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When a seed-feeding beetle is a predator and also increases the speed of seed germination: an intriguing interaction with an invasive plant

  • Amanda V. da Silva
  • Marcelo N. RossiEmail author
Original Paper

Abstract

Bruchine beetles are usually considered seed predators, particularly because these beetles consume the seed embryo and kill the seeds. Previous studies suggest that under certain conditions, these insects do not kill the embryo. In this study, we asked whether the germination speed of seeds of the invasive tree Leucaena leucocephala is enhanced by the seed-feeding beetle Acanthoscelides macrophthalmus (Coleoptera: Chrysomelidae: Bruchinae). We also tested whether differences in germination between attacked and intact seeds could be related to seed size. We finally examined whether the number of larvae per seed affected seed germination and whether seedling emergence patterns were similar to those exhibited by germination. We found that compared to intact seeds, proportionally faster germination occurred in seeds attacked by A. macrophthalmus in 14 of the 26 populations studied. In addition, those populations that presented greater germination speed in the attacked seeds during the evaluation time also had the largest seeds. Similar to the germination experiments, seedling emergence was faster in the attacked compared to the intact seeds. Our findings show that the germination speed of L. leucocephala seeds can be enhanced by A. macrophthalmus. However, this effect is much more intense when a single larva develops inside the seed. In evolutionary terms, it is possible that the selection for larger seeds is favoured, increasing the speed of seed germination and contributing to predator satiation at the seed level. However, this effect could be minimized by the production of many seeds by L. leucocephala plants, causing predator satiation by “masting” effects, which would favour the selection for higher seed numbers.

Keywords

Hard seeds Invasion ecology Leucaena leucocephala Life-history evolution Plant–insect interaction 

Notes

Acknowledgements

We thank Alicia Wood and Eloísa B. Haga for providing valuable assistance during the fieldwork. We also thank Daniela H. Maggio for help with the editing of Fig. 1 (map). We are grateful to the Fundação de Amparo à Pesquisa do Estado de São Paulo (Fapesp; no 12/11612-4) for financial support. We finally thank all the researchers from the Instituto de Botânica de São Paulo (IBT) for their assistance with the tetrazolium test. The biological material was collected according to the guidelines of the Authorization and Information System in Biodiversity (SISBIO – no 40133-1).

Supplementary material

10682_2019_9974_MOESM1_ESM.docx (24 kb)
Supplementary material 1 (DOCX 24 kb)

