Tuatara: Volume 32, April 1993
Ghost Stories: Moa, Plant Defences and Evolution in New Zealand
Ghost Stories: Moa, Plant Defences and Evolution in New Zealand.
The hypothesis that there is a large number of specific adaptations in New Zealand flora to browsing by the moa (large flightless birds) is critically discussed. While there clearly can be no definitive test of the hypothesis as the moa are extinct, the circumstantial evidence previously proposed in its favour is mostly ambiguous or irrelevant. Tests of the hypothesis based on the current ecological preferences of plants with putative anti-moa browsing adaptations are likewise inadequate or inconclusive. Experimental tests with browsing mammals are unhelpful. Of the many browsing adaptations that have been suggested, only spines and mottling of understorey leaves merit further investigation. Nevertheless, while specific adaptations to avian browsing may be rare in the New Zealand flora, more generalised anti-herbivore adaptations are common.
Before European settlement, New Zealand had no browsing or grazing mammals. Their role was filled by large flightless birds, collectively called the moa (Order Dinornithiformes). Polynesians, arriving about 1000 years ago, had hunted the moa to extinction by about 400 years ago (Anderson 1989b). New Zealand was therefore free of terrestrial browsing vertebrates from then until the European introduction of a wide range of browsing and grazing mammals, beginning with goats in the late eighteenth century.
Early this century it became apparent that introduced mammals were rapidly degrading the vegetation, primarily by killing browse-sensitive trees and shrubs and preventing regeneration (Cockayne 1928). It was widely assumed that moa had been primarily grazing birds of open grasslands and had therefore exerted insignificant browsing pressure, resulting in a low level of defences against browsers in the indigenous flora.
Greenwood and Atkinson (1977) presented a detailed argument for widespread adaptation to moa browsing in the New Zealand vegetation, greatly extending previous suggestions that moa browsing may have been responsible for the evolution of the distinctive divaricating shrubs (Carlquist 1974:242, Livingstone 1974, Taylor 1975, Melville 1978). Since 1977 the moa browsing hypothesis, although meeting some opposition (McGlone and Webb 1981), has been strongly supported in both in the scientific literature (Burrows 1980, Lowry 1980, Mitchell 1980, Caughley 1983, Lee and Johnson 1984) and in the popular media. Atkinson page 2 and Greenwood (1989) recently comprehensively revised and extended their original work, and Batcheler (1989) added some novel suggestions for possible anti-browsing adaptations.
Critics of introduced mammal control policy have pointed out that New Zealand forests and grasslands had evolved in the presence of browsing birds, and that the vegetation immediately before European settlement — from which moa had been absent for several centuries — could not have been in a natural state (Caughley 1983, Butchler 1989). Introduced mammals, they claim, are restoring a more natural vegetation. The question of whether or not the moa and other browsing birds exerted a strong or weak influence on the plants of New Zealand is therefore not only important for a complete understanding of the ecology of the present vegetation, but also has management implications.
Jared Diamond (1990) in a vivid metaphor described the New Zealand vegetation as still being influenced by the ‘biological ghosts’ of long extinct birds. Can these ghosts be laid to rest or does a complete understanding of our vegetation depend on our acknowledging their intangible but influential presence? Our aim in this paper is to subject the now reformulated moa-browsing hypothesis to critical scrutiny.
Browsing Birds in New Zealand
There were many herbivorous birds in the pre-Maori New Zealand fauna. Flighted folivores included the extant New Zealand pigeon (Hemiphaga novaeseelandiae), kokako (Callaeas cinerea), and the red-crowned and yellow-crowned parakeets (Cyanoramphus novaezelandiae and C. auriceps), all of which browse a wide range of foliage, which often makes up a significant part of their diet (Clout and Hay 1989). Flightless herbivores included the 11 extinct moa species (Anderson 1989a), the extinct flightless goose (Cnemiornis calcitrans), and the extant, but now highly restricted, takahe (Porphyrio mantelli) and kakapo (Strigops habroptius). Clout and Hay (1989) pointed out that kokako and pigeon used to be abundant throughout New Zealand, and can be significant defoliators of trees and shrubs. Kakapo were also abundant throughout, and fed widely from ground level up into the canopy. We should also not overlook the very considerable populations of insect and molluscan browsers in unmodified New Zealand forests and shrublands. Large ground-dwelling folivorous insects were probably capable of a considerable impact on the lower tiers of forest and scrubland.
However, moa were doubtlessly the dominant vertebrate browsers from ground level to a height of about 3 m. The 11 species had a range in body weight from 22 to 230 kg, and a range of head-up stature from 93 to 252 cm (Anderson 1989a). Moa ranged through the entire landscape: they occurred in subalpine grassland, shrubland, scrub, open dry forest and dense, wet, lowland forest (Worthy 1990). However, their populations were unlikely to have been large: the rapid elimination of the moa by the Maori, the number of fossil sites, and arguments based on the biomass of ratite birds in other places, all tend to suggest low densities. Moa probably had a rather slow rate of increase (Anderson 1989b). Anderson (1989a: 87) concluded that “… the total population of moas in each island was measured in tens of thousands, the South Island population was about twice that of the North, and the greatest concentration of moas occurred in the eastern half of the South Island.”
Burrows (1980a, 1980b) has shown from his analyses of fossil gizzards that some moa could cut through twigs at least 6 mm thick, and that twigs formed a normal and substantial part of the diet. He later concluded: “The Dinornis moa seem to have behaved like deer, cattle or goats, in taking a variety of food items, including browse.” (Burrows 1989). Anderson (1989a) postulated that had a large food page 3 volume requirement and were therefore rather unselective in their browsing. A combination of fibrous material, young twigs, leaves, and fruit made up the diet. Moa browse therefore was like that preferred by monogastric caecalids (such as horses), which lack a rumen and have a low ability to degrade toxins. Monogastric caecalids therefore feed mainly on plant parts low in toxic compounds — such as highly fibrous and poorly digestible stems — but to satisfy their nutritional requirements must also supplement their diet with more nutritious but better chemically defended plant parts (Guthrie 1984). The great diversity of plants found in moa gizzards therefore reflects their need to balance the nutritional aspects of their diet while avoiding toxic side effects.
