Effect of climate change on mast-seeding species: frequency of mass flowering and escape from specialist insect seed predators

Global surface temperatures are expected to increase by several degrees in the next century, with potentially large but poorly understood impacts on ecological interactions. Here we propose potential effects of increased temperatures on ecologically dominant New Zealand grasses (Chionochloa spp.) that mass flower and mast seed. Twenty-two years’ data from five masting Chionochloa species in New Zealand showed that the cue for heavy flowering was unusually high temperature in the summer of the year before flowering. Attack by predispersal insect seed predators was much reduced in mast years, apparently because predator populations were satiated. Increased temperatures would greatly decrease interannual variation in Chionochloa flowering, allowing seed predator populations to increase and potentially to devastate the seed crop annually. Similar responses are likely in masting species worldwide. This previously unrecognized effect of global warming could have widespread impacts on temperate ecosystems.     

Predator satiation and extreme mast seeding in 11 species of Chionochloa (Poaceae)

Variation in annual flowering effort is described for 16 long datasets from 11 species of Chionochloa (Poaceae) in New Zealand. All populations exhibited extreme mast seeding. The most variable species was C. crassiuscula (coefficient of variation, CV=3.02) over 26 years at Takahe Valley, Fiordland, which is the highest published CV we know of worldwide. The other populations also had high CVs (lowest CV=1.42, mean CV=1.84) which were higher than for other well‐studied genera such as Picea, Pinus and Quercus. There were also frequent years of zero flowering (mean across all populations was 37.2% zero years; maximum 53% for C. rubra and C. crassiuscula over 19 years) whereas zero years are rare in other published masting datasets.Flowering was highly synchronous among species within a site (mean r=0.886), and also (though significantly less so) among sites. Among sites, synchrony was not significantly higher within‐species (mean r=0.711) than between‐species (r=0.690). Warm summer temperatures led to heavy flowering the following summer. Flowering synchrony increased with increasing synchrony in local deseasonalised summer temperatures, and decreased with increasing distance between sites.Mast seeding has been shown in Chionochloa to reduce losses to specialist flower or seed predators. Among‐species synchrony may be adaptive if species share a common seed predator. Developing seeds of at least 10 Chionochloa species are attacked by larvae of an undescribed cecidomyiid. In Takahe Valley, where masting is most pronounced, cecidomyiids attacked all six Chionochloa species in all four years studied. Mean annual losses were almost constant (10.0 to 13.4%) while flowering effort varied 100‐fold. The invariant losses are consistent with other evidence that the cecidomyiid may have extended diapause, which would make it harder to satiate by mast seeding. We hypothesise that one possible factor favouring such extremely high levels of mast seeding in Chionochloa is that its seed predator is very hard to satiate.     

Description of Eucalyptodiplosis chionochloae sp. nov., a cecidomyiid feeding on inflorescences of Chionochloa (Poaceae) in New Zealand

Abstract

A cecidomyiid that feeds on developing seeds in the inflorescences of the New Zealand tussock grasses Chionochloa australis, C. conspicua, C. crassiuscula, C.flavescens, C. macra, C. oreophila, C. pallens, C. rigida, C. rubra, C. spiralis and C. teretifolia is formally described from C. pallens. The new species, named Eucalyptodiplosis chionochloae Kolesik, is the most ubiquitous of flower feeders of Chionochloa. Its larvae do not form galls but feed on the developing seeds in autumn, overwinter as diapausing larvae inside the floret, and pupate then rapidly eclose in summer, sometimes after extended diapause. Methods for rearing adults are described. Based on its morphological characters this species is most closely related to two described congeners that form galls on buds of Eucalyptus trees in Australia. Seed predation by Eucalyptodiplosis chionochloae larvae appears to be the primary driver of the extreme mast seeding (variation among years in flower crops) seen in the host Chionochloa species.     