References

  1. Arévalo JR, Afonso L, Naranjo A, Salas M (2010) Invasion of the Gran Canaria ravines ecosystems (Canary Islands) by the exotic species Acacia farnesiana. Plant Ecol 206:185–193CrossRefGoogle Scholar
  2. Austin PC (2017) A tutorial on multilevel survival analysis: methods, models and applications. Int Stat Rev 85:185–203CrossRefGoogle Scholar
  3. Baskin CC, Baskin JM (1998) Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, San DiegoGoogle Scholar
  4. Beckman NG, Neuhauser C, Muller-Landau HC (2012) The interacting effects of clumped seed dispersal and distance- and density-dependent mortality on seedling recruitment patterns. J Ecol 100:862–873CrossRefGoogle Scholar
  5. Bonal R, Muñoz A, Díaz M (2007) Satiation of predispersal seed predators: the importance of considering both plant and seed level. Evol Ecol 21:367–380CrossRefGoogle Scholar
  6. Branco M, Branco C, Merouani H, Almeida MH (2002) Germination success, survival and seedling vigour of Quercus suber acorns in relation to insect damage. For Ecol Manag 166:159–164CrossRefGoogle Scholar
  7. Cochard R, Jackes BR (2005) Seed ecology of the invasive tropical tree Parkinsonia aculeata. Plant Ecol 180:13–31CrossRefGoogle Scholar
  8. Costa CJ, Santos CP (2010) Teste de tetrazólio em sementes de leucena. Rev Bras Sem 32:66–72CrossRefGoogle Scholar
  9. Crawley MJ (2007) The R book. Wiley, ChichesterCrossRefGoogle Scholar
  10. Dalmolin MFS, Malavasi UC, Malavasi MM (2011) Dispersão e germinação de sementes de Leucaena leucocephala (Lam.) de Wit na região Oeste do Paraná. Semina: C Agr 32:355–362Google Scholar
  11. De Menezes LCCR, Klein J, Kestring D, Rossi MN (2010) Bottom-up and top-down effects in a pre-dispersal seed predation system: are non-predated seeds damaged? Basic Appl Ecol 11:126–134CrossRefGoogle Scholar
  12. Effowe TQ, Amevoin K, Nuto Y, Mondedji D, Glitho IA (2010) Reproductive capacities and development of a seed bruchid beetle, Acanthoscelides macrophthalmus, a potential host for the mass rearing of the parasitoid, Dinarmus basalis. J Insect Sci 10:1–14Google Scholar
  13. English KF, Olckers T (2014) Does the size of the seeds and seed pods of the invasive tree Leucaena leucocephala (Fabaceae) affect their utilization by the biological control agent Acanthoscelides macrophthalmus (Chrysomelidae: Bruchinae)? Afr Entomol 22:872–879CrossRefGoogle Scholar
  14. Fenner M, Cresswell JE, Hurley RA, Baldwin T (2002) Relationship between capitulum size and pre-dispersal seed predation by insect larvae in common Asteraceae. Oecologia 130:72–77CrossRefGoogle Scholar
  15. Fox CW, Bush ML, Messina FJ (2010) Biotypes of the seed beetle Callosobruchus maculatus have differing effects on the germination and growth of their legume hosts. Agric For Entomol 12:353–362CrossRefGoogle Scholar
  16. Fröborg H, Eriksson O (2003) Predispersal seed predation and population dynamics in the perennial understory herb Actaea Spicata. Can J Botany 81:1058–1069CrossRefGoogle Scholar
  17. Haga EB, Rossi MN (2016) The effect of seed traits on geographic variation in body size and sexual size dimorphism of the seed-feeding beetle Acanthoscelides macrophthalmus. Ecol Evol 6:6892–6905CrossRefGoogle Scholar
  18. Harms KE, Dalling JW (2000) A bruchid beetle and a viable seedling from a single diaspore of Attalea butyracea. J Trop Ecol 16:319–325CrossRefGoogle Scholar
  19. Hubbell SP (1980) Seed predation and the coexistence of tree species in tropical forests. Oikos 35:214–229CrossRefGoogle Scholar
  20. Hulme PE, Benkman CW (2002) Granivory. In: Herrera CM, Pellmyr O (eds) Plant-animal interactions: an evolutionary approach. Blackwell, Oxford, pp 132–154Google Scholar