Because sensory perception and mouth structure in birds differ substantially from those in browsing mammals, Greenwood and Atkinson (1977) asserted that anti-herbivore adaptations in New Zealand must also differ markedly from those typical of areas where mammals are the main vertebrate herbivores. Three features, they suggested, contrast moa with herbivorous mammals.
• Moa lacked a prehensile tongue and teeth, which would have made them more reliant on a clamping, pulling, and breaking feeding action, than on the cutting and chewing action of ungulates.
• In common with many other birds, moa had good colour vision but a poor olfactory sense. Hence food location and selection depended more on sight than smell.
• The beak and associated horny covering of the face would have protected the head nearly up to the full depth of the bite. Spines, which are effective against the soft noses of mammals, would have been less effective against moa.
These assumptions are only partly valid. The difference between moa and ungulate browsing is probably less than Greenwood and Atkinson (1977) initially envisaged. Both groups could cut and ingest substantial twigs; the significant difference may have been the nature of the two digestive systems. Moa probably could not debark trees and shrubs. While moa lacked soft, vulnerable noses, their eyes and tongues were certainly exposed to spines so that the presumed different reaction to spines may be relative rather than absolute.
Greenwood and Atkinson (1977) reversed the relative sensory capabilities of the moa. Moa probably had poorish vision and a well-developed offactory sense (Anderson 1989, Worthy 1990). The larger relative size of the factory area of the moa brain suggests that moa probably had a better developed sense of smell than most other bird groups (Worthy 1990). Atkinson and Greenwood (1989) suggested that as perception of the indigo-violet-red part of the light spectrum is restricted in some palaeognathous birds, these colours would also have been less apparent to moa.
Suggested Browsing Adaptations in New Zealand Plants
In this section we discuss the many features of the New Zealand flora that have been interpreted as anti-browsing adpatations (Table 1).
Toxins and other chemical defences, and low nutrient status
Batcheler (1989) suggested that because a number of low-statuted, fast-growing plants normally found on seral sites have toxins (e.g., Sophora, Coriaria, Brachyglottis repunda, Solanum have alkaloid defences), this is evidence for plant defence against moa browsing. His hypothesis, following from a similar line of reasoning by Greenwood and Atkinson (1977), is that moa browsed preferentially on nutrient-rich sites and on the lower strata of forest, and therefore high levels of defence could be expected in plants that habitually grew there. Low nutrient page 4 quality of some leaves has also been suggested as an anti-moa defence, as for instance the thick, tough, nutrient-poor leaves of Pseudopanax crassifolius (Mitchell 1980).
First of all, there is no reason to assume that toxins, carbon-based chemical defences, and low nutrient and fibrous leaves are specifically anti-moa browsing adaptations; they are effective against a wide range of herbivores, including invertebrates. All the indigenous species of flowering plants in New Zealand toxic to livestock are related to toxic species elsewhere, and no toxin restricted to New Zealand has yet been recognised (Connor 1977). The New Zealand situation appears to be a particular example of a universal trend.
Secondly, toxins may be a preferred means of defence for plants growing on nutrient-rich sites, and the concentration of toxic plants on such sites must be seen in terms of general plant defence strategies. The faster-growing a plant, the less profitable it is for it in terms of absolute growth rate to invest in defence (Coley et al. 1985). Pioneers, for example, accumulate nutrients more quickly than mature forest species, and allocate a great proportion of their resources to growth, but little to defence (Dirzo 1984). As fast-growing plants on nutrient-rich sites have more nitrogen to spare for defence than do slow-growing plants on poor sites, successional plants often possess nitrogen-based toxins such as alkaloids, which have a high turnover within the plant and can be produced in variable quantities according to need (Rhoades 1983). On the other hand, slow-growing plants in low-light, nutrient-poor, or stressed environments rarely have nitrogen-based toxins for defence, but rely on carbon-based chemicals such as polyphenolic compounds and lignins, which are less energy-demanding and use mimimal amounts of scarce nutrients. Nutritive qulity of leaves is usually low in species growing on poor soils, and such leaves tend to be sclerophyllous and are retained longer, possibly to minimise nutrient loss through herbivory, environmental stress, and nutrient leaching (Chabot and Hicks 1982). However, although low nutrient status leads to less browsing through herbivore avoidance, the long life of the leaves means the browsing that does occur has a great impact.
In general, therefore, plants growing in low-nutrient and environmentally stressed sites have well-defended leaves that are not browsed to the same extent as those from plants growing on richer sites. Fast-growing plants invest more in growth than defence, and rely on growing through their vulnerable phases, or deploy facultative defences such as highly effective low-bulk toxins. These defence strategies in the New Zealand flora are not necessarily a consequence of moa-browsing but a generalised adaptation to all herbivory.
Reduced apparency and mimicry as browsing defences
The risk of attack on a given plant by a herbivore is referred to as its “apparency”. Plants can reduce their apparency by modifications that variously make the plant look dead, as if it has already been attacked, like a non-plant object such as a stone, like another distasteful plant, or render it less visible. To a greater or lesser extent all plants employ an apparency strategy, as nearly every change in their external appearance or life history must alter the ease with which they are located and attacked by herbivores.
