MINI review MINI REVIEW Signaling & Behavior 5:1, 1-6; January 2010; © 2010 Landes Bioscience Is a common defensive strategy in ? Speculation on signal deception in the New Zealand flora

Kevin C. Burns

School of Biological Sciences; Victoria University of Wellington; Wellington, New Zealand

Key words: aposomatic colouration, cryptic colouration, herbivory, , plant defence

words, they may result from historical coevolutionary dynam- Colour is a common feature of animal defence. Herbivorous ics between plants and their herbivores, rather than present day insects are often coloured in shades of green similar to their selection pressures alone. preferred food plants, making them difficult for predators to locate. Other insects advertise their presence with bright Despite these important insights, our understanding of colour- colours after they sequester enough toxins from their food based defence in plants is in its infancy and progress hinges on plants to make them unpalatable. Some insects even switch be- quantitative tests in other parts of the globe. Previous work is tween cryptic and aposomatic coloration during development.1 also restricted largely to aposomatic, or warning colours.11 Given Although common in animals, quantitative evidence for colour- that cryptic colouration is widespread in animals, it might also based defence in plants is rare. After all, the primary function be common in plants. Yet we are far from determining if this is of plant leaves is to absorb light for photosynthesis, rather than true. reflect light in ways that alter their appearance to herbivores. Here, I discuss several New Zealand plant species that seem However, recent research is beginning to challenge the notion to be coloured in ways that would make them difficult for her- that colour-based defence is restricted to animals. bivores to locate. I suggest that these plants are anachronisms; their unusual appearance is the result of selection from flight- less browsing birds called moa, which went extinct following the Temperate deciduous forests provide what is arguably the most arrival of humans in New Zealand 750 years ago. I also discuss extraordinary display of colour in nature. Prior to leaf-fall in the difficulties associated with testing for cypsis in plants and autumn, the leaves of many deciduous tree species in Asia, Europe finish by outlining a methodological approach to test for colour- and turn red, leading to brilliantly coloured based defence in plants when the putative herbivores are either landscapes. Once thought to be a by-product of chlorophyll re- unknown or extinct. absorption prior to leaf abscission, autumn flushes in red leaf colours are now known to result from the active synthesis of red- New Zealand Lancewood coloured pigments.2,3 Although the exact reason for the produc- tion of red-coloured pigments prior to leaf-fall is unknown, it has crassifolius (A. Cunn) C. Koch , or New recently been hypothesized to be a form of defence.4 Aphids are Zealand lancewood, is one of the strangest looking plants on common phloem-feeding herbivores in deciduous forests, which Earth (Fig. 1). The primary reason for its peculiar appearance disperse from the forest floor into tree crowns in autumn, and the is that it is strongly heteroblastic, meaning its gross morphol- synthesis of red pigments could signal the timing of leaf fall and ogy undergoes sudden and dramatic changes during ontogeny. the reduction in the supply of photosynthate.5,6 Although there Although heteroblasty is unusually common in the New Zealand are also physiological explanations,7 red leaf colours could be a flora, it is exceptional in P. crassifolius. In fact, it changes in reliable signal of unpalatably to herbivores.8 appearance so completely during ontogeny that Sir Joseph Banks, Lev-Yadun and Holopainen9 recently showed that there are the famous botanist that accompanied James Cook on the voyage This manuscript has been published online, prior to printing. Once the issue is complete and page numbers have been assigned, the citation will change accordingly. the issue is complete and page numbers have Once to printing. has been published online, prior This manuscript fewer red-coloured deciduous tree species in Europe than in of the Endeavour, named the juvenile and adult forms of P. cras- North America, and they speculate that historical processes sifolius as separate species. are the cause. During the advance and retreat of glaciers in the After germinating, P. crassifolius seedlings (<10 cm tall) are Pleistocene, the European Alps would have hindered the move- immediately unusual. Instead of being green, seedling leaves ment of plants and their herbivores in response to long-term are a strange mottled-brown colour. However, once plants reach climate change. Mountain ranges in North America run perpen- approximately 10–20 cm in height, they begin to produce strik- dicular to the equator, which would facilitate these migrations. ingly different-looking leaves. These juvenile leaves are very long, Therefore, if red leaves are signals to herbivores, geographic dif- stiff and narrow. They also produce strange thorn-like dentitions ferences in leaf pigmentation may be ‘anachronistic’.10 In other along their margins, each coinciding with a distinctive patch of differently coloured leaf tissue. A final morphological transfor- Correspondence to: Kevin C. Burns; Email: [email protected] mation occurs once plants grow to approximately three metres in Submitted: 10/04/09; Accepted: 10/05/09 height, when they begin to produce green, oblong leaves that are Previously published online: rather ordinary in appearance. www.landesbioscience.com/journals/psb/article/10236