Masting of rowan <Emphasis Type="Italic">Sorbus aucuparia</Emphasis> L. and consequences for the apple fruit moth <Emphasis Type="Italic">Argyresthia conjugella</Emphasis> Zeller

 Masting of rowan Sorbus aucuparia L. has been studied in 45 sites in southern Norway for 22 years. We present data on the year-to-year variation in fruit setting of rowan, and show that masting is spatially synchronous in Norway and probably all over Fennoscandia. The apple fruit moth Argyresthia conjugella Zeller is an important seed predator on rowan. We present data on the abundance of apple fruit moth in rowanberries during these years and discuss the consequences of masting and intermasting of rowan for apple fruit moth as a pest of apple. We conclude that growth and climate have little impact on flowering intensity and suggest that masting of rowan is an adaptive defense against seed predation and a new example of predator satiation: intermast years inhibit predators and prepare the rowan for the subsequent mast. Received: September 3, 2001 / Accepted: February 24, 2003     

Kobresia tibetica tussocks facilitate plant species inside them and increase diversity and reproduction

Many plant species grow inside tussocks of some graminoids, but the underlying mechanisms remain unclear. We address whether some species occur and flower mainly inside tussocks so that species diversity and sexual reproduction are higher inside than outside tussocks, and whether relieving biological and physical stress is the mechanism associated with the facilitative process. In a heavily grazed grassland on the eastern Tibetan Plateau, where both physical (due to high altitude) and biological conditions (due to heavy grazing) are extremely harsh, we investigated vegetation in paired plots inside and outside 150 Kobresia tibetica tussocks and measured tussock basal area (=plot area). We also measured temperatures at soil surface, 5 and 10 cm depth and the number of animals (yaks, sheep and horses) grazing inside and outside tussocks. Sixty-seven percent of the species occurred and 42% flowered more frequently inside than outside tussocks, but none less frequently. Inside tussocks 78% species flowered, but outside tussocks only 31% did. Consequently, number of species, number of flowering species and number of inflorescences were all markedly larger inside than outside tussocks. Differences in number of species, number of flowering species and number of inflorescences inside and outside tussocks increased with increasing tussock basal area. Soil temperatures were lower inside than outside tussocks, but grazing intensity was much larger outside tussocks. Therefore, tussocks of K. tibetica facilitated the species inside them likely by grazing prevention, but not by increasing warmth. This study provides evidence that plant species colonizing tussocks of graminoids can be facilitated by the tussock species, and facilitation by grazing prevention may be one mechanism causing the coexistence of the species inside tussocks.     

Plant communities affect the species–area relationship on Carex sempervirens tussocks

The species–area relationship (SAR) has been extensively studied in a wide range of plant communities, but very few studies have directly addressed how plant communities affect the SAR and what are the underlying mechanisms. Many graminoids form distinct tussocks where many other plant species grow, but no study has investigated whether the SAR holds true for the vegetation on tussocks. In four plant communities on an abandoned subalpine pasture in the Swiss National Park, we made releves on 600 tussocks of Carex sempervirens and measured tussock basal area and other tussock traits. In all four communities, species richness on C. sempervirens tussocks was strongly positively related to tussock basal area (R²0.74), while other tussock traits explained very little (R²<0.04). Slope and intercept of the SAR on C. sempervirens tussocks differed significantly among the four communities. This was because plant communities affected richness in smaller tussocks (basal diameter <10 cm) but not that in large tussocks (basal diameter10 cm). We conclude that the SAR holds true for vegetation on C. sempervirens tussocks and changes with plant communities. Changes in the SAR on C. sempervirens tussocks are very likely because smaller tussocks are less independent of the plant communities than the larger ones, regarding disturbance or nutrients.     

Masting behaviour in a Mediterranean pine tree alters seed predator selection on reproductive output

• Context‐dependency in species interactions is widespread and can produce concomitant patterns of context‐dependent selection. Masting (synchronous production of large seed crops at irregular intervals by a plant population) has been shown to reduce seed predation through satiation (reduction in rates of seed predation with increasing seed cone output) and thus represents an important source of context‐dependency in plant‐animal interactions. However, the evolutionary consequences of such dynamics are not well understood.
• Here we describe masting behaviour in a Mediterranean model pine species (Pinus pinaster) and present a test of the effects of masting on selection by seed predators on reproductive output. We predicted that masting, by enhancing seed predator satiation, could in turn strengthen positive selection by seed predators for larger cone output. For this we collected six‐year data (spanning one mast year and five non‐mast years) on seed cone production and seed cone predation rates in a forest genetic trial composed by 116 P. pinaster genotypes.
• Following our prediction, we found stronger seed predator satiation during the masting year, which in turn led to stronger seed predator selection for increased cone production relative to non‐masting years.
• These findings provide evidence that masting can alter the evolutionary outcome of plant‐seed predator interactions. More broadly, our findings highlight that changes in consumer responses to resource abundance represent a widespread mechanism for predicting and understanding context dependency in plant‐consumer evolutionary dynamics.