Mottled leaves. Atkinson and Greenwood (1989) suggested that mottled leaves in seedling plants may have reduced discovery by browsing moa (e.g., Parsonsia capsularis, and Pseudopanax crassifolius juveniles). The irregular blotching breaks up the outline of the leaf, making it difficult to discern. In New Zealand leaf mosttling seems to be a common feature of many shrubs and trees. Mottling is also more common in exposed, sunlit leaves than in shaded leaves (for instance in Pseudowintera colorata). A striking feature of many mottled leaves is their page 5 resemblance to dead or senescing leaves. Stone (1979) suggested that the brown fuyenile leaves of some understorey palms in Malaysia escape browsing because of this similarity.
Some insects use colour vision and leaf patterns to locate food plants, although not as commonly as they use smell and taste (Prokopy and Owens 1983). Smith (1986) has suggested that mottling of the leaves of Byttneria aculeata (a subcanopy vine in Panama) mimics effects of leaf miners, and thus discourages ovipositing and leaf damage. He showed that mottling was more common in clearings than in shady sites, possibly because of the trade-off between reduced photosynthesis and decreased insect damage in mottled leaves, and the reverse in unmottled leaves. Givinish (1990) has shown that in northeastern North America mottled leaves are more common in herbs of shaded forest understoreys than in any other growth form, and that they are essentially absent in trees, shrubs, herbs or vines of sunny sites. He suggested that mottling camouflages from vertebrate herbivores the foliage of particularly vulnerable phenological groups (evergreens; spring ephemerals) in light-dappled understoreys. There is therefore a strong possibility that some leaf mottling is directed against herbivores, but investigation of mottled plants in New Zealand would be needed to establish whether this is so here.
Dark coloration. Dark bronze and purple leaves are common in the New Zealand flora, in particular in new foliage and the exposed foliage of high-altitude plants. Blanc (1989: quoted in Givinish 1990) suggested that dark-coloured foliage held close to the ground could be camouflaged against herbivores. In nearly all plants he examined, dark-coloured understorey leaves were within 20 cm of the ground surface. If the foliage is held higher the apparency advantage is largely lost as the leaves are viewed against a contrasting background rather than the dark soil. However, most New Zealand examples of dark-leaved understorey plants (Table 1) I hold their foliage well over 20 cm above the ground, and furthermore, the coloration of the leaves varies seasonally.
It is also possible that herbivory is not involved in the New Zealand situation. Other possible adaptive explanations for dark leaves include modification of the heat balance of the leaf, protection from ultra-violet radiation, response to frost damage, and modification of the photosynthetic capacity of the leaf. Without more investigation we cannot choose between these explanations.
Mimicry. When a plant strongly resembles another object, living or non-living, less palatable than itself, it is often regarded as a mimic. Many cases of mimicry have been alleged but are exceptionally difficult to prove, as assessment of the similarity is usually subjective (see Edmunds 1990 for a lucid discussion). Mimicry by living leaves and stems of unpalatable objects such as stones and dead twigs is essentially different from the better known examples of camouflage mimicry in the insect world. When an insect mimics a leaf, twig or stone, only in a very superficial way does it take on the characteristics of that object. It remains an insect, heterotrophic and mobile, and its energy exchanges and life-style are but marginally affected. However, when a plant mimics an inanimate object, it is changed totally. A leaf or stem that resembles a dead twig, for instance, is very different from a green leafy stem. Its changed shape, ridigity, and pigmentation will substantially alter its heat absorption, gas exchange, light energy capture, construction costs, and competitive relationships. We should therefore be cautious in assuming that a given plant is mimicking an inanimate object, however close the resemblance; its resemblance may be a consequence of environmental factors. Atkinson and Greenwood cited several examples of the various types of mimicry. None of them is convincing.
Some New Zealand plants resemble dead twigs (Table, 1). Muehlenbeckia ephedroides resembles plants from arid regions that have a similar grey pubescence and leafless habit. It is typical of exposed unstable substrates such as river beds page 6 and gravel beaches, which in common with arid regions are largely unvegetated, subject to intense solar radiation, and have a tendency to droughtiness. It could be as cogently argued that Muehlenbeckia's leafless grey stems are an adaptation to the harshness of the local environment and its prostrate habit a response to frequent flooding and abrasion.
The reduced twig-like leaves of the juveniles of forest-dwelling Pittosporum obcordatum, are assumed to increase its resemblance to a dead or partially browsed plant (Atkinson and Greenwood 1989:83). However, there are plausible reasons why a juvenile plant may restrict its photosynthetic surfaces, the most likely of which is the necessary diversion of scarce resources to roots (Wright 1992). The prominence of the whitish mark along the midrib is a consequence of the reduction of the reaf blade; it may or may not be significant in apparency.
When one plant is allegedly mimicking another plant, the problem is more complex. It first has to be established that the model is both less palatable to herbivores and more widespread and abundant than the mimic plant, and that the two taxa frequently occur together, Without these conditions, selective pressure would not be sufficient to result in mimicry. A second complexity is that in adopting the form, structure, and colour of the unpalatable model, the leaves of the mimic also begin to resemble the model in essential life functions such as light interception, heat balance, and water relations. It then becomes debatable whether it is environmental or habitat convergence, or true mimicry. Atkinson and Greenwood (1989) mentioned a number of possible examples of plant-plant mimicry. For none of them do they establish a convincing case for mimicry, although it remains a possible interpretation.
Alseuosmia pusilla is a small, usually unbranched shrub, the palatable leaves of which are strikingly similar to the red-mottled, distasteful leaves of Pseudowintera colorata. However, although A. pusilla fulfils the requirement of a mimic, in that it is less common than its model but grows with it, this is not sufficient to establish mimicry. Aside from the red mottling, which is only well developed in sun-exposed leaves, there is nothing distinctive about P. colorata leaves. Red, brown, or yellow mottling of leaves is common in New Zealand, and seems to be a response to leaf damage, especially in the presence of bright light. Other species of Alseuosmia, which have dissimilar leaves to Pseudowintera colorata, also have red and brown mottles. Moa, as they possessed an excellent sense of smell, are unlikely to have been confused by the visual similarity between the two species. Therefore, the most likely explanation of the visual similarity between the two species is chance.
