Plant structural defences against browsing birds: a legacy of New Zealand's extinct moas

Browsing by large vertebrates has been a major force in the evolution of terrestrial plants but Holocene extinctions of the browsers have left a legacy of broken biotic partnerships. Ratite birds were the largest herbivores in several regions, such as the moas of New Zealand. Many woody plants there have a distinct form of branching, described as "divaricate", with thin, wide angled, branches intertwining to form a tangled canopy. Divaricate branching has been interpreted as a form of protection against climate extremes or as an anachronistic defense against the extinct moas. Here we report the first experimental evidence that many of these plants are defended against extant ratite browsers. In feeding experiments on two tree species with different (heteroblastic) juvenile and adult branch morphology, emus and ostriches obtained adequate feeding rates from adult shoots but sub-maintenance feeding rates from juvenile shoots with the ratite-resistant traits. Divaricate juvenile shoots suffered 30–70% less biomass removal to the birds than adult shoots. Ratites browse by a distinctive clamping and tugging action. Structural defence traits that exploit the limitations of this feeding mode include narrow, strong, elastic branches that resist being torn off, wide branching angle ("divaricate") that makes shoots difficult to swallow, and small, widely spaced leaves. This novel plant architectural defence has developed in at least 20% of the native woody flora of New Zealand, including 10 heteroblastic tree species that exhibit the ratite-resistant strategy until they reach ca 3 metres height. It is also a major axis of variation amongst homoblastic woody shrub species. The defences are useless against mammalian browsers that shear shoots, contributing to marked decreases in the abundances of ratite-resistant species in New Zealand after the introduction of mammals.     

Seasonal variation in the impacts of brushtailed possums (

The seasonal variation in possum browse and foliage cover of five possum-preferred species was quantified and studied in northern Westland, New Zealand over a 24 month period. Four of the five species (Pseudopanax simplex, P. colensoi, Aristotelia serrata, and Elaeocarpus hookerianus) showed marked seasonal patterns in both browse and foliage cover, with maximum browse evident in winter/spring when foliage cover was at a minimum. There was very little browse and no seasonal pattern in foliage cover for the fifth species, Pseudopanax crassifolius. In the season of maximum browse there were significant negative correlations between browse and foliage cover for the four impacted species suggesting that the changes in foliage cover were caused by possum browsing. Mortality was highest in the two most heavily browsed species (P. simplex and P. colensoi). This seasonality in possum browse needs to be, accommodated when designing long-term surveys of possum impacts.     

Heteroblasty on Chatham Island: A comparison with New Zealand and New Caledonia

We used a comparative approach to investigate heteroblasty in the Chatham Islands. Heteroblasty refers to abrupt changes in the morphology of leaves and shoots with plant height. Common on isolated islands such as New Caledonia and New Zealand, which once had flightless, browsing birds, heteroblasty is hypothesised to be an adaptation to deter bird browsing. The Chatham Islands are a small archipelago located 800 km off the east coast of New Zealand, which has clear floristic links to New Zealand. However, unlike New Caledonia and New Zealand, the Chathams never had flightless, browsing birds. We investigated heteroblasty on the Chatham Islands by: (1) comparing height-related changes in leaf morphology and branching architecture in several plant taxa with heteroblastic relatives on the New Zealand mainland; (2) characterising changes in leaf morphology in heteroblastic tree species endemic to the Chathams; and (3) comparing overall trends in leaf heteroblasty on the Chathams with New Caledonia and New Zealand. Reversions to homoblasty were observed in the three Chatham Island taxa with heteroblastic relatives on the New Zealand mainland. However, two endemic tree species were clearly heteroblastic; both produced dramatically larger leaves as juveniles than as adults. Inter-archipelago comparisons showed that this trend in leaf morphology is rare among heteroblastic species in New Caledonia and New Zealand. Therefore, while some of our results were consistent with the hypothesis that heteroblasty is an adaptation to avoid bird browsing, other processes also appear to have shaped the expression of heteroblasty on Chatham Island.     

