Oecologia

, Volume 177, Issue 2, pp 453–466

Fruit secondary compounds mediate the retention time of seeds in the guts of Neotropical fruit bats

Plant-microbe-animal interactions - Original research

Abstract

Plants often recruit frugivorous animals to transport their seeds; however, gut passage can have varying effects on plant fitness depending on the physical and chemical treatment of the seed, the distance seeds are transported, and the specific site of deposition. One way in which plants can mediate the effects of gut passage on fitness is by producing fruit secondary compounds that influence gut-retention time (GRT). Using frugivorous bats (Carollia perspicillata: Phyllostomidae) and Neotropical plants in the genus Piper, we compared GRT of seeds among five plant species (Piper colonense, Piper peltatum, Piper reticulatum, Piper sancti-felicis, and Piper silvivagum) and investigated the role of fruit amides (piperine, piplartine and whole fruit amide extracts from P. reticulatum) in mediating GRT. Our results showed interspecific differences in GRT; P. reticulatum seeds passed most slowly, while P. silvivagum and P. colonense seeds passed most rapidly. Piplartine and P. reticulatum amide extracts decreased GRT, while piperine had no effect. In addition, we examined the effects of GRT on seed germination success and speed in laboratory conditions. For germination success, the effects were species specific; germination success increased with GRT for P. peltatum but not for other species. GRT did not influence germination speed in any of the species examined. Plant secondary compounds have primarily been studied in the context of their defensive role against herbivores and pathogens, but may also play a key role in mediating seed dispersal interactions.

Keywords

Fruit chemistry Seed dispersal Amides Carollia Piper 

Supplementary material

442_2014_3096_MOESM1_ESM.pdf (458 kb)
Supplementary material 1 (PDF 458 kb)
442_2014_3096_MOESM2_ESM.pdf (316 kb)
Supplementary material 2 (PDF 316 kb)
442_2014_3096_MOESM3_ESM.pdf (3.8 mb)
Supplementary material 3 (PDF 3870 kb)