The moa's excellent sense of smell makes the proposed mimicry between spiny-leaved Aciphylla species and some similar appearing, but non-spiny tussock-forming plants improbable. Atkinson and Greenwood (1989) link the spiny-leaved Aciphylla subflabellata and unpalatable Festuca novae-zelandiae as a Mullerian mimicry complex. Likewise, they claimed that the juvenile or young foliage of Pittosporum pimeleoides and Podocarpus acutifolius mimics the unpalatable Cyathodes juniperina. Testing how well these meet the requirement for mimicry would be difficult, and environmental explanations for convergence are probably more convincing.
Tough fibrous stems and leaves
Although numerous plants in the New Zealand flora have tough fibrous leaves, Atkinson and Greenwood (1989) singled out Pseudopanax crassifolius, P.ferox, P. lineare, Cordyline australis, and Phormium tenax, because this feature is both exceptionally well-developed and best expressed when these plants are of a height that could have permitted moa-browsing. The Pseudopanax crassifolius group-the lancewoods - have a long (up to 1 m) fibrous linear serrated leaf, which is page 7 replaced by a shorter, less sclerophyllous, ovate leaf in the adult (Gould 1993). Cordyline and Phormium leaves do not change markedly from juvenile to adult, but they are formidably tough at any stage.
Tough, fibrous stems and leaves do deter herbivores (Choong et al. 1992). However, it is likely that in many plants the anti-herbivory effects are a secondary consequence of their structural function. In the suggested New Zealand examples, the long leaves are held at angles ranging from horizontal to near vertical. The single-stemmed juveniles of Cordyline and the lancewoods gain fully adult leaves only when branching begins. Their leaves alone form the juvenile canopy and must provide the necessary extension; hence they have the strength and toughness characteristic of branches. Phormium has the form of a giant tussock, with individual leaves up to 3 m in length, thick at the base and often quite stiffly erect except for the top few centimetres, and therefore clearly acting as stems. These species have developed these leaves primarily in relation to their particular requirements for canopy formation.
Reduced leaf area
The claim that plants reduce the size of their leaves or the total area per plant, or dispense with them either entirely or seasonally primarily because of herbivory (Atkinson and Greenwood 1989, Batcheler 1989) has little merit.
Batcheler (1989) suggested that deciduousness in the New Zealand flora is related to herbivory. However, deciduousness in New Zealand species is linked to cool winters. For example: Fuchsia excorticata and Aristotelia serrata, both mainly deciduous in the South Island, are evergreen in the warmer parts of the North Island (Dawson 1988). This pattern is unlikely to result from greater moa-browsing pressure in colder areas.
The New Zealand brooms (Carmichaelia, Chordospartium, Corallospartium) follow a typical broom pattern of reducing or dispensing with leaves in favour of photosynthetic stems, an adaptation therefore unlikely to be specifically directed at moa. It is, moreover, an adaptation that probably developed to reduce water-loss rather than herbivory. However, as with many such adaptations, it undoubtedly also reduces the palatability of the plant to a range of herbivores.
Reduction in total leaf area, or loss of leaves for a period, we believe therefore is best explained by the plant being unable to afford the cost of leaves if their income in form of photosynthate is low versus outgoings such as respiration, increased root area, or stem mass. Reduction in leaf area because of an elevated risk of herbivory seems inexplicable, given that there are other ways to minimise herbivory that do not involve sacrificing photosynthetic potential.
Spines are usually a defence against animals. Spininess is in particular a characteristic of arid-land plants, and documented evidence of avoidance or lower usage of such plants by vertebrate herbivores suggests that it evolved as a defence against them (see discussion in Janzen 1986:616–620). A strong point in Greenwood and Atkinson's (1977) hypothesis is that the New Zealand flora has few spiny plants, and they made a convincing case for this being because birds have horny beaks and therefore are undeterred by spines. However, they made an exception for Aciphylla, regarding their stiff sharp pointed leaves as effective anti-browsing devices, presumably because the spines threatened the eyes of browsing birds.
Strong stiff leaves with thick cuticles will tend to be spine-like. Hence, adaptation to drying windy climates by a tussock species could bring with it spininess as a mere byproduct. As previously pointed out by McGlone and Webb (1981),
1. Nutritional test
Moa should have been attracted to plants of high nutrient status. Therefore, if a plant with a putative anti-browse feature is also nutritionally attractive to birds, it will have passed this test.
Lee and Johnson (1984) measured the concentration of several nutrients in leaves of six divaricate and four non-divaricate Coprosma species. Nitrogen, phosphorus, calcium, and sodium were all present in higher concentration in divaricating species, and only potassium was more abundant in non-divaricating species. A canonical discriminant analysis of the data showed that the leaves fell into two groups, largely on the basis of nitrogen, phosphorus and sodium, in which small-leaved divaricating species were separated from large and small-leaved non-divaricating species.
However, if we take the two most important nutrients, nitrogen and phosphorus, and plot the data (Fig 1), a less clear-cut picture emerges. The two most weakly divaricating species of the group (C. rotundifolia and C. rubra) are separated from the rest by their high levels of nitrogen and phosphorus. The other group of divaricate and non-divaricate species have substantially lower nitrogen and phosphorus levels. The least nutritious leaves among the divaricating plants, belong to the most tightly divaricating species (C. propinqua and C. crassifolia). It would be hard to argue, despite their lower nutrient levels, that any of these Coprosma spp. are unattractive to vertebrates. Coprosma lucida and C. grandifolia, the two largest and thickest leaved species, are so palatable to present day browsers that they are completely eaten out by deer in some areas (Allen et al. 1984, Wilson 1987).
