Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-23T00:24:06.095Z Has data issue: false hasContentIssue false

Fruit colour conceals endocarp dimorphism from avian seed dispersers in a tropical beach plant, Scaevola taccada (Goodeniaceae), found in Okinawa

Published online by Cambridge University Press:  08 June 2015

Keita D. Tanaka*
Affiliation:
School of Science, Rikkyo University, Room 4213, 3-34-1 Nishi-Ikebukuro, Toshima, Tokyo 171-8501, Japan
Tetsuo Denda
Affiliation:
Department of Marine and Natural Sciences, University of the Ryukyus, Room 434, Faculty building of Science, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan
Keisuke Ueda
Affiliation:
School of Science, Rikkyo University, Room 4213, 3-34-1 Nishi-Ikebukuro, Toshima, Tokyo 171-8501, Japan
Naoko Emura
Affiliation:
School of Science, Rikkyo University, Room 4213, 3-34-1 Nishi-Ikebukuro, Toshima, Tokyo 171-8501, Japan Center for Ecological Research, Kyoto University, 2-509-3 Hirano, Otsu, Shiga 520-2113, Japan
*
1Corresponding author. Email: keita.d.tanaka@gmail.com.

Abstract:

Theory predicts that honest signalling strategies will not always be evolutionarily stable in interspecific communication, yet to demonstrate such a transition of signalling modality between honesty and dishonesty in the wild would be difficult. An endocarp dimorphism has been found in Scaevola taccada fruits: a morph with a cork substrate that facilitates ocean current seed dispersal and a morph without the cork. Both types of fruit are covered with sugar-containing flesh, and are similar in size and colour to one another (at least from a human perspective). The apparent lack of external differences between morphotypes could potentially degrade mutualistic relations between the plant and seed-dispersing birds because the presence of a cork could lower the fruit's nutritional value. Thus, unless seed dispersers can discriminate between the different types of fruit, this system may provide an example of a transition between honest and dishonest signalling. We examined S. taccada fruit and leaf colours from an avian visual perspective. Even though the fruits and leaves were different in colour from one another to birds, there was no perceivable difference in the colours between fruit morphotypes. Therefore, fruit colour is not an honest indicator of reward to seed dispersers. Further, we propose an adoption of a statistical method in avian visual modelling studies that avoids the common statistical errors, such as violation of the congruence principle.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ANTONOV, A., AVILÉS, J. M., STOKKE, B. G., SPASOVA, V., VIKAN, J. R., MOKSNES, A., YANG, C., LIANG, W. & RØSKAFT, E. 2011. Egg discrimination in an open nesting passerine under dim light conditions. Ethology 117:11281137.CrossRefGoogle Scholar
AVILÉS, J. M. 2008. Egg colour mimicry in the common cuckoo Cuculus canorus as revealed by modelling host retinal function. Proceedings of the Royal Society of London series B – Biological Sciences 275:23452352.Google ScholarPubMed
AVILÉS, J. M., SOLER, J. J. & HART, N. S. 2011. Sexual selection based on egg colour: physiological models and egg discrimination experiments in a cavity-nesting bird. Behavioral Ecology and Sociobiology 65:17211730.CrossRefGoogle Scholar
AVILÉS, J. M., VIKAN, J. R., FOSSØY, F., ANTONOV, A., MOKSNES, A., RØSKAFT, E., SHYKOFF, J. A., MØLLER, A. P. & STOKKE, B. G. 2012. Egg phenotype matching by cuckoos in relation to discrimination by hosts and climatic conditions. Proceedings of the Royal Society of London series B – Biological Sciences 297:19671976.Google Scholar
BACKHAUS, W., MENZEL, R. & KREIßL, S. 1987. Multidimensional scaling of color similarity in bees. Biological Cybernetics 56:293304.CrossRefGoogle Scholar
BARTON, N. H. 2000. Genetic hitchhiking. Philosophical Transactions of the Royal Society of London Series B – Biological Sciences 355:15531562.CrossRefGoogle ScholarPubMed