  21. Jansen PA, Elschot K, Verkerk PJ, Wright SJ (2010) Seed predation and defleshing in the agouti-dispersed palm Astrocaryum standleyanum. J Trop Ecol 26:473–480CrossRefGoogle Scholar
  22. Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Syst 2:465–492CrossRefGoogle Scholar
  23. Johnson CD, Romero J (2004) A review of evolution of oviposition guilds in the Bruchidae (Coleoptera). Rev Bras Entomol 48:401–408CrossRefGoogle Scholar
  24. Kadereit G, Newton RJ, Vandelook F (2017) Evolutionary ecology of fast seed germination—a case study in Amaranthaceae/Chenopodiaceae. Perspect Plant Ecol Evol Syst 29:1–11CrossRefGoogle Scholar
  25. Karban R, Lowenberg G (1992) Feeding by seed bugs and weevils enhances germination of wild Gossypium species. Oecologia 92:196–200CrossRefGoogle Scholar
  26. Kergoat GJ, Alvarez N, Hossaert-McKey M, Faure N, Silvain JF (2005) Parallels in the evolution of the two largest new and old World seed-beetle genera (Coleoptera, Bruchidae). Mol Ecol 14:4003–4021CrossRefGoogle Scholar
  27. Kestring D, Menezes LCCR, Tomaz CA, Lima GPP, Rossi MN (2009) Relationship among phenolic contents, seed predation and physical seed traits in Mimosa bimucronata plants. J Plant Biol 52:569–576CrossRefGoogle Scholar
  28. Kigel J, Galili G (1995) Seed development and germination. Marcel Dekker, New YorkGoogle Scholar
  29. Koprdova S, Bellanger S, Skuhrovec J, Darmency H (2015) Does gall midge larvae cause pre-dispersal seed mortality and limit cornflower population growth? Acta Oecol 69:167–172CrossRefGoogle Scholar
  30. Koptur S (1998) Effect of seed damage on germination in the Common Vetch (Vicia sativa L.). Am Midl Nat 140:393–396CrossRefGoogle Scholar
  31. Lewis OT, Gripenberg S (2008) Insect seed predators and environmental change. J Appl Ecol 45:1593–1599CrossRefGoogle Scholar
  32. Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the World’s worst invasive alien species: a selection from the Global Invasive Species Database. The Invasive Species Specialist Group (ISSG), a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN), Hollands Printing Ltd, Auckland, NZGoogle Scholar
  33. McNair JN, Sunkara A, Frobish D (2012) How to analyse seed germination data using statistical time-to-event analysis: non-parametric and semi-parametric methods. Seed Sci Res 22:77–95CrossRefGoogle Scholar
  34. Medina-Rosa D, Fortes AMT, Mauli MM, Palma D, Marques DS, Corsato JM, Leszczynski R (2007) Potencial alelopático de Leucaena leucocephala (Lam.) de Wit sobre a germinação de sementes de plantas invasoras e soja. Rev Bras Bioc 5:525–527Google Scholar
  35. Mendes S, Mesquita JB, Marino RH (2011) Qualidade sanitária de sementes de Leucaena leucocephala (Lam.) De Wit armazenadas em câmara fria. Nat Res 1:15–22Google Scholar
  36. Mucunguzi P (1995) Effects of bruchid beetles on germination and establishment of Acacia species. Afr J Ecol 33:64–70CrossRefGoogle Scholar
  37. Nakai Z, Kondo T, Akimoto S (2011) Parasitoid attack of the seed-feeding beetle Bruchus loti enhances the germination success of Lathyrus japonicus seeds. Arthropod-Plant Interact 5:227–234CrossRefGoogle Scholar
  38. Neser S (1994) Conflicts of interest? the Leucaena controversy. Plant Protec N S Afr 6:8Google Scholar
  39. Okello BD, Young TP (2000) Effects of fire, bruchid beetles and soil type on germination and seedling establishment of Acacia drepanolobium. Afr J Range Forage Sci 17:46–51CrossRefGoogle Scholar
  40. Oliveira AB (2008) Germinação de sementes de leucena (Leucaena leucocephala (Lam.) De Wit.), var. K-72. Rev Biol Ciênc Terr 8:166–172Google Scholar
  41. Ollerton J, Lack A (1996) Partial predispersal seed predation in Lotus corniculatus L. (Fabaceae). Seed Sci Res 6:65–69CrossRefGoogle Scholar