We argue that the high nutritional status of small thin leaves is probably related to their high ratio of photosynthetic tissue to supporting tissue, and possibly to higher photosynthetic activity than in the larger leaves. Therefore, acquisition of a small thin leaf or of a large, thick leaf could alter the nutritional balance regardless of any other factor. Highly active leaves may be more attractive, and therefore browsed more often, but this is off-set by higher growth-rates and turn-over, as discussed above.
As they often occur as successional plants on nutrient-rich sites, but often grow slowly, and allegedly devote a high proportion of their resources to defence, divaricating plants must be seen as highly anomalous. If browsing was so intense on nutrient-rich sites in New Zealand, it would seem that high levels of defensive chemicals, in particular toxins, would be a more optimal solution, as it would demand minimal change in the structure of the plants, be more flexible, and permit faster growth.
Is this test a good one? What if nearly all divaricating plants had leaves of exceptionally low nutrient content? Would this lead to the abandonment of the browsing hypothesis? We think not. For instance, Atkinson and Greenwood (1989:88) include among adaptations to moa browsing “…linear and fibrous juvenile leaves of low nutrient value of Pseudopanax crassifolius.” If, as in the thin-leaved divaricating shrubs, the leaves of P. crassifolius juveniles had high nutrient status, this could be easily explained as the reason for their tough, fibrous nature. Low nutrient status, however, here is seen as simply another defensive strategy. A test used in this way cannot be useful.
2. Life-cycle test
The anti-browsing adaptation should be best developed at that part of the plants life-cycle when it is most exposed to moa browsing. The anti-browsing feature should not be retained when the plant is out of reach of moa.page 11
This test is based on the assumption that terrestrial vertebrate browsing necessitates a greater defence investment in foliage borne low on the plant. This is a reasonable assumption with some plants and in some habitats. For instance, in Europe, holly (Ilex aquifolium) has more abundant spines on leaves close to the ground and leaves on heavily browsed shoots have longer spines (Peterken and Lloyd 1967), and in Africa thorny plants are intrinsically thornier below 3–5 m from the ground (Milewski et al. 1991) and browsed shoots tend to become more densely spiny. However, in some situations juvenile spininess is reduced and lost in the adult form without the presence of large vertebrate herbivores. For example, in the Hawaiian Islands certain Cyanea species have juveniles that are densely armed with stout, sharp prickles, while the adults are smoother, and less prickly (Lammers 1990). The prickles are regarded as a defence against phytophagous land snails and insects. Presumably, either attacks by animals are more intense close to the ground or the effect of the browsing is more severe on the juveniles. Regardless, the greater defence of the juveniles is not in any way related to the size per se of the browsing animal. At a more general level, Lowman (1985) found that leaves closer to the ground in tropical Australian forests were grazed more heavily by insects. It would seem reasonable to suppose that similar sorts of mollusc and insect attack occurred in New Zealand, and that for whatever reason, it was more intense closer to the ground. There was a large array of flighted and climbing browsing birds and insects in pre-historic New Zealand. The prevalence or better development of a putative browsing defence when the plant is small, which is then lost or reduced at greater heights, cannot be automatically attributed to the browsing height range of moa.
Even if it is accepted that moa browsing was a decisive factor in the evolution of plants, it is by no means clear that many allegedly browse-resistant plants pass the ‘life-cycle test’. Although most divaricating plants are of low stature, nearly 20% regularly attain heights of more than 4 m, and some can grow to 12 m, thus beyond the reach of even the tallest moa. Unless the divaricating plant form is a juvenile phase only, the degree of alleged defence does not change, no matter how tall the plant. For instance, in tall divaricating plants, such as Coprosma crassifolia. Melicope simplex and Myrsine divaricata, the uppermost foliage may be 5 more metres high, and invariably more strongly divaricate than at ground level. If divarication involves a cost to the plant, we could expect it to be reduced in intensity as the risk of attack lessened.
The degree of divarication often alters markedly with the aspect of the plant. Those parts of the plant exposed to the sun or the prevailing wind are usually strongly divaricate, and leafy shoots are often protected by one or more layers of near leafless branches. Sheltered, or shaded parts are mostly less strongly divaricate, are usually leafy to the exterior, and the leaves are larger. If a divaricating plant is growing completely in shade, leaf size and leafiness approximate more closely to those of the interior of an open-grown plant, and it is rare for divarication to be as well-developed as in the open. Many (for example, Coprosma rhamnoides) develop spreading, sparsely leaved plagiotropic arrays of thin branches at intervals up the stem.
In windshorn plants degree of divarication is primarily related to exposure not to ease of access by herbivores. For example, in exposed plants of Hoheria angustifolia the small-leaved divaricating juvenile foliage will extend further up the windward side of the plant, with adult foliage at the same level on the relatively protected lee side. In extremely windy sites, adult foliage often does not extend above the level of juvenile foliage, but the stem with adult leaves grows parallel to the ground on the lee side (McGlone, pers. obs.). Similar cases can be seen when divaricating plants grow in the shelter of rocks. Why divarication should be so intense a few centimetres above the shelter of a rock, and relaxed in the lee of the page 12 rock, is not easily explained by reference to browsing.
Most divaricating plants therefore fail the life cycle test, in that they are heavily defended when apparently there is no need, such in the uppermost layers out of the reach of moa, and weakly defended, if at all, underneath a canopy well within the reach of any moa. In most open-grown plants, the lower parts of the plant and the side away from environmental exposure are inexplicably left weakly guarded.