Leaf heteroblasty is not an adaptation to shade: seedling anatomical and physiological responses to light

Heteroblastic plants produce markedly different leaf morphologies between juvenile and adult stages, while homoblastic plants exhibit little or gradual changes. We tested the hypothesis that the leaf morphology of the seedling stage of New Zealand heteroblastic species is advantageous in dealing with low light levels found in forest understorey. We used four independent contrasts of heteroblastic and homoblastic seedlings from the genera Aristotelia, Hoheria, Pseudopanax, and Melicope grown in full-sun (100% sunlight) and shade (5% sunlight) light environments in a glasshouse. The four heteroblastic species had consistently smaller leaves and lower specific leaf area than their paired homoblastic species both in sun and shade. In the shade, there were no consistent differences in leaf anatomy (thickness of leaf blade, cuticle, epidermis, and palisade mesophyll, and stomatal density × stomatal aperture length) or physiology (maximum photosynthetic rate, dark respiration, and light compensation point) between homoblastic and heteroblastic species. However, in the sun, heteroblastic A. fruticosa, P. crassifolius, and M. simplex had appreciably thicker leaf blades as well as higher maximum photosynthetic rates than their homoblastic congeners. These traits suggest heteroblastic seedlings possess leaf traits associated with an advantage in high-light environments. We conclude that the heteroblastic seedling leaf morphology is unlikely to be an adaptation to very low light. Alternative explanations for the functional significance of changing leaf morphology in association with life-stage should be sought.     

Herbivory and the evolution of divaricate plants: Structural defences lost on an offshore island

Many island plants are characterized by unique morphology. For example, the high branching angles and small leaves of divaricate plants are a common feature of the New Zealand flora. The divaricate growth form may be an adaptation to deter browsing by extinct avian herbivores (moa); alternatively aspects of the insular climate may be responsible. However, our understanding of the selective pressures responsible for the high branching angles and small leaves of divaricate plants is incomplete. Here, I tested for differences in traits associated with the divaricate growth form between plants from Chatham Island and the New Zealand mainland. Moa never reached the Chatham Islands and its flora is derived from plants on mainland New Zealand. Therefore, I predicted Chatham Island plants to have lost morphological adaptations that may have deterred moa herbivory. Traits were quantified on 316 individuals in the field, allowing for 12 island‐mainland taxonomic comparisons. Chatham Island plants consistently produced smaller branching angles, larger leaves, shorter internodes and larger stems than related mainland plants. Results are therefore consistent with the hypothesis that selection for small leaves and high angled branching may be relaxed on the Chatham Islands due to an absence of moa. Smaller branching angles and larger leaves may offer a competitive advantage to Chatham Island plants.     

Vegetative Architecture of Elaeocarpus hookerianus. Transition from Juvenile to Adult

Elaeocarpus hookerianus Raoul is a profoundly heteroblastictree native to New Zealand. We describe and quantify changesin leaf morphology and anatomy, and in branching pattern atdifferent levels of insertion. Discrete juvenile, adolescentand adult phases were identified. The divaricating juvenilebore small leaves with thin laminae and an anatomy typical ofshade-plants. Juveniles had dense canopies, many thin horizontaland vertical axes, wide branch angles and highly variable branchingpatterns. Adolescents had larger leaves, fewer horizontal axeson a single, leading vertical axis, and a more consistent branchingpattern. Adults were arborescent, producing the largest, mostdifferentiated leaves on the stoutest and longest horizontalbranches. Data indicate a three-phased strategy for: (a ) providingresponsive, energy-efficient shoot systems under low-light regimes;(b ) growing rapidly to the forest canopy; and (c ) exploitingfor the forest canopy environment. Elaeocarpus hookerianus Raoul; heteroblasty; leaf morphology; leaf anatomy; branching pattern     

