Skip to main content
SpringerLink
Log in

Modeling population dynamics of yeast-like symbionts (Ascomycota: Pyrenomycetes: Clavicipitaceae) of the planthopper Delphacodes kuscheli (Hemiptera: Delphacidae)

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Delphacodes kuscheli establish mutualistic relationship with yeast-like symbionts (YLS) that live in the fat body and are necessary for host survival and reproduction. We estimated for a host of age t, its body weight, W(t), and the number of YLS per host, YLS(t). The host body weight was calculated as: W(t) = Lm/[1+ e (d–kt)], (Lm = the maximum observed weight, and d and k are constants), and the fat body was considered a fixed proportion of W(t). We calculated the number of YLS per unit host body mass: α(t) = YLS(t)/W(t). We also calculated the number of YLS per host, cYLS(t), and analyzed the pattern of variation in both sexes adapting the expression of the logistic model: cYLS(t) = KNoert/K+(ert -1)No, (No = initial number of YLS, r = intrinsic per capita rate of natural increase, and K = variable carrying capacity). In females the carrying capacity varied according to a constant proportion of the host’s weight: K(t) = αW(t). In males α(t) was considered a decreasing function of the host age: K(t) = α(t)W(t). The coefficients No, α, and r were subjected to parameterization. We found that the patterns of W(t) and YLS(t) of D. kuscheli were similar to other planthoppers. In females YLS increased up to the adult stage and then remained almost constant, varying similarly to individual weight. In males YLS increased up to the 5th instar nymph as the individual weight did, but the number of YLS decreased in the adult stage and the correlation was not so good. The calculated number of YLS per host matches reasonably well with the number estimated experimentally both in females and males. This is the first study that quantified and modeled the dynamics of YLS endosymbionts in a Neotropical planthopper pest. The models will be used in future studies for better understand the experimental reduction of YLS in young nymphal stages.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baumman P (2005) Biology of bacteryocites-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189

    Article  Google Scholar 

  • Boito GT, Ornaghi JA (2008) Rol de los cereales de invierno y su sistema de manejo en la dinámica poblacional de Delphacodes kuscheli, insecto vector del MRCV. Agriscientia 25:17–26

    Google Scholar 

  • Brentassi ME (2004) Estudio de la interacción planta-insecto. Comportamiento alimentario del vector del Mal de Río Cuarto del maíz, Delphacodes kuscheli Fennah (Insecta: Hemiptera: Delphacidae). Doctoral thesis. La Plata, Argentina: Universidad Nacional de La Plata.

  • Brentassi ME, Remes Lenicov A (2007) Feeding behavior of the vector Delphacodes kuscheli (Hemiptera: Fulgoromorpha: Delphacidae) on maize and oat. Ann Soc Entomol Fr 43:205–212

    Google Scholar 

  • Brentassi ME, Liljhestrom G, Remes Lenicov A (2010) Endosimbiontes obligados (yeast like symbiotes) de Delphacodes kuscheli (Hemiptera: Delphacidae), vector del Mal de Río Cuarto del maíz en Argentina. Cuantificación y caracterización morfológica. Rev Argent Microbiol 42(s1):222

    Google Scholar 

  • Brentassi ME, de la Fuente D, Lameiro A (2014) Localización y caracterización morfológica de endosimbiontes obligados de Delphacodes kuscheli y Dalbulus maidis, dos especies de chicharritas vectoras de enfermedades del cultivo de maíz en Argentina (Hemiptera: Auchenorryncha). Rev Cien Morfol Soc Cien Morfol La Plata 16(s1):1–7

    Google Scholar 

  • Buchner P (1965) Endosymbiosis of animals with plant microorganisms interscience. Publishers, New York

    Google Scholar 

  • Bush AO, Holmes JC (1986) Intestinal parasites of lesser scaup ducks: patterns and associations. Can J Zool 64:132–141

    Article  Google Scholar 

  • Chen Y (2009) Variation in planthopper rice variation in planthopper-rice interactions: possible interactions among three species? In: Heong KL, Hardy B (eds) Planthoppers: new threats to the sustainability of intensive rice production system in Asia. International Rice Research Institute, Los Baños, Philippines, pp 315–326