The height at which the tough-leaved single-stemmed juvenile of Pseudopanax crassifolius begins to change into the less coriaceous and branched adult tree certainly is at about the level where moa browsing would have been greatly reduced or absent. However, measurement in a range of habitats on the height to the beginning of canopy branching (which is a conservative indication of the height at which the tough juvenile foliage is replaced by adult leaves) show a variable range of heights for changeover (Table 2). Changeover occurs at a height of 1–2 m lower in the open when the competing vegetation is low-growing than under tall dark forest canopies. Under very dark, high canopies juveniles can reach as high as 7 m, with only a small cluster of leaves at the top of a stem often less than 5 cm in diameter. Juveniles in the open tend to have abundant leaves down the length of relatively thick stems. If moa-browsing is the main reason for the juvenile form, why should it be retained at heights well above the risk of attack? We suggest that the single-stemmed juvenile is an adaptation designed to carry the stem apex to a height where branching will spread the canopy above competing foliage. There fore, the lower the light level, the longer the juvenile form is retained.
3. Site distribution test
Plants with anti-browsing features should reach their greatest abundance on fertile sites where moa are certain to have browsed most intensively, and be unimportant on sites inaccessible to moa.
Divaricating plants are more abundant on landforms characterised by soils of moderate to high fertility. They are often abundant on alluvial lowland soils, but are not so common on soils derived from mafic rocks (Lee 1992), or on acid or leached soils. However, it is possible to exaggerate the relationship. For instance, on Stewart Island, the variety and abundance of divaricating plants are greatest on alluvial flats, and shrubs such as Pseudopanax anomalus and trees with divaricating juveniles such as Prumnopity taxifolia and Plagianthus regius are virtually confined to these sites (Wilson 1987). However, despite the acid soils of low fertility that characterise the island, some divaricating shrubs are both widespread and common (e.g., Myrsine divaricata, Coprosma propinqua, Coprosma rhamnoides, and Carpodetus serratus). In the eastern and central North Island regions apparently fertile alluvial flats, containing the greatest number of divaricating species known in New Zealand, are subject to severe frosts and/or substantial seasonal water table fluctuations, conditions which most broadleaved species cannot tolerate. The relationship between divarication and soil fertility is therefore complex and of little assistance in testing the moa-browsing hypothesis.
Greenwood and Atkinson (1977), Batcheler (1989) and Atkinson and Greenwood (1989) pointed out that few if any epiphytes are divaricating, despite the their dry branch and rock environment. They saw this as contradicting claims that the divaricating habit is related to drought avoidance (see McGlone and Webb 1981), and also as demonstrating that the divaricating syndrome was rare when the risk of moa browsing was low. Some divaricating plants have developed an ability to grow in dry areas, and the small expendable leaves, near leafless exterior, and self-shading habit of many divaricating plants could help explain this. Keen (1970) concluded on the basis of experimental studies that the small-leaved divaricating page 13 plant species she examined were not more resistant to absolute drought than their large-leaved relatives but were better adapted to survive and grow in conditions of physiological drought, such as those induced by drying winds. The epiphytic environment is so demanding and specialised that few vascular plants of any sort are found as epiphytes, and in New Zealand they are most abundant when rainfall is consistent and high. Whether the absence of epiphytic divaricating plants is significant or not is therefore difficult to determine. Dawson (1988) listed only seven shrubs and small trees regularly found on tall trees. All but one have thick fleshy leaves, and the tree species have roots that eventually reach the ground. Therefore, in keeping with this highly specialised habitat, nearly all have well-developed water storage capabilities or obtain water from the ground. There is a parallel among the herbaceous monocotyledons. It is not grasses adapted to dry, open sites that have colonised tree branches, but Astelia solandri and Collospermum, which form deep soil ‘nests’ or store water in tanks. The five species of epiphytic orchids are specialists, with fleshy spreading rhizomes. A number of orchids adapted to dry droughty sites do not occur on trees.
Greenwood and Atkinson (1977) claimed that divaricating plants are rare on steep cliffs, where moa would have found it impossible to browse. Like tree brunches, cliffs present a relatively specialised environment. Many cliffs are unstable, and seem to have a large opportunistic rather than cliff-specific element in their vegetative cover. Furthermore, cliffs vary greatly in all sorts of characteristics, including accessibility. Sheltered moist cool and relatively stable cliff sites are not favourable to divaricating plants, but sunny dry windy and exposed cliffs on Banks Peninsula have an abundance of divaricating plants (Hugh Wilson, pers comm).
We have discussed above why toxic foliage in seral vegetation is not necessarily a defence against moa browsing, but a more general adaptation to herbivore attacks on palatable, fast-growing plants. The argument could be reversed. Fast-growing but browse-sensitive plants characteristic of fertile soils, for example, Aristotelia serrata and Fuchsia excorticata, could be equally well taken as evidence that moa did not have a substantial effect on the vegetation on such soils.
4. Geographic distribution test
Areas known not to have had moa should have reduced numbers of species and smaller populations of plants with strongly developed anti-herbivore defences, than in areas that had moa.
We are certain that moa did not occur on most offshore islands more than a few kilometres from the mainland, although Stewart Island had moa (Anderson 1989). This test therefore contrasts islands with mainland sites.
Greenwood and Atkinson (1977) showed that the percentage of divaricating plants (in relation to the woody flora) on moa-free islands was lower than on comparable areas of coastal mainland (4.7% versus 10%). In general, the coastal mainland sites had more woody species (average 47) than the island sites (32). However, the Chatham Islands have a percentage of divaricating plants (8%) not much lower than the New Zealand flora as a whole, and higher than two of the mainland coastal areas chosen as comparisons. The low numbers of species involved and differences in climatic conditions between island and mainland sites (which are only rough proxies for islands) make this comparison of doubtful significance.
