Diversity of ichneumonoidea (Hymenoptera) in three types of land use in a multiple production agroecosystem in Xmatkuil, Yucatan, Mexico.

L. E. Castillo-Sánchez1; J. J. Jiménez-Osornio2; H. Delfín-González2; J. Ramírez Pech2; J. R. Canul-Solís1; A. Gonzalez-Moreno3; M. J. Campos-Navarrete1*

1. Tecnológico Nacional de México, I.T. Tizimín. km. 3.5 carretera final aeropuerto Cupul a Tizimín. Tizimín, Yucatán, México. , Tecnológico Nacional de México,

<city>Tizimín</city>
<state>Yucatán</state>
, México , 2. Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Carretera Mérida-Xmatkuil Km. 15.5. Mérida, Yucatán, México., Universidad Autónoma de Yucatán, Universidad Autónoma de Yucatán,
<city>Mérida</city>
<state>Yucatán</state>
, Mexico ,
3. Tecnológico Nacional de México, I.T. Conkal. Avenida Tecnológico, s/n. C.P. 97345, Conkal, Yucatán, México. , Tecnológico Nacional de México,
<postal-code>97345</postal-code>
<city>Conkal</city>
<state>Yucatán</state>
, México

Correspondence: *. Corresponding Author: Campos-Navarrete, M. J., Tecnológico Nacional de México, I.T. Tizimín. km. 3.5 carretera final aeropuerto Cupul a Tizimín. Tizimín, Yucatán, México. E-mail: E-mail:


Abstract

The presence of natural enemies can be influenced by many factors like the type of land use. These organisms are considered of great importance due to the pest control they perform without causing disturbance to the environment. In this study, the structure of the community of the Ichneumonoidea superfamily was analyzed, in three sites of an agroecosystem with different types of land use. Sampling was carried out in the period of July 2004 to June 2005. Twenty-four yellow traps and one Malaise trap were placed per site, in three fixed transects of 35 m in length. Traps remained open for two days per month. A total of 1052 individuals, 37 subfamilies, 107 genera and 306 morphospecies were recorded. For the Braconidae family, 553 individuals belonging to 21 subfamilies, 57 genera and 172 morphospecies were collected. For the Ichneumonidae family, 499 individuals belonging to 16 subfamilies, 50 genera and 134 morphospecies were collected. The family garden site presented a higher diversity for both families. Richness estimators point out that family garden and secondary vegetation presented a higher richness, abundance and diversity of parasitoid species; where the koinobiont habits are frequently present. According to these results, it can be hypothesized that a high diversity of plant species favors beneficial factors for parasitoid survival.

Received: 2018 July 23; Accepted: 2018 December 10

revbio. 2019 Nov 14; 6: e543
doi: 10.15741/revbio.06.e543

Keywords: Key words: Ichneumonidae, Braconidae, Hymenoptera, parasitoid wasps, richness.

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 %

TFN1*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

TFN2*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.


fn1Cite this paper: Castillo-Sánchez, L. E.; Jiménez-Osornio, J. J.; Delfín-González, H.; Ramírez Pech. J.; Canul-Solís, J. R.; Gonzalez-Moreno, A.; Campos-Navarrete, M. J. (2019). Diversity of ichneumonoidea (Hymenoptera) in three types of land use in a multiple production agroecosystem in Xmatkuil, Yucatan, Mexico. Revista Bio Ciencias 6, e543. doi: https://doi.org/10.15741/revbio.06.01.18

Acknowledgements

Authors thank to UADY-CCBA, to CONACyT for The grant of LECS Master, to Dr. Enrique Reyes Novelo for his observations and commentaries on previous versions of this work.

Appendix
Annex A.

