First Report of Predation by a Stink Bug on a Walking-Stick Insect with Reflections on Evolutionary Mechanisms for Camouflage

doi:10.21203/rs.2.10812/v1

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First Report of Predation by a Stink Bug on a Walking-Stick Insect with Reflections on Evolutionary Mechanisms for Camouflage

https://doi.org/10.21203/rs.2.10812/v1

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Objective: The stink bug Supputius cincticeps is a well-known neotropical, generalist predator. However, in contrast to other predators, S. cincticeps also need to feed on plants to complete its life cycle. The aim of this report is to describe predation by S. cincticeps on Cladomorphus phyllinus, a walking-stick insect that feeds on leaves of several fruit trees, and is considered one of the largest walk-stick insect species in the Southern Hemisphere. Also a new hypothesis for camouflage is discussed. Results: Suputius cincticeps, recently brought from nature, was accidentally introduced into a colony of C. phyllinus, while feeding them with guava leaves. Once the nymph of S. cincticeps detected the C. phyllinus female it displayed immediately feeding behavior. Both adults and nymphs of C. phyllinus were observed to be predated by S. cincticeps. This new predatory interaction offers a novel evolutionary hypothesis for camouflage based on horizontal transfer of genes a process that might be occurring in nature. Keywords: Phasmatodea, Asopinae, predation, camouflage

Entomology

Phasmatodea

Asopinae

predation

camouflage

The predatory stink bugs (subfamily Asopinae) is the only group of Pentatomidae that needs to feed on other arthropods to complete their life cycle, contrasting with other groups of the family that are mostly phytophagous [1, 2]. Asopinae is considered and recognized as a natural taxon, distributed worldwide and comprising approximately 63 genera and 303 species [3, 4]. Predatory stink bugs are also important tools in biological control: several species are used to control populations of other insects in agricultural systems, reducing need for some pesticides [2, 5, 6].

The predatory stink bug Supputius cincticeps (Stål, 1860) is a well-known, generalist predator that feeds mostly on larvae of Lepidoptera [7] and other insects under lab conditions [8]. However, in contrast to other predators, S. cincticeps also need to feed on plants to complete its life-cycle (R. Brugnera, unpublished data). This insect inhabits several ecosystems, and is widely distributed across the Neotropical region [9]. Supputius cincticeps is considered important in biological control in crops and forests, particularly in Brazil, which has led to detailed studies of its biology, behavior, morphology and reproduction [6, 2, 10].

Cladomorphus phyllinus Gray, 1835 is a walking-stick insect (Order Phasmatodea). The Order includes 13 families, 523 genera and 2.822 species. Of these species, 591 occur in the Neotropical region [11], and more than 200 in Brazil [12]. Cladomorphus phyllinus feeds on leaves of several fruit trees, and is considered one of the largest walk-stick insect species in the Southern Hemisphere, where female can reach 22 cm long [13]. The entire group is little studied [14, 15], particularly the South American species [11].

Presenting a biological cycle of around 280 days from egg to adult, C. phyllinus can be reared under conditions of captivity [16].

In 1917, we captured four females and two males, from secondary fragments of the Atlantic Forest near Petrópolis, Rio de Janeiro, Brazil (22º 30' 18" S; 43º 10' 43" W; 809m); these individuals were used to establish a robust colony of more than 200 individuals. In order to record bionomical aspects, individuals are being kept in captivity. The colonies are being maintained under environmental conditions ranging in temperature from 15-32°C and 65-93% relative humidity. Adult specimens are kept in enclosures housing from 10 to 20 individuals and provided with leaves from Psidium guajava (guava trees) as a primary food source.

The C. phyllinus specimens mentioned in this paper were identified [17, 11] and deposited in the collection Jane Costa & Lima Neiva of the Oswaldo Cruz Institute Entomological Collection , Fiocruz [18, 19].

