Ichneumonidae (Hymenoptera) from a high mountain forest in Tamaulipas and new generic records for Mexico

G. M. Alvarez-Cabrera1; E. Ruíz-Cancino1*; J.M. Coronado-Blanco1; J. Treviño-Carreón1; A.I. Khalaim1, 2

1. Facultad de Ingeniería y Ciencias, Universidad Autónoma de Tamaulipas, Centro Universitario Adolfo López Mateos, C.P. 87149, Cd. Victoria, Tamaulipas, México., Universidad Autónoma de Tamaulipas, Facultad de Ingeniería y Ciencias, Universidad Autónoma de Tamaulipas,

<postal-code>87149</postal-code>
<city>Cd. Victoria</city>
<state>Tamaulipas</state>
, Mexico , 2. Instituto Zoológico, Academia de Ciencias de Rusia, 199034 San Petersburgo, Rusia., Instituto Zoológico, Academia de Ciencias de Rusia,
<city>San Petersburgo</city>
, Russia

Correspondence: *. Corresponding Author: Ruíz-Cancino, Enrique.Universidad Autónoma de Tamaulipas, Facultad de Ingeniería y Ciencias, Centro Universitario Adolfo López Mateos, C.P. 87149, Cd. Victoria, Tamaulipas, México. Phone: +52(834) 31 8 18 00. E-mail: E-mail:


Abstract

Parasitoid wasps of the family Ichneumonidae form one of the largest groups of insects in the order Hymenoptera, some species are important agents of biological control of agricultural or forest pests, other are bioindicators and some are pollinators. The objective of this research was to know the richness, diversity and equity of the ichneumonids collected in one high mountain forest in Miquihuana, Tamaulipas, Mexico. Ichneumonids were collected from August 2011 to August 2012 in a Malaise trap installed in one Pinus pseudostrobus Lindl. forest with a dense chaparral of Quercus miquihuanensis Nixon and Muller at 2,550 masl. Thirteen subfamilies, 63 genera and 133 species were found. There is high species richness but low diversity of species. Ten genera are new records for Mexico: Aclastus Foerster, Arotrephes Townes, Distathma Townes, Gnypetomorpha Foerster, Pleurogyrus Townes, Lysibia Foerster, Stiboscopus Föerster and Tricholinum Föerster in Cryptinae, besides Deleboea Cameron in Banchinae, and Lethades Davis in Ctenopelmatinae. For the State of Tamaulipas, México, 16 genera are new records, including the 10 noted above, besides Mnioes (Banchinae), Amphibulus, Stilpnus (Cryptinae), Asthenara (Ctenopelmatinae), Sathropterus (Tersilochinae) and Hercus (Tryphoninae).

Received: 2017 December 19; Accepted: 2018 May 18

revbio. 2020 Mar 23; 5(spe1): e421
doi: 10.15741/revbio.05.nesp.e421

Keywords: Key words: Wasps, Parasitoids, Biological control, Pine and Oak forest.

Introduction

Ichneumonidae is the family with the bigger number of species of parasitoid insects of the order Hymenoptera (Haraldseide, 2015). Townes (1969) estimated that more than 60,000 species half a century ago. Gauld et al., (2002) estimated that there could exist more than 100,000 species in the world, while in Yu et al., (2016), reported 25,285 species of 1,601 genera and 44 subfamilies.

There have been estimated between 3,215 and 4,544 species in Mexico (Ruíz et al., 2014) and more than 1,300 species have been registered (García-Ramírez et al., 2016). 28 subfamilies and 373 genera have been reported until 2016; which is why it is recommended to perform more research in the country (Ruíz-Cancino et al., 2014); Ruíz-Cancino, 2015); the genera Labilochus was described from Tamaulipas (Khalaim et al., 2017), being a total of 374 genera for Mexico.