References

  1. Allaire JJ, Horner J, Marti V, Porte N (2014) Markdown: markdown rendering for R. R package version 0.7. http://cran.r-project.org/web/packages/markdown/
  2. Amitai O, Holtze S, Barkan S, Amichai E, Korine C, Pinshow B, Voigt CC (2010) Fruit bats (Pteropodidae) fuel their metabolism rapidly and directly with exogenous sugars. J Exp Biol 213:2693–2699. doi:10.1242/jeb.043505 PubMedCrossRefGoogle Scholar
  3. Baldwin JW, Whitehead SR (2014) Data from: Fruit secondary compounds mediate the retention time of seeds in the guts of Neotropical fruit bats. Dryad Digital Repository. doi:10.5061/dryad.51q1p Google Scholar
  4. Bartón K (2013) MuMIn: multimodel inference. R package version 1.9.13. http://cran.r-project.org/web/packages/MuMIn/
  5. Bates D, Mächler M, Bolker B (2014) lme4: Linear mixed-effects models using S4 classes. R package version 1.1-5. http://cran.r-project.org/web/packages/lme4/
  6. Bizerril MX, Raw A (1998) Feeding behavior of bats and the dispersal of Piper arboreum seeds in Brazil. J Trop Ecol 14:109–114. doi:10.1017/S0266467498000108 CrossRefGoogle Scholar
  7. Bodmer R (1991) Strategies of seed dispersal and seed predation in Amazonian ungulates. Biotropica 23:255–261CrossRefGoogle Scholar
  8. Bolker B (2008) Ecological models and data in R. Princeton University Press, PrincetonGoogle Scholar
  9. Bolker B, R Development Core Team (2014) bbmle: tools for general maximum likelihood estimation. R package version 1.0.16. http://cran.r-project.org/web/packages/bbmle/
  10. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens M, Henry H, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. doi:10.1016/j.tree.2008.10.008 PubMedCrossRefGoogle Scholar
  11. Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach, 1st edn. Springer, New YorkCrossRefGoogle Scholar
  12. Chaves MCD, Santos B (2002) Constituents from Piper marginatum fruits. Fitoterapia 73:547–549. doi:10.1016/S0367-326X(02)00167-3 CrossRefGoogle Scholar
  13. Cipollini M (2000) Secondary metabolites of vertebrate-dispersed fruits: evidence for adaptive functions. Rev Chil Hist Nat 73:421–440. doi:10.4067/S0716-078X2000000300006 CrossRefGoogle Scholar
  14. Cipollini M, Levey DJ (1997) Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. Am Nat 150:346–372PubMedCrossRefGoogle Scholar
  15. Cosyns E, Delporte A, Lens L, Hoffmann M (2005) Germination success of temperate grassland species after passage through ungulate and rabbit guts. J Ecol 93:353–361. doi:10.1111/j.0022-0477.2005.00982.x CrossRefGoogle Scholar
  16. Daws MI, Burslem D, Crabtree LM, Kirkman P, Mullins CE, Dallin JW (2002) Differences in seed germination responses may promote coexistence of four sympatric Piper species. Funct Ecol 16:258–267. doi:10.1046/j.1365-2435.2002.00615.x CrossRefGoogle Scholar
  17. de O Chaves MC, de F Júnior AG, d O Santos BV (2003) Amides from Piper tuberculatum fruits. Fitoterapia 74:181–183. doi:10.1016/S0367-326X(02)00321-0 PubMedCrossRefGoogle Scholar
  18. Dyer LA, Dodson CD, Stireman JO, Tobler MA, Smilanich AM, Fincher RM, Letourneau DK (2003) Synergistic effects of three Piper amides on generalist and specialist herbivores. J Chem Ecol 29:2499–2514. doi:10.1023/A:1026310001958 PubMedCrossRefGoogle Scholar
  19. Dyer LA, Richards J, Dodson CD (2004a) Isolation, synthesis, and evolutionary ecology of Piper amides. In: Dyer L, Palmer (eds) Piper: a model genus for studies in phytochemistry, ecology, and evolution. Kluwer Academic, New York, pp 117–139. doi: 10.1007/978-0-387-30599-8_7
  20. Dyer LA, Letourneau DK, Dodson CD, Tobler MA, Stireman JO, Hsu A (2004b) Ecological causes and consequences of variation in defensive chemistry of a Neotropical shrub. Ecology 85:2795–2803. doi:10.1890/03-0233 CrossRefGoogle Scholar
  21. Estrada-Villegas S, Perez-Torres J, Stephenson P (2007) Seed dispersal by bats in a mountain forest edge. Ecotropica 20:1–14Google Scholar
  22. Felipe F, Filho J, Silveria J, Uchoa D, Pessoa O, Viana G (2007) Piplartine, an amide alkaloid from Piper tuberculatum, presents anxiolytic and antidepressant effects in mice. Phytomedicine 14:605–612. doi:10.1016/j.phymed.2006.12.015 CrossRefGoogle Scholar
