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Introduction
The Ichneumonidae superfamily is a megadiverse group of the Hymenoptera order, including two families, Ichneumonidae and Braconidae, which possess 24,281 and 19,434 worldwide described species, respectively (Yu et al., 2012). Most of the Ichneumonidae species are considered as parasitoids, which is indicative of its importance for the functioning of ecosystems (Wahl & Sharkey, 1993). As a part of biodiversity, its high number of species and habits stand out and provide a regulation service for its host populations (lepidopters, coleopters and dipters) (Shaw & Huddleston, 1991). This makes this group attractive in natural and managed systems for its use from the anthropogenic point of view (integrated pest control) (Nicholls, 2008).
According to Ruiz-Cancino et al. (2014), there is a register of 1291 species of the Ichneumonidae family for Mexico, which represents 5.3 % of the total, with more than 300 genera, 59 % of the species are neotropical, 29 % are neotropical-nearctic, 10 % are nearctic and the remaining 2% have another distribution, while 45 % are endemic for the moment, suggesting a need for carrying on with studies on this group of Hymenoptera.
The loss of ground cover vegetation, the conversion and fragmentation of natural areas in the ecosystems, generated by the expansion of human activities like agriculture, urbanization and industry, is a worldwide reality (Alphan et al., 2009; Tang et al., 2012). These activities disturb species living and depending on vegetation, they have effects depending on the distribution area of the species and on its habitat requirements (Scolozzi & Geneletti, 2012). Therefore, the use of agriculture land and biodiversity conservation is traditionally considered as incompatible (Schroth et al., 2004).
Most of the species living in rainforest remnants interact with agricultural systems but the contribution of the type of management for the survival of species has sometimes been ignored, as well as the potential value of agroecosystems for conservation (Perfecto & Vandermeer, 2012). In these systems, the diversity of vegetal species has effects on secondary productivity similar to natural systems. In this sense, environments with a higher diversity of vegetal species have been observed to promote increases in richness and abundance in trophic levels (Campos-Navarrete et al., 2015).
In this context, the present study was proposed with the purpose of knowing the structure of the community of the Ichneumonoidea superfamily in a multiple production agroecosystem, in which three areas with different management and land use were compared with the purpose of analyzing its influence on the structure of the associated Ichneumonoidea community, known for its role as parasitoid in ecosystems. Particularly, it was required to know whether the type of land use presents a positively influence when there has been a higher diversity of vegetal species associated to each land use. Regarding the functional role of ichneumonoidea, their biology is expected to be mainly koinobiont (specialist), but idiobiont (generalist) in sites of lower diversity, due to an influence of the vegetal diversity at superior trophic levels and to the presence of associated hosts.
Materials and Methods
Area of study
The study was performed in a farm situated at km 1.6 of Xmatkuil-Dzununcan Street, located at 20° 51’ 58’’ N and 89° 38’ 52’’ W, in the state of Yucatan, Mexico. The region where the farm is located is a karstic plain characterized by wide unevenness due to the unequal emersion of limestone deposits. In the zone, lithosol and rendzina soils dominate (Duch, 1991). The type of predominant vegetation is deciduous forest. The most abundant woody species are Acacia gaumeri, Acacia pennatula, Mimosa bahamensis, Havardia albicans and Gymnopodium floribundum (Olmsted et al., 1999). The climate of the region is tropical with summer rains (Aw), with an average annual temperature higher than 26 °C and 984.4 mm of annual precipitations (Orellana et al., 1999). The locality has six hectares, in which there are well differentiated zones according to the different type of management and land use they present. For this study, three sampling sites were selected: a) zone of 10 years secondary vegetation derived from deciduous forest (SV), b) area of family garden in which there are diverse fruit trees and some forest species (FG) and c) zone of dismantled area intended for horticultural cultivation (HC).
Ichneumonoidea sampling
Malaise traps (Townes model) and yellow traps (plates of 20 cm in height per 8 cm in width at the base and 14 cm in width in the upper part) were used, recommended to capture Hymenoptera (Nieves & Rey de Castillo, 1991). In each sampling site, three fix transects of 35 cm in length were established, the separation between transects and traps was of five meters. The orientation of transects was North-South. In total, 24 yellow traps and one Malaise trap were placed per sampling site. All traps remained active during two days a month during the period from July 2004 to June 2005. Distances between SV and HC group of traps was of 300 m, between SV and FG areas was of 200 m and finally between FG and HC was of 300 m. Taxonomic determination of sampled organisms was performed by means of the specialized literature (Wharton et al., 1997; Townes 1969, 1970a, b, 1971, Gauld 1991, 1997, Gauld et al., 1998) and by means of the comparison of sampled organisms of the Regional Entomological Collection (CERUADY) and of the collection of the Faculty of Biological Sciences (FCB-UANL). Samples were not separated at the species level and were separated under the morphospecies concept (Pik et al., 1999).