Many of the species of Ichneumonidae possess a high level of specialty and occupy a high trophic level for being parasitoid wasps, with which accomplish the regulatory function on the arthropod populations (Rodríguez et al., 2005), mainly on other insects and on some arachnids; the attack range of the Ichneumonidae family is limited within the immature stage (O’Connor et al., 2007), in other words larvas and pupas from other species of holometabolous insects; species from the orders Lepidoptera, Hymenoptera, Diptera, Coleoptera, Neuroptera y Mecoptera (Stary et al., 1988) are considered as hosts and a small number of species develop in the spiders’ ovisacs and act as predators when feeding on multiple individuals of the guest (O’Connor et al., 2007). For this reason, they are being implemented as agents of biological control of agricultural and forest pests (Bennet, 2008), due to the use and handling of natural enemies, it represents a strategy that does not affect the biological equilibrium, therefore, its application is ecological and sustainable (Gutiérrez-Ramírez et al., 2013).

Additionally, the ichneumonids can be considered as bioindicators because they represent the diversity of attacking hosts (Sharkey, 2007) and some are reported as pollinators; so is the case for the orchids from the genera Cryptostylis, where floral aromas that simulate sexual pheromones of the female, copulates on the flower and pollinates after having resting in another orchid (Gaskett et al., 2008; Weinstein et al., 2016). The objective of this article was to get to know the richness, diversity, and equity of the ichneumonids collected in a Malaise trap in the Ejido La Marcela, Miguihuana, Tamaulipas, Mexico.

Materials and Methods

The research was developed in a locality in Ejido La Marcela, belonging to the municipality of Miquihuana in the state of Tamaulipas, Mexico, at the coordinates 23º40’ 38.4’’ latitude N, 99º49’ 17.03’’ longitude W, at an altitude of 2,550 masl; it has a template climate and extreme with rain in Summer (Gobierno del Estado de Tamaulipas, 2018).

The collecting of ichneumonids was carried out with a Malaise trap of 1.8 meters height with a black and white cloth, which remained installed during 13 months (August 2011 - August 2012) in a forest dominated by Pinus pseudotrobus Lindl in the arboreal stratum, and by dense chaparral of Quercus miquihuanensis Nixon and Muller in the bushy stratum; during this period, the samples were collected every two weeks. For the taxonomic determination subfamily keys of Townes and Townes (1966) were applied, modified by Ruíz-Cancino et al., (2014) to include the subfamilies that were registered previously for Mexico; the genera keys of Townes and Townes (1966), Townes (1969, 1970a, 1970b, 1971), Dasch (1974), Heinrich (1977), Gauld (2000), Kasparyan and Ruíz (2005, 2008); and the species with the ones from Humala (2010), Kasparyan (2006) and Kasparyan and Ruíz (2005, 2008); in addition to the description from Labilochus in Khalaim et al., (2017). The material is found stored in the Coleccion de Ichneumonidae del Museo de la Facultad the Ingenieria y Ciencias de la Universidad Autonoma de Tamaulipas, in Ciudad Victoria, Tamaulipas, Mexico.

For the statistical analysis of the data, the recommended indexes by Moreno (2001) were applied to determine the richness, diversity and equity. For the richness of the species, the Margalef (DMg) (1958) index was applied, who points out that, if the result is lower than two, the richness is low, but if it is greater than five, the richness is high; for which the following formula was applied:

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where S represents the number of species and N the total number of individuals.

The Shannon-Wiener (H’) (1949) index is applied to measure the diversity of species, the values obtained are expressed with a positive number, in which the majority of the ecosystems varies between one (low diversity) and five (high diversity), even if the values superior to three are typically interpreted as diverse; this is obtained by using the following formula:

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where pi is the proportion of the total of the sample belonging to the species.

In order to know the equity of the species, the Pielou (J’) (1969) index was calculated, whose value fluctuates from zero to one, where zero indicates an invalid equity, one indicates that all species are equally abundant; this is obtained by applying the following formula:

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where H’ is the Shannon-Wiener index and N is the total number of collected individuals. For the simplification of the information referring to the dates of sampling, the date was organized according to the four seasons. The sampling began in the summer 2011 and ended in the summer 2012.