  23. Fleming TH (1988) The short-tailed fruit bat—a study of plant-animal interactions, 2nd edn. University of Chicago Press, ChicagoGoogle Scholar
  24. Fleming TH (2004) Dispersal ecology of Neotropical Piper shrubs and treelets. In: Dyer L, Palmer (eds) Piper: a model genus for studies in phytochemistry, ecology, and evolution. Kluwer Academic, New York, pp 58–77. doi: 10.1007/978-0-387-30599-8_4
  25. Fleming TH, Heithaus ER (1981) Frugivorous bats, seed shadows, and the structure of tropical forests. Biotropica 13:45–53CrossRefGoogle Scholar
  26. Frankie GW, Baker HG, Opler PA (1974) Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. J Ecol 62:881–919CrossRefGoogle Scholar
  27. Freeland WJ, Calcott PH, Anderson LR (1985) Tannins and saponin: interaction in herbivore diets. Biochem Syst Ecol 13:189–193. doi:10.1016/0305-1978(85)90078-X CrossRefGoogle Scholar
  28. Galindo-Gonzalez J, Guevara S, Sosa VJ (2000) Bat- and bird-generated seed-rain at isolated trees in pastures in a tropical rainforest. Conserv Biol 16:1693–1703. doi:10.1111/j.1523-1739.2000.99072.x CrossRefGoogle Scholar
  29. Gentry AH (1990) Four neotropical rainforests. Yale University Press, New HavenGoogle Scholar
  30. Hlavackova L, Urbanova A, Ulicna O, Janega P, Cerna A, Babal P (2010) Piperine, active substance of black pepper, alleviates hypertension induced by NO synthase inhibition. Bratisl Med J 111:426–431Google Scholar
  31. Holdridge LR (1967) Life zone ecology, 1st edn. Tropical Science Center, San JoséGoogle Scholar
  32. Hothorn T, Bretz F, Westfall P, Heilberger RM, Schuetzenmeister A (2014) multcomp: simultaneous inference in general parametric models. R package version 1.3-2. http://cran.r-project.org/web/packages/multcomp/
  33. Howe H, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–208. doi:10.1146/annurev.es.13.110182.001221 CrossRefGoogle Scholar
  34. Izhaki I (2002) Emodin–a secondary metabolite with multiple ecological functions in higher plants. New Phytol 155:205–217. doi:10.1046/j.1469-8137.2002.00459.x CrossRefGoogle Scholar
  35. Janzen DH (1981) Enterolobium cyclocarpum seed passage rate and survival in horses, Costa Rican Pleistocene seed dispersal agents. Ecology 62:593–601. doi:10.2307/1937726 CrossRefGoogle Scholar
  36. Kato MJ, Furlan M (2007) Chemistry and evolution of the Piperaceae. Pure Appl Chem 79:529–538. doi:10.1351/pac200779040529 CrossRefGoogle Scholar
  37. Levey DJ, Tewksbury JJ, Izhaki I, Tsahar R, Haak DC (2007) Evolutionary ecology of secondary compounds in ripe fruit: case studies with capsaicin and emodin. In: Dennis AJ, Schupp EW, Green RJ, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CABI, United Kingdom, pp 37–59. doi: 10.1079/9781845931650.0000
  38. Liu Y, Yadev VR, Aggarwal BB, Nair MG (2010) Inhibitory effects of black pepper (Piper nigrum) extracts and compounds on human tumor cell proliferation, cyclooxygenase enzymes, lipid-peroxidation and nuclear transcription factor-kappa-B. Nat Prod Commun 5:1253–1257PubMedCrossRefGoogle Scholar
  39. Loiselle BA (1990) Seeds in droppings of tropical fruit-eating birds: importance of considering seed composition. Oecologia 82:494–500. doi:10.1007/BF00319792 CrossRefGoogle Scholar
  40. Lopez JE, Vaughan C (2004) Observations on the role of frugivorous bats as seed dispersers in Costa Rican secondary humid forests. Acta Chiropterol 6:111–119. doi:10.3161/001.006.0109 CrossRefGoogle Scholar
  41. Mason JR, Bean NJ, Shah PS, Clark L (1991) Taxon-specific differences in responsiveness to capsaicin and several analogues: correlates between chemical structure and behavioral aversiveness. J Chem Ecol 17:2539–2551. doi:10.1007/BF00994601 PubMedCrossRefGoogle Scholar
  42. McDade LA, Bawa KS, Hespenheide HA, Hartshorn GS (1994) La Selva, Ecology and natural history of a neotropical rainforest, 1st edn. University of Chicago Press, ChicagoGoogle Scholar
  43. McKey D (1975) The ecology of coevolved seed dispersal systems. In: Gilbert LE, Raven PH (eds) Coevolution of animals and plants. University of Texas Press, Austin, pp 159–191Google Scholar