    Google Scholar 

  • Chen CC, Cheng LL, Kuan CC, Hou RF (1981a) Studies on the intracellular yeast like symbiote in the brown planthopper, Nilparvata lugens (Stål) I Histological observations and population changes of the symbiote. Z Angew Entomol 91:321–327

    Article  Google Scholar 

  • Chen CC, Cheng LL, Hou RF (1981b) Studies on the intracellular yeast like symbiote in the brown planthopper. Nilaparvata lugens (Stål) II. Effects of antibiotics and elevated temperature on the symbiotes and their host. J Appl Entomol 92:440–449

    Google Scholar 

  • Cheng DJ, Hou RF (2001) Histological observations on transovarial transmission of a yeast-like symbiote in Nilaparvata lugens Stål (Homoptera: Delphacidae). Tissue Cell 33:273–279

    Article  CAS  PubMed  Google Scholar 

  • Costamagna A, Remes Lenicov A, Zanelli M (2005) Maize and oat antixenosis and antibiosis against Delphacodes kuscheli (Homoptera: Delphacidae), vector of “Mal de Río Cuarto” of maize in Argentina. J Econ Entomol 98:1374–1381

    Article  CAS  PubMed  Google Scholar 

  • Day NE (1966) Fitting curves to longitudinal data. Biometrics 22:276–291

    Article  CAS  PubMed  Google Scholar 

  • Dean RL, Collins JV, Locke M (1985) Structure of the fat body. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Pergamon, New York, pp 155–210

    Google Scholar 

  • Denno RF, Roderick GK (1990) Population biology of planthoppers. Annu Rev Entomol 35:489–520

    Article  Google Scholar 

  • Douglas E (1998) Nutritional interactions in insect–microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37

    Article  CAS  PubMed  Google Scholar 

  • Ferrater JB, De Jong PW, Dicke M, Chen YH, Horgan FG (2013) Symbiont-mediated adaptation by planthoppers and leafhoppers to resistant rice varieties. Arthropod Plant Interact 7:591–605

    Article  Google Scholar 

  • Ferrater JB, Naredo AI, Almazan MLP, De Jong PW, Dicke M, Horgan FG (2015) Varied responses by yeast-like symbionts during virulence adaptation in a monophagous phloem-feeding insect. Arthropod Plant Interact 9:215–224

    Article  Google Scholar 

  • Fukatsu T, Ishikawa H (1992) Soldier and male of an eusocial aphid Colophina arma lack endosymbiont: implications for physiological and evolutionary interaction between host and symbiont. J Insect Physiol 38:1033–1042

    Article  Google Scholar 

  • Haefner JW (1996) Modeling biological systems. Principles and applications, New York, USA

    Book  Google Scholar 

  • Hongoh Y, Ishikawa H (1997) Uric acid as a nitrogen resource for the brown planthopper, Nilaparvata lugens: Studies with synthetic diets and aposymbiotic insects. Zool Sci 14:581–586

    Article  CAS  Google Scholar 

  • Kaltenpoth M, Goettler W, Koehler S, Strohm E (2010) Life cycle and population dynamics of a protective insect symbiont reveal severe bottlenecks during vertical transmission. Evol Ecol 24:463–477

    Article  Google Scholar 

  • Koga R, Tsuchida T, Fukatsu T (2003) Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc R Soc Lond B 270:2543–2550

    Article  Google Scholar 

  • Kono M, Koga R, Shimada M, Fukatsu T (2008) Infection dynamics of coexisting Beta- and Gammaproteobacteria in the nested endosymbiotic system of mealybugs. Appl Environ Microbiol 74:4175–4184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lampel G (1959) Geschlecht und Symbiose bei den Pemphiginen. Z Morphol Okol Tiere 48:320–348

    Article  Google Scholar 

  • Lease HM, Wolf BO (2011) Lipid content of terrestrial arthropods in relation to body size, phylogeny, ontogeny and sex. Physiol Entomol 36:29–38

    Article  CAS  Google Scholar 

  • Lee YH, Hou FR (1987) Physiological roles of yeast like symbiote in reproduction and embryonic development of the brown planthopper, Nilparvata lugens Stål. J Insect Physiol 33:851–860

    Article  Google Scholar 

  • Lenardón SL, March GJ, Nome SF, Ornaghi JA (1998) Recient outbreak of “Mal de Río Cuarto” virus on corn in Argentina. Plant Dis 82:448