Results and Discussion

461 specimens of Ichneumonidae were captured in the Ejido La Marcela, municipality of Miquihuana, Tamaulipas, Mexico, belonging to 13 subfamilies, 63 genera were determined, six species and also 127 morphospecies were separated, being 244 females and 217 males. Ten genera are new registers for Mexico. Because the Malaise trap used is 1.87 meter-height, it is thought that the ichneumonids obtained mainly belonged from the oak of chaparral and herbaceous plants.

In comparison to the 1,115 ichneumonids reported by Rodríguez-Mota et al., (2015) as a product of the capture with the Malaise trap during a year in Jaumave, Tamaulipas, Mexico, in an association of Pinus nelsonii Shaw, P. cembroides Zucc. and Juniperus flaccida Schltdl at an altitude of 1,450 masl, but closed to a source of water, in the current research, carried out in another locality in the same south-western region of the state, only a third part of the individuals was obtained in a vegetation dominated by Pinus pseudostrobus in the arboreal stratum, and by Quercus miquihuanensis in the bushy stratum, in where there is no near water source, in addition to the low temperatures that could be factors that had an influenced on the number of specimens and consequently, on the diversity of the Ichneumonidae species.

In Appendix 1, the list of subfamilies, genera and species of Ichneumonidae is presented, where the Cryptinae subfamily strands out with 23 genera and 50 morphospecies also a tribe of five morphospecies, being 55 morphospecies. Eight genera of this subfamily are new registers for Mexico (Aclastus, Arotrephes, Distathma, Gnypetomorpha, Lysibia, Pleurogyrus, Scrobiculus, Tricholinum). Aclastus had been reported of Canada, USA, Europe and Asia (holartico oriental); Arotrephes of anada, USA, and Europe (holartico); Distathma of Brazil, Chile, Philippines, and Afghanistan (neotropical, oriental y paleartico); Gnypetomorpha of Europe (pelartico); Lysibia of Canada, USA, Costa Rica, Brazil, Argentina, Europe, and Asia (holartico, orientalm, and neotropical); Pleurogyrus of USA and Europe (holartico); Scrobiculus of Peru and Granada (neotropical); and Tricholinum of Europe and Japan (paleartico and oriental) (Yu et al., 2016)

Out of the genera of the Cryptinae subfamily already known in Mexico, Phygadeuon showed the biggest number of morphospecies and specimens (7 morphospecies, with 44 specimens), followed by Gelis (7, 29), Ethelurgus (5, 6) and Isdromas (4, 5). The second most abundant was Campopleginae with 9 genera and 27 morphospecies and includes 135 especimens; the more well represented were Diadegma (7 morphospecies, 61 specimens), Hyposoter (6, 20), Campoplex (5, 6) y Campoletis (3, 41). On the third place, there is Ichneumoninae with 8 genera, 14 morphospecies and 61 specimens, the most collected genera were Phaeogenes (three morphospecies, 15 specimens) and it is followed by Dicaelotus (2, 25) and Ichneumon (2, 8).

The other two new registers for Mexico are the genera Deleboea (Banchinae) and Lethades (Ctenopelmatinae). Deleboea was only known from Ecuator and Lethadesfrom the US, Europe y Asia (Yu et al., 2016). For the state of Tamaulipas, 16 genera are new registers, including the previous ten, in addition to Mnioes (Banchinae), Amphibulus, Stilpnus (Cryptinae), Asthenara (Ctenopelmatinae), Sathropterus (Tersilochinae) and Hercus (Tryphoninae).

In relation to the indexes calculated for each of the four seasons, through the Margalef index (DMg) the richness was determined; the obtained values are greater than five, for summer, autumn, and spring, where the richness is high while as for winter the richness is medium (Table 1). In the same way Rodríguez-Mota et al., (2015) reported a greater richness of species for spring and summer, being lower in winter.

Table 1.

Richness, diversity and equity of Ichneumonidae by season of the year in La Marcela, Miquihuana, Tamaulipas, Mexico. August 2011-August 2012.