  44. Mishra P, Sinha S, Guru SK, Bhushan S, Vishwakarma RA, Ghosal S (2011) Two new amides with cytotoxic activity from the fruits of Piper longum. J Asian Nat Prod Res 13:143–148. doi:10.1080/10286020.2010.546789 PubMedCrossRefGoogle Scholar
  45. Morandim AA, Pin AR, Pietro NA, Alecio AC, Kato MJ, Young CM, Oliveira JW, Furlan M (2010) Composition and screening of antifungal activity against Cladosporium sphaerospermum and Cladosporium cladosporioides of essential oils of leaves and fruits of Piper species. Afr J Biotechnol 9:6135–6139. doi:10.5897/AJB09.1956 Google Scholar
  46. Murray KG, Russell S, Picone CM, Winnett-Murray K, Sherwood W, Kuhlmann ML (1994) Fruit laxatives and seed passage rates in frugivores: consequences for plant reproductive success. Ecology 75:989–994. doi:10.2307/1939422 CrossRefGoogle Scholar
  47. Muscarella R, Fleming TH (2007) The role of frugivorous bats in tropical forest succession. Biol Rev Camb Philos 82:573. doi:10.1111/j.1469-185X.2007.00026.x CrossRefGoogle Scholar
  48. Nerurkar PV, Dragull K, Tang C-S (2004) In vitro toxicity of kava alkaloid, pipermethystine, in HepG2 cells compared to kavalactones. Toxicol Sci 79:106–111. doi:10.1093/toxsci/kfh067 PubMedCrossRefGoogle Scholar
  49. O’Hara RB, Kotze DJ (2010) Do not log-transform count data. MEE 1:118–122. doi:10.1111/j.2041-210X.2010.00021.x CrossRefGoogle Scholar
  50. Palmeirim JM, Gorchoy DL, Stoleson S (1989) Trophic structure of a neotropical frugivore community: is there competition between birds and bats? Oecologia 79:403–411. doi:10.1007/BF00384321 PubMedCrossRefGoogle Scholar
  51. Parmar VS, Jain SC, Bisht KS, Jain R, Taneja P, Jha A, Tyagi OD, Prasa AK, Wengel J, Olsen CE (1997) Phytochemistry of the genus Piper. Phytochemistry 46:597–673. doi:10.1016/S0031-9422(97)00328-2 CrossRefGoogle Scholar
  52. R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. ISBN3-900051-07-0. http://www.R-project.org/
  53. Rali T, Wossa SW, Leach DN, Waterman PG (2007) Volatile chemical constituents of Piper aduncum L. and Piper gibbilimbum C. DC (Piperaceae) from Papua New Guinea. Molecules 12:389–394. doi:10.3390/12030389 PubMedCrossRefGoogle Scholar
  54. Richards FJ (1959) A flexible growth function for empirical use. J Exp Bot 10:290–301. doi:10.1093/jxb/10.2.290 CrossRefGoogle Scholar
  55. Richards LA, Dyer LA, Smilanich AM, Dodson CD (2010) Synergistic effects of amides from two Piper species on generalist and specialist herbivores. J Chem Ecol 36:1105–1113. doi:10.1007/s10886-010-9852-9 PubMedCrossRefGoogle Scholar
  56. Rodrigues RV, Lanznaster D, Tagliari D, Balbinot L, Gadotti V, Alves V, Facundo V, Santos A (2009) Antinociceptive effect of crude extract, fractions and three alkaloids obtained from fruits of Piper tuberculatum. Biol Pharm Bull 32:1809–1812. doi:10.1248/bpb.32.1809 PubMedCrossRefGoogle Scholar
  57. Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188:333–353. doi:10.1111/j.1469-8137.2010.03402.x PubMedCrossRefGoogle Scholar
  58. Scott IM, Puniani E, Durst T, Phelps D, Merali S, Assabgui RA, Sanchez-Vindas P, Poveda L, Philogene BJR, Arnason JT (2002) Insecticidal activity of Piper tuberculatum Jacq. extracts: synergistic interaction of piperamides. Agric For Entomol 4:137–144. doi:10.1046/j.1461-9563.2002.00137.x CrossRefGoogle Scholar
  59. Sharma G, Mishra B (2007) Piperine—a therapeutic agent and a bioavailability enhancer. Pharm Res 6:129–133Google Scholar
  60. Shilton LA, Altringham JD, Compton SG, Whittaker RJ (1999) Old world fruit bats can be long-distance seed dispersers through extended retention of viable seeds in the gut. Proc R Soc B 266:219–223. doi:10.1098/rspb.1999.0625 PubMedCentralCrossRefGoogle Scholar
  61. Siddiqui B, Gulzar T, Begum S, Afshan F, Sattar FA (2005) Insecticidal amides from fruits of Piper nigrum Linn. Nat Prod Res 19:143–150. doi:10.1080/14786410410001704750 PubMedCrossRefGoogle Scholar
  62. Struempf HM, Schondube JE, del Rio CM (1999) The cyanogenic glycoside amygdalin does not deter consumption of ripe fruit by cedar waxwings. Auk 116:749–758CrossRefGoogle Scholar
