each species that was collected during the evaluation was mounted on entomological pins and/ or placed in alcohol, labelled and registered in the Entomology Museum of the Universidad Nacional Agraria La Molina.

Taxonomic identification
The collected individuals were identified by specialists in the laboratory of the Klaus Raven Büller Entomology Museum of the Universidad Nacional Agraria La Molina using identification keys and comparing them with samples in the museum collection.

Results
In total, 66,901 insects were collected during the study period, with 96.6% of these species developing in and mainly inhabiting the soil.These soil insects included members of the Orthoptera, Blattodea, Dermaptera, Coleoptera and Hymenoptera (Fig. 1).
On the first collection date (16 March 2013), 19,881 insects were captured, most of which belonged to the family Formicidae (Fig. 2).An overall decrease in the number of insects was observed until 13th April, when 719 individuals were captured, with a slight increase recorded on 6th April (2,573 individuals) because a large number of ants were captured in one of the traps.The second highest number of insects was captured on 20th April (18,649 individuals), with 3,000-9,000 individuals of the Formicidae family recorded in three pitfall traps.However, the number then decreased again from 27th April to 25th May, when the lowest number of insects was captured throughout the entire study period (486 individuals).A slight increase in the number was observed in the last two evaluations (1,315 individuals on 1st June and 1,567 individuals on 8th June).

Order Orthoptera
Members of the families Acrididae and Gryllidae were recorded in the samples.
A low abundance of Acrididae was observed among the samples, with only two individuals in the nymphal stage being identified as 'Gen sp1'.Generally, adults of this family are found to be feeding on the leaves of plants.However, most nymphs are found in the ground, which explains why only this stage was captured in the pitfall traps.The family Grylidae was represented by Gryllus assimilis (Fabricius, 1775), with 189 individuals captured in total.Particularly high numbers of this species were captured on 16th March (24 individuals), 6th April (25 individuals) and 18th May (19 individuals; Fig. 3).

Order Blattodea
Six individuals belonging to the family Blatellidae were collected; however, they could not be identified and were recorded as Gen sp1.

Order Coleoptera
Five families were recorded in the order Coleoptera: Carabidae, Staphylinidae, Scarabaeidae, Elateridae and Tenebrionidae.Among these, members of the family Carabidae were most abundant (76.6%, 966 individuals),    followed by Tenebrionidae (11.82%, 149 individuals), Elateridae (9.99%, 126 individuals), Staphylinidae (1.1%, 14 individuals) and Scarabaeidae (0.5%, 6 individuals; Fig. 5).Although insects belonging to other families were identified, these were not included in this study because they are not considered to be soil invertebrates.The two individuals of Gen sp. were captured on 20th April and 4th May, whereas Tetragonoderus sp. was only collected on 25th May.In contrast, N. peruviana was collected on 10 of the 13 collection dates, with a maximum of three individuals recorded in a collection.Similarly, B. peruvianus was captured throughout the study period, with a maximum of 80 individuals captured on 25th May and a minimum of 10 individuals captured on 24th April (Fig. 6).

Family Carabidae
Finally, a high number of Tetracha chilensis was captured on 16th March (295 individuals), 23th March (141 individuals) and 30th March (78 individuals).However, the population subsequently decreased, with no individuals captured on the last three collection dates (Fig. 6).

Family Staphylinidae
In the family Staphylinidae, two individuals of the species Platydracus notatus (Solsky, 1872)

Family Tenebrionidae
Four species of Tenebrionidae were recorded: Epitragopsis  The largest number of Epitragopsis sp. was recorded on the first collection date (16th March), with 16 individuals captured (Fig. 8).Subsequently, the population decreased, with no individuals recorded on two occasions.High numbers of Gondwanocrypticus sp. were recorded on the second collection date (8 individuals), following which few or no individuals were collected in the subsequent evaluations (Fig. 8).Blapstinus holosericius showed peaks on 20th April (8 individuals) and 27th April (7 individuals) and was not recorded on 16th March (Fig. 8).Finally, one individual of Hipalmus costatus was recorded on 20th April.

Order Hymenoptera
Several taxa in the family Formicidae were recorded during the study period, including Linepithema sp.Linepithema sp. was the most abundant taxon, with 19,130 individuals recorded on the first collection date, following which the population decreased remarkably (Fig. 9).Further, a second peak was recorded on 20th April (18,463 individuals), whereas the lowest collection was recorded on 25th May (384 individuals).
The highest number of Tetramorium sp. was obtained on the first collection date (173 individuals), following which the number of individuals gradually decreased, approaching the lowest record of only 2 individuals on 25th May (Fig. 10).In contrast, the highest number of Brachymyrmex sp. was collected on the last collection date (633 individuals), whereas only 6 individuals were collected on 25th May (Fig. 10).

Orthoptera
The number of G. assimilis captured generally increased on the dates when irrigation occurred (Fig. 3).The abundance of litter on the field beneath the lucumo trees provided a refuge for these insects, with individuals being captured in the pitfall traps while they were moving.Unlike Acrididae adults, Gryllidae adults are not very commonly found on trees, resulting in the traps collecting both first stage and adult individuals.This species is considered to be a potential pest of crops such as corn (Sánchez & Vergara, 2014).