Season of the year Number of DMg H’ J’
species individuals
Summer 2011 33 53 5.217 0.249 0.041
Summer 2012 46 94 7.337 0.324 0.053
Autumn 2012 38 83 6.033 0.309 0.050
Winter 2012 20 38 3.098 0.206 0.034
Spring 2012 72 193 11.576 0.365 0.059
Total 461 28.043 1.203 0.196

The Shannon-Wiener index (H’) was used to know the diversity in each season of the year, it was observed that in the whole collecting period the diversity was low, although the one obtained in spring is grater (0.365) in comparison to the other three seasons. The value from the Pielou indez was lower than one, pointing out that, all species show different abundance (Table 1).

The most abundant subfamilies were Cryptinae, Campopleginae and Ichneumoninae, which had the greater richness of the species (Table 2). When comparing with the study carried out by Pérez-Urbina et al., (2010) in the Canon del Novillo, in Ciudad Victoria, a dry zone of Tamaulipas, Mexico, indicate that Campopleginae, Cryptinae and Ichneumoninae the most abundant subfamilies with 289, 143, and 42 specimens respectively, and Cryptinae and Ichnaumonidae had the greater richness of species.

Table 2.

Richness, diversity and equity of the subfamilies of Ichneumonidae in La Marcela, Miquihuana, Tamaulipas, Mexico. August 2011- August 2012.


Subfamily Number of DMg H’ J’
species individuals
Alomyinae 1 2 0.00 0.024 0.004
Banchinae 7 34 0.98 0.192 0.031
Campopleginae 28 135 4.40 0.360 0.059
Cryptinae 55 151 8.80 0.366 0.060
Ctenopelmatinae 3 3 0.33 0.033 0.005
Ichneumoninae 14 61 2.12 0.268 0.044
Mesochorinae 4 14 0.49 0.106 0.017
Metopiinae 5 9 0.65 0.077 0.013
Orthocentrinae 6 23 0.82 0.150 0.024
Oxytorinae 1 1 0.00 0.013 0.002
Pimplinae 4 19 0.49 0.131 0.021
Tersilochinae 2 3 0.16 0.033 0.005
Tryphoninae 4 6 0.49 0.057 0.009
Total 133 461 19.57 1.808 0.295

Rodríguez-Mota et al., (2015) found that the subfamilies with greater abundance were Campopleginae and Cryptinae with 296 and 250 specimens respectively; however, the greater richness of species in this place was only presented by Cryptinae. Therefore, for the current site of study as for the other researches carried out in dry zones of the state, Cryptinae has the greater richness of species, although it differs in its abundance. The predominance of these subfamilies in the site of study as in the other mentioned localities can be because they are more cosmopolitan (Yu et al., 2016), being more adapted to diverse climatic conditions. Gauld (2006) had already indicatd that Cryptinae was probably the richest group of ichneumonids in species of the Neotropical region.

Basing on the results of the richness, diversity, and equity of the subfamilies of Ichneumonidae, the ones that show the greater richness index value (DMg) were Cryptinae (8.80) and Campopleginae (4.40). Said subfamilies were also the most diverse with an index (H’) of 0.366 (Cruptinae) and 0.360 (Campopleginae) and with low diversity for the rest of the subfamilies. In relation to equity (J’), all the subfamilies are different because their value is very inferior than one (Table 2).

Conclusion

In the Ejido La Marcela, Tamaulipas, Mexico, a high richness of Ichneumonidae (DMg between 5.217 abd 11.576 per season) exists and a low diversity of species (H’ between 0.206 and 0.365), while the Pielou index value (J’ = 0.196), indicates that all species show different abundance. The ten new registers increase the number of genera of Ichneumonidae to 384 for the Mexican Republic.


fn1Cite this paper: Alvarez-Cabrera, G. M., Ruíz-Cancino, E., Coronado-Blanco, J.M., Treviño-Carreón, J., Khalaim, A.I. (2018). Ichneumonidae (Hymenoptera) from a high mountain forest in Tamaulipas and new generic records for Mexico. Revista Bio Ciencias 5(nesp), e421. doi: https://doi.org/10.15741/revbio.05.nesp.e421

Acknowledgements

To the project PROPEP “Estudios taxonómicos y biológicos de plagas y enemigos naturales en México” to the Facultad de Ingeniería y Ciencias de la Universidad Autónoma de Tamaulipas y al Consejo Nacional de Ciencia y Tecnología, for their help.

