Mick E. Hanley

Seedling herbivory, community composition and plant life history traits

Abstract Despite the voluminous literature documenting plant-animal interactions, it is only recently that ecologists have begun to focus upon the importance of seedling herbivory in plant communities. This review aims to synthesize our current understanding of the effect that selective seedling removal by herbivores has in shaping post-disturbance plant community structure. In order to do this I describe how individual seedling and plant community characteristics influence the likelihood of seedling herbivory. I argue that seedling palatability, size and morphology, together with the frequency, distribution and timing of seedling emergence all play a significant role in determining seedling regeneration success in the face of herbivore attack. I also outline how current plant defence theories can be related to recent field observations concerning seedling acceptability and removal. In addition, I suggest that those seedling characteristics which provide the emerging plant with some degree of resistance against herbivory should be viewed as one component of a suite of plant life history traits affecting seedling regeneration success or failure. In view of the increasing importance of comparative methods in plant ecology, I propose that future research should integrate seedling acceptability with other plant life history traits thought to affect seedling regeneration. Recent work suggests that seed size may be paramount in determining regeneration success. I explore the possibility that seed size and seedling acceptability may be linked and discuss how these two factors may interact along successional gradients in plant communities.

Pre-germination temperature and the survivorship and onward growth of Mediterranean fire-following plant species

Abstract The role of heat shock in the induction of seed germination for numerous Mediterranean fire-following plant species is well documented. However, the influence of pre-germination heating of seeds upon seedling survivorship and onward growth has not been studied. The aim of the experiments described here was to investigate how a range of heat treatments affects seedling survivorship and onward growth for six common fire-following Mediterranean plant species (Anthyllis vulneraria, Cistus creticus, C. salvifolius, Hippocrepis unisiliquosa, Pinus brutia and P. halepensis). In the first experiment, seeds of five species were heated to temperatures ranging between 80°C and 120°C (at 10°C intervals) for 10 min and subsequent seedling growth monitored over 8 weeks. Survivorship for two pine species (Pinus halepensis and Pinus brutia) was reduced after seeds were heated above 90°C. Onward growth for Pinus halepensis and the legume, Anthyllis vulneraria, was negatively affected by increasing pre-germination temperature. Survivorship and growth for both Cistus species was unaffected by heating seeds up to 110°C. The second experiment examined more closely seedling performance of Hippocrepis unisiliquosa seedlings when seeds were heated to temperatures ranging between 50°C and 90°C (at 10°C intervals) for 5, 10, 15 and 20 mins. Increasing pre-germination temperature and the length of time seeds were exposed to heating significantly reduced seedling growth rates in this species. The effect of fire on seedling emergence, growth and survivorship in the field is discussed with reference to the adaptation of the six species to post-fire regeneration and the patterns of seedling regeneration observed in the field.

Impacts of seedling herbivory on plant competition and implications for species coexistence

BACKGROUND AND AIMS Although the causes and consequences of seedling herbivory for plant community composition are well understood, the mechanisms by which herbivores influence plant species recruitment to the established phase remain less clear. The aim was to examine how variation in the intensity of seedling herbivory interacts with growth-defence trade-offs and herbivore feeding preferences to affect plant community development. METHODS Using 14-d-old seedlings of Trifolium pratense and T. repens, relative growth and susceptibility to herbivory by the snail Helix aspersa was quantified to elucidate putative growth-defence trade-offs for these species. Then mixed assemblages of 14-d-old Trifolium seedlings were exposed to herbivory by zero, two, five or ten snails and determined how variation in the intensity of herbivory affected competitive interactions into the mature phase (as measured by total plant biomass at 120 d old). KEY RESULTS In the absence of herbivory, communities were dominated by T. pratense; a result expected on the basis that it yielded larger and presumably more competitive seedlings. However, when seedlings were exposed to herbivory, the balance of competition shifted. At low levels of herbivory (two snails), both Trifolium species contributed equally to total plant biomass. More intense herbivory (five snails) resulted in almost total mortality of T. pratense and dominance of the mature community by T. repens. The most intense herbivory (ten snails) effectively removed all seedlings from the experimental community. CONCLUSIONS The study illustrates a mechanism whereby spatio-temporal fluctuations in seedling herbivory, when coupled with species-specific variation in competitive ability and sensitivity to herbivore attack, can differentially influence plant recruitment into the mature phase. This mechanism may be a key element in our attempts to understand plant species coexistence, since fluctuations in plant recruitment are fundamental to the many theories that view coexistence as a consequence of a spatio-temporal lottery for dominance over regeneration micro-sites.

Bioenergy, Food Production and Biodiversity – An Unlikely Alliance?