Dermaptera
Low numbers of individuals were captured between the third and fifth collection dates and during the final collection.This may have occurred because of irrigation during the study period, which displaced individuals that were present in the irrigation furrows.On the dates with

Blattodea
Members of the order Blattodea are known to be omnivores; therefore, their presence may have been supported by the refuge areas and diverse food sources that were available.

Coleoptera
Among the members of the family Carabidae, Tetracha chilensis and Blennidus peruvianus were the most abundant.A high abundance of the former species can be explained by the large number of refuge areas that were observed in lucumo fields; as a result, a wide variety of arthropods were available in the soil as a food source for this species.B. peruvianus has been reported to be one of the most abundant soil predators in the fields of several crops such as sweet potato, asparagus, bean, potato and tomato (Vergara & Amaya de Guerra, 1978;Velapatiño, 1997;Schuller & Sánchez, 2003;Rondón & Vergara, 2004).Among the least abundant species, Notiobia peruviana is considered to be a highly polyphagous species; however, it appears to primarily feed on the seeds of various plants (Nisensohn, Faccini, Montero, & Lietti, 1999;Lietti, et al., 2000;Arndt & Kirmse, 2002, as cited by Yábar, Castro, Melo, & Gianoli, 2006).

Staphylinidae
Staphylinidae is the family that showed the highest diversity of species with regard to the others families.Most Staphylinidae are predators of insects and other invertebrates; however, some feed on fungi or decomposing organic matter and most live among the leaf litter of forests and mosses (Arnett & Thomas, 2001), which resembles the habitat observed in lucumo fields.

Scarabaidae
Members of this family are usually found in places with abundant decomposing organic matter.Consequently, fruit fields, particularly perennial crops, represent a favourable agro-ecosystem for these insects because of the large number of leaves and fruits that fall on the ground.

Elateridae
The decrease in the number of the members of this family during the last evaluations coincided with the end of the harvest period in the field.Probably, conditions in this period were not favorable these insects.Moreover, Rondón & Vergara (2004) identified Conoderus sp. in a sweet potato field in Cañete, Lima, supporting its presence in this region.

Tenebrionidae
No specific information could be obtained regarding the behaviours or characteristics of Gondwanocrypticus sp., B. holosericius and H. costatus.However, Epitragopsis olivaceus (Erichson, 1847) was previously recorded in a sweet potato field in Cañete (Rondón & Vergara, 2004), although this may have been a different species from that observed here.Tenebrionidae are known to be saprophagous and generally feed on a various decaying plants and fungi (Van et al., 2000).Therefore, these insects may have fallen into the traps while searching for shelter and/or food because these conditions are common in lucumo fields.

Hymenoptera
Formicidae are known to inhabit the soil and litter (Fernández, 2003), which commonly occurs in lucumo fields.Furthermore, the large distance between plants enabled these insects to establish their nests throughout the entire field.Several nests were located on the edges of the water channels and were disturbed by the irrigation, which may have displaced the ants and resulted in their capture.

Conclusions
Soil insects belonging to the orders Orthoptera, Dermaptera, Blattodea, Coleoptera and Hymenoptera were captured in pitfall traps installed in a lucumo field in Lima, Peru between March and June 2013.Members of the order Hymenoptera were most abundant, followed by Coleoptera, Orthoptera, Dermaptera and Blattodea.
In the order Orthoptera, members of the family Gryllidae were identified, with Gryllus assimilis (Fabricius, 1775) being the most abundant.In the order Dermaptera, Euborellia annulipes (Lucas, 1847) in the family Anisolabididae was recorded, whereas in the order Blattodea, members of the family Blatellidae were collected.Four families in the order Coleoptera were recorded, among which Carabidae was the most abundant, with Tetracha chilensis (Laporte, 1834) being predominant.In the family Staphylinidae, the subfamily Oxytelinae was the most abundant, whereas Ataenius sp.(Scarabaeidae), Conoderus sp.(Elateridae) and Epitragopsis sp.(Tenebrionidae) were additionally present.Finally, three species were identified in the order Hymenoptera, belonging to the family Formicidae: Linepithema sp., Tetramorium sp. and Brachymyrmex sp.; Linepithema sp. was found to be the most abundant.

Figure 1 .
Figure 1.Insects that were captured in pitfall traps installed in a field of lucumo (Pouteria lucuma L.) in La Molina, Lima, Peru between March and June 2013.

Figure 2 .
Figure 2. Changes in the number of soil insects captured in pitfall traps installed in a field of lucumo (Pouteria lucuma L.) in La Molina, Lima, Peru between March and June 2013.

Figure 5 .
Figure 5. Families of soil insects in the order Coleoptera that were captured in pitfall traps in a field of lucumo (Pouteria lucuma L.) in La Molina, Lima, Peru in March-June 2013.

Figure 9 .
Figure 9. Incidence of Linepithema sp. in pitfall traps installed in a field of lucumo (Pouteria lucuma L.) in La Molina, Lima, Peru in March-June 2013.