Abstract
Many plants produce colour-polymorphic fruits. However, the processes responsible for the evolution and maintenance of fruit colour polymorphisms are poorly understood. We investigated the fruit colour polymorphism in Gaultheria depressa var. novae-zealandiae (Ericaceae), a predominantly bird-dispersed, alpine shrub from New Zealand, by testing whether colour morph frequencies vary geographically to maximise fruit-foliage colour contrasts. We also conducted a seed germination experiment to test whether fruit colour morphs vary in their susceptibility to UV damage. Results showed that ‘red’ fruits were more abundant at lower elevations, while ‘white’ fruits were predominant at higher elevations. Leaf colours shifted from ‘green’ in appearance at lower elevations to ‘red’ at higher elevations. Analyses of fruit-foliage colour contrasts showed that ‘red’ fruits were more conspicuous at lower elevations, and ‘white’ fruits were more conspicuous at higher elevations, which was consistent with the hypothesis that colour morph frequencies vary geographically to maximise their conspicuousness to dispersers. However, ‘red’ fruits were generally more conspicuous than ‘white’ fruits, regardless of elevation, indicating that the maintenance of the polymorphism could not be attributed to fruit-foliage colour contrasts alone. The seed germination experiment showed that ‘white’ fruits were more resistant to UV damage, suggesting the preponderance of ‘white’ fruited individuals in the landscape results from a greater degree of protection from UV damage. The fruit colour polymorphism in Gaultheria depressa var. novae-zealandiae therefore appears to be maintained by trade-offs between conspicuousness to dispersers and tolerance to UV damage, advocating a pluralistic approach to the problem in the future.
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References
Albrecht J, Hagge J, Schabo DG, Schaefer HM, Farwig N (2018) Reward regulation in plant–frugivore networks requires only weak cues. Nat Commun 91:1–11
Allen M, McKenzie R (2005) Enhanced UV exposure on a ski-field compared with exposures at sea level. Photochem Photobiol Sci 4:429–437
Amico GC, Rodriguez-Cabal MA, Aizen MA (2011) Geographic variation in fruit colour is associated with contrasting seed disperser assemblages in a south-Andean mistletoe. Ecography 34:318–326
Bach CE, Kelly D (2004) Effects of forest edges, fruit display size, and fruit colour on bird seed dispersal in a New Zealand mistletoe, Alepis flavida. N Z J Ecol 28:93–103
Ballaré CL, Caldwell MM, Flint SD, Robinson SA, Bornman JF (2011) Effects of solar ultraviolet radiation on terrestrial ecosystems. Patterns, mechanisms, and interactions with climate change. Photochem Photobiol Sci 10:226–241
Bannister P (1990) Seed germination in Gaultheria antipoda, G. depressa, and Pernettya macrostigma. NZ J Bot 28:357–358
Bhatt A, Bhat NR, Carón MM, Gallacher D (2019) Dimorphic fruit colour is associated with differences in germination of Calligonum comosum. Botany 97:263–268
Blumthaler M, Ambach W, Ellinger R (1997) Increase in solar UV radiation with altitude. J Photochem Photobiol B 39:130–134
Burns KC (2005) Does mimicry occur between fleshy-fruits? Evol Ecol Res 7:1067–1076
Burns KC (2006) Weta and the evolution of fleshy fruits in New Zealand. N Z J Ecol 30:405–406
Burns KC (2015) The color of plant reproduction: macroecological trade-offs between biotic signaling and abiotic tolerance. Front Ecol Evol 3:118
Burns KC, Dalen JL (2002) Foliage color contrasts and adaptive fruit color variation in a bird-dispersed plant community. Oikos 963:463–469
Burns KC, Cazetta E, Galetti M, Valido A, Schaefer HM (2009) Geographic patterns in fruit colour diversity: do leaves constrain the colour of fleshy fruits? Oecologia 1592:337–343
Cazetta E, Schaefer HM, Galetti M (2009) Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds. Evol Ecol 23:233–244
Chen LX, Xu ST, Ding WH, Li JM, Alpert P (2020) Genetic diversity and offspring fitness in the red and white fruit color morphs of the wild strawberry Fragaria pentaphylla. J Plant Ecol 13:36–41