  42. Orozco-Almanza MS, León-García LP, Grether R, García-Moya E (2003) Germination of four species of the genus Mimosa (Leguminosae) in a semi-arid zone of Central Mexico. J Arid Environ 55:75–92CrossRefGoogle Scholar
  43. Peguero G, Bonal R, Espelta JM (2014) Variation of predator satiation and seed abortion as seed defense mechanisms across an altitudinal range. Basic Appl Ecol 15:269–276CrossRefGoogle Scholar
  44. Perea R, San Miguel A, Gil L (2011) Leftovers in seed dispersal: ecological implications of partial seed consumption for oak regeneration. J Ecol 99:194–201CrossRefGoogle Scholar
  45. Perea R, López D, San Miguel A, Gil L (2012) Incorporating insect infestation into rodent seed dispersal: better if the larva is still inside. Oecologia 170:723–733CrossRefGoogle Scholar
  46. Perea R, Fernandes GW, Dirzo R (2018) Embryo size as a tolerance trait against seed predation: contribution of embryo-damaged seeds to plant regeneration. Perspect Plant Ecol Evol Syst 31:7–16CrossRefGoogle Scholar
  47. Pereira ACF, Fonseca FSA, Mota GR, Fernandes AKC, Fagundes M, Reis-Júnior R, Faria ML (2014) Ecological interactions shape the dynamics of seed predation in Acrocomia aculeata (Arecaceae). PLoS ONE 9:e98026CrossRefGoogle Scholar
  48. R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. Version 3.5.1Google Scholar
  49. Raghu S, Wiltshire C, Dhileepan K (2005) Intensity of pre-dispersal seed predation in the invasive legume Leucaena leucocephala is limited by the duration of pod retention. Austral Ecol 30:310–318CrossRefGoogle Scholar
  50. Ramírez N, Traveset A (2010) Predispersal seed-predation by insects in the Venezuelan Central Plain: overall patterns and traits that influence its biology and taxonomic groups. Perspect Plant Ecol Evol Syst 12:193–209CrossRefGoogle Scholar
  51. Ribeiro-Costa CS, Almeida LM (2012) Seed-chewing beetles (Coleoptera: Chrysomelidae: Bruchinae). In: Panizzi AR, Parra JRP (eds) Insect bioecology and nutrition for integrated pest management. CRC Press, Boca Raton, pp 325–352CrossRefGoogle Scholar
  52. Rodrigues LMS, Viana JH, Ribeiro-Costa CS, Rossi MN (2012) The extent of seed predation by bruchine beetles (Coleoptera: Chrysomelidae: Bruchinae) in a heterogenous landscape in southeastern Brazil. Coleopt Bull 66:271–279CrossRefGoogle Scholar
  53. Rose KE, Louda SM, Rees M (2005) Demographic and evolutionary impacts of native and invasive insect herbivores on Cirsium canescens. Ecology 86:453–465CrossRefGoogle Scholar
  54. Rossi MN, Rodrigues LMS, Ishino MN, Kestring D (2011) Oviposition pattern and within-season spatial and temporal variation of pre-dispersal seed predation in a population of Mimosa bimucronata trees. Arthropod-Plant Interact 5:209–217CrossRefGoogle Scholar
  55. Scherer LM, Zucareli V, Zucareli CA, Fortes AMT (2005) Alelopathic effects of aqueous extracts of leucena (Leucaena leucocephala Wit) leave and fruit on germination and root growth of canafistula (Peltophorum dubium Spreng). Semin-Ciênc Agrár 26:161–166CrossRefGoogle Scholar
  56. Sharratt MEJ, Olckers T (2012) The biological control agent Acanthoscelides macrophthalmus (Chrysomelidae: Bruchinae) inflicts moderate levels of seed damage on its target, the invasive tree Leucaena leucocephala (Fabaceae), in the KwaZulu-Natal coastal region of South Africa. Afr Entomol 20:44–51CrossRefGoogle Scholar
  57. Shoba Z, Olckers T (2010) Reassessment of the biology and host range of Acanthoscelides macrophthalmus (Chrysomelidae: Bruchinae), a seed-feeding beetle released for the biological control of Leucaena leucocephala in South Africa. Afr Entomol 18:1–9CrossRefGoogle Scholar
  58. Southgate BJ (1979) Biology of the Bruchidae. Annu Rev Entomol 24:449–473CrossRefGoogle Scholar
  59. StatSoft Inc (2012) Statistica (data analysis software system). Tulsa, OK, version 11.0Google Scholar