Of more significance are species or closely related species that occur on islands and the mainland, but differ in degree of divarication. Greenwood and Atkinson (1977) noted that a non-divaricating relative of Myrsine divaricata and a non-divaricating form of Coprosma propinqua occur on the Poor Knights Islands and page 14 the Chatham Islands, respectively. As well, Plagianthus ragius and Sophora microphylla have non-divaricating juveniles on the Chatham Islands, (Greenwood 1992). However, when examined in detail, these cases seem less convincing.
Sophora microphylla also has non-divaricating juvenile populations on the mainland, and the divaricating form is best expressed only in the far south and south-east of the South Island (Godley 1979) and in the east of the North Island. Myrsine divaricata is abundant on the subantarctic Auckland Island, which Greenwood and Atkinson (1977) attribute to the relatively recent colonization of the subantarctics from the mainland at the end of the Last Glaciation. Even allowing that this is so, it still does not alter the fact that one of the most consistently and tightly divaricated species, and one highly resistant to browsing by ungulates at present, has successfully invaded browse-free islands and remained unaltered through at least several thousand years. We, on the other hand, would stress the windy cool climates of the subantarctic islands in contrast to the mild, humid climates of the Poor Knights Islands. Corokia cotoneaster is strongly divaricating with small exterior leaves in inland districts of the North and South Island; under the milder conditions of coastal Taranaki, a form of this species is far less divaricating and has larger leaves borne on the exposed tips of the branches. A further counter example is Phormium, which is widespread on many islands, including Norfolk Island. If the tough, and not easily browsed Phormium persists in the absence of any browsing pressure at all, it is a strong argument for its leaf morphology not being primarily a browsing defence. Island plants in general tend to have larger leaves than typical mainland forms, and Greenwood (1992) pointed out that a range of woody species on the Chatham Islands have larger leaves than mainland forms, especially as juveniles. The comparative rarity of strongly divaricating plants on islands could therefore simply be related to greater success of broadleaved plants in the milder, less variable climates of offshore islands (Dawson 1988).
In general, we are dubious the geographic distribution test is satisfactory. Islands differ so much from mainland situations the only convincing test would be similar islands with and without moa. What evidence there is appears to support the view that it is not prehistoric moa presence or absence but current climatic conditions which control the numbers and abundance of divaricating plants on islands. We would suggest that the other putative anti-moa adaptations would likewise show no consistent geographic relationship to the past distribution of moa.
5. The ‘absence of herbivore’ test
Where vertebrate terrestrial herbivores are or were absent, heavily defended plants should be at a competitive disadvantage in relation to less well defended plants.
This is not a test proposed by Atkinson and Greenwood (1989) but one that should be considered. A major weakness of the moa-browsing hypothesis is the way that divaricating plants and other plants with supposed anti-browsing defences remained abundant in the absence of substantial browse pressure and in the presence of fast-growing competitors. A fair assumption is that anti-browsing strategies come with some cost to the plant. Nevertheless, divaricating plants, and other plants with supposed anti-browsing features, can be successful in the absence of any browsing pressure, and in the presence of ‘normal’ large-leaved, fast-growing competitors. With the extenction of the moa some 400 years ago, and major depletion starting about 600 years ago (Anderson 1989), non-defended plants have had between 300 and 500 years without significant browsing to overwhelm their defended competitors. That this did not happen is clear from the abundance of divaricating plants, spiny plants, plants with tough leaves, and dark page 15 or mottled coloration at the time of European settlement.
A possible counter to this argument is that although defended against browsing, these plants are better adapted to their characteristic environments than other species, and therefore will not be outcompeted, even in the absence of browsing. If this is granted, it leaves the problem of what it is about plants with these defence strategies that makes them so suitable for these environments.
The argument can be reversed: if browsing pressure was strong enough to induce in the vegetation such a wide range of anti-browsing strategies, it follows that before the extinction of the moa, many palatable and weakly defended plant species should have been restricted by browsing. This contention is not supported by the fossil evidence. Pollen of highly palatable species of Griselinia, Pseudopanax, Aristotelia, and Fuchsia are not often abundant in the fossil record because of poorly-distributed grains, but as far as can be told, they neither increase or decrease with the elimination of the moa. At some pre-human sites they are at times abundant (McGlone, Neall and Clarkson 1988), and this suggests that moa-browsing pressure was certainly not sufficient to restrict them.
As far as we are aware, there has been only one attempt to experimentally investigate the nature of browsing on putatively moa-defended plants. However, this investigation, reported in Atkinson and Greenwood (1989:87), is badly flawed.
‘The main restriction to mammalian browsing of divaricating plants appears to be mechanical. In a feeding trial of 3 replicates I.A.E.A. offered fresh leafy branches of Psedopanax anomalous, to 3 cattle and 3 goats, all pasture fed animals. In all cases the branches were briefly sniffed and then either nibbled sparingly or ignored. After removing all the leaves from these branches, and offering them again to the goats, they were rapidly consumed (leaving none for the trials with the cattle!).’
Livestock are not closely related to moa, and moa browsed in a different manner and had different sensory capabilities. Furthermore, the livestock were pasture-fed animals unaccustomed to browsing. Therefore, we cannot be sure that their reaction to the branches was not one of unfamiliarity, whereas the stripped leaves resembled their normal diet. This experiment therefore adds nothing to our knowledge of how any animals may have fed on a divaricating plant. But why use mammalian browsing to test an hypothesis centred on moa? For instance, many divaricating plants can resist browsing by deer, goats, hares, and possums in the wild (see, for example, Clarkson 1986:46–47). However, we believe that browsing resistance in these plants is but a side effect of an adaptation to a set of environmental stresses and is a consequence of the unique climatic and biological history of New Zealand. Studies of mammal browsing are largely irrelevant, as most of the putative anti-moa strategies are not common in other regions with large populations of indigenous mammalian herbivores.