Cordero RR, Damiani A, Jorquera J, Sepúlveda E, Caballero M, Fernandez S, Feron S, Llanillo PJ, Carrasco J, Laroze D, Labbe F (2018) Ultraviolet radiation in the Atacama Desert. Antonie Van Leeuwenhoek 111:1301–1313
de Camargo MGG, Cazetta E, Schaefer HM, Morellato LPC (2013) Fruit color and contrast in seasonal habitats–a case study from a cerrado savanna. Oikos 122:1335–1342
Duan Q, Goodale E, Quan RC (2014) Bird fruit preferences match the frequency of fruit colours in tropical Asia. Sci Rep 41:1–8
Duthie C, Gibbs G, Burns KC (2006) Seed dispersal by weta. Science 311:1575–1575
Endler JA, Mielke PW (2005) Comparing entire colour patterns as birds see them. Biol J Lin Soc 864:405–431
Fadzly N, Jack C, Schaefer HM, Burn KC (2009) Ontogenetic colour changes in an insular tree species: signalling to extinct browsing birds? New Phytol 184:495–501
Figueroa JA, Castro SA (2002) Effects of birdingestion on seed germination of four woody species of the temperate rainforestof Chiloé island, Chile. Plant Ecol 160:17–23
Fritsch PW, Lu L, Bush CM, Wagstaff SJ, Kron KA (2021) Phylogenetic analysis supports the allochthonous origin of gynodioecy in New Zealand Gaultheria Kalm ex L. NZ J Bot 59:175–197
Gervais JA, Noon BR, Willson MF (1999) Avian selection of the color-dimorphic fruits of salmonberry, Rubus spectabilis: a field experiment. Oikos 84:77–86
Goldsmith TH (1990) Optimization, constraint, and history in the evolution of eyes. Q R Biol 65:281–322
Gould KS (2004) Nature’s Swiss army knife: the diverse protective roles of anthocyanins in leaves. J Biomed Biotechnol 5:321–325
Grant RH, Heisler GM, Gao W (2002) Estimation of pedestrian level UV exposure under trees. Photochem Photobiol 75:369–376
King P, Milicich L, Burns KC (2011) Body size determines rates of seed dispersal by giant king crickets. Popul Ecol 53:73–80
Körner C, Kèorner C (1999) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, Berlin
Landi M, Tattini M, Gould KS (2015) Multiple functional roles of anthocyanins in plant-environment interactions. Environ Exp Bot 119:4–17
Larsen H, Burns KC (2012) Seed dispersal effectiveness increases with body size in New Zealand alpine scree weta (Deinacrida connectens). Austral Ecol 37:800–806
Liley JB, McKenzie RL (2006) Where on Earth has the highest UV. UV Radiat Eff 68:36–37
Lim G, Burns KC (2021) Do fruit reflectance properties affect avian frugivory in New Zealand? New Zealand J Bot. https://doi.org/10.1080/0028825X.2021.2001664
Lomáscolo SB, Speranza P, Kimball RT (2008) Correlated evolution of fig size and color supports the dispersal syndromes hypothesis. Oecologia 156:783–796
Lu L, Fritsch PW, Matzke NJ, Wang H, Kron KA, Li DZ, Wiens JJ (2019) Why is fruit colour so variable? Phylogenetic analyses reveal relationships between fruit-colour evolution, biogeography and diversification. Glob Ecol Biogeogr 28:891–903
MatLab. (2018) 9.7.0.1190202 R2019b. Natick, Massachusetts The MathWorks Inc
McKenzie RL, Johnston PV, Smale D, Bodhaine BA, Madronich S (2001) Altitude effects on UV spectral irradiance deduced from measurements at Lauder, New Zealand, and at Mauna Loa Observatory. Hawaii Geophys Res 106:22845–22860
Moore S, Bannister P (2002) Aspects of the germination of some New Zealand Ericaceae. Special Publication-Agronomy Society of New Zealand, 83–90
Ordano M, Blendinger PG, Lomáscolo SB, Chacoff NP, Sánchez MS, Nunez Montellano MG et al (2017) The role of trait combination in the conspicuousness of fruit display among bird-dispersed plants. Funct Ecol 31:1718–1727
Ozel HB, Abo Aisha AES, Cetin M, Sevik H, Zeren Cetin I (2021) The effects of increased exposure time to UV-B radiation on germination and seedling development of Anatolian black pine seeds. Environ Monit Assess 193:1–11
Poole AL, Adams NM (1994) Trees and shrubs of New Zealand. Manaaki Whenua Press, Lincoln, Canterbury, New Zealand
R Core Team (2018) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/
Schaefer HM, Ruxton GD (2011) Plant-animal communication. OUP Oxford, Oxford
Schaefer HM, Schaefer V, Levey DJ (2004) How plant–animal interactions signal new insights in communication. Trends Ecol Evol 19:577–584
Scholtyßek C, Kelber A (2017) Color vision in animals: from color blind seals to tetrachromatic vision in birds. Der Ophthalmologe Zeitschrift Der Deutschen Ophthalmologischen Gesellschaft 114(11):978–985