List of morphospecies of the Braconidae family collected in three types of land uses from an agroecosystem in Xmatkuil, Yucatan, Mexico. (SC=Secondary Vegetation, FG=Family Garden, HC=Horticultural Cultivation) Biology (K=koinobiont, I= idiobiont)

Subfamily HC SV FG Biology Subfamily HC SV FG Biology
Agathidinae Cheloninae
Bassus sp. 1 - - 2 K Phanerotoma sp. 1 - - 1 K
Alysiinae Phanerotoma sp. 2 1 - 5 K
Alysia sp. 1 - 1 - K Pseudophanerotoma sp. 1 - - 1 K
Alysiasta sp. 1 - - 2 K Pseudophanerotoma sp. 2 - - 1 K
Aphaereta sp. 1 1 - - K Pseudophanerotoma sp. 3 - - 5 K
Cratospila sp. 1 - 1 - K Doryctinae
Dapsilarthra sp. 1 - - 1 K Acanthorhogas sp. 1 - 2 - I
Dinotrema sp. 1 - 2 - K Acrophasmus sp. 1 1 - - I
Dinotrema sp. 2 - 2 - K Acrophasmus sp. 2 - 1 - I
Blacinae Acrophasmus sp. 3 - 3 - I
Blacus sp. 1 - 6 - K Acrophasmus sp. 4 - 1 - I
Blacus sp. 2 - 1 - K Acrophasmus sp. 5 - 1 - I
Blacus sp. 3 - 2 - K Acrophasmus sp. 6 - 1 - I
Blacus sp. 4 - - 2 K Acrophasmus sp. 7 - 1 - I
Braconinae Allorhogas sp. 1 - 1 1 ?
Bracon sp. 1 - - 1 I Heterospilus sp. 1 - - 1 I
Bracon sp. 2 - 1 - I Heterospilus sp. 2 - 1 - I
Bracon sp. 3 - - 1 I Heterospilus sp. 3 1 - 2 I
Bracon sp. 4 1 - - I Heterospilus sp. 4 - 1 - I
Bracon sp. 5 - - 2 I Heterospilus sp. 5 - 3 3 I
Bracon sp. 6 - - 2 I Heterospilus sp. 6 1 1 1 I
Cyclaulax sp. 1 - - 1 I Heterospilus sp. 7 - 6 2 I
Digonogastra sp. 1 - 1 - I Heterospilus sp. 8 - 7 - I
Cardiochilinae Heterospilus sp. 9 - 3 1 I
Cardiochiles sp. 1 - - 1 K Heterospilus sp. 10 - 1 - I
Cenocoeliinae Heterospilus sp. 11 - 1 - I
Cenocoelius sp. 1 - 1 1 I Heterospilus sp. 12 - 5 2 I
Cheloninae Heterospilus sp. 13 - 10 5 I
Chelonus sp. 1 - - 1 K Heterospilus sp. 14 - 2 2 I
Chelonus sp. 2 - - 2 K Heterospilus sp. 15 - 3 2 I
Chelonus sp. 3 1 - 1 K Heterospilus sp.16 - 2 - I
Microchelonus sp. 1 4 - 14 K Heterospilus sp. 17 - 3 2 I
Microchelonus sp. 2 - 2 1 K Heterospilus sp. 18 - 2 - I
Microchelonus sp. 3 - 4 4 K Heterospilus sp. 19 - 1 - I
Microchelonus sp. 4 - 2 - K Heterospilus sp. 20 - 2 - I
Microchelonus sp. 5 - 8 7 Heterospilus sp. 21 - 2 - I
Doryctinae Meteorinae
Heterospilus sp. 22 - 2 2 I Meteorus sp. 1 - - 1 K
Heterospilus sp. 23 - 7 1 I Microgastrinae
Notiospathius sp. 1 - 17 1 I Apanteles sp. 1 2 - - K
Notiospathius sp. 2 - 6 2 I Apanteles sp. 2 - 1 2 K
Rhaconotus sp. 1 - 1 - I Apanteles sp. 3 - - 6 K
Rhaconotus sp. 2 - - 2 I Apanteles sp. 4 - - 1 K
Euphorinae Apanteles sp. 5 1 - - K
