Diapriinae Wasps (Hymenoptera: Diaprioidea: Diapriidae) Associated with Ants (Hymenoptera: Formicidae) in Argentina

We provide an overview of diapriid wasps associated with ants in Argentina and the diversity of interactions they have developed with their hosts. As a result, we report 16 species of nine genera of Diapriinae, two new geographic distributions, three new association records, illustrations, and photographs.We highlightmyrmecophile symphylic species, with a high degree of integration with the host ants, adaptation being morphological and behavioral. A table with diapriid species and ant hosts is given.


Introduction
Diapriids are primary endoparasitoids of larvae-pupae or pupae, principally of dipterans, but a number of species are closely associated with ant nests.However, there are few behavioral data on host-diapriid myrmecophile interactions.Huggert and Masner [1] hypothesized that the ancestors of diapriines guests changed from Diptera to Formicidae.The intermediates in the presumed sequence of hosts seem to be the numerous synoeketic Diptera living in the refuse depot and bivouacs of various army ants of the subfamily Ecitoninae.Diapriines females, in the search for potential hosts, would have progressively integrated with formicids.According to Masner (personal communication) this change would have occurred more frequently in the Neotropical region where these ants have high distribution.The guests switch mechanism has determined morphological and behavioral specialization, manifested by the degree of integration of diapriines to ant colonies.These symphyles are often highly adapted to their hosts, exhibiting morphological and behavioral adaptations to living with ants (extensive morphological mimicry of the host ants coloration, ocellus regression, similar sculpture, presence of appeasement substances in specialized structures and trichomes, trophallaxis, etc.), which aid them in avoiding detection and/or aggression by host ants.Ants seem to have preference to lick certain parts of diapriid body to get exudates [2].The adaptations include secondary apterism in which the wings of wasps are bitten off by either the parasite itself or its host.During the alate phase, the adults probably disperse, as the alate individuals, caught by sweeping, in Malaise traps and significantly by light traps indicating also the nocturnal activity in this phase of life [2].The secondary apterism occurs in several species of diapriines, for example, Asolenopsia rufa Kieffer, Bruchopria pentatoma Kieffer, Bruchopria hexatoma Kieffer, Notoxoides pronotalis (Borgmeier), herein studied.
The current knowledge indicates that only a few diapriids are parasitoids of ant brood, attacking as solitary or gregarious koinobiont endoparasitoids of the host larvae, and worker and/or reproductive immature stages can be parasitized.From 121 diapriine species in 34 genera that had been collected in association with ants, development of immature stages as parasitoids of ant larvae has been demonstrated for only 26 species in seven genera, most of which are only known at the level of morphospecies [3].There are only two species and one morphospecies recorded in Argentina as ant parasitoids [4].
A large number of diapriine wasps became associated with various groups of ants in Central and South America.

Psyche
The associations are especially well developed with army ants (Ecitonini) and leaf cutting ants (Attini) with some 20 genera of Diapriinae already involved [5].The vast majority of these species belong to Diapriini, although there are some exceptions like Bruchopria species that belong to the tribe Spilomicrini [6].
The New World fungus-growing ants (Hymenoptera: Formicidae: Attini) are especially diverse in the tropics.As true for the most social insects, they accumulate significant stores of resources within their nests, attracting a diverse array of predators, microbial pathogens, and parasites [7].We studied aspects of the intensity and prevalence of these littleknown diapriine wasps that attack the larvae of the fungusgrowing ant, Acromyrmex lobicornis Emery, and noted a remarkably diverse community of parasitoids within host population from four localities of La Pampa, Argentina [4,8].In some cases, the rates of parasitoidism can reach high levels.Loiácono et al. [4] collected 1560 wasps (adults and immatures) from 430 parasitized larvae from three partial colonies of Acromyrmex, which shows how prevalent these wasps can be in attacking the ants.Fernández-Marin et al. [9] found that between 27% and 70% of the colonies of two species of Cyphomyrmex Mayr were parasitized by one species in Puerto Rico and by up to four concurrent morphospecies of diapriids in Panama.Similarly, Pérez-Ortega et al. [7] reported that another fungus-growing ant, Trachymyrmex cf.zeteki, was attacked by a diverse community of diapriids in Panama, with a mean intensity of larval parasitism per ant colony of 33.9%, and prevalence across all ant populations of 27.2%.Lachaud and Pérez Lachaud [3], based on the abundance and success in attacking ants, considered that diapriids and another group of microhymenopterans, the eucharitids, seem excellent potential models to explore how parasitoids impact ant colony demography, population biology, and ant community structure [3].
In this paper, we provide an overview of the diversity of diapriid wasps associated with ants in Argentina and the diversity of interactions they have developed with their hosts.

Material and Methods
Specimens for this study were reared in laboratory [4] or collected from ant nests, killed in alcohol, and mounted on cards or microscopic slides for further studies.Observations of the specimens were made through a stereomicroscope Leica S8APO.The photographs were taken by Daniel A. Aquino with a Leica DFC295 camera attached to the stereomicroscope.Digital images were mounted using open software CombineZM [30] and enhanced using Photoshop.Scanning micrographs were taken with a JEOL JSMT100 at Museo de La Plata operating at 15 KV.
Sharkey [31] was followed for the higher-level phylogeny of the Hymenoptera order, Bolton for ant valid names [32], Masner and García [5] for diapriid systematics, and Yoder et al. web site [33] for interactive keys and links.
Diapriid and ant specimens examined in this study are deposited at Museo de La Plata (Buenos Aires, Argentina).Most of them were collected and determined by Bruch and Ogloblin in Argentina.Type material of Szelenyiopria reinchenspergeri (Ferrière) was loan by Hungarian Natural History Museum.
Distribution.Tropical lowlands of Central and South America [5].
Distribution.The genus is well represented in North and South America, rarely in Chile [5].
Biology.Several species were reared from various dipterous hosts, and some were collected in ant nests [5].