     

Effects of sedge and cottongrass tussocks on plant establishment patterns in a post-mined peatland,northern Japan

Facilitation (positive inter-specific interaction) plays an important role in promoting succession in harsh environments. To examine whether tussocks facilitate the establishment of other species, after peat mining, investigations were carried out in a formerly Sphagnum-dominated wetland (Sarobetsu mire, northern Japan). Two tussock-forming species, Carex middendorffii and Eriophorum vaginatum, have established in sparsely vegetated areas, with a dry ground surface, since peat extraction ended. The following factors were examined, in three microhabitats created by tussocks (center = raised tussock center, edge = tussock edge covered with litter, and flat = flat areas without tussocks): (1) relationships between tussock microhabitats and plant distributions, and (2) the effects of tussocks on survival, growth, flowering and seed immigration of common species. Two (1 × 10 m) plots were established, in each of three sparsely vegetated sites, in September 2005. Tussocks were mapped in each plot, and species, location, flowering, growth stage (seedling, juvenile and fertile) and size of all plants were recorded, during snow-free periods from September 2005 to September 2006. Seed traps were used to investigate seed dispersal from June to October 2006. Four native species, Drosera rotundifolia, Lobelia sessilifolia, Moliniopsis japonica, Solidago virgaurea, and an exotic species, Hypochaeris radicata, were most common. During seedling and juvenile stages, these species were distributed more densely at the tussock edge than in the flat areas, but were less common at the center. H. radicata had a higher survival rate at the edge than in the flat during the winter. The annual growth of H. radicata, L. sessilifolia and S. virgaurea was higher at the edge. Seed traps detected that D. rotundifolia seeds accumulate more at the edge. In conclusion, tussocks facilitated plant establishment in the edge microhabitat by providing litter cover, enhancing seed accumulation, germination and survival, and thus promoted revegetation. However, Sphagnum mosses have not established in the study sites, and the vegetation differs strongly from the areas where no peat mining had taken place.     

Age-states,population structure,and seedling regeneration of Chionochloa pallens in Canterbury alpine grasslands,New Zealand

Abstract. Age-states, population structure, and seedling regeneration of the grass Chionochloa pallens were investigated in eight alpine grassland stands representing the range of canopy cover (ca. 5–75 %) and basal area (112 - 3889 m²/ha^-1) in the headwaters of the Avoca catchment, Canterbury, New Zealand. In open-canopy stands (< 50 % canopy cover, < 2000 m²/ha^-1 basal area) C. pallens individuals were clearly distinguishable. Rela-tionshipsbetweenbasal diameter, number of tillers, height, and % crown death suggested four putative age-states: ‘seedlings‘, ‘juvenile tussocks’, ‘mature tussocks’ and ‘senescent tussocks’. Four types of population structure were identified depending onthe proportions of seedlings and juvenile and mature tussocks. C. pallens seedlings were present in seven stands at densities ranging from 0.6 to 123.4 / m². They were most frequent on microsites protected from frost-heave by short herbaceous vegetation or litter, but with little competition from taller vegetation. Differences in seedling densities between stands partly reflected the proximity and abundance of seed sources and degree of protection from frost-heave. C. pallens population structures appear to be influenced by the frequency and magnitude of geomorphic disturbances and browsing by introduced animals.     

Masting uncoupling: mast seeding does not follow all mast flowering episodes in a dioecious juniper tree