  63. Tewksbury JJ, Nabhan GP (2001) Seed dispersal: directed deterrence by capsaicin in chillies. Nature 412:403–404. doi:10.1038/35086653 PubMedCrossRefGoogle Scholar
  64. Tewksbury JJ, Levey DJ, Huizinga M, Haak DC, Traveset A (2008a) Costs and benefits of capsaicin-mediated control of gut retention in dispersers of wild chilies. Ecology 89:107–117. doi:10.1890/07-0445.1 PubMedCrossRefGoogle Scholar
  65. Tewksbury JJ, Reagan KM, Machnicki NJ, Carlo TA, Haak DC, Peñaloza ALC, Levey DJ (2008b) Evolutionary ecology of pungency in wild chilies. Proc Natl Acad Sci 105:11808–11811. doi:10.1073/pnas.0802691105 PubMedCentralPubMedCrossRefGoogle Scholar
  66. Thies W, Kalko E, Schnitzler H (1998) The roles of echolocation and olfaction in two Neotropical fruit-eating bats, Carollia perspicillata and C. castanea, feeding on Piper. Behav Ecol Sociobiol 42:397–409. doi:10.1007/s002650050454 CrossRefGoogle Scholar
  67. Timm RM (1994) Mammals. In: McDade LA, Bawa KS, Hespenheide HA, Hartshorn GA (eds) La Selva: ecology and natural history of a Neotropical rain forest. University of Chicago Press, Chicago, pp 394–397Google Scholar
  68. Traveset A (1998) Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspect Plant Ecol 1:151–190. doi:10.1078/1433-8319-00057 CrossRefGoogle Scholar
  69. Tsoar A, Shohami D, Nathan R (2011) A movement ecology approach to study seed dispersal and plant invasion: an overview and application of seed dispersal by fruit bats. In: Richardson DR (eds) Fifty years of invasion ecology: the legacy of Charles Elton, pp 101–119. doi: 10.1002/9781444329988.ch9
  70. van der Pijl L (1982) Principles of dispersal in higher plants, 3rd edn. Springer, New YorkCrossRefGoogle Scholar
  71. Vasques da Silva R, Navickiene HM, Kato MJ, Bolzani S, Meda CI, Young MC, Furlan M (2002) Antifugal amides from Piper arboreum and Piper tuberculatum. Phytochemistry 59:521–527. doi:10.1016/S0031-9422(01)00431-9 PubMedCrossRefGoogle Scholar
  72. Voigt CC, Capps KA, Dechmann DKN, Michener RH, Kunz TH (2008) Nutrition or detoxification: why bats visit mineral licks of the Amazonian rainforest. PLoS One 3:e2011. doi:10.1371/journal.pone.0002011 PubMedCentralPubMedCrossRefGoogle Scholar
  73. Wahaj SA, Levey DJ, Sanders AK, Cipollini ML (1998) Control of gut retention time by secondary metabolites in ripe Solanum fruits. Ecology 79:2309–2319. doi:10.2307/176824 CrossRefGoogle Scholar
  74. Whitehead SR (2013) Ecological costs and benefits of secondary metabolites in animal-dispersed fruits. PhD dissertation, Department of Ecology and Evolutionary Biology, University of ColoradoGoogle Scholar
  75. Whitehead SR, Bowers MD (2013) Evidence for the adaptive significance of secondary compounds in vertebrate-dispersed fruits. Am Nat 182(5):563–577. doi:10.1086/673258 PubMedCrossRefGoogle Scholar
  76. Whitehead SR, Bowers MD (2014) Chemical ecology of fruit defense: synergistic and antagonistic interactions among amides from Piper. Funct Ecol. doi:10.1111/1365-2435.12250 Google Scholar
  77. Whitehead SR, Jeffrey CS, Leonard MD, Dodson CD, Dyer LA, Bowers MD (2013) Patterns of secondary metabolite allocation to fruits and seeds in Piper reticulatum. J Chem Ecol 39:1373–1384PubMedCrossRefGoogle Scholar
  78. Wickham H (2009) ggplot2: elegant graphics for data analysis, 1st edn. Springer, New YorkCrossRefGoogle Scholar
  79. Xie Y (2014) knitr: a general-purpose package for dynamic report generation in R. R package version 1.6. http://cran.r-project.org/web/packages/knitr/
  80. Yang Y, Lee SG, Lee HK, Kim MK, Lee SH, Lee HS (2002) A piperidine amide extracted from Piper longum L. fruit shows activity against Aedes aegypti mosquito larvae. J Agric Food Chem 50:3765–3767. doi:10.1021/jf011708f PubMedCrossRefGoogle Scholar
  81. Zuur AF, Ieno EN, Walker NJ, Savliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R, 1st edn. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.School of Natural ScienceHampshire CollegeAmherstUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA

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