Why did heterospory evolve?

The primitive land plant life cycle featured the production of spores of unimodal size, a condition called homospory. The evolution of bimodal size distributions with small male spores and large female spores, known as heterospory, was an innovation that occurred repeatedly in the history of land plants. The importance of desiccation‐resistant spores for colonization of the land is well known, but the adaptive value of heterospory has never been well established. It was an addition to a sexual life cycle that already involved male and female gametes. Its role as a precursor to the evolution of seeds has received much attention, but this is an evolutionary consequence of heterospory that cannot explain the transition from homospory to heterospory (and the lack of evolutionary reversal from heterospory to homospory). Enforced outcrossing of gametophytes has often been mentioned in connection to heterospory, but we review the shortcomings of this argument as an explanation of the selective advantage of heterospory. Few alternative arguments concerning the selective forces favouring heterospory have been proposed, a paucity of attention that is surprising given the importance of this innovation in land plant evolution. In this review we highlight two ideas that may lead us to a better understanding of why heterospory evolved. First, models of optimal resource allocation – an approach that has been used for decades in evolutionary ecology to help understand parental investment and other life‐history patterns – suggest that an evolutionary increase in spore size could reach a threshold at which small spores yielding small, sperm‐producing gametophytes would return greater fitness per unit of resource investment than would large spores and bisexual gametophytes. With the advent of such microspores, megaspores would evolve under frequency‐dependent selection. This argument can account for the appearance of heterospory in the Devonian, when increasingly tall and complex vegetative communities presented competitive conditions that made large spore size advantageous. Second, heterospory is analogous in many ways to anisogamy. Indeed, heterospory is a kind of re‐invention of anisogamy within the context of a sporophyte‐dominant land plant life cycle. The evolution of anisogamy has been the subject of important theoretical and empirical investigation. Recent work in this area suggests that mate‐encounter dynamics set up selective forces that can drive the evolution of anisogamy. We suggest that similar dispersal and mating dynamics could have underlain spore size differentiation. The two approaches offer predictions that are consistent with currently available data but could be tested far more thoroughly. We hope to re‐establish attention on this neglected aspect of plant evolutionary biology and suggest some paths for empirical investigation.     

Tracking wind‐dispersed seeds using 15N‐isotope enrichment

Seed dispersal influences a wide range of ecological processes. However, measuring dispersal patterns, particularly long‐distance dispersal, has been a difficult task. Marking bird‐dispersed seeds with stable ¹⁵N isotopes has been shown to be a user‐friendly method to trace seed dispersal. In this study, we determined whether ¹⁵N urea solution could be used to enrich seeds of two common wind‐dispersed plants, Eupatorium glaucescens (Asteraceae) and Sericocarpus tortifolius (Asteraceae). We further tested if the water type (distilled versus tap) in ¹⁵N urea solutions influences the level and variability of enrichment of plant seeds, and if increasing spraying frequency per se increases enrichment. Because droughts may lower seed set or kill plants, we wanted to investigate if the additional use of an externally applied anti‐transpirant affects the intake of externally applied ¹⁵N into seeds. The results demonstrate that ¹⁵N enrichment of seeds can facilitate dispersal experiments with wind‐dispersed plants. The use of distilled water in ¹⁵N urea solutions did not increase ¹⁵N enrichment compared to tap water. Further, enrichment was more efficient at lower spray frequencies. Both the use of tap water and low frequencies could lower time, effort and project costs. The results suggest that species can be protected from drought using an anti‐transpirant without decreasing the incorporation of ¹⁵N into seeds.     

