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Notes on the predation of an assassin bug by a spider in a Neotropical cave
expand article infoLeopoldo Ferreira de Oliveira Bernardi, Vinícius da Fontoura Sperandei§, Lívia Dorneles Audino|, Carlos Henrique Sena, Jessica Aline Alves#
‡ Programa de Pós-Graduação em Entomologia, Lavras, Brazil
§ Universidade Federal de São João Del Rei, São João del Rei, Brazil
| Biodata Consultoria Ambiental, Lavras, Brazil
¶ Biocenose Consultoria Ambiental, Sete Lagoas, Brazil
# Empresa ILCOM mineração e comércio, Sete Lagoas, Brazil
Open Access

Abstract

Intraguild predation have rarely been documented in scientific literature, even though this type of interaction can affect population dynamics and competition. In this study we present an intraguild predation event that occurred at different times, but in the same cave, where we observed spiders of the species Enoploctenus cyclotorax preying on specimens of assassin bug Zelurus diasi. Inside the studied caves, food resources are scarce and populations can be fairly small in size. It is possible, therefore, that these events are the result of ecological pressures imposed by the hypogean environment.

Keywords

Brazil, intraguild, invertebrates, Zelurus, Enoploctenus

The study of ecological interactions is essential to understand how subterranean communities are assembled, however, few studies addressing this theme have been conducted so far. In the Neotropical region, research that aimed to elucidate the relationships among cave species are even scarcer and little is known about how such interactions can influence the communities present in the hypogean environment (Ferreira and Martins 1999; Bernardi et al. 2010; Souza-Silva and Ferreira 2014; Resende and Bichuette 2016; Vasconcelos et al. 2017). Even more unusual are reports about intraguild predation interactions (Souza-Silva and Ferreira 2014; Resende and Bichuette 2016). Although rare, this type of interaction is potentially important, since it may decrease competition between apex predators, affecting population dynamics more strongly than the commonly observed predation and competition interactions (Polis et al. 1989; Finke and Denno 2006; Moeller et al. 2019). Thus, in this study, we report the occurrence of intraguild predation events involving a spider species (Araneae: Ctenidae: Enoploctenus cyclotorax) (Bertkau 1880) and an assassin bug species (Hemiptera: Reduviidae: Zelurus diasi) (Costa Lima 1940) (Figure 1), in a limestone cave located in the Sete Lagoas municipality, Minas Gerais state, Brazil (Figure 2).

Figure 1. 

Adult specimens of Zelurus diasi (left) and Enoploctenus cyclotorax (right) observed in the study area.

Figure 2. 

Location of the cave where we observed the intraguild predation events in Sete Lagoas, Minas Gerais, Brazil.

We observed the intraguild predation events during a cave fauna monitoring project involving 26 caves near a mining area. We have been monitoring those caves since 2016, visiting each cave seasonally. Six visits have been made so far (September 2016, January 2017, January and June 2018 and May 2019). During data collection, we have sampled the distributions of cave species larger than 1 cm, counting these species through visual sense and spatial plotting individuals on the cave map. The time we spent on the monitoring varied for each cave. Because every cave environment is different and unique, the necessary sampling time may increase or decrease. However, the average sampling time was 12 minutes per 10 m² per cave. The team was always composed by three biologists with experience in cave fauna collection, as recommended by Weinstein and Slaney (1995).

The studied caves are in the area of the Cerrado biome, but in a very anthropized region. The caves are located in a small patch of vegetation, surrounded by planted pastures. The karst relief where the caves are located is part of the Bambuí Group, which consists of gray limestone interspersed with marble and slate. The climate is Humid subtropical climate (Cwa) (Peel et al. 2007) with an annual average temperature of 21.5 °C and the distribution of average rainfall throughout the year for the region is 1328.7 mm, but marked by a conspicuous annual variation (drought and rainy periods) (INMET 2019).

We observed the intraguild predation in one of the studied caves (WGS84 – 19°29'45"S, 44°13'12"W). This cave presents a small underground space with a horizontal projection of 5.2m, volume of 2.2 m3 and area of 5.3 m2. The access to the underground is a small entrance. The main portion of the cave is composed of a single passage that presents a strongly ascending floor, towards the end of the cave. Despite the relatively small size, it is possible to distinguish two zonations inside the cave: (i) entrance, which is photic and (ii) middle/distal portion, which is dysphotic. The entrance of the cave is located approximately one meter above the epigeal floor. Such morphology combined with the cave slope make it difficult for organic matter to enter from the epigean to the hypogean environment. The main organic resource observed inside the cave is mid-sized mammal feces.