www.landesbioscience.com Plant Signaling & Behavior 1 down the oesophagus.14 Thorns that arise from stems, such as those produced by many species of Acacia for protection against large mammals, are ineffective deterrents to bird browsers and are correspondingly rare in the New Zealand flora. In order to deter bird browsers, plants need other types of defence.15-20 Fadzly et al.12 found that colour may have been a critical compo- nent of a defensive strategy that evolved in P. crassifolius to deter moa browsing. Spectrographic analyses of seedling leaves from the perspective of birds indicate that their mottled brown colour would have made them very dif- ficult for moa to locate amongst a background of leaf litter on the for- est floor. The juvenile leaves would have been difficult for moa to swal- low, given that moa lacked teeth. Without the ability to chew, they had to swallow leaves whole or at least in large pieces, which would have been a difficult task, thanks in part to their long, rigid shape and sharp lateral spines. Spectrometric analyses showed that the distinc- tive colour patches associated with each spine would have been par- ticularly conspicuous to birds, who are sensitive to bright (achromatic) visual signals. Paleoecological records indicate that the maxi- mum browsing height of the tall- est moa species was approximately three metres.13 So the sudden shift to leaves that are ordinary in size, shape and colour at approximately three metres roughly coincides with a height refuge from bird browsers. These results are important for Figure 1. Mottled-brown seedling leaves (A), stiff, serrated juvenile leaves (B) and ordinary-looking adult plants (C) of Pseudopanax crassifolius. two reasons. First, they provide one of the first quantitative exam- ples for crypsis in plants. Second, So why is P. crassifolius so unusual looking? A recent study sug- they illustrate that plants can alternate colour-based defensive gests that browsing birds may have selected for its unusual appear- strategies during ontogeny, switching from being cryptically ance.12 Prior to human arrival, New Zealand lacked native land coloured as seedlings, to aposomatically coloured as juveniles and mammals (except for two species of bat) and instead was home to ultimately colour-undefended as adults, once they grew above the giant, flightless birds called moa.13 Because birds lack teeth and reach of the putative browser. Many animals switch colour-based cannot chew, they must swallow leaves whole, by first placing them defensive strategies during ontogeny.1 Fadzly et al.12 show evolu- in their bill and then snapping their head forward to orient them