Litostolus sp. 1 - - 1 K Apanteles sp. 6 - - 2 K
Microctonus sp. 1 1 - 1 K Apanteles sp. 7 - - 1 K
Microctonus sp. 2 - 1 1 K Apanteles sp. 8 - - 9 K
Microctonus sp. 3 - - 1 K Apanteles sp. 9 - - 1 K
Gnamptodontinae Apanteles sp. 10 - - 1 K
Gnamptodon sp. 1 - - 1 ? Apanteles sp. 11 - 2 1 K
Pseudognaptodon sp. 1 - 5 1 K Apanteles sp. 12 - 1 1 K
Pseudognaptodon sp. 2 - - 1 K Apanteles sp. 13 1 - - K
Pseudognaptodon sp. 3 1 - - K Apanteles sp. 14 1 3 8 K
Homolobinae Apanteles sp. 15 - - 3 K
Exosticolus sp. 1 - 1 1 K Choeras sp. 1 - - 1 K
Hormiinae Cotesia sp. 1 - - 1 K
Allobracon sp. 1 - - 1 I Cotesia sp. 2 - - 7 K
Hormius sp. 1 - 3 1 I Cotesia sp. 3 - - 1 K
Hormius sp. 2 - - 1 I Cotesia sp. 4 - - 4 K
Pambolus sp. 1 - 8 1 I Cotesia sp. 5 - - 2 K
Pambolus sp. 2 - 9 1 I Deuterixys sp. 1 - 1 - K
Pambolus sp. 3 - 5 2 I Deuterixys sp. 2 - - 4 K
Pambolus sp. 4 - 3 1 I Diolcogaster sp. 1 - 2 2 K
Parahormius sp. 1 - 1 - I Diolcogaster sp. 2 - 1 - K
Parahormius sp. 2 - - 1 I Diolcogaster sp. 3 1 - 1 K
Ichneutinae Diolcogaster sp. 4 - - 2 K
Helconichia sp. 1 - 1 - K Diolcogaster sp. 5 - 1 10 K
Paroligoneurus sp. 2 - 3 - K Diolcogaster sp. 6 - 2 3 K
Macrocentinae Diolcogaster sp. 7 - - 11 K
Austrozele sp. 1 - 1 - K Glyptapanteles sp. 1 - 1 2 K
Austrozele sp. 2 - - 1 K Glyptapanteles sp. 2 - - 5 K
Mendesellinae Glyptapanteles sp. 3 2 1 1 K
Epsilogaster sp. 1 - 1 2 ? Glyptapanteles sp. 4 - 2 4 K
Microgastrinae Miracinae
Glyptapanteles sp. 5 1 1 1 K Mirax sp. 6 - - 5 K
Glyptapanteles sp. 6 - 1 - K Mirax sp. 7 - - 2 K
Hypomicrogaster sp. 1 - - 1 K Opiinae
Iconella sp. 1 - - 1 K Opius sp. 1 - 3 3 K
Iconella sp. 2 - - 1 K Opius sp. 2 - 1 - K
Microplitis sp. 1 - - 1 K Opius sp. 3 - - 3 K
Microplitis sp. 2 - - 1 K Opius sp. 4 - - 2 K
Microplitis sp. 3 1 - - K Opius sp. 5 - - 1 K
Parapanteles sp. 1 - - 1 K Opius sp. 6 - 1 - K
Parapanteles sp. 2 - - 2 K Opius sp. 7 1 2 4 K
Parapanteles sp. 3 - - 2 K Opius sp. 8 - - 1 K
Parapanteles sp. 4 - - 2 K Orgilinae
Pseudapanteles sp. 1 - - 1 K Orgilus sp. 1 - 1 - K
Pseudapanteles sp. 2 - 1 3 K Stantonia sp. 1 5 3 4 K
Pseudapanteles sp. 3 - 1 - K Rogadiinae
Rhygoplitus sp. 1 2 1 12 K Choreborogas sp. 1 - 4 - K
Rhygoplitis sp. 2 5 - 14 K Choreborigas sp. 2 - 3 - K
Miracinae Polystenidea sp. 1 1 - - K
Mirax sp. 1 - 1 1 K Rogas sp. 1 - 3 1 K
Mirax sp. 2 1 2 1 K Rogas sp. 2 - 1 2 K
Mirax sp. 3 - - 1 K Rogas sp. 3 - - 1 K
Mirax sp. 4 - - 1 K Rogas sp. 4 - - 1 K
Mirax sp. 5 - - 2 K Stiropius sp. 1 - - 1 K
Yelicones sp. 1 - 1 1 K

