Seed dispersal in the mycoheterotrophic orchid Yoania japonica: Further evidence for endozoochory by camel crickets

• Although orthopterans are rarely considered to be effective seed dispersal agents, the large flightless crickets known as ‘weta’ have been suggested to function as ecological replacements for small mammals in New Zealand, where such mammals are absent. In addition, a recent study reported that camel crickets mediate seed dispersal of several heterotrophic plants, including Yoania amagiensis in Japan.
• I investigated the seed dispersal mechanism of Yoania japonica because the fruit morphology is similar to Y. amagiensis. Specifically, I aimed to determine whether Y. japonica fruits are consumed by camel crickets and, if so, whether the seeds defecated by camel crickets remains intact, by checking seed viability with TTC staining, and whether germination rate is different between seeds collected directly from fruits and defecated seeds by comparing in situ seed germinability.
• The present study provides evidence that camel crickets function as seed dispersal agents of Y. japonica. Camel crickets were important consumers of Y. japonica fruits, and a substantial portion of the consumed seeds remained viable after passing through the digestive tract. In situ seed germination experiments revealed that the seeds defecated by camel crickets actually germinated in the field. In addition, the germination rate of defecated seeds was even higher than that of intact seeds, although the difference was not significant.
• Taken together with recent reports of insect‐mediated endozoochory, such a seed dispersal system may be common in plants with fleshy indehiscent fruits and small seeds, even in locations where other seed dispersal agents are present.

     

The role of frugivorous birds in fruit removal and seed germination of the invasive alien Cotoneaster franchetii in central Argentina

Many invasive plant species have fleshy fruits that are eaten by native frugivorous birds which disperse their seeds and may facilitate their germination, playing an important role in plant invasion success. The fleshy‐fruited shrub Cotoneaster franchetii (Rosaceae) is an important invasive alien in the mountainous regions of central Argentina. To determine the role of avian frugivorous in fruit removal of this species, we conducted a frugivore exclusion experiment including bagged and unbagged branches in 75 plants of C. franchetii. At the end of the dispersal period, we compared the percentage of missing fruits (removed by birds + naturally dropped) in unbagged branches with the percentage of naturally dropped fruits in bagged branches. To assess whether any mechanism acting on seeds during their passage through bird guts (de‐inhibition by pulp removal and/or seed scarification) affects seed germination of this species, we compared percentage and speed of germination among seeds obtained from faeces of the native frugivorous Turdus chiguanco, from manually de‐pulped fruits, and from intact fruits. The percentage of missing fruits per shrub in unbagged branches was significantly higher than the percentage of naturally dropped fruits in bagged branches, suggesting that frugivorous birds play an important role in fruit removal of C. franchetii in the study area. Seeds from bird faeces and from manually de‐pulped fruits germinated in higher percentage and faster than seeds from intact fruits. Germination percentage and speed of seeds from manually de‐pulped fruits were significantly higher than those of gut‐passed seeds. These results indicate that T. chiguanco increases and accelerates seed germination of C. franchetii through pulp removal, but not through seed scarification. Overall, our findings indicate that native frugivorous birds facilitate the dispersal and germination success of C. franchetii, likely playing an important role in its invasion throughout the mountainous region of central Argentina.     

Seed germination and dormancy traits of forbs and shrubs important for restoration of North American dryland ecosystems

• In degraded dryland systems, native plant community re‐establishment following disturbance is almost exclusively carried out using seeds, but these efforts commonly fail. Much of this failure can be attributed to the limited understanding of seed dormancy and germination traits.
• We undertook a systematic classification of seed dormancy of 26 species of annual and perennial forbs and shrubs that represent key, dominant genera used in restoration of the Great Basin ecosystem in the western United States. We examined germination across a wide thermal profile to depict species‐specific characteristics and assessed the potential of gibberellic acid (GA₃) and karrikinolide (KAR₁) to expand the thermal germination envelope of fresh seeds.
• Of the tested species, 81% produce seeds that are dormant at maturity. The largest proportion (62%) exhibited physiological (PD), followed by physical (PY, 8%), combinational (PY + PD, 8%) and morphophysiological (MPD, 4%) dormancy classes. The effects of chemical stimulants were temperature‐ and species‐mediated. In general, mean germination across the thermal profile was improved by GA₃ and KAR₁ for 11 and five species, respectively. We detected a strong germination response to temperature in freshly collected seeds of 20 species. Temperatures below 10 °C limited the germination of all except Agoseris heterophylla, suggesting that in their dormant state, the majority of these species are thermally restricted.
• Our findings demonstrate the utility of dormancy classification as a foundation for understanding the critical regenerative traits in these ecologically important species and highlight its importance in restoration planning.