Evolutionary selective forces, like predator satiation and pollination efficiency, are acknowledged to be major causes of masting (the variable, periodic and synchronic production of seeds in a population). However, a number of recent studies indicate that resources might also play an important role on shaping masting patterns. Dioecious masting species offer a privileged framework to study the role of resources on masting variation, since male and female plants often experience different reproductive costs and selective pressures. We followed masting and reproductive investment (RI) of the dioecious tree Juniperus thurifera in two populations along 10 years and studied the different response of males and females to experimentally increased water and nutrient availability in a third population. Juniperus thurifera females invested in reproduction three times more resources than males. Such disparity generated different resource‐use strategies in male and female trees. Tree‐ring growth and water use efficiency (WUE) confirmed that sexes differed in their resource investment temporal pattern, with males using current resources for reproduction and females using resources accumulated during longer periods. Watered and fertilized female trees presented significantly higher flowering reproductive investments than males and experienced an extraordinary mast‐flowering event. However, seeding RI and mast seeding were not affected by the treatment. This suggests that although resource availability affects the reproductive output of this species, there are other major forces regulating masting on J. thurifera. During 10 years, J. thurifera male and female trees presented high and low flowering years more or less synchronously. However, not all mast flowering episodes resulted in mast seeding, leading to masting uncoupling between flowering and seeding. Since flowering costs represent only 1% of females’ total reproductive investments, masting uncoupling could be a beneficial bet‐hedging strategy to maximize reproductive output in spite of unpredictable catastrophic events.     

Avian predation at a Southern Rockhopper Penguin colony on Staten Island,Argentina

We studied predation risk in relation to nest location and subcolony size in Southern Rockhopper Penguins (Eudyptes chrysocome chrysocome) during the chick-rearing period. Striated Caracaras (Phalcoboenus australis), the main predator, preferentially attacked from tussock grasses which are found in the periphery of all subcolonies (peripheral tussocks) and often scattered within them (central tussocks). The greatest numbers of predation and attempted predation events were observed on nests in the periphery of the subcolony next to peripheral tussocks, and on those nests next to central tussocks. Central tussocks offer Striated Caracaras an additional “edge” area from which to prey, much in the same way as do the peripheral tussocks. Predation rate per individual was not correlated with subcolony size possibly due to the presence of central tussocks which, by creating an extra edge area, change the subcolony shape. There is a suggestion (P = 0.06) of increased probability of nest success with subcolony size.     

Fire temperatures and postfire plant community dynamics in Ecuadorian grass páramo

Three aspects of the páramo vegetation's response to fires were investigated: the measurement of fire temperatures, general observations of changes in plant communities following fires, and monitoring the fate of individual plants after burning.Fire temperatures were strongly influenced by the physiognomy of the vegetation, dominated by tussocks of Calamagrostis spp. Temperatures were highest amongst the upper leaves of the tussock (sometimes >500°C). The middle levels of the tussock experienced temperatures in excess of 400°C, but in the dense leaf bases temperatures were often below 65°C. On the ground between tussocks, temperatures were variable, whereas 2 cm below ground temperatures failed to reach 65°C.Plant survival depended on the intensity of the fire and the plant's position within the tussock structure. Survival was often the result of high temperature avoidance (with buds shielded by other plant parts or buried beneath the soil surface).Post-fire Calamagrostis tiller mortality rates were high and tussock regrowth was slow. Some other species appear to maintain their populations by exploiting this recovery phase for seedling establishment on tussocks.Between tussocks, changes of occupancy at the level of the individual plants were greater after fire than in control vegetation. Most transitions were random. Those which departed from random often involved gaps and were related to post-fire mortality, regrowth from below-ground parts, colonisation or, in the case of a clonal mat-forming species, to spatial rearrangement of rosettes. Recovery was slower at higher altitude. Recovery was much slower in burned plots when the upper 2 cm of soil was removed (along with buried plant parts) compared with burned plots.Qualitative observations suggest that recovery may consist of a cyclical process, mediated by the serial dominance of several species that are physiognomically important.The frequency of fires determines the amount of fuel accumulated within grass tussocks and some plants may be unable to survive repeated burning. Chance survival of species in unburned patches of vegetation and random colonisation of gaps may be important determinants of subsequent community structure.     

