Gasteruptiidae (Hymenoptera, Evanioidea) of three savannah phytophysiognomies of the Estação Ecológica do Jataí, in southeastern Brazil, under three sampling methods and a new record for Gasteruption helenae Macedo, 2011

Abstract

In this study, the Gasteruptiidae species found at the Estação Ecológica de Jataí (EEJ), in Luiz Antonio, São Paulo, Brazil, were documented, based on a survey carried out with Malaise, Moericke and light traps that lasted for three years, between January 2007 and December 2009. During the samplings at EEJ, 13 female specimens of Gasteruption Latreille, 1796 were captured: six of G. bispinosum Kieffer, 1904, six of G. brasiliense (Blanchard, 1840) and a single specimen of G. helenae Macedo, 2011 that is the first record for São Paulo state.

Key words
Brazilian savannah; Gasteruption bispinosum; Gasteruption brasiliense; Gasteruption helenae; Neotropical Region

INTRODUCTION

Gasteruptiidae (Hymenoptera: Evanioidea) is a small and distinctive group of parasitic wasps with worldwide distribution (Gauld 2006, Zhao et al. 2012). They are recognized from other wasps by the elongated neck-like propleuron, the highly attached metasoma on the propodeum and the swollen hind tibiae (Zhao et al. 2012, Tan et al. 2016). The family is comprised of about 500 described species, divided in two subfamilies: Gasteruptiinae and Hyptiogastrinae (Crosskey 1953, Jennings & Austin 2002, Gauld 2006, Smith 2006, Macedo 2011).

Macedo (2009) revised the Gasteruptiinae and proposed the division of the subfamily into four genera: the cosmopolitan Gasteruption Latreille, 1796, predominant, with some 400 species, and other three genera restricted to the Neotropical region: Plutofoenus Kieffer, 1911, Trilobitofoenus Macedo, 2009 and Spinolafoenus Macedo, 2009, with seven species in total. The Neotropical fauna of Hyptiogastrinae includes two Pseudofoenus Kieffer species (Jennings & Austin 2002). Macedo (2011) revised the Neotropical fauna of Gasteruption and found 26 species, 10 of them with recorded occurrence for Brazil and five for the state of São Paulo.

Larval instars of Gasteruptiidae act as predator-inquilines in nests of solitary bees including Apidae, Colletidae, Crabronidae, Halictidae, Megachilidae, and Stenotritidae (Jennings & Austin 2004, Zhao et al. 2012); there is no direct evidence for wasps being hosts of Gasteruptiidae (Crosskey 1953, Gauld 1995, Jennings & Austin 1997a, b, 2004).

Very little is known about the hosts of Neotropical Gasteruptiidae, with only four known hosts: Gasteruption brachychaetum Schrottky, 1906 - host: Hylaeus sp. (Hym.: Colletidae) (Macedo et al. 2012), G. floridanum (Bradley, 1908) - hosts: Hylaeus cressoni (Cockerell, 1907) (Hym.: Colletidae) and Trypoxylon frigidum Smith, 1856 (Hym.: Crabronidae) (Walkley 1967), G. kaweahense (Bradley, 1909) - host: Ceratina pacifica Smith, 1907 (Hym.: Apidae) (Daly et al. 1967, Parker & Bohart 1968) and G. visaliae (Bradley, 1909) - host: H. cressoni (Parker & Bohart 1968).

This study aimed to characterize the diversity of Gasteruptiidae collected in areas of riparian vegetation, Brazilian savannah, and savannah woodland vegetation at Estação Ecológica de Jataí (EEJ), to evaluate the collection methods used to catch this group of parasitoids and provide new distribution records.

Knowledge about the composition of the parasitic Hymenoptera fauna in the Cerrado Biome is very important: this environment is one of most threatened by human action in the world. Using comparison of images from the Landsat and CBERS satellites the Brazilian Ministry of the Environment mapped the deforestation in Cerrado between 2002 and 2008 and found that the Cerrado vegetation cover suppressed was 85,074 km², which accounts approximately 14,000 km² deforested annually in that period (Brasil 2009).

