Skip to main content
Log in

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

  • Plant-microbe-animal interactions - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

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.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4a–e

Similar content being viewed by others

References

  • 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/

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Bartón K (2013) MuMIn: multimodel inference. R package version 1.9.13. http://cran.r-project.org/web/packages/MuMIn/

  • 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/

  • 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

    Article  Google Scholar 

  • Bodmer R (1991) Strategies of seed dispersal and seed predation in Amazonian ungulates. Biotropica 23:255–261

    Article  Google Scholar 

  • Bolker B (2008) Ecological models and data in R. Princeton University Press, Princeton

    Google Scholar 

  • 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/

  • 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

    Article  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach, 1st edn. Springer, New York

    Book  Google Scholar 

  • Chaves MCD, Santos B (2002) Constituents from Piper marginatum fruits. Fitoterapia 73:547–549. doi:10.1016/S0367-326X(02)00167-3

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cipollini M, Levey DJ (1997) Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. Am Nat 150:346–372

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • Estrada-Villegas S, Perez-Torres J, Stephenson P (2007) Seed dispersal by bats in a mountain forest edge. Ecotropica 20:1–14

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Fleming TH (1988) The short-tailed fruit bat—a study of plant-animal interactions, 2nd edn. University of Chicago Press, Chicago

    Google Scholar 

  • 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

  • Fleming TH, Heithaus ER (1981) Frugivorous bats, seed shadows, and the structure of tropical forests. Biotropica 13:45–53

    Article  Google Scholar 

  • 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 62:881–919

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gentry AH (1990) Four neotropical rainforests. Yale University Press, New Haven

    Google Scholar 

  • 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 111:426–431

    CAS  Google Scholar 

  • Holdridge LR (1967) Life zone ecology, 1st edn. Tropical Science Center, San José

    Google Scholar 

  • 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/

  • Howe H, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–208. doi:10.1146/annurev.es.13.110182.001221

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kato MJ, Furlan M (2007) Chemistry and evolution of the Piperaceae. Pure Appl Chem 79:529–538. doi:10.1351/pac200779040529

    Article  CAS  Google Scholar 

  • 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

  • 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 5:1253–1257

    Article  PubMed  Google Scholar 

  • Loiselle BA (1990) Seeds in droppings of tropical fruit-eating birds: importance of considering seed composition. Oecologia 82:494–500. doi:10.1007/BF00319792

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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, Chicago

    Google Scholar 

  • 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 159–191

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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/

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Richards FJ (1959) A flexible growth function for empirical use. J Exp Bot 10:290–301. doi:10.1093/jxb/10.2.290

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sharma G, Mishra B (2007) Piperine—a therapeutic agent and a bioavailability enhancer. Pharm Res 6:129–133

    CAS  Google Scholar 

  • 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

    Article  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Struempf HM, Schondube JE, del Rio CM (1999) The cyanogenic glycoside amygdalin does not deter consumption of ripe fruit by cedar waxwings. Auk 116:749–758

    Article  Google Scholar 

  • Tewksbury JJ, Nabhan GP (2001) Seed dispersal: directed deterrence by capsaicin in chillies. Nature 412:403–404. doi:10.1038/35086653

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 394–397

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • van der Pijl L (1982) Principles of dispersal in higher plants, 3rd edn. Springer, New York

    Book  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Whitehead SR (2013) Ecological costs and benefits of secondary metabolites in animal-dispersed fruits. PhD dissertation, Department of Ecology and Evolutionary Biology, University of Colorado

  • 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

    Article  PubMed  Google Scholar 

  • 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 

  • 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 39:1373–1384

    Article  CAS  PubMed  Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis, 1st edn. Springer, New York

    Book  Google Scholar 

  • 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/

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Savliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R, 1st edn. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgments

María Fernanda Obando Quesada provided invaluable assistance in the field. Martina Nagy assisted with animal care. Deane Bowers provided laboratory mentorship, and Larry Winship helped with the germination experiments. The Sistema Nacional de Areas de Conservacion (SINAC)-Ministerio de Ambiente y Energía kindly allowed us to conduct the fieldwork in Costa Rica (Resoluciónes 017-2011-SINAC and 075-2012-SINAC). The Organization for Tropical Studies and La Selva Biological Station staff provided logistical support. This project was made possible by a National Science Foundation-Research Experience for Undergraduates grant DBI 0851933 awarded to J. W. B. through the Organization for Tropical Studies. Partial funding was also provided by National Science Foundation grant DEB 1210884 to S. R. W. and Deane Bowers, and a Samuel Morris Endowed Fund grant (2011) to J. W. B. The authors declare no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Justin W. Baldwin.

Additional information

Communicated by Colin Mark Orians.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baldwin, J.W., Whitehead, S.R. Fruit secondary compounds mediate the retention time of seeds in the guts of Neotropical fruit bats. Oecologia 177, 453–466 (2015). https://doi.org/10.1007/s00442-014-3096-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-3096-2

Keywords

Navigation