    Article  Google Scholar 

  • Lu ZX, Yu XP, Chen JM, Zheng XS, Xu HX, Zhang JF, Chen LZ (2004) Dynamics of yeast-like symbiote and its relationship with the virulence of brown planthopper, Nilaparvata lugens Stål, to resistant rice varieties. J Asia Pac Entomol 7:317–323

    Article  Google Scholar 

  • Michalik A, Jankowska W, Szklarzewicz T (2009) Ultrastructure and transovarial transmission of endosymbiotic microorganisms in Conomelus anceps and Metcalfa pruinosa (Insecta: Hemiptera: Fulgoromorpha). Folia Biol (Kraków) 57:131–137

    Article  Google Scholar 

  • Moran N (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci U S A 15:8627–8633

    Article  Google Scholar 

  • Moran N, Tran P, Gerardo NM (2005) Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial Phylum Bacteroidetes. Appl Environ Microbiol 71:8802–8810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishikori K, Morioka K, Kubo T, Morioka M (2009) Age-and morph-dependent activation of the lysosomal system and Buchnera degradation in aphid endosymbiosis. J Insect Physiol 55:351–357

    Article  CAS  PubMed  Google Scholar 

  • Noda H (1974) Preliminary histological observation and population dynamics of intracellular yeast-like symbiotes in the smaller brown planthopper, Laodelphax striatellus (Homoptera: Delphacidae). Appl Entomol Zool 9:275–277

    Google Scholar 

  • Noda H (1977) Histological and histochemical observation of intracellular yeast-like symbiotes in the fat body of the smaller brown planthopper, Laodelphax striatellus (Homoptera: Delphacidae). Jpn Soc Appl Entomol Zool 12:134–141

    Google Scholar 

  • Noda H, Koizumi Y (2003) Sterol biosynthesis by symbiotes: cytochrome P450 sterol C-22 desaturase genes from yeast like symbiotes of rice planthoppers and anobiid beetles. Insect Biochem Mol Biol 33:649–658

    Article  CAS  PubMed  Google Scholar 

  • Noda H, Saito T (1979) The role of intracellular yeast like symbiotes in the development of Laodelphax striatellus (Homoptera: Delphacidae). Appl Entomol Zool 14:453–458

    CAS  Google Scholar 

  • Noda H, Nakashima N, Koizumi M (1995) Phylogenetic position of yeast like symbiotes of rice planthoppers based on partial 18S r DNA sequences. Insect Biochem Mol Biol 25:639–646

    Article  CAS  PubMed  Google Scholar 

  • Ornaghi JA, Boito G, Sánchez G, March G, Beviacqua J (1993) Studies on the populations of Delphacodes kuscheli Fennah in different years and agricultural areas. J Genet Breed 47:277–282

    Google Scholar 

  • Remes Lenicov AM, Paradell S (2012) Morfología y biología de especies vectoras de virus y mollicutes al maíz en la Argentina (Insecta: Hemiptera: Cicadomorpha-Fulgoromorpha). In: Giménez Pecci MP, Laguna SL, Lenardón SL (eds) Enfermedades del maíz producidas por virus y mollicutes en Argentina. Ediciones INTA, Buenos Aires, pp 125–152

    Google Scholar 

  • Remes Lenicov AM, Virla E (1999) Delfácidos asociados al cultivo de maíz en la República Argentina (Insecta: Homoptera: Delphacidae). Rev Fac Agron 104:1–15

    Google Scholar 

  • Remes Lenicov AM, Virla E, Tesón A, Dagoberto E, Huguet N (1985) Gac Agron 5:251–258

    Article  Google Scholar 

  • Remes Lenicov AM, Virla E, Dagoberto E (1991) Cambios estacionales en la población del vector del Mal de Río Cuarto (Delphacodes kuscheli Fennah, 1955) en cultivos de avena y sus malezas circundantes en Sampacho, Córdoba. (Insecta: Homoptera: Fulgoroidea). Actas “Taller de actualización sobre Mal de Río Cuarto”. INTA, Buenos Aires- Pergamino, Argentina, 116–129

  • Royama T (1992) Analytical population dynamics. Chapman and Hall, London

    Book  Google Scholar 

  • Sasaki T, Hayashi H, Ishikawa H (1991) Growth and reproduction of the symbiotic and aposymbiotic pea aphids Acyrthosiphon pisum maintained on artificial diets. J Insect Physiol 37:749–756