This inventory will assist in the provision of subsidies, however modest, for possible conservation strategies for Cerrado biome species, as well as to highlight the importance of conducting research in the few natural areas of the Cerrado Biome that still exist in the State of São Paulo.

MATERIALS AND METHODS

The studied specimens were collected in samplings occurred between January 2007 and December 2009 at EEJ, an environmental preservation area, which has 9,074 ha and is located in the municipality of Luiz Antônio, São Paulo State, Brazil. Habitats of the EEJ include dry mesophytic semideciduous forest and the Brazilian savannah (Kronka et al. 2005); remnants of Eucalyptus sp. and Pinus sp. cultivars; and aquatic habitats located near Mogi-Guaçu River. The climate is Köpen AW type (tropical with wet summers and dry winters) and the total annual rainfall of 1,433 mm is concentrated between November and April; the mean annual temperature is 21.7°C (Cavalheiro et al. 1990).

Sampling of Hymenoptera was performed every two weeks between December 2006 and November 2009 as described in Versuti et al. (2014).

In the laboratory, Gasteruptiidae were separated from other Hymenoptera and stored in plastic vials with 70% ethanol and later air dried, mounted on entomological pins and labeled.

The specific identifications of the studied specimens were made by A.C.C. Macedo.

Images were taken using a digital camera Leica MC170 HD attached to a stereomicroscope Leica M205C APO and specimens illuminated with high diffuse dome illumination Leica LED5000 HDI. Focus stacking of images was done using Helicon Focus (version 5.3). The figures were prepared using Adobe Photoshop (version 11.0).

The voucher specimens examined in this study have been deposited in the Coleção Entomológica do Laboratório de Sistemática e Bioecologia de Parasitoides e Predadores (LRRP# 2695-2703, 5305-5308), of the Instituto Biológico / Ribeirão Preto (Ribeirão Preto, SP, Brazil), N.W. Perioto, curator. The collections were done under a Brazilian Biodiversity Information and Authorization System (SISBIO) license# 16473-1.

Examined material

Gasteruption bispinosum

Kieffer, 1904

Figure 1

Figure 1
Gasteruption bispinosum Kieffer, 1904, habitus. Scale bar = 2 mm.

Brasil, SP, Luiz Antonio, Est. Ecológica de Jataí, 21°37ʹ23,7ʺS / 47°48ʹ27,8ʺW, Mata ciliar, arm. Malaise, 7/XI/2007, 10/XII/2008, 16/IX/2009, NW Perioto e equipe, cols., LRRP# 2695, 2697, 2696, 3♀ (LRRP); same data except 21°36ʹ47ʺS / 47°49ʹ04ʺW, arm. luminosa, 23/XII/2008, 28/I/2009, LRRP# 2698, 2699, 2♀ (LRRP); same data except 21°36ʹ11,6ʺS / 47°46ʹ10,1ʺW, Cerradão, 11/X/2007, LRRP# 2701, 1♀ (LRRP).

Gasteruption brasiliense

(Blanchard, 1840)

Figure 2

Figure 2
Gasteruption brasiliense (Blanchard, 1840), habitus. Scale bar = 2 mm.

Brasil, SP, Luiz Antonio, Est. Ecológica de Jataí, 21°35ʹ17,7ʺS / 47°47ʹ28,2ʺW, Cerrado, arm. Malaise, 5/XII/2007, 15/X/2009, NW Perioto e equipe, cols., LRRP# 2702, 2703, 2♀ (LRRP); same data except 21°36ʹ47,0ʺS / 47°49ʹ04,0ʺW, Mata ciliar, arm. luminosa, 19/XII/2007, LRRP# 5305, 5306, 5307, 3♀ (LRRP) and 15/IV/2009, LRRP# 5308, 1♀ (LRRP).

Gasteruption helenae

Macedo, 2011

Figure 3

Figure 3
Gasteruption helenae Macedo, 2011, habitus. Scale bar = 2 mm.