We observed intraguild predation events at two different times. The first record was during the dry season, in September 2016, when a female of Enoploctenus cyclotorax was spotted preying on an adult Zelurus diasi (we could not identify the sex because the specimen had the abdomen smashed, probably by the spider). We observed the second eventin January 2017, during the rainy season. In this occasion we found an adult female spider E. cyclotorax preying upon a juvenile Z. diasi (Figure 3).

Figure 3. 

Intraguild predation between female Enoploctenus cyclotorax and adult Zelurus diasi observed during the study.

Zelurus and Enoploctenus are voracious predators with a wide distribution in caves and epigean environment of Brazilian territory (Pinto-da-Rocha 1995; Pellegatti-Franco 2004; Ferreira et al. 2016). Both species have a similar diet, eating a wide variety of invertebrates, such as crickets, cockroaches, scorpions, beetles, velvet worms, wasps, harvestmen and pseudoscorpions (Pellegatti-Franco 2004; Willemart and Pellegatti-Franco 2006; Fischer et al. 2006; Franco 2006; Franco and Monge-Nájera 2016; Grossi et al. 2012; Lira et al. 2016; Stevenson and Stohlgren 2015; Westcott et al. 2016). Intraguild predation is a potentially dangerous strategy, because the prey (in this case, Z. diasi) is also a predator, armed and capable of killing. In addition, some Reduviidae produce a repulsive substance that may deter other predators (Evangelin et al. 2014). However, in the cave environment, the ability to catch and feed on other predators may be an advantageous behavior, since caves are notoriously known for their scarcity of food resources (Poulson and White 1969, Simon et al. 2007). The studied cave is known by its food scarcity and low density of potential prey for the Zelurus and Enoploctenus species, with only a few large-sized invertebrate species observed during the monitoring. During the study, we noticed that the cave where the events of intraguild predation occurred had a reduced number of prey. In this cave, we sampled only two other invertebrate species that could be potential prey for Enoploctenus and Zelurus.

Furthermore, these potential prey species have a body size compatible with other prey used by these species on previous studies. The potential prey are Lepidoptera from the genus Hypena (Noctuidae), which had an observed abundance ranging from 0 to 3 adult individuals. Although juvenile Lepidoptera from this genus are also potential prey of Zelurus, they were observed, but not accounted for the study. We also observed a small number of individuals of Endecous crickets (Phalangopsidae) (zero to one adult) during the visits to the cave. The E. cyclotorax spiders had their abundance ranging between 0 and 2 specimens during the monitoring, and Z. diasi was the only species observed in all six visits, showing an abundance of 4 to 8 individuals during the monitoring. The other species observed in the cave were spiders (Mesabolivar sp., Plato sp. and Isoctenus sp.), ants (Solenopsis sp.), booklice (not identified) and mites (Erythracarus sp.). We considered those invertebrate species as potential preys to Zelurus and Enoploctenus, because we have previously observed these invertebrates’ species being preyed by Zelurus and Enoploctenus in other caves of the same area.

It is noteworthy mentioning that Zelurus is apparently not a frequent prey for spider species. Thus, it may be that they use specimens of this group as a resource only in very specific situations. In the study conducted by Pellegatti-Franco (2004) regarding the feeding behavior of Ctenus fasciatus, several species were offered as prey to this spider. Some of them, such as crickets, cockroaches, small vertebrates and even other spiders were accepted and used as a resource. However, species of the genus Zelurus were not preyed by C. fasciatus spiders.

Even though intraguild predation may be a rare phenomenon, it can be beneficial for predators, for example decreasing competition for prey (Polis et al. 1989). In caves where resource and prey are scarce, this may be an important factor, maintaining the species in that challenging environment. In conclusion, we suggest that unfavourable circustances may have led the spiders to prey upon an unconventional type of prey.

Acknowledgements

We thank to Coordination of Improvement of Higher Level Personnel (CAPES-National Postdoctoral Program) for providing financial support and postdoctoral scholarships to the first author Bernardi LFO. And we are grateful to ILCOM – Mineração Indústria e Comércio for logistic support during field activities.