2 Plant Signaling & Behavior Volume 5 Issue 1 tion might sometimes favour a similar colour-based strategy in plants.

New Zealand Mistletoes

Rather than referring to a sin- gle phylogenetic lineage, the term ‘mistletoe’ refers to a poly- phyletic group of plants that have evolved parasitic lifestyles independently.21,22 There are two main phylogenetic lin- eages of mistletoes: the family Loranthaceae, which evolved in the Southern hemisphere, and the family Viscaceae, which evolved in the northern hemisphere.23,24 Both lineages have since dis- persed out of their native hemi- spheres and many geographic locales now house members of both families. Figure 2. Korthasella salicornioides infecting Leptospermum scoparium. Australasia is home to an unusually high diversity of Loranthaceous mistletoes, which show varying degrees of host of alpine habitat. Alpine habitat does not support forest and is specialisation; some species are found on only a single host spe- instead inhabited by herbs, tussocks and short-statured shrubs. cies, while other exploit a large number of different host species. Alpine areas in New Zealand also contain a distinctive type Several previous observers have noted that Australian mistletoes of rocky habitat called ‘scree slopes’, which occur on especially often resemble their hosts with striking accuracy. Possums (order steep, alpine terrain. Scree slopes are demanding places for plants Phalangeriformes) are important, arboreal browsers in Australian to grow, because the soil surface is comprised of large rocks that forests and many host trees are heavily defended chemically. are moving continuously down slope. Although these rocks move If Australian mistletoes have evolved to mimic their hosts mor- slowly, over the course of a perennial plant’s lifespan this move- phologically, possums may confuse them with their chemically ment acts to separate vegetative plant parts from their root sys- defended hosts.25,26 tems. Numerous plant species from a wide range of phylogenetic A similar situation may occur in New Zealand. Some backgrounds have adapted to this harsh habitat by producing Viscaceous mistletoes, such as Korthalsella salicornioides (A. Cunn) stems that connect above- and below-ground tissues by continu- Tiegh., parasitise shrubs and small trees and often look remark- ously elongating as vegetative plant parts are pulled down-slope ably similar to their preferred hosts (Fig. 2). Common herbivores away from their root systems. such as insects might therefore have difficulties distinguishing Another distinctive attribute of plant species that are adapted mistletoes from chemically defended hosts. On the other hand, to scree slopes is that they are very difficult to find.27 Scree Loranthaceous mistletoes in New Zealand look quite different slopes are typically slate-grey or even black, and plants such as from their preferred hosts. One difference between families that Notothlaspi rosulatum match the colour of their rocky habitat may explain their apparent differences in host resemblance is that with surprising accuracy (Fig. 3). Whether moa included them in Viscaceous mistletoes attack mostly small-statured hosts, while the diet regularly is not known. However, if they did their colour Loranthaceous species usually attack taller trees. Therefore, if may have made them easy for moa of overlook. New Zealand mistletoes have evolved to resemble their preferred Substrate colour matching seems to occur in a wide range of hosts, the putative herbivore may have attacked small-statured other plant species inhabiting permanently rocky habitat. Perhaps hosts preferentially. Although it is difficult to pinpoint which the best-known example is the genus Lithops, which grows in the herbivore this might be, one obvious candidate is moa. rocky deserts of Southern and rightly deserves its common name ‘stone plant’, given their remarkable resemblance to rocks Scree Plants and small pebbles. Like New Zealand scree plants, the ‘stone plant’ syndrome is not restricted to this genus, and many spe- Approximately 15 million years ago New Zealand began a period cies from a range of phylogenetic backgrounds appear to have of very rapid tectonic uplift, which transformed New Zealand converged on this distinctive appearance. Other notable exam- into a mountainous archipelago characterised by extensive areas ples of cryptically coloured plants inhabiting rocky habitats are

www.landesbioscience.com Plant Signaling & Behavior 3 Figure 3. Notothlaspi rosulatum in flower.

­short-statured cacti in North American deserts (Mammillaria A Hypothesis spp.28) and herbs that inhabit serpentine grasslands of (e.g., Streptanthus spp., Strauss unpubl.). Under what conditions is crypsis a viable defensive strategy in plants? Several conditions are necessary: (1) Plants need to be preyed upon by visually orientated herbivores. If a plant’s main herbivores locate plants using olfactory or tactile cues, visual