Divaricating shrubs in Patagonia and New Zealand

There are at least three hypotheses to account for the abundance of divaricating shrubs in New Zealand: 1) Ratites in the form of 11 species of moa, led to divarication for browse protection (Greenwood and Atkinson, 1977); 2) Divarication evolved as a microclimatic shield (McGlone and Webb, 1981); 3) Divarication evolved to aid leaves in light harvesting (Kelly, 1994). In Patagonia before human arrival, there were browsing mammals in addition to the ratite rhea. To examine the possible influence of the different grazing animals on the degree of divarication in Patagonian shrubs, a transect was established across Argentine Patagonia at c.40 degrees S lat., from Andean forests to the shrub desert of the east, providing a rainfall gradient from 3000mm to 134mm annual precipitation. Divarication Indices of Atkinson (1992), I-ATK and Kelly (1994), I-KEL were calculated for all shrubs encountered at 20 sites along this gradient. As I-KEL gave zero values for four leafless shrubs, including the important Mulinum spinosum, this index was not further used for distributional analyses. I-ATK gave 18 species as fully divaricate (I-ATK > 14) and 8 as semi- divaricate (I-ATK <14) The highest values of I-ATK were lower than in New Zealand (Atkinson 1992), a function of a lower number of wide-angle branches (>90 degrees) in Patagonia. All except two species were spiny, as were most other shrubs on the traverse. Unlike the majority of divaricates in New Zealand which retain divarication in dense forest, none of the Patagonian shrubs are divaricate in forest and only two species divaricate in more open forest and scrub. Divaricate cover increased steeply along the traverse through drier, open forest and seral scrub. Once out of the seral scrub zone into arid country, a different suite of divaricate taxa was encountered. The diversity and cover of divaricates rose to reach a maxima at 134 mm annual precipitation. In Patagonia, divarication and spininess could be responses to the indigenous browsing mammals that are common in the semiarid and arid zones, or to climate.     

Site conditions affect seedling distribution below and outside the crown of kauri trees (

It has been suggested that plants can change soil characteristics via their litter to favour their own species. The New Zealand kauri tree (Agathis australis) presents an interesting case for studying such a positive feedback between plant and soil because it has a huge impact upon the soil. We hypothesised that, under mature kauri trees, compared with sites outside the projection of the crown, seedlings of angiosperm trees are relatively rare, while kauri seedlings are relatively common, due to the poor soil conditions and the higher light intensity. We counted seedlings under and outside the crowns of kauri trees and correlated the presence of these seedlings to measured site conditions. The results confirm the hypotheses and indicate that the establishment of kauri seedlings is favoured by the open canopy and high light intensities below kauri. The low nutrient availability under kauri appears to be unfavourable for the survival of angiosperm seedlings but not for the survival of kauri seedlings. Since the lower nitrogen availability under kauri is due to sequestration of nitrogen in the organic layer under kauri, a positive feedback between kauri and the soil is likely.     

Leaf Heteroblasty in Pseudopanax crassifolius: Functional Significance of Leaf Morphology and Anatomy

Pseudopanax crassifolius (A. Cunn.) C. Koch. is a strongly heteroblastictree indigenous to New Zealand. Changes in the morphology andanatomy of leaves are described for seedling, juvenile, transitionaland adult phases of development. Seedlings produce five leaftypes; all are relatively small, thin, anthocyanic, have a lowspecific weight, and are anatomically comparable to the leavesof many shade plants. Juvenile leaves are long, linear, deflexed,coriaceous and sharply-toothed. They have a high specific weight,a thick, ornamented cuticle, a multiseriate hypodermis composedof collenchyma, well developed palisade and many spongy mesophylllayers. Juvenile leaves are strong relative to adult leavesand to the leaves of other species. Leaf strength is providedby fibres associated with the midrib. Adult leaves are shorter,broader and less massive than juvenile leaves, and are orientedhorizontally. Transitional leaves are morphologically intermediatebetween juvenile and adult leaves. The anatomy of juvenile,transitional and adult leaves is similar. The heteroblasticseries may be associated with changes in leaf construction costs,light interception and heat dissipation.Copyright 1993, 1999Academic Press Lancewood, Pseudopanax crassifolius (A. Cunn.) C. Koch., leaf heteroblasty, anatomy, morphology, structural adaptations     

Effects of Selective Logging on Populations of Two Tropical Understory Herbs in an Amazonian Forest1