Annex B.

List of morpho-species of the Ichneumonidae family collected in three types of land uses from an agroecosystem in Xmatkuil, Yucatán, Mexico. (SC=Secondary Vegetation, FG=Family Garden, HC=Horticultural Cultivation) Biology (K=koinobiont, I= idiobiont)

Subfamily HC SV FG Biology Subfamily HC SV FG Biology
Anomaloninae Cremastinae
Anomalon sp. 1 7 - 16 K Trathala sp1 - - 1 K
Anomalon sp. 2 23 - 4 K Trathala sp. 2 - - 1 K
Anomalon sp. 3 - - 1 K Trathala sp. 3 - - 1 K
Anomalon sp. 4 1 - 9 K Xiphosomella sp. 1 - - 1 K
Barylypa sp. 1 2 - 21 K Xiphosomella sp. 2 - - 1 K
Barylypa sp. 2 - - 1 K Cryptinae
Barylypa sp 3 - - 1 K Acerastes sp. 1 - 1 - I
Barylypa sp. 4 - - 6 K Acerastes sp. 2 - 24 2 I
Banchinae Acerastes sp. 3 - 2 6 I
Eudeleboea sp. 1 - - 3 K Acerastes sp. 4 - 1 - I
Eudeleboea sp. 2 - - 2 K Bicryptella sp. 1 - 15 - I
Eudeleboea sp. 3 - - 1 K Bicryptella sp. 2 - - 1 I
Eudeleboea sp. 4 - 1 - K Bicryptella sp. 3 - 4 - I
Lissocaulus sp. 1 - 1 - K Cestrus sp. 1 - 1 - I
Meniscomorpha sp. 1 - - 4 K Clasis sp. 1 - 1 - ?
Meniscomorpha sp. 2 - 1 4 K Cryptanura sp. 1 - 5 1 I
Syzeuctus sp. 1 - 1 - K Cryptanura sp. 2 - 5 - I
Campopleginae Dicamixus sp. 1 - 2 - I
Dusona sp. 1 1 - 1 K Dismodix sp. 1 - - 1 I
Venturia sp. 1 - - 1 K Glodianus sp. 1 - 1 - I
Xanthocampoplex sp. 1 - 1 2 K Glodianus sp. 2 - 8 3 I
Xanthocampoplex sp. 2 - 1 - K Glodianus sp. 3 - 2 - I
Xanthocampoplex sp. 3 - - 6 K Glodianus sp. 4 - 1 - I
Cylloceriinae Glodianus sp. 5 - - 1 I
Cylloceria sp. 1 - - 2 K Glodianus sp. 6 - - 1 I
Cremastinae Glodianus sp. 7 - - 1 I
Eiphosoma sp. 1 2 8 1 K Hemicallidiotes sp. 1 - 1 - I
Eiphosoma sp. 2 - 1 2 K Lamprocryptidea sp. 1 - 3 3 I
Eiphosoma sp. 3 - - 2 K Lamprocryptidea sp. 2 - 2 - I
Eiphosoma sp. 4 - - 1 K Lamprocrypridea sp. 3 - 2 - I
Pristomerus sp. 1 - - 1 K Lamprocryptidea sp. 4 1 - 1 I
Temelucha sp. 1 - 1 - K Lamprocryptidea sp. 5 - - 1 I
Temelucha sp. 2 2 - 4 K Lamprocryptidea sp. 6 - - 1 I
Temelucha sp. 3 - - 1 K Lamprocryptidea sp. 7 - 1 - I
Temelucha sp. 4 - - 1 K Lamprocryptus sp. 1 - 1 - I
Cryptinae Lamprocryptus sp. 2 - - - I
Lymeon sp. 1 - 4 5 I Ichneumoninae
Lymeon sp. 2 - 1 2 I Centeterus sp. 8 - 2 - K
Lymeon sp. 3 - 5 - I Centeterus sp. 9 - - 2 K
Lymeon sp. 4 - - 1 I Centeterus sp. 10 - 1 - K
Lymeon sp. 5 - 1 2 I Centeterus sp. 11 - - 1 K
Lymeon sp. 6 - 1 - I Centeterus sp. 12 - 1 - K
Lymeon sp. 7 - - 2 I Centeterus sp. 13 - - 1 K
Lymeon sp. 8 - 1 - I Centeterus sp. 14 - 1 - K
Lymeon sp. 9 - 1 - I Coelichneumon sp. 1 - 1 - K
Lymeon sp. 10 - - 2 I Macrojoppa sp. 1 - - 1 K