Brasil, SP, Luiz Antonio, Est. Ecológica de Jataí, 21°35ʹ17,7ʺS / 47°47ʹ28,2ʺW, Cerrado, arm. Malaise, 5/XII/2007, NW Perioto e equipe, cols.; LRRP# 2700, 1♀ (LRRP).

RESULTS AND DISCUSSION

Gasteruptiidae is occasionally collected on insect surveys with Malaise traps but, in several studies carried out in Brazil in areas of Atlantic Forest (Azevedo et al. 2002, 2003, Perioto & Lara 2003, Perioto et al. 2005, Sobczak & Vasconcelos Neto 2015, among others), Brazilian savannah (Perioto et al. 2008, Lara et al. 2015) and in cultivated areas (Klesener et al. 2013) none of these insects were obtained.

In this study, carried out at EEJ, a large sampling effort was employed to capture parasitic Hymenoptera: a. 6,570 trap-days with Malaise traps, divided into 2,190 trap-days in each one of the three studied environments - Brazilian savannah, savannah woodland vegetation and riparian vegetation; b. 6,570 trap-days with Moericke traps, divided into 730 trap-days in Brazilian savannah and savannah woodland vegetation, respectively, and 2,190 trap-days in riparian vegetation and, c. 624 trap-days with a light trap in riparian vegetation, totaling an effort of 10,844 trap-days.

During the three years of sampling at EEJ only 13 (all female) specimens of Gasteruption were obtained: six of G. bispinosum Kieffer, 1904, six of G. brasiliense (Blanchard, 1840) and a single specimen of G. helenae Macedo, 2011 (Table I. The fact that all Gasteruptiidae obtained were collected between September and January allows us to infer that, at the EEJ, the highest frequency of Gasteruptiidae occurs in the hottest and humid months of the year.

Table I
Species of Gasteruption Latreille, 1796 obtained at the Estação Ecológica de Jataí between January 2007 and December 2009: number of specimens per environment, trap used, and sample effort in trap-days.

Species of Gasteruption	n	Environment	Trap	Sampling effort (in trap-days)
G. bispinosum Kieffer, 1904	1	savannah woodland vegetation	Malaise	2190
G. bispinosum Kieffer, 1904	3	riparian vegetation	Malaise	730
G. bispinosum Kieffer, 1904	2	riparian vegetation	light trap	312
G. brasiliense (Blanchard, 1840)	2	Brazilian savannah	Malaise	1095
G. brasiliense (Blanchard, 1840)	4	riparian vegetation	light trap	156
G. helenae Macedo, 2011	1	Brazilian savannah	Malaise	2190

The small number of specimens collected precludes more sophisticated analyzes of abundance and population fluctuation. The reasons that lead to this small catch rate are unknown and factors such their development in small populations and/or the low efficiency of the traps used should be taken into account.

Of the six specimens of G. bispinosum captured, five were obtained from the riparian forest and one from the savannah woodland vegetation; four of them were collected with Malaise traps and two with light traps. Of the six specimens of G. brasiliense captured, four were obtained from the riparian forest, all of them with light traps, and two from the Brazilian savannah, with Malaise traps. The only specimen of G. helenae was obtained from Brazilian savannah and was captured with Malaise traps (Table I). No one Gasteruptiidae was captured with Moericke traps.

Almost 50% of the specimens of Gasteruptiidae obtained were captured with light traps (Table I); such fact indicates that the use of this colection artifact, unusual for the capture of this group of insects, can increase the availability of these insects in collections; also indicates the necessity of future studies on the behavior of such insects since it is presumed that they have diurnal habits.

Gasteruption bispinosum and G. brasiliense (Blanchard, 1840) have known occurrences for the State of São Paulo (Macedo 2011). Gasteruption helenae is now mentioned by the first time for that state, so this study extends its range about 1,700 km northeast, 2,200 km southwest and 470 km northeast in Entre Rios (Argentina), La Paz (Bolivia) and Curitiba (Brazil), respectively, the previous records (Figure 4).