Simpson MJA (1978) Lichens of Nelson Lakes National Park, New Zealand. NZ J Bot 16:507–527
Sinnott-Armstrong MA, Downie AE, Federman S, Valido A, Jordano P, Donoghue MJ (2018) Global geographic patterns in the colours and sizes of animal-dispersed fruits. Glob Ecol Biogeogr 27:1339–1351
Sinnott-Armstrong MA, Donoghue MJ, Jetz W (2021) Dispersers and environment drive global variation in fruit colour syndromes. Ecol Lett 24:1387–1399
Sommaruga R (2001) The role of solar UV radiation in the ecology of alpine lakes. J Photochem Photobiol, B 62(1–2):35–42
Stoddard MC, Prum RO (2008) Evolution of avian plumage color in a tetrahedral color space: A phylogenetic analysis of new world buntings. Am Nat 1716:755–776
Sun Q, Wu L, Yang Y, Zhao J, Zhang Y (2021) Geographic variation of fruit color dimorphism in Viscum coloratum (Kom.) Nakai in Northeast China. Flora 280:151846
Torres M, Frutos G, Duran JM (1991) Sunflower seed deterioration from exposure to UV-C radiation. Environ Exp Bot 31:201–207
Traveset A, Willson MF (1998) Ecology of the fruit-colour polymorphism in Rubus spectabilis. Evol Ecol 123:331–345
Valenta K, Nevo O (2020) The dispersal syndrome hypothesis: how animals shaped fruit traits, and how they did not. Funct Ecol 34(6):1158–1169
Valenta K, Kalbitzer U, Razafimandimby D, Omeja P, Ayasse M, Chapman CA, Nevo O (2018) The evolution of fruit colour: phylogeny, abiotic factors and the role of mutualists. Sci Rep 81:1–8
Vazquez MS, Rodriguez-Cabal MA, Amico GC (2022) The forest gardener: A marsupial with a key seed-dispersing role in the Patagonian temperate forest. Ecol Res 37:270–283
Voigt FA, Bleher B, Fietz J, Ganzhorn JU, Schwab D, Böhning-Gaese K (2004) A comparison of morphological and chemical fruit traits between two sites with different frugivore assemblages. Oecologia 141:94–104
Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc B 265:351–358
Wang QW, Hidema J, Hikosaka K (2014) Is UV-induced DNA damage greater at higher elevation? Am J Bot 101:796–802
Webb CJ, Simpson MJA (2001) Seeds of New Zealand: gymnosperms and dicotyledons. Manuka Press, Christchurch, New Zealand
Whitney KD (2005) Linking frugivores to the dynamics of a fruit color polymorphism. Am J Bot 92:859–867
Whitney KD, Stanton ML (2004) Insect seed predators as novel agents of selection on fruit color. Ecology 85:2153–2160
Willson MF, Whelan CJ (1990) The evolution of fruit color in fleshy-fruited plants. Am Nat 1366:790–809
Wotton DM, Drake DR, Powlesland RG, Ladley JJ (2016) The role of lizards as seed dispersers in New Zealand. J R Soc N Z 46:40–65
Wyman TE, Trewick SA, Morgan-Richards M, Noble AD (2011) Mutualism or opportunism? Tree fuchsia (Fuchsia excorticata) and tree weta (Hemideina) interactions. Austral Ecol 36:261–268
Young LM, Bell RJ (2010) Frugivory and primary seed dispersal by a New Zealand falcon (Falco novaeseelandiae) at Red Tarns, Mt Sebastapol, New Zealand. Notornis 57:94–95
Young LM, Kelly D (2014) Current rates of fruit removal and seed dispersal in New Zealand fleshy-fruited mountain plants. N Z J Ecol 38:288–296
Young LM, Kelly D, Nelson XJ (2012) Alpine flora may depend on declining frugivorous parrot for seed dispersal. Biol Cons 147:133–142
Acknowledgements
The authors would like to thank Dr Richard McKenzie of NIWA for his invaluable advice.
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This research was supported by the Wellington Botanical Society and the Centre for Biodiversity and Restoration Ecology, Victoria University of Wellington.
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GL and KCB conceived the idea, designed the methods, and wrote the manuscript together. GL collected and analysed the data.
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Communicated by Francisco E Fonturbel.
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Lim, G., Burns, K.C. Maintenance of a fruit colour polymorphism along an elevational gradient in the Southern Alps of New Zealand. Oecologia 201, 83–90 (2023). https://doi.org/10.1007/s00442-022-05287-5
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DOI: https://doi.org/10.1007/s00442-022-05287-5