Basalys sp.
Material Studied.One female and 1 male (microscopic slide) collected with the "Argentine ant, " Linepithema humile (Mayr), Argentina, Buenos Aires, J. C.  but he did not describe it.We also considered that material studied belong to genus Basalys, as it was established by Masner.
Distribution.Doliopria is restricted to the New World, with only a few species in the Nearctic region and with a high number of undescribed species in tropical America [5].
Biology.Associated with attini ants Acromyrmex lundii (Guérin-Méneville) [12] (Figure 3  Distribution.Restricted to lowland rainforests of continental South America [5]. Biology.Members of Notoxoides display some of the most advanced associations with ants.So far, ants of genera Neivamyrmex and Eciton (Ecitonini) were recorded as hosts [19].Adult wasps are frequently collected in light traps.Wings may be lost to typical alectomy as indicated by shriveled wing rudiments in some specimens [5].
Biology.Associated with Eciton dulcium Forel and Neivamyrmex sulcatus (Mayr) [44].Remarks.Bruch always sent to Kieffer diapriid samples to be studied.As we mentioned, he was an excellent scientific illustrator (Figure 5) [46] and an important photographer as is shown in (Figure 6) Neivamyrmex pseudops, ant host of Notoxoides pedisequus [47].We observed numerous both alate and dealate individuals found dependent on the phase of life.As is mentioned [2], during the alate phase, numerous adults were caught by light traps as we observed in the female material light collected by Bruch.
Lachaud [48] mentioned that ants search actively for some chemical substances produced by glands at the basis of the setae present on the diapriid cuticle; similarly we observed the presence of peculiar neck hairs in N. pronotalis [20].Fabritius, 1974 [49].Szelenyiopria Fabritius, 1974: 54 [49].
Biology.Szelenyiopria lucens (Loiácono) from Uruguay is the first member of the tribe Diapriini in the New World positively reared from ants.Loiácono [21] reports up to three wasps per mature larva of Acromyrmex ambiguus (Emery) (Attini).Members of Szelenyiopria show no specialized structures known among other myrmecophilic Diapriini; Masner and García [5] assumed that the specialized setae with truncate apices are outlet of chemical substances.
Material Studied.One female, Argentina, Salta, 2-6-II-1950, Golbach coll.Remarks.Most females of this genus have 11-segmented antennae, but material studied here presents antenna 12segmented as mentioned by Masner and García [5] for undescribed species.We considered that these specimens belong to Szelenyiopria genus by the most important feature, the presence on entire body of specialized straight setae, truncate apically.
Remarks.Hölldobler and Wilson [54] mentioned specimens of genus Bruchopria, as Solenopsis guest.Masner and García [5] mentioned "wings often bitten off by ants." Loiácono et al. [26] studied alated and dealated individuals of Bruchopria species.The action of dealation has not been observed.The presence of tegulae with normal development and wing stumps demonstrates that the apterism has a secondary origin, caused by the autotomy or by bites of the host ants.The apices of the wing stumps of all individuals examined were regular suggesting that the wings are bitten or torn off close to the tegulae.The fact that specimens are dealated allows them to move into the mound galleries and chambers.Kieffer, 1921 [12] (Figures 9(a), 10(a), and 10(b)) .Bruchopria hexatoma Kieffer, 1921: 39 [12].Bruchopria hexatoma : Borgmeier, 1939: 543 [44].
Distribution.The genus is distributed in the New World [5].

Psyche
Biology.Primary parasitoidism solitary and gregarious of various Diptera; few species were reared from Coleoptera [5].Herein, we studied samples associated with a Solenopsidini ant.

Discussion
The knowledge of the biology and behavior of these myrmecophilic diapriids and the nature of their interactions with ants has progressed in Argentina since 1980 [63] to present.There are nine genera recorded from Argentina, which represents about 50% of the genera mentioned by Masner and García [5] from the New World.
The study of Diapriidae Collection housed at División Entomología of Museo de La Plata, which includes Bruch and Ogloblin myrmecophilic diapriid specimens, allowed us to report 16 species of nine genera of Diapriinae associated with ants in Argentina.It is interesting to highlight that Asolenopsia rufa, Notoxoides pronotalis, Bruchopria pentatoma, and B. hexatoma are the species with a high degree of integration with the host ants, adaptation being both morphological and behavioral.
We mentioned for the first time the associations between the "argentine ant, " Linepithema humile, and both Basalys sp. and Trichopria sp., Pentapria cf.nodicornis and Solenopsis saevissima, and Spilomicrus sp. and Solenopsidini ant.
Doliopria myrmecobia is a new record to Misiones.The only described species of Szelenyiopria occurs in La Pampa province, S. pampeana; an undescribed species is known to us from Córdoba.
We considered that Szelenyiopria pampeana and Trichopria formicans parasitoids of Acromyrmex species in Argentina seem excellent potential models to explore how parasitoids impact ant colony demography, population biology, and ant community structure.
) and 10(b)), and most of them are accompanied by the host ants (Figure9(b)).Unfortunately, the types of the species