BIONDINI, M. E., MIELKE, P. W. & REDENTE, E. F. 1991. Permutation techniques based on Euclidean analysis spaces: a new and powerful statistical method for ecological researches. Pp. 221240 in Feoli, F. & Orlóci, L. (eds.). Computer assisted vegetation analysis. Kluwer, Dordrecht.CrossRefGoogle Scholar
BOLKER, B. M., BROOKS, M. E., CLARK, C. J., GEANGE, S. W., POULSEN, J. R., STEVENS, H. H. & WHITE, J.-S. S. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24:127135.CrossRefGoogle ScholarPubMed
CASSEY, P., EWEN, J. G., MARSHALL, N. J., VOROBYEV, M., BLACKBURN, T. M. & HAUBER, M. E. 2009. Are avian eggshell colours effective intraspecific communication signals in the Muscicapoidea? A perceptual modelling approach. Ibis 151:689698.CrossRefGoogle Scholar
EDWARDS, D. P. & YU, D. W. 2007. The role of sensory traps in the origin, maintenance, and breakdown of mutualism. Behavioral Ecology and Sociobiology 61:13211327.CrossRefGoogle Scholar
EMURA, N., KAWAKAMI, K., DEGUCHI, T. & SONE, K. 2012. Potential role of frugivorous birds in the recovery process of forest vegetation after feral goat eradication in Mukojima Island, the Bonin Islands. Journal of Forest Research 17:352359.CrossRefGoogle Scholar
EMURA, N., DENDA, T., SAKAI, M. & UEDA, K. 2014. Dimorphism of the seed-dispersal organ in a pantropical coastal plant, Scaevola taccada: heterogeneous population structures between islands and microhabitat types. Ecological Research 29:733740.CrossRefGoogle Scholar
ENDLER, J. A. & MIELKE, P. W. 2005. Comparing entire colour patterns as birds see them. Biological Journal of the Linnean Society 86:405431.CrossRefGoogle Scholar
ENDLER, J. A., WESTCOTT, D. A., MADDEN, J. R. & ROBSON, T. 2005. Animal visual systems and the evolution of color patterns: sensory processing illuminates signal evolution. Evolution 59:17951818.Google ScholarPubMed
FADZLY, N., BURNS, K. C. & ZUHARAH, W. F. 2013. Evaluating frugivore-fruit interactions using avian eye modelling. Tropical Life Sciences Research 24:3150.Google ScholarPubMed
FEENEY, W. E., STODDARD, M. C., KILNER, R. M. & LANGMORE, N. E. 2014. “Jack-of-all-trades” egg mimicry in the brood parasitic Horsfield's bronze-cuckoo? Behavioral Ecology 25: 13651373.CrossRefGoogle Scholar
FORSMAN, A., SANESJÖ, J., CAESAR, S. M. & KARLSON, M. 2008. A model of ecological and evolutionary consequences of color polymorphism. Ecology 89:3440.CrossRefGoogle Scholar
FOSTER, M. S. & DELAY, L. S. 1998. Dispersal of mimetic seeds of three species of Ormosia (Leguminosae). Journal of Tropical Ecology 14:389411.CrossRefGoogle Scholar
FRECKLETON, R. P. & CÔTÉ, I. M. 2003. Honesty and cheating in cleaning symbioses: evolutionarily stable strategies defined by variable pay-offs. Proceedings of the Royal Society of London series B: Biological Sciences 270:299305.CrossRefGoogle ScholarPubMed
GALETTI, M. 2002. Seed dispersal of mimetic fruits: parasitism, mutualism, aposematism or exaptation? Pp. 177191 in Levey, D. J., Silva, W. R. & Galettti, M. (eds.). Seed dispersal and frugivory: ecology, evolution and conservation. CABI Publishing, New York.Google Scholar
GIGORD, L. D. B., MACNAIR, M. R. & SMITHSON, A. 2001. Negative frequency-dependent selection maintains a dramatic flower color polymorphism in the rewardless orchid Dactylorhiza sambucina (L.) Soò. Proceedings of the National Academy of Sciences USA 98:62536255.CrossRefGoogle ScholarPubMed
GILLESPIE, R. G., BALDWIN, B. G., WATERS, J. M., FRASER, C. I., NUKULA, R. & RODERICK, G. K. 2012. Long-distance dispersal: a framework for hypothesis testing. Trends in Ecology and Evolution 27:4756.CrossRefGoogle ScholarPubMed
GRAY, S. M. & MCKINNON, J. S. 2007. Linking color polymorphism maintenance and speciation. Trends in Ecology and Evolution 22:7179.CrossRefGoogle ScholarPubMed
HADFIELD, J. D. 2010. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. Journal of Statistical Software 33:122.CrossRefGoogle Scholar
HART, N. S. 2001. Variations in cone photoreceptor abundance and the visual ecology of birds. Journal of Comparative Physiology A 187:685698.CrossRefGoogle ScholarPubMed