    Article  CAS  Google Scholar 

  • Sasaki T, Kawamura M, Ishikawa H (1996) Nitrogen recycling in the brown planthopper, Nilaparvata lugens: Involvement of yeast-like endosymbionts in uric acid metabolism. J Insect Physiol 42:125–129

    Article  CAS  Google Scholar 

  • Seidl I, Tisdell C (1998) Carrying capacity reconsidered: from Malthus’ population theory to cultural carrying capacity. Queensland, Australia

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. Freeman, WH, New York

    Google Scholar 

  • Suh SO, Noda H, Blackwell M (2001) Insect symbiosis: derivation of yeast-like endosymbionts within an entomopathogenic filamentous lineage. Mol Biol Evol 18:995

    Article  CAS  PubMed  Google Scholar 

  • Toth L (1933) Ueber die fruehembrvonale Entwicklunn der vivipamn Aphiden. Z Morphol Okol Tiere 27:692–731

    Article  Google Scholar 

  • Toth L (1937) Entwicklungsxyklus und Symbiose von Pemphigus spirothecae Pass (Aphidina). Z Morphol Okol Tiere 33:412–437

    Article  Google Scholar 

  • Undeen AH, Vávra J (1997) Research methods for entomopathogenic protozoa. In: Lacey LA (ed) Manual of techniques in insect pathology. Academic, San Diego, pp 117–151

    Chapter  Google Scholar 

  • Vigneron A, Masson F, Vallier A, Balmand S, Rey M, Vincent-Monégat C, Aksoy E, Aubailly-Giraud E, Zaidman-Rémy A, Heddi A (2014) Insects recycle endosymbionts when the benefit is over. Curr Biol 24:2267–2273

    Article  CAS  PubMed  Google Scholar 

  • Wan G, Li G, Tao X, Pan W, Sword GA, Chen F (2015) Rice stripe virus counters reduced fecundity in its insect vector by modifying insect physiology, primary endosymbionts and feeding behavior. Sci Rep 5:12527. doi:10.1038/srep12527

    Article  PubMed  PubMed Central  Google Scholar 

  • Wetzel JM, Ohnishi M, Fujita T, Nakanishi K, Naya Y, Noda H, Sugiura M (1992) Diversity in steroidogenesis of symbiotic microorganisms from planthoppers. J Chem Ecol 18:2083–2094

    Article  CAS  PubMed  Google Scholar 

  • Xet-Mull A, Quesada T, Espinoza AM (2004) Phylogenetic position of the yeast-like symbiotes of Tagosodes orizicolus (Homoptera: Delphacidae) based on 18S ribosomal DNA partial sequences. Rev Biol Trop 52:777–785

    PubMed  Google Scholar 

  • Zera AJ, Denno RF (1997) Physiology and ecology of dispersal polymorphism in insects. Annu Rev Entomol 42:207–230

Download references

Acknowledgments

This study was supported by Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), and Universidad Nacional de La Plata (PPID – UNLP 2014). The authors especially thank Dr. Hiroaki Noda for his time to review our manuscript and particularly for his valuable comments and suggestions.

Author information

Authors and Affiliations

  1. Centro de Estudios Parasitológicos y de Vectores (CONICET-UNLP), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), La Plata, 1900, Argentina

    Gerardo Liljesthröm

  2. División Entomología. Facultad de Ciencias Naturales y Museo, UNLP. Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC), La Plata, 1900, Argentina

    María Eugenia Brentassi

  3. División Entomología. Facultad de Ciencias Naturales y Museo, UNLP. CONICET, La Plata, 1900, Argentina

    Ana María Marino de Remes Lenicov

Authors
  1. Gerardo Liljesthröm
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. María Eugenia Brentassi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ana María Marino de Remes Lenicov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María Eugenia Brentassi.

Ethics declarations

Disclosure

The authors have no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liljesthröm, G., Brentassi, M.E. & Marino de Remes Lenicov, A.M. Modeling population dynamics of yeast-like symbionts (Ascomycota: Pyrenomycetes: Clavicipitaceae) of the planthopper Delphacodes kuscheli (Hemiptera: Delphacidae). Symbiosis 72, 171–181 (2017). https://doi.org/10.1007/s13199-016-0452-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-016-0452-5

Keywords

Search

Navigation