School of Biological Sciences, Plymouth University, DrakeCircus PL4 8AA Plymouth, UKReceived 27 November 2013; accepted 20 January 2014IntroductionThe global demand for bioenergy is set to increase to apoint where it may supply up to one-third of globalprimary energy by 2050 (IEA, 2012). Current cultivationof biofuel and bioenergy crops has attracted consider-able criticism due to their encroachment into areas tra-ditionally occupied by food crops and natural andseminatural ecosystems. Among the most notorious ofthese bioenergy crops are sugarcane, jotropha, ethanolmaize, and palm oil, crops closely associated with biodi-versity and habitat loss, water deficit, and perhaps mostironically, given their potential for greenhouse gas emis-sions reduction, negative impacts on carbon storage andsequestration (Fargione et al., 2008; Martinelli & Filoso,2008; Koh et al., 2009; Romijn, 2011). In the medium-term bioenergy demand is likely to be met by so-calledsecond-generation (2G) lignocellulose crops, principallyperennial grasses and woody trees (Somerville et al.,2010). Many of the problems associated with establishedfirst-generation biofuel crops, which are often also foodcrops, could be avoided by cultivating 2G bioenergycrops on existing farmland. However, this option isoften undesirable due to increasing food demand andthe potential displacement of food crops (Dauber et al.,2010; Godfray et al., 2010; Gelfand et al., 2013). This con-flict between land use objectives, the so-called ‘food,energy, environment trilemma’ (Tilman et al., 2009),raises concerns that increased demand for bioenergycrops will displace food production and/or cause fur-ther destruction of natural and seminatural (so-calledmarginal) ecosystems. The problems of potential biodi-versity loss and land competition with food productionremain central to the debate surrounding the possiblecontribution that bioenergy crops could make towardsmeeting renewable energy and greenhouse gas emis-sions targets (Nonhebel, 2012). Policy makers are leftstruggling with the problems that have doggedbioenergy cultivation for decades; where should 2G bio-energy crops be planted and what proportion of landshould they occupy? Such questions raise doubts as tothe viability of bioenergy as a major future energysource; a major recent report into bioenergy crop viabil-ity in the United States concluded that economic andenvironmental uncertainty will strongly limit futuredeployment of 2G crops (Committee on Economic E Carvell et al., 2007, 2011;Whittingham, 2011), but this approach is not widelyapplied to bioenergy crops at present. Our second pro-posal is that new bioenergy plantations are located in amore strategic way that considers landscape context andis sensitive to how they affect biodiversity and ecosystemservices (Table 2). This involves planning the spatialarrangement of bioenergy plantations so that they inter-act positively with other landscape units. It also requiresan understanding of how the impact of bioenergy cropson biodiversity and food security varies depending upon

Contrasting impacts of pollen and seed dispersal on spatial genetic structure in the bird-pollinated Banksia hookeriana

In plants, pollen- and seed-dispersal distributions are characteristically leptokurtic, with significant consequences for spatial genetic structure and nearest-neighbour mating. However, most studies to date have been on wind- or insect-pollinated species. Here, we assigned paternity to quantify effective pollen dispersal over 9 years of mating, contrasted this to seed dispersal and examined their effects on fine-scale spatial genetic structure, within the bird-pollinated shrub Banksia hookeriana (Proteaceae). We used 163 polymorphic amplified fragment length polymorphism markers to assess genetic structure and pollen dispersal in a spatially discrete population of 112 plants covering 0.56 ha. Spatial autocorrelation analysis detected spatial genetic structure in the smallest distance class of 0–5 m (r=0.025), with no significant structure beyond 8 m. Experimentally quantified seed-dispersal distances for 337 seedlings showed a leptokurtic distribution around a median of 5 m, reaching a distance of 36 m. In marked contrast, patterns of pollen dispersal for 274 seeds departed strikingly from typical near-neighbour pollination, with a distribution largely corresponding to the spatial distribution of plants. We found very high multiple paternity, very low correlated paternity and an equal probability of siring for the 50 closest potential mates. Extensive pollen carryover was demonstrated by multiple siring in 83 of 86 (96.5%) two-seeded fruits. Highly mobile nectar-feeding birds facilitate this promiscuity through observed movements that were effectively random. As the incidence of bird-pollination is markedly greater in the Southwest Australian Floristic Region than elsewhere, our results have broad and novel significance for the evolution and conservation for many species in Gondwanan lineages.

Seedling-herbivore interactions: insights into plant defence and regeneration patterns.

BACKGROUND Herbivores have the power to shape plant evolutionary trajectories, influence the structure and function of vegetation, devastate entire crops, or halt the spread of invasive weeds, and as a consequence, research into plant-herbivore interactions is pivotal to our understanding of plant ecology and evolution. However, the causes and consequences of seedling herbivory have received remarkably little attention, despite the fact that plants tend to be most susceptible to herbivory during establishment, and this damage can alter community composition and structure. SCOPE In this Viewpoint article we review why herbivory during early plant ontogeny is important and in so doing introduce an Annals of Botany Special Issue that draws together the latest work on the topic. In a synthesis of the existing literature and a collection of new studies, we examine several linked issues. These include the development and expression of seedling defences and patterns of selection by herbivores, and how seedling selection affects plant establishment and community structure. We then examine how disruption of the seedling-herbivore interaction might affect normal patterns of plant community establishment and discuss how an understanding of patterns of seedling herbivory can aid our attempts to restore semi-natural vegetation. We finish by outlining a number of areas where more research is required. These include a need for a deeper consideration of how endogenous and exogenous factors determine investment in seedling defence, particularly for the very youngest plants, and a better understanding of the phylogenetic and biogeographical patterns of seedling defence. There is also much still be to be done on the mechanisms of seedling selection by herbivores, particularly with respect to the possible involvement of volatile cues. These inter-related issues together inform our understanding of how seedling herbivory affects plant regeneration at a time when anthropogenic change is likely to disrupt this long-established, but all-too-often ignored interaction.