Climatic sensitivity of species’ vegetative and reproductive phenology in a Hawaiian montane wet forest

Understanding how tropical tree phenology (i.e., the timing and amount of seed and leaf production) responds to climate is vital for predicting how climate change may alter ecological functioning of tropical forests. We examined the effects of temperature, rainfall, and photosynthetically active radiation (PAR) on seed phenology of four dominant species and community-level leaf phenology in a montane wet forest on the island of Hawaiʻi using monthly data collected over ~ 6 years. We expected that species phenologies would be better explained by variation in temperature and PAR than rainfall because rainfall at this site is not limiting. The best-fit model for all four species included temperature, rainfall, and PAR. For three species, including two foundational species of Hawaiian forests (Acacia koa and Metrosideros polymorpha), seed production declined with increasing maximum temperatures and increased with rainfall. Relationships with PAR were the most variable across all four species. Community-level leaf litterfall decreased with minimum temperatures, increased with rainfall, and showed a peak at PAR of ~ 400 μmol/m²s⁻¹. There was considerable variation in monthly seed and leaf production not explained by climatic factors, and there was some evidence for a mediating effect of daylength. Thus, the impact of future climate change on this forest will depend on how climate change interacts with other factors such as daylength, biotic, and/or evolutionary constraints. Our results nonetheless provide insight into how climate change may affect different species in unique ways with potential consequences for shifts in species distributions and community composition.     

How intraspecific variation in seed‐dispersing animals matters for plants

Seed dispersal by animals is a complex phenomenon, characterized by multiple mechanisms and variable outcomes. Most researchers approach this complexity by analysing context‐dependency in seed dispersal and investigating extrinsic factors that might influence interactions between plants and seed dispersers. Intrinsic traits of seed dispersers provide an alternative way of making sense of the enormous variation in seed fates. I review causes of intraspecific variability in frugivorous and granivorous animals, discuss their effects on seed dispersal, and outline likely consequences for plant populations and communities. Sources of individual variation in seed‐dispersing animals include sexual dimorphism, changes associated with growth and ageing, individual specialization, and animal personalities. Sexual dimorphism of seed‐dispersing animals influences seed fate through diverse mechanisms that range from effects caused by sex‐specific differences in body size, to influences of male versus female cognitive functions. These differences affect the type of seed treatment (e.g. dispersal versus predation), the number of dispersed seeds, distance of seed dispersal, and likelihood that seeds are left in favourable sites for seeds or seedlings. The best‐documented consequences of individual differences associated with growth and ageing involve quantity of dispersed seeds and the quality of seed treatment in the mouth and gut. Individual specialization on different resources affects the number of dispersed plant species, and therefore the connectivity and architecture of seed‐dispersal networks. Animal personalities might play an important role in shaping interactions between plants and dispersers of their seeds, yet their potential in this regard remains overlooked. In general, intraspecific variation in seed‐dispersing animals often influences plants through effects of these individual differences on the movement ecology of the dispersers. Two conditions are necessary for individual variation to exert a strong influence on seed dispersal. First, the individual differences in traits should translate into differences in crucial characteristics of seed dispersal. Second, individual variation is more likely to be important when the proportions of particular types of individuals fluctuate strongly in a population or vary across space; when proportions are static, it is less likely that intraspecific differences will be responsible for changes in the dynamics and outcomes of plant–animal interactions. In conclusion, focusing on variation among foraging animals rather than on species averages might bring new, mechanistic insights to the phenomenon of seed dispersal. While this shift in perspective is unlikely to replace the traditional approach (based on the assumption that all important variation occurs among species), it provides a complementary alternative to decipher the enormous variation observed in animal‐mediated seed dispersal.     

Zeitaufwand für das Ernten und Verstecken von Kiefernsamen bei Dünnschn?bligen Tannenh?hern (Nucifraga caryocatactes macrorhynchos) im Fernen Osten Russlands