This study examined the effects of (1) rime elapsed after logging and (2) logging intensity on the total, juvenile, and adult densities, and on reproduction of Calathea altissima and Ischnosiphon amuma (Matantaceae), two monocot herb species in the understory of Central Amazonian forests. Logging was carried out experimentally at various intensities in eight plots (4 ha each) during 1987 and three plots in 1993. Five plots were left as experimental controls. In 1998, total and adult densities of the two species were greater in the plots logged 11 years before than in controls. For I. arouma, total and adult densities were also higher in the plots logged 5 years before; however, juvenile densities were less affected. The intensity of logging influenced adult density of both species but not total or juvenile densities. Densities of reproductive individuals of both species were higher in the logged areas and increased with logging intensity. The effects of time after logging and logging intensity on reproduction were indirect due to the greater number of adult plants in those areas. The observed effects were probably mediated by changes in canopy cover in logged areas. Greater light intensities in logging gaps, roads, and their margins may lead to increased reproduction, recruitment, growth, and survival, which in turn can lead to increased plant density. These results indicate that logging has long–term effects on understory plant populations.     

A morphological change in the fungal symbiont Neotyphodium lolii induces dwarfing in its host plant Lolium perenne

The endophytic fungus Neotyphodium lolii forms symbiotic associations with perennial ryegrass (Lolium perenne) and infection is typically described as asymptomatic. Here we describe a naturally occurring New Zealand N. lolii isolate that can induce dwarfing of L. perenne and suppress floral meristem development in the dwarfed plants. Further to this we demonstrate that the observed host dwarfing correlates with a reversible morphological change in the endophyte that appears associated with colony age. Mycelium isolated from normally growing plants had a typical cottony appearance in culture whereas mycelium from dwarfed plants appeared mucoid. Cottony colonies could be induced to turn mucoid after prolonged incubation and seedlings inoculated with this mucoid mycelium formed dwarfed plants. Mucoid colonies on the other hand could be induced to form cottony colonies through additional further incubation and these did not induce dwarfing. The reversibility of colony morphology indicates that the mucoid dwarfing phenotype is not the result of mutation. Ten isolates from other locations in New Zealand could also undergo the reversible morphological changes in culture, induce dwarfing and had the same microsatellite genotype as the original isolate, indicating that a N. lolii genotype with the ability to dwarf host plants is common in New Zealand.     

Vegetative Architecture of Elaeocarpus hookerianus. Periodic Growth Patterns in Divaricating Juveniles

Elaeocarpus hookerianus Raoul, a canopy tree native to New Zealand,has a divaricating juvenile stage. The juvenile produces shortshoots on both vertical and horizontal axes in the spring; longshoots are formed and expand most in summer months. Axes haveregions of long internodes interspersed with regions of shortinternodes. Long internodes are associated with production ofsinuate, linear-lanceolate leaves, the outgrowth of many lateralbranches, and a wide angle of divergence between terminal andlateral axes. Regions with short internodes bear smaller, obovateleaves, and lateral outgrowth is suppressed. Periodicity ininternode length is synchronous for first- and second-orderhorizontal axes at comparable distances along a branch. Verticalaxes elongate more extensively, bear more linear lanceolateleaves, and branch more prolifically than horizontal axes. Topologicalgrowth, as determined by monthly estimates of mean order andof partition asymmetry, is similar for vertical and horizontalaxes; both become more symmetrical towards the end of the season.Most leaves fall, and growth halts over winter months. The characteristichabit of juvenileE. hookerianus results from weak apical controlof lateral shoot outgrowth, and periodic growth that providesfor efficiency in light capture and expenditure for structuralsupport. Vertical axes are considered to ‘explore’the environment peripheral to the plant's canopy, whereas horizontalaxes ‘exploit’ the canopy volume already captured. Elaeocarpus hookerianus Raoul; divaricating; architecture; periodic growth patterns     

Testing the effect of restoration‐focused silviculture on oak regeneration and groundlayer plant communities in urban–exurban oak woodlands