While providing recently collected guava leaves to one of the colonies, a fifth instar nymph of S. cincticeps was introduced accidentally into the one of the enclosures housing 20 adult female of C. phyllinus. Once the nymph detected an adult female of C. phyllinus, it began immediately to display feeding behavior. It first chose to attempt feeding at the pulvilo, which resulted in the repulsive reaction of the adult female showing some sensitivity, manifested as movements of the leg in a manner for scraping off as irritant (Fig 1A). The S. cincticeps nymph persisted, appeared to succeed at sucking the pulvilo for approximately 3 min. The S. cincticeps nymphmoved to another region of the leg and commenced to feed on the mid-tibia (Fig 1B).

The asopine nymph was then transferred to a small pot together with five first-instar nymphs of C. phyllinus, along with some leaves from Calliandra brevipes Benth,1840, a food source C. phyllinus nymphs. Two days later, S. cincticeps was recorded feeding on C. phyllinus nymphs; S. cincticeps nymph fed upon all five nymphs of C. phyllinus over the succeeding nine days, leaving the completely dry, dead bodies of the C. phyllinus nymphs in the bottom of the pot. The nymph of S. cincticeps did not survive to adulthood: died three days after its last meal, feeding on C. phyllinus first-instar nymphs (Fig 2)

This report is the first to document predation of S. cincticeps on C. phyllinus. Supputius cinctipes is known for its eclectic feeding behavior, attacking a variety of insects. It has been evaluated carefully as a potential candidate for natural control of agricultural pests. This group of insects can also feed on plant sap when insect prey is scarce [20-23]; this alteration in food source, referred to as zoophytophagous behavior, facilitates increased survival of nymphs and extends the longevity and fecundity of adult insects [24, 25]. Some species need plants for completing the developmental cycle. Supputius cincticeps following the rule, dies in the nymphal stage if some vegetal is not available for feeding.

These stink bugs can be phytozoophagous or zoophytophagous: phytozoophagous insects are herbivores that occasionally feed on small insects; and vice versa for zoophytophagous insects [21, 26]. These feeding habits elucidate how pentatomid predators use different food sources as well as ecological and evolutionary changes in feeding [27, 28]. The zoophytophagous S. cincticeps can be an important component of biological control programs of soybean pests, and pests of other beans, and cotton in Brazil [29], especially pest species of Lepidoptera, Coleoptera, Diptera, and Hemiptera [30- 32]. They apparently see improved development and reproduction of zoophytophagous predators when they feed on both plants and insects [33].

Possible mechanisms into how morphological changes arise that provide camouflage to insects for escaping predators have long been discussed [34]. The most prevalent concept is that new morphologies evolved through the traditional combination of germ-line mutations and natural selection [35]. However, one can easily speculate that other mechanisms could be used to generate different camouflage strategies. Give the diverse predatory feeding behavior of S. cincticeps, we propose that the camouflage of C. phyllinus could be facilitated by horizontal or lateral transfer of plant-derived genetic material leading to development of a form resembling a tree stem.

While unprecedented and speculative, a hypothesis based on transfer of genetic material is plausible since the predatory Pentatomidae feed by inserting their stylet into the body of the prey, and injecting toxins, enzymes, or both, before sucking prey tissues [30, 36]. Asopines are known to use the plant juices for producing saliva, which will be used for predation activity [1]. This behavior could also provide a conduit by which to introduce plant genes, or any bacteria or virus that coexists with the plant.

Horizontal transfer of genes was first reported in 1928 [37] and, is now accepted as an important mechanism for evolutionary processes. Horizontal transfer is known to have occurred among prokaryotes [ 38, 39] and the phenomenon appears to have had significance for unicellular eukaryotes as well [40]. Still, the prevalence and importance of horizontal transfer in the evolution of multicellular- eukaryotes remain unclear [41]. Some clear examples have been documented, such aspea aphids (Acyrthosiphon pisum) which have multiple genes from fungi [42]. Plants, fungi, and microorganisms can synthesize carotenoids, but torulene made by pea aphids is the only carotenoid known to be synthesized by an organism in the animal kingdom [43]. Also, HhMAN1, a gene in the genome of the coffee borer beetle (Hypothenemus hampei), resembles bacterial genes, and is thought to be transferred from bacteria in the beetle's gut [44].

Here we report a generalist predator S. cincticeps feeding on C. phyllinus, the latter of which presents a camouflage in the form of an intriguing phenotype, the “walking stick” body form. We propose a novel hypothesis: that the camouflage could have been arisen via of a plant morph gene to the insect genome by an insect vector.