Seedling herbivory and the influence of plant species richness in seedling neighbourhoods

The aim of this experiment was to determine how increasing species richness within artificially created grassland gaps affected the overall magnitude of seedling losses to, and the selectivity of, seedling herbivores. Using chemical exclusion methods, the influence of molluscs the principal invertebrate herbivores in temperate grasslands, was assessed at three levels of plant species diversity (3, 6, and 12 species per gap). In comparison with ungrazed controls, mollusc herbivory significantly reduced seedling numbers. However, the total number of seedlings killed by molluscs was unrelated to the number of seedling species present in the gap. Furthermore, there was no evidence to suggest that seedling species diversity influenced rates of mollusc selection of the three individual species (Agrostis capillaris, Senecio jacobaeae, and Taraxacum officinale) present in each diversity treatment. This work highlights the preferential selection by molluscs of broad-leaved herb species over neighbouring grass seedlings. However the results also suggest that when presented with an increasing choice of different seedling species, the overall magnitude and selectivity of seedling removal by molluscs remains unchanged.

Pregermination heat shock and seedling growth of fire-following Fabaceae from four Mediterranean-climate regions

The role of heat-shock in stimulating the germination of soil-stored seeds from fire-following plant species is well known. However, the effects of high pre-germination temperatures on subsequent seedling growth are less well understood. In this study, we examined the effect of pre-germination heat shock at five temperatures (60°, 75°, 90°, 105° and 120°C, each applied for 5 min) on the seedling growth of four, fire-following Fabaceae species from four Mediterranean-type ecosystems; Hippocrepis multisiliquosa (Israel), Gastrolobium villosum (Western Australia), Cyclopia pubescens (South Africa) and Lupinus succulentus (California). Following heat treatment and subsequent germination, seedlings were grown in controlled conditions before being harvested at either 10, 20- or 40 d old. A significant increase in mean dry weight biomass was found at 10 days for Hippocrepis seedlings germinated from seeds pre-heated to 90°C. However, subsequent comparison of mean dry weight biomass for seedlings of this species at 20 and 40 d old showed no significant response to heat shock pre-treatment. Similarly, an initial increase in growth of Gastrolobium seedlings germinated from seeds heated to 90° and 105°C disappeared as the plants matured. Seedling growth of Lupinus and Cyclopia was unaffected by the pre-germination heat treatment of their seeds. Since seedling competition is influenced by the size and growth rates of neighbouring plants, any changes in seedling growth rates as a consequence of the temperature environment experienced by their seeds, may therefore influence patterns of post-fire plant community recovery.

Evaluating ecosystem processes in willow short rotation coppice bioenergy plantations

Despite a growing body of research linking bioenergy cultivation to changing patterns of biodiversity, there has been remarkably little interest in how bioenergy plantations affect key ecosystem processes underpinning important ecosystem services. In this study, we compare how the processes of predation by ground arthropods and litter decomposition varied between Short Rotation Coppice (SRC) willow bioenergy plantations and alternative land‐uses: arable and set‐aside (agricultural land taken out of production). We deployed litter bags to measure variation in decomposition, and a prey removal assay coupled with pitfall traps and direct searches to investigate variation in predation pressure. Decomposition rate was higher in willow SRC and set‐aside than in cereal crops. Willow SRC had the highest abundance and diversity of ground‐dwelling arthropod predators, but land‐use had no detectable influence on predation of fly pupae or the combined activity‐density of the two principal Coleoptera families (carabids and staphylinids). Overall, our study demonstrates that the conversion of arable land to SRC may have implications for the rate of some, but not all, ecosystem processes, and highlights the need for further research in this area.

Facing the future: the importance of substratum features for ecological engineering of artificial habitats in the rocky intertidal

Coastal defences are proliferating in response to climate change, leading to the creation of more vertical substrata. Efforts are being made to mitigate their impacts and create novel habitats to promote biodiversity. Little is known about the effect of aspect (i.e. north–south directionality) and inclination on intertidal biodiversity in artificial habitats. Artificial and natural habitats were compared to assess the role of aspect and substratum inclination in determining patterns of biodiversity at two tidal heights (high and mid). We also compared grazing activity between north- and south-facing surfaces in natural habitats to examine the potential for differential grazing pressure to affect community structure and functioning. Results were variable but some clear patterns emerged. Inclination had no effect on biodiversity or abundance. There was a general trend towards greater taxon richness and abundance on north-facing than south-facing substrata in natural and artificial habitats. On natural shores, the abundance and grazing activity of ‘southern’ limpets (i.e. Patella depressa) was greater on south-facing than north-facing substrata, with possible implications for further range-expansion. These results highlight the importance of incorporating shaded habitats in the construction of artificial habitats. These habitats may represent an important refuge from grazing pressure and thermal and desiccation stress in a warming climate.