Throughout their global range, oak‐dominated ecosystems have undergone state changes in stand structure and composition. Land managers face an especially acute challenge in restoring oak ecosystems and promoting oak regeneration in urban–exurban areas, where high‐intensity silvicultural treatments are often not feasible. To investigate low‐intensity management alternatives which could be widely applied in urban–exurban forests, a large‐scale adaptive management experiment was implemented in Lake County, IL, in 2012. Five canopy manipulation treatments of varying intensity, timing, and spatial aggregation were replicated across three study areas and oak seedlings were under‐planted into treatment units following management. Responses of understory light environment, shrub and groundlayer plant communities, and survival and growth of underplanted oak seedlings were evaluated. Understory light availability, canopy openness, total groundlayer plant cover, and groundlayer species diversity all differed among treatments. However, although understory light availability was significantly increased by canopy manipulation, groundlayer communities and oak seedling survival and growth did not differ among treatments. High overall seedling survival rates suggest current conditions are amenable to oak regeneration, but long‐term monitoring will be needed to assess the potential for seedlings to transition to the sapling and canopy layers. Early results demonstrate that canopy‐focused silvicultural treatments can affect the understory light environment and, to some degree, groundlayer plant communities. However, underplanting of oak seedlings paired with subcanopy thinning may be sufficient to restore an oak seedling layer, and (when necessary or preferred) canopy manipulation could potentially be deferred until later in the restoration timeline to promote oak recruitment.     

Leaf orientation and light interception by juvenile Pseudopanax crassifolius(Cunn.) C. Koch in a partially shaded forest environment

Leaf orientations and light environments were recorded for 40 juvenile Pseudopanax crassifolius trees growing in New Zealand in a partially shaded, secondary forest environment. Efficiencies of interception of diffuse and direct light by the observed leaf arrangments were calculated relative to those of three hypothetical leaf arrangements. Canopy gaps above the study plants were unevenly distributed with respect to azimuth and elevation above the horizon. Our results indicate that photosynthetically active radiation (PAR) received from the sides is more important than that received from directly above. In 33 of the plants leaf orientation was found to be significantly clustered towards one azimuth. The mean azimuth and the mean angle of declination were different for each plant. Leaves were steeply declined, and oriented towards the largest canopy gap at each site. Steep leaf angles reduced interception of direct and diffuse PAR when compared to interception by plant with a hypothetical horizontal leaf arrangement. When compared to a hypothetical arrangement with steep leaf declination and a uniform azimuth distribution, the observed leaf arrangement increased the efficiency of interception of diffuse PAR, but had a variable effect on the interception of direct PAR. Results indicate that the developing leaves of juvenile P. crassifolius orient towards the strongest sources of diffuse light, regardless of their value as a source of direct light. By maximising diffuse light interception while reducing direct light interception, leaf orientation may be a partial determinant of the types of habitats exploited by this species. This study emphasises the importance of considering diffuse light interception for plants growing in partially shaded environments.     

Size‐dependent microhabitat use and intraspecific competition in Cottus gobio

An electrofishing survey of daytime shelter microhabitat use of bullhead Cottus gobio in a southern English chalk stream revealed positive selection for moderate water velocity, vegetation cover and coarse substrata. Water depth, other forms of cover, shade and substratum embeddedness had no significant influence on the distribution of fish. Microhabitat use was size‐dependent, with patches occupied by adult fish containing coarser substrata and less blanket weed ( Cladophora algae) than those occupied by smaller juvenile conspecifics. Differences in substratum use between size‐classes were less pronounced in parts of the stream shaded by the tree canopy. In laboratory tanks stocked at low fish density, both juveniles and adults favoured use of cobbles over pebbles. The response of fish to increased conspecific density was size‐dependent; juveniles reduced use of the coarse substratum whereas adults maintained their predominance in this habitat. An apparently greater shift by juveniles when in the presence of adults was significant at α = 0·10 only, as was an apparent reduction in interactions between size‐classes under low light intensity. The displacement of small juvenile fish from the preferred cobble substratum is consistent with the hypothesis that intraspecific competition contributes to the size‐related microhabitat shift observed in the field. Although there was a tendency for the strength of competition to be reduced at low light levels, the mechanism by which tree canopy cover affects microhabitat use remains uncertain.     