Appendix
Appendix 1. Ichneumonidae captured in one high mountain forest in Miquihuana, Tamaulipas, Mexico. August 2011- August 2012..

Subfamily
Genus and/or species
Season of the year Sex
Summer Fall Winter Spring Total Males Females
Alomyinae
Centeterus sp. 2 2 2 0
Banchinae
* Deleboea sp. 2 1 3 0 3
Lissonota sp. 1 1 1 1 0
Lissonota sp. 2 1 1 2 4 1 3
Lissonota sp. 3 4 3 7 0 7
Lissonota sp. 4 6 10 16 0 16
Lissonota sp. 5 2 2 0 2
Mnioes sp. 1 1 1 0
Campopleginae
Casinaria sp. 1 2 2 0 2
Casinaria sp. 2 1 1 0 1
Campoletis sp. 1 5 5 5 15 7 8
Campoletis sp. 2 1 2 3 6 2 4
Campoletis sp. 3 3 1 16 20 6 14
Campoplex sp. 1 1 1 0 1
Campoplex sp. 2 2 2 0 2
Campoplex sp. 3 1 1 0 1
Campoplex sp. 4 1 1 1 0
Campoplex sp. 5 1 1 0 1
Cymodusa sp. 1 1 0 1
Diadegma sp. 1 5 20 4 15 44 7 37
Diadegma sp. 2 3 3 2 1
Diadegma sp. 3 2 1 3 0 3
Diadegma sp. 4 1 1 0 1
Diadegma sp. 5 1 1 1 0
Diadegma sp. 6 1 1 0 1
Diadegma sp. 7 1 1 1 5 8 3 5
Hyposoter sp. 1 1 1 0 1
Hyposoter sp. 2 1 1 0 1
Hyposoter sp. 3 4 2 6 3 3
Hyposoter sp. 4 2 2 0 2
Hyposoter sp. 5 1 1 0 1
Hyposoter sp. 6 6 1 2 9 5 4
Phobocampe sp. 1 1 1 0
Prochas sp. 1 1 0 1
Venturia sp. 1 1 0 1
Cryptinae
* Aclastus sp. 1 1 0 1
Amphibulus sp. 1 1 1 1 0
Amphibulus sp. 2 1 1 1 0
Aptesis sp. 1 1 0 1
* Arotrephes sp. 1 1 0 1
Compsocryptus sp. 1 1 0 1
Cryptus sp. 1 2 3 1 2
* Disthatma sp. 1 1 1 0 1
Disthatma sp. 2 1 1 0 1
Disthatma sp. 3 1 1 0 1
Endasys sp. 1 1 1 0
Epelaspis sp. 4 3 7 7 0
Ethelurgus sp. 1 1 1 2 0 2
Ethelurgus sp. 2 1 1 0 1
Ethelurgus sp. 3 1 1 0 1
Ethelurgus sp. 4 1 1 1 0
Ethelurgus sp. 5 1 1 0 1
Gelis sp. 1 1 2 5 5 13 10 3
Gelis sp. 2 2 4 1 7 6 1
Gelis sp. 3 1 1 1 0
Gelis sp. 4 1 2 1 4 2 2
Gelis sp. 5 1 1 0 1
Gelis sp. 6 2 2 0 2
Gelis sp. 7 1 1 0 1
* Gnypetomorpha sp. 1 1 1 0
Hemiteles sp. 1 1 0 1
Isdromas sp. 1 1 1 0 1
Isdromas sp. 2 1 1 0 1
Isdromas sp. 3 1 1 0 1
Isdromas sp. 4 1 1 2 0 2
Latosculum sp. 1 1 1 0 1
Latosculum sp. 2 1 1 2 2 0
Latosculum sp. 3 2 2 2 0
* Lysibia sp. 1 1 0 1
Messatoporus sp. 1 1 2 0 2
Orthizema sp. 1 1 1 2 0 2
Orthizema sp. 2 1 1 0 1
Orthizema sp. 3 1 1 11 13 12 1
Phygadeuon sp. 1 2 2 2 0
Phygadeuon sp. 2 2 1 1 4 0 4
Phygadeuon sp. 3 1 1 0 1
Phygadeuon sp. 4 1 1 0 1
Phygadeuon sp. 5 1 1 0 1
Phygadeuon sp. 6 3 3 3 0