Deep molecular studies at the level of genome sequencing are needed to test this hypothesis opening new models and interesting possibilities in the universe of the genome interactions and dynamics.

Limitations

-The new interaction between a stink bug and a walk-stick insect here reported was not recorded in natural environment. However, S. cincticeps presented its predatory behavior immediately after its accidental introduction in one of the enclosures, housing C. phyllinus specimens.

- The report of the predation by S. cincticeps on C. phyllinus offer a new evolutionary hypothesis on camouflage based on horizontal transfer of genes however, genome sequencing analyses to test this hypothesis are required.

Acknowledgments

We are grateful to Instituto Chico Mendes de Conservação da Biodiversidade for issuing collecting permits. We would like to thank Dr. Andrew Townsend Peterson for reviewing the text and for valuable comments and suggestions; Gustavo de Frontin Werneck for helping the maintenance of the insect colonies; CNPq for financial support.

Authors’ contributions

JC identified walking-stick insect, kept the insect colonies, recorded the predation and wrote the paper. LC reared the insects, wrote the paper. DWPJr wrote the paper. RB and JG identified stink bug and wrote the paper. All authors read and approved the final manuscript.

Funding

JC is recipient for a Research Productivity Fellowship from Brazilian National Council for Scientific and Technological Development.

Availability of data and materials

Studied specimens were deposited at the collection Jane Costa & Lima Neiva of the entomological collection of the Oswaldo Cruz Institute, Fiocruz, Brazil.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Author details

¹Laboratory of Entomological Biodiversity, Oswaldo Cruz Institute, Fiocruz, Av. Brasil, 4365 Manguinhos, Rio de Janeiro, Brasil, Cep 21040-360. ²Center of Technological Development in Health (CDTS)/National Institute of Science and Technology for Innovation on Neglected Diseases (INCT-IDN), FIOCRUZ, Rio of Janeiro, RJ, Brazil . ³Laboratory of Entomology Systematics, Department of Zoology & Graduate Program on Animal Biology, Federal University of Rio Grande do Sul, Brazil.