Figure 4
Map indicating the known occurrences of Gasteruption helenae Macedo, 2011 (black dots with white marks) and the new record of distribution (black dot with red mark). TC = Tropic of Capricorn.

ACKNOWLEGMENTS

We thank to Instituto Nacional de Ciência e Tecnologia dos Hymenoptera Parasitoides (CNPq/Fapesp/Capes) for the financial support and to the anonymous reviewers for their critical reading.

REFERENCES

• AZEVEDO CO, CORRÊA MS, GOBBI FT, KAWADA R, LANES GO, MOREIRA AR, REDIGHIERI ES, SANTOS LM & WAICHERT C. 2003. Perfil das famílias de vespas parasitoides (Hymenoptera) em uma área de Mata Atlântica da Estação Biológica de Santa Lúcia, Santa Tereza, ES, Brasil. Bol Mus Biol Mello Leitão 16: 39-46.
• AZEVEDO CO, KAWADA R, TAVARES MT & PERIOTO NW. 2002. Perfil da fauna de himenópteros parasitóides (Insecta, Hymenoptera) em uma área de Mata Atlântica do Parque Estadual da Fonte Grande, Vitória, ES, Brasil. Rev Bras Entomol 46: 133-137.
• BRASIL. 2009. Ministry of Environment. Brazilian Forest Service. Brazilian forests at a glance. Reference period: 2005-2009. Brasília: Ministério do Meio Ambiente, 120 p.
• CAVALEIRO F ET AL. 1990. Propostas preliminares referentes ao plano de zoneamento e manejo da Estação Ecológica do Jataí. Acta Limnol Bras 3: 951-968.
• CROSSKEY RW. 1953. A revision of the genus Hyptiogaster Kieffer (Hymenoptera: Gasteruptionidae), with descriptions of two new genera and three new species. Trans R Entomol Soc Lond 104: 347-384.
• DALY HV, STAGE GI & BROWN T. 1967. Natural enemies of bees of the genus Ceratina (Hymenoptera: Apoidea). Ann Entomol Soc Am 60: 1273-1282.
• GAULD ID. 1995. The evaniomorph parasitoid families. Gasteruptiidae. In: Hanson PE and Gauld ID (Eds). The Hymenoptera of Costa Rica, Oxford, New York, London: Oxford University Press, p. 193-195.
• GAULD ID. 2006. Familia Gasteruptiidae. In: Hanson PE and Gauld ID (Eds), Hymenoptera de la Región Neotropical, Gainesville: The American Entomological Institute, p. 221-223.
• JENNINGS JT & AUSTIN AD. 1997a. Revision of the Australian endemic genus Hyptiogaster Kieffer (Hymenoptera: Gasteruptiidae), with descriptions of seven new species. J Nat Hist 31: 1533-1562.
• JENNINGS JT & AUSTIN AD. 1997b. Revision of Aulacofoenus Kieffer (Hymenoptera: Gasteruptiidae), hyptiogastrine wasps with a restricted Gondwanic distribution. Invertebr Taxon 11: 943-976.
• JENNINGS JT & AUSTIN AD. 2002. Systematics and distribution of world hyptiogastrine wasps (Hymenoptera: Gasteruptiidae). Invertebr Syst 16: 735-811.
• JENNINGS JT & AUSTIN AD. 2004. Biology and host relationships of aulacid and gasteruptiid wasps (Hymenoptera: Evanioidea): a review. In: Rajmohana K, Sudheer K, Kumar PG and Santhosh S (Eds). Perspectives on Biosystematics and Biodiversity, Kerala: University of Calicut, Systematic Entomology Research Scholars Association, p. 187-215.
• KLESENER DF, SANTOS RSS & MENEZES JR AO. 2013. Diversidade e atividade de voo de himenópteros parasitóides em pomar de macieira em Vacaria, RS. EntomoBrasilis 6: 108-112.