Phygadeuon sp. 7 8 1 1 22 32 31 1
* Pleurogyrus sp. 1 1 1 0 1
Pleurogyrus sp. 2 1 1 0 1
* Scrobiculus sp. 1 1 2 4 3 1
Stilpnus sp. 1 4 1 6 6 0
* Tricholinum sp. 1 1 1 0
Phygadeuontini sp. 1 1 2 3 3 0
Phygadeuontini sp. 2 2 2 2 0
Phygadeuontini sp. 3 1 1 0 1
Phygadeuontini sp. 4 1 1 1 0
Phygadeuontini sp. 5 1 1 1 0
Ctenopelmatinae
Asthenara sp. 1 1 1 1 0
Asthenara sp. 2 1 1 1 0
* Lethades sp. 1 1 1 0
Ichneumoninae
Dicaelotus sp. 1 9 7 2 4 22 19 3
Dicaelotus sp. 2 2 1 3 3 0
Ichneumon sp. 1 1 1 1 0
Ichneumon sp. 2 7 7 5 2
Oedicephalus sp. 1 1 1 0
Oreohoplis sp. 2 1 3 2 1
Phaeogenes sp. 1 1 1 1 3 1 2
Phaeogenes sp. 2 7 3 1 11 11 0
Phaeogenes sp. 3 1 1 1 0
Rubicundiella sp. 1 1 1 0
Stenobarichneu sp. 1 1 1 0
Trogomorpha sp. 2 2 0 2
Joppini sp. 2 2 2 0
Phaeogenini sp. 1 1 1 3 1 2
Mesochorinae
Mesochorus sp. 1 2 1 3 2 1
Mesochorus sp. 2 1 1 2 2 0
Mesochorus sp. 3 3 1 4 2 2
Mesochorus sp. 4 3 2 5 2 3
Metopiinae
Hypsicera sp. 1 3 3 3 0
Hypsicera sp. 2 1 1 1 0
Hypsicera sp. 3 2 2 0 2
Exochus sp. 2 2 0 2
Leurus sp. 1 1 1 0
Orthocentrinae
Batakomacrus hidalgo 4 4 0 4
Humala, 2010
Chilocyrtus sp. 1 11 3 14 0 14
Chilocyrtus sp. 2 2 2 0 2
Orthocentrus sp. 1 1 1 1 0
Orthocentrus sp. 2 1 1 1 0
Orthocentrus sp. 3 1 1 1 0
Oxytorinae
Oxytorus sp. 1 1 0 1
Pimplinae
Iseropus hylesiae Kasparyan, 2006 10 10 0 10
Pimpla punicipes Cresson, 1874 3 4 7 2 5
Pimpla sanguipes Cresson (1872) 1 1 0 1
Scambus sp. 1 1 0 1
Tersilochinae
Labilochus brevipalpis 1 1 0 1
Khalaim & Ruíz-Cancino
Sathropterus pumilus 2 2 0 2
Holmgrem, 1860
Tryphoninae
Atopotrophos sp. 1 2 3 1 2
Hercus sp. 1 1 0 1
Netelia sp. 1 1 1 0
Phytodietus sp. 1 1 1 0
Total 147 83 38 193 461 217 244

TFN1* New records for Mexico


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Revista Bio Ciencias, Año 11, vol. 7,  Enero 2020. 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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Revista Bio Ciencias por Universidad Autónoma de Nayarit se encuentra bajo una licencia de Creative Commons Reconocimiento-NoComercial-SinObraDerivada 4.0 Internacional

Fecha de última actualización 18 de Noviembre de 2020

 

licencia de Creative Commons Reconocimiento-NoComercial-SinObraDerivada 4.0 Internacional