4 Plant Signaling & Behavior Volume 5 Issue 1 mimicry would obviously be ineffective. (2) Plants need to be habitat specialists, such that they grow in environments that pro- vide a consistent visual background. Plant species that utilise a wide range of habitats lack a specific background that they can evolve to resemble, which would likely inhibit the evolution of crypsis, unless species were locally adapted to different habitats. ‘Null models’ are pattern-generating algorithms that simulate (3) Plants must be short-statured, such that they grow in close biological patterns in the absence of a structuring process.31,32 physical proximity to the visual background generated by their Simply put, null models test hypotheses by comparing field obser- preferred habitat. By definition, an object is cryptic because it vations to randomised expectations. Although they are power resembles its background. So when a plant grows away from a tools for identifying patterns in field observations, they cannot background that it resembles, it looses any effect of crypsis. (4) be used to precisely identify the processes responsible for them. The preferred habitat must be unpalatable. If the visual back- By providing a means to test whether a plant shows an ground of a preferred habitat were itself palatable, for instance unusual likeness to the appearance of its preferred habitat, null when mistletoes parasitize palatable hosts, there would be no models can provide the foundations for a research program on adaptive benefit to resembling it. Under these four circum- plant crypsis. Qualitative judgements based on human vision are stances, crypsis appears to be a viable defensive strategy in plants. insufficient to identify cryptic plants, because the human eye dif- Although there is little evidence to support this hypothesis to fers markedly from most herbivores, but see ref. 33. Apparently date, this may be due to a lack of investigative effort rather than cryptic colour patterns could also arise by chance relatively easily. realism. A plant whose colour is determined solely by physiological pro- cesses could easily disperse by chance into an environment that A Methodological Framework to Test for Crypsis is coloured similarly. To test whether a scree plant is cryptically coloured, null How does one test the hypothesis that a plant is cryptically models can be used to redistribute a population of such plants coloured? The most obvious way is to conduct an experiment across a range of alpine habitats. Differences between the spec- by manipulating the plant’s colour and offering it to herbivores. tral properties of leaves and each alpine habitat can then be cal- An experimental approach is the only way to provide a direct culated to establish whether scree plants are less conspicuous in link between plant colour and herbivore damage. Unfortunately, their preferred habitat relative to other potentially suitable habi- this might not always be possible. There are numerous obstacles tats. Similarly, null model simulations can be used to simulate to designing effective experiments in ecology.29 One such barrier the distribution of mistletoes among potential host species. The to experimental tests of plant crypsis is an absence of appropri- conspicuousness of observed mistletoe-host species combinations, ate techniques to manipulate the colour of plants leaves. In the both in terms of morphology and reflectance spectra,34,35 can then case of New Zealand, another serious problem is that an impor- be compared to all other potential mistletoe-host species combina- tant group of herbivores is now extinct, which makes a direct tions. If observed species combinations are less conspicuous than experimental approach impossible. Abiguity concerning putative what would be expected by chance pairings of mistletoes and their herbivores may also be the rule rather than an exception. Some hosts, one can conclude a cryptic pattern exists. Null model com- researchers have argued that this situation applies to most plants parisons also can be recalculated according to the visual systems across the globe: of different types of herbivores,36 to test whether results change “Living organisms are beautifully built to survive and reproduce from the perspective of different types of herbivores. in their environments. Or that is what Darwinians say. But actu- While this approach cannot establish whether herbivores ally it isn’t quite right. They are beautifully built for survival in would actually overlook a plant, it can be used to establish their ancestor’s environments… Since modern man has drastically whether a plant is especially inconspicuous. This is a powerful changed the environment of many animals and plants over a time insight and an important first step in testing the crypsis hypoth- scale that is negligible by evolutionary standards, we can expect esis. By providing a means to test for a cryptic pattern, null mod- to see anachronistic adaptations everywhere.” (Richard Dawkins, els can lead the way to understanding whether plants sometimes quoted by30). hide from predators. Many scientific disciplines, such as astrophysics, geology and palaeontology, suffer from an inability to conduct manipulations Acknowledgements as a regular part of scientific inquiry. Similarly, experimentation I would like to thank Nicholas Gotelli, Kevin Goold, Martin is beyond the reach of most questions in biogeography, because Schaeffer and Sharon Strauss for helpful comments and discus- most biogeographic phenomena operate on spatial and temporal sions concerning plant colours. scales that are too large to manipulate. Instead, biogeographers rely on observations and indirect hypothesis testing, in much the same way as astrophysicists, geologists and palaeontologists. However, biogeographers have developed a useful methodological tool that can be used to good effect under these circumstances.