• KRONKA FJN, NALON MA & MATSUKUMA CK. 2005. Inventário florestal da vegetação natural do Estado de São Paulo, São Paulo: Secretaria do Meio Ambiente/Instituto Florestal, Imprensa Oficial, 200 p.
• LARA RIR, FERNANDES DRR, VERSUTI DR, TANGO MFA & PERIOTO NW. 2015. Sampling and diversity of Hymenoptera (Insecta) in an orange orchard/Brazilian savannah fragment interface. EntomoBrasilis 8: 51-57.
• MACEDO ACC. 2009. Generic classification for the Gasteruptiinae (Hymenoptera: Gasteruptiidae) based on a cladistic analysis, with the description of two new Neotropical genera and the revalidation of Plutofoenus Kieffer. Zootaxa 2075: 1-32.
• MACEDO ACC. 2011. A revision of Gasteruption Latreille (Hymenoptera: Gasteruptiidae) in the Neotropical Region. Zootaxa 3030: 1-62.
• MACEDO ACC, CORDEIRO GD & ALVES-DOS-SANTOS I. 2012. Entering behavior of Gasteruption brachychaetum Schrottky (Hymenoptera, Gasteruptiidae) into a nest of Hylaeus Fabricius (Hymenoptera, Colletidae). Rev Bras Entomol 56: 325-328.
• PARKER FD & BOHART RM. 1968. Host-parasite associations in some twig-nesting Hymenoptera from western North America. Part II. Pan-Pac Entomol 44: 1-6.
• PERIOTO NW & LARA RIR. 2003. Himenópteros parasitoides (Insecta: Hymenoptera) da Mata Atlântica. I. Parque Estadual da Serra do Mar, Ubatuba, SP, Brasil. Arq Inst Biol 70: 441-445.
• PERIOTO NW, LARA RIR & SELEGATTO A. 2005. Himenópteros parasitoides da Mata Atlântica. II. Núcleo Grajaúna, Rio Verde da Estação Ecológica Juréia-Itatins, Iguape, SP, Brasil. Arq Inst Biol 72: 81-85.
• PERIOTO NW, LARA RIR, VACARI AM, FAVORETO L, MIRANDA NF, CHAGAS FILHO NR & PESSOA R. 2008. Diversidade de himenópteros parasitoides (Hymenoptera) na Estação Ecológica de Jataí, Luiz Antônio, SP, Brasil. Rev Agric 83: 125-135.
• SMITH DR. 2006. Familia Gasteruptiidae. In: Fernándes F and Sharkey MJ (Eds). Introduccíon a los Hymenoptera de la Región Neotropical, Bogotá D.C.: Sociedad Colombiana de Entomologia y Universidad Nacional de Colombia, p. 807-809.
• SOBCZAK JF & VASCONCELLOS NETO J. 2015. Famílias de himenópteros parasitoides na Serra do Japi, Jundiaí, São Paulo, Brasil. Arq Inst Biol 82: 1-4.
• TAN JL, ACHTERBERG C VAN & TAN QQC. 2016. Four new species of Gasteruption Latreille from NW China, with an illustrated key to the species from Palaearctic China (Hymenoptera, Gasteruptiidae). ZooKeys 612: 51-112.
• VERSUTI DR, PAZ CCP, LARA RIR, FERNANDES DRR & PERIOTO NW. 2014. Comparative abundance and diversity of Dryininae (Hymenoptera, Dryinidae) in three savannah phytophysiognomies in southeastern Brazil, under three sampling methods. Rev Bras Entomol 58: 273-279.
• WALKLEY LM. 1967. Evanioidea. In: Krombein KV and Burks BD (Eds). Hymenoptera of America North of Mexico, Synoptic Catalog (Agriculture Monograph No. 2) Second Supplement. Washington, DC: United States Government Printing Office, p. 284-285.
• ZHAO KX, ACHTERBERG CV & XU ZF. 2012. A revision of the Chinese Gasteruptiidae (Hymenoptera, Evanioidea). ZooKeys 237: 1-123.

Publication Dates

• Publication in this collection
  28 Oct 2020
• Date of issue
  2020

History

• Received
  10 Oct 2018
• Accepted
  17 Dec 2018