我国温带山地森林48种常见树种叶片重量-出叶强度的关系

叶片是植物的主要光合器官, 其质量与数量的权衡关系体现植物对环境的适应策略。在全球气候变化的背景下, 研究叶片质量与数量关系有助于理解植物对环境变化的响应趋势。该研究应用标准化主轴回归方法, 探讨了我国温带山地森林中48个常见树种的单叶干重与出叶强度的权衡关系。结果表明, 所有物种以及落叶阔叶林、常绿和落叶阔叶树种、单叶以及亚冠层阔叶树种的单叶干重与出叶强度表现为异速生长关系; 针叶林、针阔混交林、常绿及落叶针叶树种、复叶以及冠层阔叶树种则表现为等速生长关系。研究结果表明, 叶大小和出叶强度并无恒定的权衡关系。     

Changes in Nucleic Acids Associated with Maturation and Senescence in Hedera helix

Significant changes in nucleic acids are associated with both maturation and senescence of Hedera helix leaf tissues. DNA content was unaffected by senescence, and there were no quantitative differences between juvenile and transitional forms. The adult tissue, however, contained less DNA than the other forms. The total RNA content was reduced by senescence in juvenile and transitional tissue but not in adult. Maturation, on the other hand, progressively decreased the total RNA content. Similar changes in sRNA and rRNA indicate that maturation involves quantitative changes in these fractions. Quantitative differences in the nucleotide analyses suggest that different sRNA and rRNA species are responsible for the biological processes associated with maturation.     

Springs and wire plants: anachronistic defences against Madagascar's extinct elephant birds

The extinction of large vertebrates in the last few millennia has left a legacy of evolutionary anachronisms. Among these are plant structural defences that persist long after the extinction of the browsers. A peculiar, and controversial, example is a suite of traits common in divaricate (wide-angled branching) plants from New Zealand. Divaricate architecture has been interpreted as an adaptive response to cold climates or an anachronistic defence against the extinct moas. Madagascar, a larger tropical island, also had a fauna of large flightless birds, the elephant birds. If these extinct ratites selected for similar plant defences, we expected to find convergent features between New Zealand and Malagasy plants, despite their very different climates. We searched the southern thickets of Madagascar for plants with putative anti-ratite defences and scored candidate species for a number of traits common to many New Zealand divaricates. We found many Malagasy species in 25 families and 36 genera shared the same suite of traits, the 'wire plant' syndrome, as divaricates in New Zealand that resist ratite browsing. Neither ecologically, nor phylogenetically, matched species from South Africa shared these traits. Malagasy wire plants differ from many New Zealand divaricates in lacking the distinctive concentration of leaves in the interior of shrubs. We suggest that New Zealand divaricates have a unique amalgam of traits that acted as defences and also confer tolerance to cold. We conclude that many woody species in the thickets of southern Madagascar share, with New Zealand, anachronistic structural defences against large extinct bird browsers.     

Dynamics of phytoplankton growth in the Waikato River,North Island,New Zealand

The Waikato River (latitude 38°S, longitude 176°E, North Island, New Zealand) is overwhelming y dominated by diatoms (mainly Melosira species) while blue-green and green algae are of minor importance. Both laboratory and in situ nutrient enrichment experiments showed enhanced growth of natural and index blue-green and green algae by addition of phosphate and nitrate. These algae were also shown to require higher temperature and light intensity than the diatoms. On the other hand, Waikato River with its higher silica content, moderate range of temperature and running water habitat was more favourable an environment for diatoms.     

Woodland canopy structure and the light response of juvenile Quercus lobata (Fagaceae)

I investigated competition for light between canopy plants and juvenile valley oaks (Quercus lobata Nee) in a mixed-broadleaf woodland of California's northern Coast Ranges. Canopy effects on understory light supply were separated among the overlying adult valley oak, the adult's woody understory, and neighboring trees and shrubs through a series of light sampling surveys and measurements of the number, size, and spatial distribution of neighboring plants. Light supply in the understory was primarily influenced by neighboring plants, with no detectable effect of the overlying adult valley oak. Light supply in the understory averaged 25% full sun due to a high frequency of canopy gaps and a typically open understory. Seedling response to understory light supply was investigated in an experimental sunfleck gradient (10%, 19%, and 100% full sun). Between 10% and 100% full sun, seedling growth increased by 90% and the shoot:∗∗∗root ratio changed from 1.561 to 0.607. Shade seedlings were also taller and produced fewer, larger, and thinner leaves than seedlings grown in full sun. A field survey of the spatial distribution and crown morphology of saplings and young adults found 1) the distance between young valley oaks and neighboring overstory trees to increase with neighbor size, and 2) crowns of the young oaks to be skewed away from neighbors. Although shading by the canopy was only moderate, canopy effects on understory light supply may restrict juvenile recruitment of valley oak in this woodland.