  60. Stone BC (1970) The flora of Guam. Micronesica 6:1–659Google Scholar
  61. Tadros MJ, Samarah NH, Alqudah AM (2011) Effect of different pre-sowing seed treatments on the germination of Leucaena leucocephala (Lam.) and Acacia farnesiana (L.). New For 42:397–407CrossRefGoogle Scholar
  62. Takakura K (2002) The specialist seed predator Bruchidius dorsalis (Coleoptera: Bruchidae) plays a crucial role in the seed germination of its host plant, Gleditsia japonica (Leguminosae). Funct Ecol 16:252–257CrossRefGoogle Scholar
  63. Takakura K (2004) Variation in egg size within and among generations of the bean weevil, Bruchidius dorsalis (Coleoptera: Bruchidae): effects of host plant quality and paternal nutritional investment. Ann Entomol Soc Am 97:346–352CrossRefGoogle Scholar
  64. Tomaz CA, Kestring D, Rossi MN (2007) Effects of the seed predator Acanthoscelides schrankiae on viability of its host plant Mimosa bimucronata. Biol Res 40:281–290CrossRefGoogle Scholar
  65. Tuda M (2007) Applied evolutionary ecology of insects of the subfamily Bruchinae (Coleoptera: Chrysomelidae). Appl Entomol Zool 42:337–346CrossRefGoogle Scholar
  66. Tuda M, Wu L-H, Tateishi Y, Niyomdham C, Buranapanichpan S, Morimoto K, Wu W-J, Wang C-P, Chen Z-Q, Zhu H-Y, Zhang Y-C, Murugan K, Chou L-Y, Johnson CD (2009) A novel host shift and invaded range of a seed predator, Acanthoscelides macrophthalmus (Coleoptera: Chrysomelidae: Bruchinae), of an invasive weed, Leucaena leucocephala. Entomol Sci 12:1–8CrossRefGoogle Scholar
  67. Tuller J, Paula EL, Maia LF, Moraes R (2015) Seed predation food web, nutrient availability, and impact on the seed germination of Senegalia tenuifolia (Fabaceae). Rev Biol Trop 63:1149–1159CrossRefGoogle Scholar
  68. Vallejo-Marin M, Dominguez CA, Dirzo R (2006) Simulated seed predation reveals a variety of germination responses of neotropical rain forest. Am J Bot 93:369–376CrossRefGoogle Scholar
  69. Vandenbussche F, Petrasek J, Zadnikova P, Hoyerová K, Pesek B, Raz V, Swarup R, Bennett M, Zazimalova E, Benkova E, Straeten D (2010) The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Aradopsis thaliana seedlings. Development 137:577–606CrossRefGoogle Scholar
  70. Visser MD, Muller-Landau HC, Wright SJ, Rutten G, Jansen PA (2011) Tri-trophic interactions affect density dependence of seed fate in a tropical forest palm. Ecol Lett 14:1093–1100CrossRefGoogle Scholar
  71. Williams RD, Hoagland RE (2007) Phytotoxicity of mimosine and albizziine on seed germination and seedling growth of crops and weeds. Allelopathy J 19:423–430Google Scholar
  72. Wood A, Haga EB, Costa VA, Rossi MN (2017) Geographic distribution, large-scale spatial structure and diversity of parasitoids of the seed-feeding beetle Acanthoscelides macrophthalmus. Bull Entomol Res 107:322–331CrossRefGoogle Scholar
  73. Wu L-H, Wang C-P, Wu W-J (2012) Description and differentiation of the four larval instars of Acanthoscelides macrophthalmus (Coleoptera: Chrysomelidae: Bruchinae). Ann Entomol Soc Am 105:259–267CrossRefGoogle Scholar
  74. Xu Y, Shen Z, Li D, Guo Q (2015) Pre-dispersal seed predation in a species- rich forest community: patterns and the interplay with determinants. PLoS ONE 10:e0143040CrossRefGoogle Scholar
  75. Zar JH (1999) Biostatistical analysis. Prentice Hall, Upper Saddle RiverGoogle Scholar
  76. Zhang M, Dong Z, Yi X, Bartlow AW (2014) Acorns containing deeper plumule survive better: how white oaks counter embryo excision by rodents. Ecol Evol 4:59–66CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Laboratório de Ecologia Populacional (LEPOP), Department of Ecology and Evolutionary BiologyFederal University of São PauloDiademaBrazil

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