Data analysis
In order to analyze the influence of the vegetal diversity in the structure of the parasitoid community, species richness, abundance, local diversity (Delfín & Burgos, 2000) were considered, as well as parasitism strategies (koinobiont or idiobiont) according to Hanson & Gauld (2006).
Species richness of each sampling site was evaluated with Chao1 and first order Jacknife estimators; given that Chao1 is based on the number of scarce species (singletons and doubletons) found in the sample and first order Jacknife is based on the number of unique species (Colwell & Coddington, 1994). Both estimators were analyzed with EstimateS 8.2 software (Colwell, 2009). Abundance was considered as the number of present individuals in each site for registered species and local diversity was analyzed using Shannon-Wiener index (Moreno, 2001; Magurran, 2013) with R software in the BiodiversityR module (R Development Core Team, 2017). Each species found was classified in a strategy of koinobiont (specialist) or idiobiont (generalist) parasitism and the frequency of each strategy per site was analyzed.
To compare local diversity among sites, Sörensen coefficient of similarity was estimated, based on qualitative data to calculate the similarity of morphospecies among sampling sites (Moreno, 2001; Magurran, 2013). In the case of species richness, abundance and number of koinobiont and idiobiont species with respect to each sampling site were analyzed through a Generalized Linear Model (GLM) with a Poisson distribution, using R 2.5.1 software (R Development Core Team, 2017).
Results and Discussion
A total of 1,052 individuals were sampled, corresponding to two families (Braconidae and Ichneumonidae), 37 subfamilies, 107 genera and 306 morphospecies (Annex A and B). The Braconidae family was represented by 553 individuals belonging to 21 subfamilies, 57 genera and 235 morphospecies. Microgastrinae and Doryctinae were the subfamilies with the highest quantity of morphospecies, including 32.5 % and 24.4 % of total sampled individuals, respectively. In the case of the Ichneumonidae family, a total of 499 individuals were recorded, belonging to 16 subfamilies, 50 genera and 166 morphospecies. Cryptinae and Ichneumoninae were the subfamilies with the highest quantity of morphospecies, including 30.5 % and 9.4 % of total sampled individuals, respectively.
Braconidae found in this work constitute 84 % of the 25 families (Delfín et al., 2002) and 29 % of the 194 genera (Coronado & Zaldívar, 2013) reported for Yucatán. For the Ichneumonidae family, 57 % of the 28 subfamilies were obtained and el 12 % of the 343 genera which are reported for México (Ruíz-Cancino et al., 2014). Results are similar to those reported by Chay et al. (2006), who found 21 subfamilies and 84 genera for the Braconidae family and 19 subfamilies and 54 genera for the Ichneumonidae family in a study realized in a comparable system. However, in this research work no new species were recorded.
In general, the highest species richness and abundance were found in the family garden site (FG), followed by the secondary vegetation site (SV) and finally in the horticultural cultivation site (HC); the differences found were statistically significant (F=17.2, g.l.=2, p=0.000; F=12.7, g.l.=2, p=0.000); however, no significant differences were found between the families for both variables (F=2.0, g.l.=1, p=0.153; F=0.22, g.l.=1, p=0.63) (Table 1). For the Braconidae family, the highest species richness and abundance were in the family garden site (FG), followed by the secondary vegetation site (SV) and finally in the horticultural cultivation site (HC) and differences were significant, respectively (F=13.2, g.l.=2, p=0.000; F=12.8, g.l.=2, p=0.000). This pattern was found for the Ichneumonidae family (F=6.9, g.l.=2, p=0.000; F=4.62, g.l.=2, p=0.01).