De Clercq P. Predatory stink bugs (Pentatomidae: Asopinae). In: Capinera JL (ed) Encyclopedia of insects. 2. Kluwer Academic Publishers, Dordrecht. 2008;p3042-5.
Grazia J, Panizzi AR, Greve C, Schwertner CF, Campos LA, Garbelotto TA, Fernandes JAM. Stink Bugs (Pentatomidae) In: Panizzi AR, Grazia J (eds.) True Bugs (Heteroptera) of the Neotropics. Springer, Dordrecht. 2015;p681-756.
Gapud VP. A. generic revision of the subfamily Asopinae, with consideration of its phylogenetic position in the family Pentatomidae and superfamily Pentatomoidea (Hemiptera Heteroptera). Entomol. 1991;8(3):865–961
Rider DA, Schwertner CF, Vilímová J, Rédei D, Kment P, Thomas DB. Higher Systematics of the Pentatomoidea. In: McPherson (Ed.), Invasive Stink Bugs and Related Species (Pentatomoidea). CRC Press. 2018;26:201pp
De Clercq P. Predaceous stink bugs (Pentatomidae: Asopinae). In: Schaefer CW, Panizzi AR. Heteroptera of economic importance. CRC Press, Boca Raton, Florida. 2000;p737-89.
Pires EM, Soares MA, Nogueira RM, Zanuncio JC, Moreira PSA, Oliveira MA. Seven decades of studies with Asopinae predators in Brazil (1930-2014). Biosci J. 2015;31(5):1530–49.
Zanuncio JC, Alves JB, Zanuncio TV, Garcia JF. Hemipterous predators of eucalypt doliator caterpillars. For Eco Menag. 1994;65:65-73.
Zanuncio TV, Zanuncio JC, Vilela EF, Sartório RC. Aspectos biológicos da fase adulta de Supputius cincticeps Stal, 1860 (Hemiptera: Pentatomidae), predador de lagartas desfolhadoras de eucalipto. IPEF. 1992;45:35-9.
Thomas DB. Taxonomic synopsis of the Asopine Pentatomidae (Heteroptera) of the Western Hemisphere. Ann Entomol Soc Am. 1992;16:156p.
Zanuncio JC, Tavares WS, Fernandes BV, Wilcken CF, Zanuncio TV. Production and use of Heteroptera predators for the biological control of Eucalyptus in Brazil. Ekoloji. 2014;23(91):98-104.
Otte D, Brock P. Phasmida species file: catalog of stick and leaf insects of the world.2^th Insect Diversity. J Acad Nat Sci Phila. 2005;414p.
Zompro O, Domenico FC. Catalogue of the type material of Phasmatodea (Insecta) deposited in Brazilian Museums. Iheringia Ser Zool. 2005;95:255-9.
Brock PD. Rearing and studying stick and leaf-insects. Bull Amat Ent Soc. 1992;22:73p.
Bradley JC, Galil BS. The taxonomic arrangement of the Phasmatodea with keys to the subfamilies and tribes. Proc Entomol Soc Wash 1977;79:176-208.
Zompro O. A generic revision of the insect order Phasmatodea: the New World genera of the stick insect subfamily Diapheromeridae: Diapheromerinae = Heteronemiidae: Heteronemiinae sensu Bradley & Galil, 1977. Revue Suisse de Zoologie. 2001;108:189-255.
Alvarenga CD, Souza HR, Giustolin TA, Matrangolo CAR, Silva JF. Biologia de Cladomorphus phyllinus Gray (Phasmatodea: Phasmatidae) em folhas de goiabeira (Psidium guajava) Entomo Brasilis. 2018;11(2):65-9.
Sellick JTC. Descriptive terminology of the phasmid egg capsule, with an extended key to the phasmid genera based on egg structure. Syst 1997;22:97-122.
Costa j, Cerri D Sá MR, Lamas CJE. Coleção Entomológica do Instituto Oswaldo Cruz: resgate do acervo científico-histórico disperso pelo Massacre de Manguinhos. Hist Ciênc Saúde-Manguinhos. 2008;15:401-10.
Cerri D, Coelho C, Felix M, Costa J. O Pavilhão Mourisco e a Coleção Entomológica do Instituto Oswaldo Cruz: conservação preventiva e interdisciplinaridade. Museologia e Patrimônio. 2014;7(2):107-21.
Zeng F, Cohen A C. Comparison ofαamylase and proteinase activities of a zoophytophagous and two phytozoophagous Heteroptera. Biochem. Physiol. A. 2000;126:101-6.
Coll M, Guershon M. Omnivory in terrestrial arthropods: mixing plant and prey diet. Rev. Entomol. 2002;47:267-97.
Sinia A, Roitberg B, Mcgregor RR, Gillespie DR. Prey feeding increases water stress in the omnivorous predator Dicyphus hesperus. Entomol. Exp. Appl. 2004;110:243-8.
Torres JB, Barros EM, Coelho RR, Pimentel RMM. Zoophytophagous pentatomids feeding on plants and implications for biological control. Arthropod-Plant Interactions. 2010;4:219-27
Lambert AM. Effects of prey availability, facultative plant feeding, and plant defenses on a generalist insect predator. Arthropod-Plant Inte. 2007;1:167-73.