Lymeon sp. 11 - 1 - I Macrojoppa sp. 2 - 1 - K
Pachysomoides sp. 1 - 1 1 I Oedicephalus sp. 1 - 1 - K
Pachysomoides sp. 2 - 2 - I Oedicephalus sp. 2 - 1 - K
Pachysomoides sp. 3 - - 1 I Rubicundiella sp. 1 - 2 - K
Picrocryptoides sp. 1 - - 2 I Rubicundiella sp. 2 - 1 - K
Picrocryproides sp. 2 - - 1 I Trogus sp. 1 - 1 - K
Picrocryptoides sp. 3 - 2 2 I Lycorininae
Rhinium sp. 1 - 1 - I Licorina sp. 1 - 1 - K
Stiboscopus sp. 1 - 1 - I Metopiinae
Trychosis sp. 1 - - 1 I Colpotrochia sp. 1 - - 3 K
Ctenopelmatinae Microleptinae
Mesoleptidea sp. 1 1 1 - K Blapticus sp. 1 - 87 4 ?
Philotymma sp. 1 - 2 - K Blapticus sp. 2 - 1 - ?
Ichneumoninae Blapticus sp. 3 - 1 - ?
Carinodes sp. 1 - 1 - K Orthocentrinae
Carinodes sp. 2 - - 2 K Orthocentrus sp. 1 1 14 2 K
Carinodes sp. 3 - 3 - K Orthocentrus sp. 2 - - 10 K
Carinodes sp. 4 - 1 - K Stenomacrus sp. 1 - 1 2 K
Carinodes sp. 5 - - 1 K Ophioninae
Carinodes sp. 6 - 1 - K Enicospilus sp. 1 1 - 1 K
Carinodes sp. 7 - - 1 K Enicospilus sp. 2 - - 1 K
Carinodes sp. 8 - 1 - K Enicospilus sp. 3 - 1 1 K
Centeterus sp. 1 - 4 2 K Oxytorinae
Centeterus sp. 2 - 4 - K Oxytorus sp. 1 - 1 - K
Centeterus sp. 3 - 1 - K Pimplinae
Centeterus sp. 4 - 1 - K Tromatobia sp. 1 - 1 1 I
Centeterus sp. 5 - 2 - K Tryphoninae
Centeterus sp. 6 - 2 1 K Monoblastus sp. 1 - - 1 K
Centeterus sp. 7 - - 1 K Monoblastus sp. 2 - - 2 K
Monoblastus sp. 3 - 1 - K

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Revista Bio Ciencias, Año 12, vol. 8,  Enero 2021. Sistema de Publicación Continua editada por la Universidad Autónoma de Nayarit. Ciudad de la Cultura “Amado Nervo”,  Col. Centro,  C.P.: 63000, Tepic, Nayarit, México. Teléfono: (01) 311 211 8800, ext. 8922. E-mail: revistabiociencias@gmail.com, revistabiociencias@yahoo.com.mx, http://revistabiociencias.uan.mx. Editor responsable: Dr. Manuel Iván Girón Pérez. No. de Reserva de derechos al uso exclusivo 04-2010-101509412600-203, ISSN 2007-3380, ambos otorgados por el Instituto Nacional de Derechos de Autor. Responsable de la última actualización de este número Dr. Manuel Iván Girón Pérez. Secretaria de Investigación y Posgrado, edificio Centro Multidisciplinario de Investigación Científica (CEMIC) 03 de la Universidad Autónoma de Nayarit. La opinión expresada en los artículos firmados es responsabilidad del autor. Se autoriza la reproducción total o parcial de los contenidos e imágenes, siempre y cuando se cite la fuente y no sea con fines de lucro.

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