HART, N. S., PARTRIDGE, J. C., CUTHILL, I. C. & BENNETT, A. T. D. 2000. Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L) and the blackbird (Turdus merula L). Journal of Comparative Physiology A 186:375387.CrossRefGoogle ScholarPubMed
HOWARTH, D. G., GUSTAFSSON, M. H. G., BAUM, D. A. & MOTLEY, T. J. 2003. Phylogenetics of the genus Scaevola (Goodeniaceae): implication for dispersal patterns across the Pacific Basin and colonization of the Hawaiian Islands. American Journal of Botany 90:915923.CrossRefGoogle ScholarPubMed
KAWAKAMI, K., MIZUSAWA, L. & HIGUCHI, H. 2009. Re-established mutualism in a seed-dispersal system consisting of native and introduced birds and plants on the Bonin Islands, Japan. Ecological Research 24:741748.CrossRefGoogle Scholar
KOSHITAKA, H., KINOSHITA, M., VOROBYEV, M. & ARIKAWA, K. 2008. Tetrachromacy in a butterfly that has eight varieties of spectral receptors. Proceedings of the Royal Society of London series B – Biological Sciences 275:947954.Google Scholar
LANGMORE, N. E., STEVENS, M., MAURER, G., HEINSOHN, R., HALL, M. L., PETERS, A. & KILNER, R. M. 2011. Visual mimicry of host nestlings by cuckoos. Proceedings of the Royal Society of London series B – Biological Sciences 278:24552463.Google ScholarPubMed
LEGENDRE, P. & LEGENDRE, L. 1998. Numerical ecology. (Second edition). Elsevier, Amsterdam. 853 pp.Google Scholar
MAIA, R., ELIASON, C. M., BITTON, P.-P., DOUCET, S. M. & SHAWKEY, M. D. 2013. pavo: an R package for the analysis, visualization and organization of spectral data. Methods in Ecology and Evolution 4:906913.CrossRefGoogle Scholar
ÖDEEN, A., HÅSTAD, O. & ALSTRÖM, P. 2011. Evolution of ultraviolet vision in the largest avian radiation – the passerines. BMC Evolutionary Biology 11:313.CrossRefGoogle ScholarPubMed
OSORIO, D., MIKLÓSI, A. & GONDA, Z. S. 1999. Visual ecology and perception of coloration patterns by domestic chicks. Evolutionary Ecology 13:673689.CrossRefGoogle Scholar
OSORIO, D. & VOROBYEV, M. 1996. Colour vision as an adaptation to frugivory in primates. Proceedings of the Royal Society of London series B – Biological Sciences 263:593599.Google ScholarPubMed
RAUFASTE, N. & ROUSSET, F. 2001. Are partial Mantel tests adequate? Evolution 55:17031705.Google ScholarPubMed
SARKER, D. 2008. Lattice: multivariate data visualization with R. Springer, New York. 268 pp.CrossRefGoogle Scholar
SIDDIQI, A., CRONIN, T. W., LOEW, E. R., VOROBYEV, M. & SUMMERS, K. 2004. Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. Journal of Experimental Biology 207:24712485.CrossRefGoogle ScholarPubMed
STODDARD, M. C. & PRUM, R. O. 2008. Evolution of Avian plumage color in tetrahedral color space: a phylogenetic analysis of New World buntings. American Naturalist 171:755776.CrossRefGoogle ScholarPubMed
STODDARD, M. C. & PRUM, R. O. 2011. How colorful are birds? Evolution of the avian plumage color gamut. Behavioral Ecology 22:10421052.CrossRefGoogle Scholar
STODDARD, M. C. & STEVENS, M. 2011. Avian vision and the evolution of egg color mimicry in the common cuckoo. Evolution 65:20042013.CrossRefGoogle ScholarPubMed
STUART-FOX, D. 2005. Deception and the origin of honest signals. Trends in Ecology and Evolution 20:521523.CrossRefGoogle ScholarPubMed
TANAKA, K. D. In press. A colour to birds and to humans: why is it so different? Journal of Ornithology.Google Scholar
TANAKA, K. D., MORIMOTO, G., STEVENS, M. & UEDA, K. 2011. Rethinking visual supernormal stimuli in cuckoos: visual modeling of host and parasite signals. Behavioral Ecology 22:10121019.CrossRefGoogle Scholar
VOROBYEV, M. & OSORIO, D. 1998. Receptor noise as a determinant of colour thresholds. Proceedings of the Royal Society of London series B – Biological Sciences 265:351358.CrossRefGoogle ScholarPubMed
VOROBYEV, M., OSORIO, D., BENNETT, A. T. D., MARSHALL, N. J. & CUTHILL, I. C. 1998. Tetrachromacy, oil droplets and bird plumage colours. Journal of Comparative Physiology A 183:621633.CrossRefGoogle ScholarPubMed