Sex ratio of Nysius huttoni White (Hemiptera: Lygaeidae) in field and laboratory populations

Abstract

We studied the parasitoids of three insect seed predators of the mast-seeding genus Chionochloa spp. (snow tussocks) at Mt Hutt, New Zealand. Megacraspedus calamogonus (Lepidoptera: Gelechiidae) is parasitised by four species, three Hymenoptera (Zealachertus tortriciphaga [Eulophidae], Diadegma sp. [Ichneumonidae] and Dolichogenidea sp. [Braconidae]) and one Diptera (Uclesiella sp. [Tachinidae]). Diplotoxa similis (Diptera: Chloropidae) is parasitised by Callitula sp. (Hymenoptera: Pteromalidae). Eucalyptodiplosis chionochloae (Diptera: Cecidomyiidae) is parasitised by two Hymenoptera, Gastrancistrus sp. (Pteromalidae) and Zelostemma chionochloae (Platygastridae); all three species have extended diapause. Overall parasitism was 68.5% in M. calamogonus, 1% in D. similis, and 41% in E. chionochloae. Such parasitism in M. calamogonus and E. chionochloae may reduce seed predation in Chionochloa and alter the selective benefit of mast seeding (predator satiation) to the plant. However, seed predation is still high at many sites, so some of the seed predators and parasitoids may be food-limited (bottom-up regulation).     

Snow tussocks, chaos, and the evolution of mast seeding

One hitherto intractable problem in studying mast seeding (synchronous intermittent heavy flowering by a population of perennial plants) is determining the relative roles of weather, plant reserves, and evolutionary selective pressures such as predator satiation. We parameterize a mechanistic resource-based model for mast seeding in Chionochloa pallens (Poaceae) using a long-term individually structured data set. Each plant's energy reserves were reconstructed using annual inputs (growing degree days), outputs (flowering), and a novel regression technique. This allowed the estimation of the parameters that control internal plant resource dynamics, and thereby allowed different models for masting to be tested against each other. Models based only on plant size, season degree days, and/or climatic cues (warm January temperatures) fail to reproduce the pattern of autocovariation in individual flowering and the high levels of flowering synchrony seen in the field. This shows that resource-matching or simple cue-based models cannot account for this example of mast seeding. In contrast, the resource-based model pulsed by a simple climate cue accurately describes both individual-level and population-level aspects of the data. The fitted resource-based model, in the absence of environmental forcing, has chaotic (but often statistically periodic) dynamics. Environmental forcing synchronizes individual reproduction, and the models predict highly variable seed production in close agreement with the data. An evolutionary model shows that the chaotic internal resource dynamics, as predicted by the fitted model, is selectively advantageous provided that adult mortality is low and seeds survive for more than 1 yr, both of which are true for C. pallens. Highly variable masting and chaotic dynamics appear to be advantageous in this case because they reduce seed losses to specialist seed predators, while balancing the costs of missed reproductive events.     

Description,phenology and biology of Zelostemma chionochloae Buhl sp. nov., a platygastrid parasitoid of Eucalyptodiplosis chionochloae (Diptera: Cecidomyiidae) in New Zealand

Abstract

A platygastrid wasp that feeds on the snow tussock flower midge in the inflorescences of New Zealand snow tussock grasses (Chionochloa spp.) is formally described. Zelostemma chionochloae is a specialist natural enemy of Eucalyptodiplosis chionochloae Kolesik which is the most ubiquitous and sophisticated seed predator of Chionochloa. Z. chionochloae is a koinobiont parasitoid and some larvae enter prolonged diapause inside their host for at least 2 years. Methods for adult rearing are described. The phenology of Z. chionochloae is highly synchronised with its host even after 2 years in diapause. Parasitism levels were found to differ between years and elevations, while sex ratios differed among years. Z chionochloae probably suffers inter‐specific competition with another host‐specific hymenopteran parasitoid (Gastrancistrus sp.) which also parasitises E. chionochloae.     

Spatial dynamics of specialist seed predators on synchronized and intermittent seed production of host plants

Masting, the synchronized and intermittent seed production by plant populations, provides highly variable food resources for specialist seed predators. Such a reproductive mode helps minimize seed losses through predator satiation and extinction of seed predator populations. The seed predators can buffer the resource variation through dispersal or extended diapause. We developed a spatially explicit resource-consumer model to understand the effect of masting on specialist seed predators. The masting dynamics were assumed to follow a resource-based model for plant reproduction, and the population dynamics of the predator were represented by a spatially extended Nicholson-Bailey model. The resultant model demonstrated that when host plants reproduce intermittently, seed predator populations go locally extinct, but global persistence of the predator is facilitated by dispersal or extended diapause. Global extinction of the predator resulted when the intermittent reproduction is highly synchronized among plants. An approximate invasion criterion for the predators showed that negative lag-1 autocorrelation in seeding reduces invasibility, and positive lag-1 cross-correlation enhances invasibility. Spatial synchronization in seeding at local scale caused by pollen coupling (or climate forcing) further prevented invasion of the predators. If the predators employed extended diapause, extremely high temporal variability in reproduction was required for plants to evade the predators.     