www.landesbioscience.com Plant Signaling & Behavior 5 References 13. Worthy T, Holdaway RH. The lost world of the 24. Watson DM. Mistletoe: A unique constituent of moa: prehistoric life of New Zealand. University of canopies worldwide. In Forest canopies (Lowman 1. Booth CL. Evolutionary significance of ontoge- Canterbury Press 2002. MD, Rinker HB, eds.,), London UK, Elsevier 2004. netic colour change in animals. Biol J Linn Soc 2008; 14. Bond WJ, Lee WG, Craine JM. Plant structural 25. Barlow BA, Weins D. Host-parasite resemblance in 40:125-63. defences against browsing birds: a legacy of New Australian mistletoes:the case for cryptic mimicry. 2. Lee DW. Anthocyanins in autumn leaf senescence. Zealand’s extinct . Oikos 2004; 104:500-8. Evolution 1977; 31:69-84. Adv Bot Res 2002; 37:147-65. 15. Greenwood RM, Atkinson IAE. Evolution of the 26. Canyon DV, Hill CJ. Mistletoe host-resemblance: 3. Gould KS. Nature’s Swiss army knife: the diverse divaricating plants in New Zealand in relation to A study of herbivory, nitrogen and moisture in two protective roles of anthocyanins in leaves. J Biomed Moa browsing. Proc N Z Ecol Soc 1977; 24:21-33. Australian mistletoes and their host trees. Aust J Ecol Biotech 2004; 5:314-20. 16. Givnish TJ, Sytsma KJ, Smith JF, Hahn WJ. Thorn- 1997; 22:395-403. 4. Archetti M. The origin of autumn colours by coevolu- like prickles and heterophylly in Cynae: adaptations 27. Carlquist S. Island Biology. Columbia University tion. Journal of Theoretical Biology 2000; 205:625- to extinct avian browsers on Hawaii? Proc Nat Acad Press 1974. 30. Sci USA 1994; 91:2810-4. 28. Hernández HM, Gómez-Hinostrosa C, Bárcenas 5. Archetti M, et al. Unravelling the evolution of 17. Burns KC, Dawson JW. A morphological comparison RT. Diversity, spatial arrangement, and endemism autumn colours: an interdisciplinary approach. Trend of leaf heteroblasty between New Caledonia and New of Cactaceae in the Huizache area, a hot-spot in the Ecol Evol 2009; 24:166-73. Zealand. N Z J Bot 2006; 44:387-96. Chihuahuan Desert. Biod Conser 2001; 10:1097- 6. Döring TF, Archetti M, Hardie J. Autumn leaves 18. Burns KC, Dawson JW. Heteroblasty on Chatham 112. seen through herbivore eyes. Proc R Soc B 2009; Island: a comparison with New Zealand and New 29. Underwood AJ. Experiments in Ecology. Cambridge 276 :1654-7. Caledonia. N Z J Ecol 2009; 33:In press. Univ Press 1997. 7. Lee DW, Gould KS. Why leaves turn red. Am Sci 19. Bond WJ, Silander JA. Springs and wire plants: 30. Barlow C. The ghosts of evolution. Nonsensical 2002; 90:524-32. anachronistic defences against Madagascar’s extinct fruits, missing partners, and other ecological anach- 8. Chittka L, Döring TF. Are autumn foliage colors red elephant birds. Proc Royal Soc Lond, B 2007; ronisms. New York NY, USA: Basic Books 2000; signals to aphids? PLoS Biol 2007; 5:187. 274:1985-92. 304. 9. Lev-Yadun S, Holopainen JK. Why red-dominated 20. Eskildsen LI, Olesen JM, Jones CG. Feeding response 31. Gotelli NJ, Graves GR. Null models in ecology. autumn leaves in America and yellow-dominated of the Aldabra giant tortoise (Geochelone gigantea) to Smith Inst Press USA 1996. autumn leaves in northern Europe? New Phytol island plants showing heterophylly. J Biogeogr 2004; 32. Gotelli NJ. Research frontiers in null model analysis. 2009; 183:506-12. 31:1785-90. Gbl Ecol Biogeogr 2001; 10:337-43. 10. Janzen DH, Martin PS. Neotropical anachronisms: 21. Norton DA, Carpenter MA. Mistletoes as parasites: 33. Barrett SCH. Crop mimicry in weeds. Econ Bot the fruits the gomphotheres ate. Science 1982; host specificity and speciation. Trend Ecol Evol 1998; 1983; 37:255-82. 215 :19-27. 13:101-5. 34. Endler JA, Mielke PW. Comparing entire colour 11. Lev-Yadun S. Aposomatic (warning) colouration 22. Press MC, Phoenix GK. Impacts of parasitic plants patterns as birds see them. Biol J Linn Soc 2005; in plants. Baluška F, (ed.,), Plant-Environment on natural communities. New Phytol 2005; 166:737- 86:405-31. Interactions, Signalling and Communication in 51. 35. Beaumont S, Burns KC. Vertical gradients in leaf Plants. Springer-Verlag, Berlin 2009; 167-202. 23. Shaw DC, Watson DM, Mathiasen RL. Comparison trait diversity in a New Zealand forest. Trees 2009; 12. Fadzly N, Jack C, Schaefer HM, Burns KC. of dwarf mistletoes (Arceuthobium spp., Viscaceae) in 23:328-39. Ontogenetic colour changes in an insular tree species: the western United States with mistletoes (Amyema 36. Schaefer HM, Schaefer V, Vorobyev M. Are fruit Signalling to extinct browsing birds? New Phytol spp., Lornathaceae) in Australia—ecological analogs colors adapted to consumer vision and birds equally 2009; 184:495-501. and reciprocal models for ecosystem management. efficient in detecting colorful signals? Am Nat 2007; Aust J Bot 2004; 52:481-98. 169:159-69.

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