Table 1 Species richness and their estimators for Braconidae and Ichneumonidae families in each sampling site.
| Sampling sites | Family | Estimators | ||
|---|---|---|---|---|
| Chao 1 | Jacknife 1er orden |
|||
| Secondary Vegetation (SG) | Estimated Richness | Bra | 136 | 136 |
| Ich | 170 | 128 | ||
| Observed Richness | Bra | 89 | 89 | |
| Ich | 77 | 77 | ||
| % Colected | Bra | 65.4 % | 65.4 % | |
| Ich | 43.5 % | 60.2 % | ||
| Family Garden (FG) | Estimated Richness | Bra | 188 | 188 |
| Ich | 122 | 123 | ||
| Observed Richness | Bra | 122 | 122 | |
| Ich | 77 | 77 | ||
| % Colected | Bra | 64.8 % | 64.8 % | |
| Ich | 63.1 % | 62.6 % | ||
| Horticultural cultivation (HC) | Estimated Richness | Bra | 61 | 40 |
| Ich | 17 | 19 | ||
| Observed Richness | Bra | 24 | 24 | |
| Ich | 12 | 12 | ||
| % Colected | Bra | 39.3 % | 60 % | |
| Ich | 70.6 % | 63.2 % | ||
*Braconidae (Bra) and Ichneumonidae (Ich).
The estimated value for species richness, based on Chao1 and first order Jacknife estimators, was higher than the observed value for both parasitoid families. For the Braconidae family, between 39 and 65 % of the general estimated richness was sampled, being the secondary vegetation site (SV) the best represented. For the Ichneumonidae family, between 43 and 70 % of the estimated richness was sampled, the horticultural cultivation site (HC) being the site with the highest percentage of sampling (Table 1).
Regarding local diversity, the pattern was the same as the previous, generally, and for the Braconidae family respect to the Ichneumonidae family, a higher diversity in the family garden site (FG), followed by the secondary vegetation site (SV) and finally the horticultural cultivation site (HC) (Table 1). The results of the coefficient of similarity reflect that the secondary vegetation site (SV) and the family garden site (FG) present the highest similarity for the present morphospecies, for both parasitoid families, 0.85 and 0.93, respectively (Table 2). Particularly, in the Braconidae family, the highest number of simple, doble, unique and duplicated morphospecies was found. However, in the secondary vegetation site (SV), the Ichneumonidae family was the one with the highest abundance, simple and unique morphospecies.
Table 2 Abundance, species diversity, number of morphospecies per biology type for Braconidae and Ichneumonidae families in each sampling site.
| SV | FG | HC | ||||
|---|---|---|---|---|---|---|
| Bra | Ich | Bra | Ich | Bra | Ich | |
| Number of individuals | 225 | 267 | 290 | 189 | 38 | 43 |
| Shannon-Wiener Index | 4.14 | 3.17 | 4.42 | 3.88 | 2.95 | 1.67 |
| Total number of morphospecies | 89 | 77 | 122 | 77 | 24 | 12 |
| Simple morphospecies (singletons) | 43 | 50 | 65 | 42 | 18 | 7 |
| Double morphospecies (doubletons) | 18 | 12 | 30 | 12 | 3 | 3 |
| Unique morphospecies | 52 | 56 | 72 | 51 | 18 | 8 |
| Duplicates morphospecies | 20 | 8 | 31 | 17 | 3 | 2 |
| Number of koinobionts | 47 | 39 | 89 | 50 | 20 | 30 |
| Number of idiobionts | 39 | 34 | 30 | 26 | 4 | 5 |
| Unknown biology | 2 | 4 | 3 | 1 | 0 | 0 |
*Braconidae (Bra), Ichneumonidae (Ich), Secondary Vegetation (SV), Family Garden (FG), Horticultural Cultivation (HC).
Diversified systems as well as agroforest systems, where the two sites with the highest diversity of vegetal species, the family garden site (FG) and the secondary vegetation site (SV), can be catalogued, have been observed to help to conserve biodiversity, because they provide habitats for species which are able to tolerate some levels of perturbation (Jose, 2009). Moreover, they contain a higher plant diversity, which could imply different levels (species, genetics, functional, phylogenetic) that in systems as monocultures, in general is translated in a positive effect on the primary productivity and in a benefice to arthropod associated communities (Haddad et al., 2009; Campos-Navarrete et al., 2015).