Disease resistance in Arabidopsisthaliana increases the competitive ability and the predicted probability of long‐term ecological success under disease pressure

Evidence is mounting that flowering by the mast-fruiting Dipterocarpaceae in Southeast Asia is triggered by ENSO events such that seeds are dispersed at the end of ENSO droughts. These droughts induce substantial defoliation and mortality of canopy trees, producing a favorable environment for seedling recruitment in the forest understory. Therefore, seedling release following droughts may have selected for synchronized, supra-annual fruiting in these rain forests. Currently, mast fruiting in Southeast Asia is generally regarded as an evolutionary response to seed predation by nomadic vertebrates. Separating the two causes for mast fruiting, seedling release and predator satiation, may be difficult if they are coupled in nature by ENSO droughts. Nevertheless, if the cue for masting is environmental, then the post-ENSO seedling environment should be considered a potential cause for masting, and if it operates in conjunction with predator satiation, then it may have provided the initial stimulus for supra-annual synchrony in fruiting.     

Seasonal changes in photosynthetic activity of snow tussocks (Chionochloa spp.) along an altitudinal gradient in Otago,New Zealand

Summary Photosynthetic characteristics were studied in Chionochloa rigida, an altitudinally widespread snow tussock and a closely related high-altitude species C. macra. Along a gradient from near sea level to 1600 m there were no consistent differences in maximum photosynthetic capacity which averaged 4.5 mol CO₂ m^-2s^-1. The photosynthetic temperature optimum ranged between 15 and 18°C and there was only a limited capacity for seasonal adjustment. Net photosynthesis was light-saturated at about 500 mol photons m^-2s^-1. In winter, the photosynthetic capacity decreased significantly with increasing altitude of origin of the snow tussocks. A transplant experiment indicated this was partly genetically controlled.     

Light field heterogeneity among tussock grasses: Theoretical considerations of light harvesting and seedling establishment in tussocks and uniform tiller distributions

Although the tussock growth form of caespitose graminoids is widespread, the effect of this growth form on light interception and carbon gain of tillers has received little attention. Daily incident photosynthetic photon flux density (PFD_inc) and carbon gain in monospecific stands of tussock grasses were compared with those of a hypothetical distribution with the equivalent tiller density per total ground area, but evenly distributed rather than clumped in tussocks. This was computed for two tussock grasses Pseudoroegneria spicata (Pursh) A. Löve (bluebunch wheatgrass) and Agropyron desertorum (Fisch, ex Link) Schult. (creasted wheatgrass) at different plant densities. Daily PFD_inc and net photosynthesis (A) were greater if tillers were distributed uniformly rather than clumped in tussocks, except when the density of tussocks was so great as to approach a uniform canopy. When tussock density per ground area was low, much of the difference between tussock and uniform tiller densities in PFD_inc and A was due to shading within the tussocks; up to 50–60% of the potential carbon gain was lost in A. desertorum due to shading within tussocks. In a matrix of tussocks, the light field for establishing seedlings was very heterogeneous; potential A ranged from 7 to 96% relative to an isolated seedling. The mean of daily PFD_inc and A for seedlings in a tussock stand were nearly identical to the values in corresponding stands of uniform tiller distributions. It is hypothesized that the loss of A resulting from clumping tillers into tussocks is offset by benefits of protecting sequestered belowground resources from invasion by seedlings of competitors.     

Effect of photoperiod on the development and diapause of the green lacewing Chrysopa pallens (Neuroptera: Chrysopidae)

To investigate the physiology of Chrysopa pallens, the effect of photoperiod on diapause and development was examined in a Japanese population (33.4°N). The response stage for diapause of C. pallens was considered to be the prepupal stage. The critical photoperiod for diapause induction at 20.0°C was between 13 h light : 11 h dark (LD 13:11) and LD 14:10. The larval developmental period was affected by photoperiod: larvae in diapause took longer to complete their development. This difference of larval developmental period in relation to photoperiod was considered to be an adjustment of larval diapause timing.