References

  • Bernardi LFO, Dantas-torres F, Labruna MB, Ferreira RL (2010) Spider preying on ticks in a Brazilian cave. Speleobiology Notes 2: 15–18.
  • Evangelin G, Horne B, Muthupandi M, John WS (2014) Venomous saliva of non-haematophagous reduviid bugs (Heteroptera: Reduviidae): A review. Biolife 2(2): 615–626.
  • Ferreira RL, Martins RP (1999) Trophic structure and natural history of bat guano invertebrate communities, with special reference to Brazilian caves. Tropical Zoology 12(2): 231–252. https://doi.org/10.1080/03946975.1999.10539391
  • Ferreira MIG, Ferreira RL, Gil-Santana HR (2016) The genus Zelurus Hahn, 1826, in Brazilian caves: description of new species and comments on the potential distribution of the genus in South America. Zootaxa 4170(2): 250–270. https://doi.org/10.11646/zootaxa.4170.2.2
  • Fischer ML, Vasconcellos-Neto J, Dos Santos Neto LG (2006) The prey and predators of Loxosceles intermedia (Mello-Leitao 1934) (Araneae, Sicariidae). The Journal of Arachnology 34(2): 485–488. https://doi.org/10.1636/M03-51.1
  • Franco R, Monge-Nájera J (2016) Inverted roles: spider predation upon Neotropical velvet worms (Epiperipatus spp.; Onychophora: Peripatidae). Cuadernos de Investigación UNED 8(2): 171–173. https://doi.org/10.22458/urj.v8i2.1557
  • Grossi PC, Koike RM, Gil-Santana HR (2012) Predation on Leptinopterus Hope species (Coleoptera, Lucanidae) by three species of Reduviidae (Hemiptera, Heteroptera) in the Atlantic Forest, Brazil. EntomoBrasilis 5(2): 88–92. https://doi.org/10.12741/ebrasilis.v5i2.199
  • Lira A, Araújo V, Albuquerque C (2016) Predation of a scorpion (Scorpiones: Buthidae) by an assassin bug (Heteroptera: Reduviidae) in the Brazilian Atlantic Forest. Turkish Journal of Zoology 40(2): 294–296. https://doi.org/10.3906/zoo-1504-27
  • Moeller HV, Neubert MG, Johnson MD (2019) Intraguild predation enables coexistence of competing phytoplankton in a well mixed water column. Ecology 100(12): e02874. https://doi.org/10.1002/ecy.2874
  • Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrology and earth system sciences discussions 4(2): 439–473. https://doi.org/10.5194/hess-11-1633-2007
  • Pellegatti-Franco F (2004) Biologia e ecologia populacional de Ctenus fasciatus (Mello-Leitão) e Enoploctenus cyclothorax (Bertkau) em cavernas do Alto Ribeira, Iporanga, SP (Araneae: Ctenidae). Tese de Doutorado, Instituto de Biociências, Universidade de São Paulo, São Paulo, 141 pp. https://doi.org/10.11606/T.41.2005.tde-21032006-190436
  • Pinto-da-Rocha R (1995) Sinopse da fauna cavernícola do Brasil (1907–1994). Papéis Avulsos de Zoologia 39: 61–172.
  • Simon KS, Pipan T, Culver DC (2007) A conceptual model of the flow and distribution of organic carbon in caves. Journal of Cave and Karst Studies 69(2): 279–284.
  • Souza-Silva M, Ferreira RL (2014) Loxosceles spiders (Araneae: Sicariidae) preying on invertebrates in Brazilian caves. Speleobiology Notes 6: 27–32.
  • Stevenson DJ, Stohlgren KM (2015) Predation on the scorpion Centruroides hentzi (Banks) (Scorpiones: Buthidae) by the assassin bug Microtomus purcis (Drury) (Insecta: Hemiptera: Reduviidae). Southeastern Naturalist 14(1): 1–4. https://doi.org/10.1656/058.014.0101
  • Vasconcelos ACO, Bernardi LFO, Ferreira RL (2017) Uncommon record of a whip spider (Amblypygi: Charinidae) parasitized by a chigger mite (Parasitengona, Trombiculidae: Leeuwenhoekiinae). International Journal of Acarology 43: 343–346. https://doi.org/10.1080/01647954.2017.1317022
  • Weinstein P, Slaney D (1995) Invertebrate faunal survey of Rope Ladder cave, Northern Queensland: a comparative study of sampling methods. Journal of Australian Entomological Society 34: 233–236. https://doi.org/10.1111/j.1440-6055.1995.tb01329.x
  • Westcott RL, Nápoles JR, Jendek E (2016) Two observations of assassin bugs (Hemiptera: Reduviidae) feasting on adult jewel beetles (Coleoptera: Buprestidae), with notes on adults of other buprestid species and their predators. The Coleopterists Bulletin 70(2): 384–387. https://doi.org/10.1649/0010-065X-70.2.384
  • Willemart RH, Kaneto GE (2004) On the natural history of the Neotropical spider Enoploctenus cyclothorax (Araneae, Ctenidae). Bulletin of the British Arachnological Society 13(2): 53–59.
  • Willemart RH, Pellegatti-Franco F (2006) The spider Enoploctenus cyclothorax (Araneae, Ctenidae) avoids preying on the harvestman Mischonyx cuspidatus (Opiliones, Gonyleptidae). The Journal of Arachnology 34(3): 649–653. https://doi.org/10.1636/S05-70.1