Of all the many suggestions put forward for specific anti-moa-browsing strategies in the New Zealand flora, we believe that only spines in Aciphylla and dark or mottled leaves in juvenile plants are worth investigation as possible anti-moa adaptations. Nevertheless, while we largely dismiss the notion of widespread specific adaptations to moa-browsing, we are convinced by the evidence for generalised adaptations against browsers. As elsewhere in the world, tough, low- page 16 nutrient, unpalatable, and toxic leaves give a measure of protection against all leaf-eating animals. We also believe the evidence points towards vertebrate browsing in pre-human New Zealand being at a much lower level than that prevailing now. Therefore, although moa on certain sites and at certain times may have had a considerable influence, overall this was not enough to promote widespread anti-browsing adaptations specifically directed towards them. In particular, we see no reason to abandon the commonsense notion that on moist sunny nutrient-rich sites, fast-growing large-leaved trees and shrubs would have prevailed, relying (as do such plants in other areas of the globe) on their chemical defences and productivity to survive the combined effects of vertebrate and invertebrate attack. If plant communities on nutrient-rich sites are dominated by small-leaved and slow-growing shrubs, we suggest that environmental factors are responsible.
It would be difficult enough to achieve resolution of the question of evolution of anti-browsing adaptations if the moa and other extinct browsing birds were extant. In their absence, and therefore the absence of any but the most scanty evidence as to their sensory capabilities and diet preferences, the task is formidable. We stress that demonstration of the resistance of some elements of the New Zealand flora to present day mammalian browsing is not convincing evidence that such plants were adapted to vertebrate browsing.
There is therefore little hope of settling the browsing question by this sort of debate, in which the evidence is indirect and disputed. We need a more sophisticated approach towards understanding the various adaptations and peculiarities of the New Zealand flora. Only by exploring a much wider range of ecological hypotheses than those currently proposed will we be able to realistically appraise the likelihood that some of those forms and structures can be explained only by herbivory. It is primarily for this reason that we suggest that the most fruitful way forward is the study of our plants in relation to the primary influences of the physical environment.
We thank our many colleagues both in New Zealand and elsewhere who have either endured with good grace our persistent attempts to destroy their belief in the presence of specific adaptations to moa browsing in the New Zealand flora, or have assisted us with debate and information. In particular, Ian Atkinson, Tony Druce, Eric Godley, John Lawton, Bill Lee, David Lloyd, Peter Wardle, Colin Webb, and Hugh Wilson have been generous with their time and insights. We thank Peter Wardle, Beverley Clarkson and Joanna Orwin for their critical reading of the manuscript. We also thank Mike and Rowan Glynn, and Joan Esterle for assistance with the field measurement of Pseudopanax branching heights under trying conditions.
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Fig. 1. Nitrogen and phosphorus concentrations in leaves of selected Coprasma spp. Data replotted from Lee and Johnson (1984).
|Suggested Adaptations to MOA Browsing in New Zealand|
|Toxic or distasteful foliage|
|Cassinia leptophylla, Coriaria spp., Halocarpus spp., Lagarostrobus colensoi, Lepidothammus, Pseudowintera, Preridium esculentum and many others.|
|Camouflage, mottled and dark coloration (mainly in juveniles)|
|Carmichaelia arborea var, Parsonsia capsularis, Elaeocarpus hookerianus, Pittosporum patulum, P. obcordatum, Pseudopanax crassifolius, P. lineure, P. ferox, Dacrycarpus dacrydioides, Prumnopitys taxifolia.|
|(i) of other plants (model in brackets)|
|Alseuosmia pusilla (Pseudowintera colorata); Celmisia lyallii Celmisia petrei (Aciphylla spp.): Aciphylla subflabellata/Festuca novae-zelandiae (Mullerian mimicry?); Pittosporum pimeleoides (Leucopogon fasciculatus); Podocarpus acutifolius/Pittosporum divaricatum (Cyathodes juniperina).|
|(ii) of litter or dead twigs|
|Helichrysum depressum, Muehlenbeckia ephedroides, Parsonsia capsularis, Pittosporum obcordatum.|
|(ii) of dead standing growth|
|Many divaricating shrubs and juveniles|
|Reduced leaf area|
|Clematis afoliata, Carmichaelia spp., Hoheria sextylosa, Rubus squarrosus.|
|Fuchsia excorticata, Sophora spp., Plagianthus regins.|
|Tough fibrous leaves and stems|
|Carmichaelia arborea var, Pseudopanax crassifolius, P. ferox, P. lineare, Phormium spp., Cordyline australis, and most divaricating plants.|
|Spines and spine-tipped leaves|
|Aciphylla spp.; Podocurpus spp.; Urtica ferox|
|The divaricating plant syndrome|
|Densely-twiggy, interlaced, small-leaved shrubs, small trees or tree juveniles, comprising about 60 species.|
|Site||Vegetation||Average height to branch (m)||Range||N|
|L. Mahinapua, Westland, (site 1)||Terrace rimu forest||5.16||7.0–3.5||16|
|Hinewai, Banks Peninsula||Red beech forest||4.5||6.0–3.4||17|
|L. Mahinapua, (site 2)||Seral edge of rimu forest||3.7||4.4–3.0||8|
|Kawhaka Forest, Westland||manuka scrub||3.7||4.4–3.1||14|
|Kowhai Bush, Canterbury.||Open mountain beech forest||3.5||3.9–1.8||8|
|Arahua, Westland.||Edge of low-growing (10–2m) podoearp-broadleaf forest||3.25||3.9–2.6||12|
|Ahuriri Bush, Port Hills, Christchurch,||Bracken scrub||3.0||3.3–2.4||4|