Particularly, richness, abundance and diversity of species of both parasitoid families were found to be higher in the family garden site (FG) and the secondary vegetation site (SV), which may be due to the fact they are habitats offering different resources as nectar, refuge and mating sites, phytophage host plants and hosts that are attractive to different parasitoid species (Altieri & Nicholls, 2004; Landis et al., 2000). Areas with the highest diversity, the family garden site (FG) and the secondary vegetation site (SV) present a higher diversity of vegetal species, mainly arboreal, compared to the horticultural cultivation site (HC) which does not possess arboreal species. This can be associated with what was mentioned by Fraser et al. (2007), Randlkofer et al. (2010), Barbieri & Dias (2012), who suggest the existence of a pattern representing a positive association between the structural diversity of the vegetation and the one of parasitoid insects. Additionally, diversified systems are more heterogeneous like land used in this research work and can modify habits of consumption and dietary behaviour of herbivores and predators, for instance, by complementing their diets and by means of the offer of sites with a higher disponibility of refuges (Agrawal et al., 2006; Castagneyrol et al., 2012; Hambäck et al., 2014).
Particularly in this studied system, it was suggested that the agroecological management realized in the area of the family garden site (FG) favors the presence of parasitoids, together with the exclusion of agrochemicals, mixed plantations contribute to the presence of such insects (Nicholls, 2008), since it would allow the generation of suitable conditions, like the permanence of hosts for immature stages, nectar for adults, frequent water and refuge allowing the increase of parasitoid populations (Tschartnke et al., 2005; Maeto et al., 2009). Regarding the secondary vegetation site (SV), an area of succession of deciduous forest that naturally existed in the agroecosystem, probably operate as a refuge for parasitoids and allow them to disperse through the different areas within the agroecosystem (Chay et al., 2006).
The most frequent biology was the koinobiont regarding the idiobiont one for the total and for each family, although there was no statistically significant difference (F=1.44, g.l.=1, p=0.55; Braconidae F=0.80, g.l.=1, p=0.46; Ichneumonidae F=0.63, g.l.=1, p=0.46). A higher number of koinobionts was present in the family garden site (FG) and the secondary vegetation site (SV), but no significant differences were found among sites (F=4.02, g.l.=2, p=0.07) (Table 2).
Regarding the parasitism strategy, the koinobiont mode is the one of higher presence in the three sites, result which coincides with what was established by Askew & Shaw (1986), Wharton et al. (1997) and Hawkins (1994), who considered that idiobiont species are less abundant in tropical regions. Among the various explanations of this pattern, koinobionts have a trend through specialization with regards to their hosts, while in the case of idiobionts, they are generalists, which Is associated to the effects of land use and to the associated vegetal diversity in the previously mentioned upper trophic levels.
The effect of land use, together with the associated vegetal diversity in the upper trophic levels, has been essentially explained because the highest diversity, when generating a more complex environment, consequently offers a higher quantity of refuges and preys (Russell, 1989; Campos-Navarrete et al., 2015), which in turn generates increases in predation rates, causing a reduction in prey abundance for parasitoids (“bottom-up” effects). Obviously, this type of effects is highly relevant to be considered in the design of productive systems as forest cultivations, due to its potential in pest control (Russell, 1989; Abdala-Roberts et al., 2015). This last factor can reduce or increase prey abundance (herbivores) according to characteristics like diet specialization (generalists vs. specialists) (Jactel & Brockerhoff, 2007). For instance, there are evidences showing that for specialists, the effects of an increase in diversity can be negative, due to the low density of its priority resource (Hambäck et al., 2014). In contrast, for generalists, the effects of an increase in diversity can vary and, in some cases, be positive, due to their mixed diet and to the increase in availability of refuge sites (Unsicker et al., 2008; Castagneyrol et al., 2013). In this sense, the presence of herbivores can mediate its interaction with the following trophic level of consumers where parasitoids are included (Abdala-Roberts et al., 2016).
Conclusions
Although these results support the foretold in literature, it is necessary to consider that there are ecological and evolutionary aspects of parasitoids that remain unknown. Particularly, the amplitude of hosts in species can change in space and time; there is evidence for the high behavioral plasticity of some individuals, allowing them to adapt to environmental changes and irregularities, to be successful organisms (Gröbler & Lewis, 2008; Santos & Quicke, 2011). In this sense, the present work provides information on parasitoid diversity in anthropogenic habitats, however, how interactions between parasitoids and hosts are structured in terms of parasitism rates and its high sensibility in human-managed environments, remained to be evaluated.