Holtz AM, de Almeida GD, Fadini MAM, Zanuncio-Junior JS, Zanuncio TV, Zanuncio JC. Survival and reproduction of Podisus nigrispinus (Heteroptera: Pentatomidae): effects of prey scarcity and plant feeding. Chil J Agr Res. 2010;69:468-72.
Shakya S, Weintraub PG, Coll M. Effect of pollen supplement on intraguild predatory interactions between two omnivores: the importance of spatial dynamics. Biol. Control. 2009;50:281-7.
Guedes BAM, Zanuncio JC, Ramalho FS, Serrão JE. Midgut morphology and enzymes of the obligate zoophytophagous stinkbug Brontocoris tabidus (Signoret, 1863) (Heteroptera: Pentatomidae). Pan-Pac. Entomol. 2007;83:66-74.
Fialho MCQ, Zanuncio JC, Neves CA, Ramalho FS, Serrão JE. Ultrastructure of the digestive cells in the midgut of the predator Brontocoris tabidus (Heteroptera: Pentatomidae) after different feeding periods on prey and plants. Ann. Entomol. Soc. Am. 2009;102:119-27.
Zanuncio JC, Lacerda MC, Junior JSZ, Zanuncio TV, Da Silva AMC, Espindula MC. Fertility table and rate of population growth of the predator Supputius cincticeps (Heteroptera: Pentatomidae) on one plant of Eucalyptus cloeziana in the field. Ann Appl Biol. 2004;144:351-61.
Lemos WP, Zanuncio JC, Serrão JE. Attack behavior of Podisus rostralis (Heteroptera: Pentatomidade) adults on caterpillars of Bombyx mori (Lepidoptera: Bombycidae). Braz Arch Biol Technol.2005;48:975-81.
Lemos WP, Ramalho FS, Serrão JE, Zanuncio JC, Bauce E. Diet affects reproduction and number of oocytes per ovary of the predator Podisus nigrispinus (Dallas) (Heteroptera : Pentatomidae). Animal Biology. 2006;56:279-87.
Silva RB, Corrêa AS,Della Lucia TMC, Pereira IA, Cruz I, Zanuncio JC. Does the aggressiveness of the prey modify the attack behavior of the predator Supputius cincticeps (Stål) (Hemiptera, Pentatomidae)? Rev Bras Entomol 2012;56:244-8.
Zanuncio JC, Lacerda MC, Zanuncio Júnior JS, Silva JS, Zanuncio TV, Silva AMC, Espíndola MC. Fertility table and rate of population growth of the predator Supputius cincticeps (Heteroptera: Pentatomidae) on one plant of Eucalyptus cloeziana in the field. Ann Appl Entomol. 2004;144:357-61.
Stevens M, Merilaita S. Animal camouflage: current issues and new perspectives. Phil Trans Soc B. 2009;364:423-7.
Forbes Dazzled and Deceived: Mimicry and Camouflage Yale University Press.2009;p102-3.
Azevedo DO, Zanuncio JC, Zanuncio JS, Martins GF, Marques-Silva S, Sossai MF, Serrão JE. Biochemical and morphological aspects of salivary glands of the predator Brontocoris tabidus (Heteroptera: Pentatomidae). Braz Arch Biol Technol. 2007;50:469-77.
Griffith F. The Significance of Pneumococcal Types. J Hyg Cambridge Univ Press. 1928;27(2):113-59.
Jain R, Rivera MC, Lake JA. Horizontal gene transfer among genomes: The complexity hypothesis.Proc Natl Acad Sci. 1999;96(7):3801–6.
Lake JA, Rivera Deriving the genomic tree of life in the presence of horizontal gene transfer: conditioned reconstruction. Mol Biol Evol. 2004;21:681-90.
Bapteste E, Susko E, Leigh J, MacLeod D, Charlebois RL, Doolittle WF Do orthologous gene phylogenies really support tree-thinking?.BMC Evol Biol. 2005;5(1):33.
Richardson AO, Palmer JD. Horizontal Gene Transfer in Plants. J Exp Bot.2007;58(1):1-9.
Moran NA, Jarvik T. Lateral Transfer of Genes from Fungi underlies carotenoid production in aphids. 2010;328(5978):624-7.
Fukatsu T. A fungal past to insect color. Science. 2010;328(5978):574-5.
Acuña R, Padilla BE, Flórez-Ramos CP, Rubio JD, Herrera JC, Benavides P, Lee SJ, Yeats TH, Egan AN, Doyle JJ, Rose JK. Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proc Natl Acad Sci. 2012;109(11):4197-202.

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First Report of Predation by a Stink Bug on a Walking-Stick Insect with Reflections on Evolutionary Mechanisms for Camouflage

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Abstract

Figures

Introduction

Materials and Methods

Results

Discussion

Limitations

Declarations

Acknowledgments

Authors’ contributions

Funding

Availability of data and materials

Ethics approval and consent to participate

Consent for publication

Competing interests

Author details

References

Status:

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