Zusammenfassung In einem Vorkommen des Dünnschnäbligen Tannenhähers an der Küste des Ochotskischen Meeres im Fernen Osten Sibiriens wurde das Ernten und Verstecken von Samen aus den Zapfen der Zwergzirbelkiefer (Pinus pumila) untersucht. Der Inhalt von durchschnittlich 2,8 Zapfen, das sind etwa 80 Samen, wurde in der gefüllten Kehltasche transportiert und auf eine Anzahl unter niedriger Zwergstrauchvegetation gelegener Bodenverstecke verteilt. Die Verstecke wurden in annähernd linearer Anordnung ohne Bevorzugung einer bestimmten Himmelsrichtung angelegt. Die Versteckserien enthielten im Median 79, maximal mehr als 120 Samen, das Einzelversteck durchschnittlich 19,6 Samen. Das Ernten und Leeren eines Zapfens geschah im Schnitt innerhalb von 47 s. Für das Verstecken einer Füllung des Kehlsacks benötigten die Vögel ca. 170 s. Für das gesamte Beschaffen und Verstecken eines einzelnen Kiefernsamens errechnet sich ein durchschnittlicher Zeitbedarf von 3,26 s. Nach 20 Tagen war der Zapfenvorrat in der lokalen Kiefernpopulation erschöpft. Jeder Häher hat nach den Hochrechnungen bis zu 100.000 Samen vergraben.

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Harvesting and caching capacities of Thin-billed Nutcrackers in the Russian Far East

Summary At the Ochotskian sea coast Thin-billed Eurasian Nutcrackers (Nucifraga caryocatactes macrorhynchos) harvested seeds of ripe cones of the brush pinePinus pumila in late summer. The mean number of seeds carried in their sublingual pouch was 80, which respresents the harvestable contents of 2.8 cones. These were distributed in an average of 5 caches, exclusively in the soil under low tundra vegetation. Caches were organized in nearly straight lines. Series contained a mean of 82.7 seeds, single caches a mean of 19.6 seeds. Plucking one cone and harvesting its seeds took 47 seconds on average. The caching of a complete pouchful took on average 123.4 seconds. The time invested for harvesting and caching one single seed was calculated at 3.26 seconds. Within three weeks in July, an average individual bird was calculated to have cached a total of up to 100,000 seeds.

     

The use of a rapid radiolabeling method for measuring ingestion rates of detritivores

Utilization of the organic components of senescent Spartina alterniflora Loisel detritus by the grass shrimp, Palaemonetes pugio Holthuis, was investigated in laboratory feeding studies. A ¹⁴C-dimethyl sulfate labeling procedure was utilized to label the sterilized detritus. The formed covalent bond is stable to autoclaving, freezing and extremes of pH. An ingestion rate of 2.0 × 10^?4CS·h^?1 was determined for P. pugio. Estimates for rate of incorporation, gross growth efficiency, and total biomass incorporated are presented. An inverse relationship was demonstrated between shrimp size and rates of ingestion and incorporation.     

cDNA and protein sequence of a major pea seed albumin (PA 2 : Mr≈26 000)

Summary Pea albumin 2 (PA2:M_r26000) is a major component of the albumin fraction derived from aqueous salt extracts of pea seed. Sodium dodecylsulfate-polyacrylamide gel electrophoresis and chromatography on DEAE-Sephacel resolve PA2 into two closely related components (PA2a and PA2b). A cDNA clone coding for one of these components has been sequenced and the deduced amino acid sequence compared with partial, chemically-determined sequences for cyanogen bromide peptides from both PA2 components. Complete amino acid sequences were obtained for the C-terminal peptides. The PA2 molecule of 230 amino acids contains four imperfect repeat sequences each of approximately 57 amino acids in length.The combined sequence data, together with a comparison of PA2-related polypeptides produced in vitro and in vivo, indicate that PA2 is synthesized without a signal sequence and does not undergo significant post-translational modification. Although both forms of PA2 contain Asn-X-Thr consensus sequences, neither form is glycosylated. Accumulation of PA2 contributes approximately 11% of the sulfur-amino acids in pea seeds (cysteine plus methionine equals 2.6 residues percent). Suppression of levels of PA2 polypeptides and their mRNAs in developing seeds of sulfur-deficient plants is less marked than that for legumin, in spite of the lower content of sulfur-amino acids in legumin.