     

Effects of seed traits on the potential for seed dispersal by fish with contrasting modes of feeding

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Species‐Specific PCR‐Based Assay for Identification and Detection of Phomopsis (Diaporthe) azadirachtae Causing Die‐Back Disease in Azadirachta indica

Die‐back disease caused by Phomopsis (Diaporthe) azadirachtae is the devastating disease of Azadirachta indica. Accurate identification of P. azadirachtae is always problematic due to morphological plasticity and delayed appearance of conidia. A species‐specific PCR‐based assay was developed for rapid and reliable identification of P. azadirachtae by designing a species‐specific primer‐targeting ITS region of P. azadirachtae isolates. The assay was validated with DNA isolated from different Phomopsis species and other fungal isolates. The PCR assay amplified 313‐bp product from all the isolates of P. azadirachtae and not from any other Phomopsis species or any genera indicating its specificity. The assay successfully detected the pathogen DNA in naturally and artificially infected neem seeds and twigs indicating its applicability in seed quarantine and seed health testing. The sensitivity of the assay was 100 fg when genomic DNA of all isolates was analysed. The PCR‐based assay was 92% effective in comparison with seed plating technique in detecting the pathogen. This is the first report on the development of species‐specific PCR assay for identification and detection of P. azadirachtae. Thus, PCR‐based assay developed is very specific, rapid, confirmatory and sensitive tool for detection of pathogen P. azadirachtae at early stages.     

White‐tailed deer as the last megafauna dispersing seeds in Neotropical dry forests: the role of fruit and seed traits

Endozoochory is a prominent form of seed dispersal in tropical dry forests. Most extant megafauna that perform such seed dispersal are ungulates, which can also be seed predators. White‐tailed deer (Odocoileus virginianus) is one of the last extant megafauna of Neotropical dry forests, but whether it serves as a legitimate seed disperser is poorly understood. We studied seed dispersal patterns and germination after white‐tailed deer gut passage in a tropical dry forest in southwest Ecuador. Over 23 mo, we recorded ca 2000 seeds of 11 species in 385 fecal samples. Most seeds belonged to four species of Fabaceae: Chloroleucon mangense, Senna mollissima, Piptadenia flava, and Caesalpinia glabrata. Seeds from eight of the 11 species dispersed by white‐tailed deer germinated under controlled conditions. Ingestion did not affect germination of C. mangense and S. mollissima, whereas C. glabrata showed reduced germination. Nevertheless, the removal of fruit pulp resulting from ingestion by white‐tailed deer could have a deinhibition effect on germination due to seed release. Thus, white‐tailed deer play an important role as legitimate seed dispersers of woody species formerly considered autochorous. Our results suggest that more research is needed to fully understand the ecological and evolutionary effects of the remaining extant megafauna on plant regeneration dynamics in the dry Neotropics.     

Evaluating the Qualitative Effectiveness of a Novel Pollinator: a Case Study of Two Endemic Hawaiian Plants

In situations where native mutualists have become extinct, non‐native species may partner with remnant native species. However, non‐native mutualists may differ behaviorally from extinct native mutualists. In the case of pollination, novel relationships between natives and non‐natives could differ both quantitatively and qualitatively from native–native relationships. In Hawai'i, the non‐native Japanese White‐eye (Zosterops japonicus) has largely replaced endemic birds as pollinator of the endemic Clermontia parviflora and C. montis‐loa. We surveyed Clermontia patches and found that they ranged from 106 to 1198 m in diameter. We performed manual pollination of flowers with pollen taken from plants at five distance categories, ranging from 0 (self‐fertilization) to 20 km, and examined the germination of resulting seeds. We used radiotelemetry to estimate daily Japanese White‐eye movement distances. Percent germination of seeds after short‐ to intermediate‐distance pollination crosses (i.e., 20–1200 m, or intra‐patch pollen transfer distances) significantly exceeded germination of seeds from selfed trials for C. parviflora. No significant differences in germination rates among treatments were detected for C. montis‐loa. The maximum daily movement distances of radio‐tracked birds were generally <1 km. Together, these results suggest that this novel pollinator may be an effective mutualist for both Clermontia species. This study serves as an example of research examining qualitative components of novel mutualism, which are generally neglected relative to quantitative components.     

The nuclear protein Poly(ADP‐ribose) polymerase 3 (AtPARP3) is required for seed storability in Arabidopsis thaliana

The deterioration of seeds during prolonged storage results in a reduction of viability and germination rate. DNA damage is one of the major cellular defects associated with seed deterioration. It is provoked by the formation of reactive oxygen species (ROS) even in the quiescent state of the desiccated seed. In contrast to other stages of seed life, DNA repair during storage is hindered through the low seed water content; thereby DNA lesions can accumulate. To allow subsequent seedling development, DNA repair has thus to be initiated immediately upon imbibition. Poly(ADP‐ribose) polymerases (PARPs) are important components in the DNA damage response in humans. Arabidopsis thaliana contains three homologues to the human HsPARP1 protein. Of these three, only AtPARP3 was very highly expressed in seeds. Histochemical GUS staining of embryos and endosperm layers revealed strong promoter activity of AtPARP3 during all steps of germination. This coincided with high ROS activity and indicated a role of the nuclear‐localised AtPARP3 in DNA repair during germination. Accordingly, stored parp3‐1 mutant seeds lacking AtPARP3 expression displayed a delay in germination as compared to Col‐0 wild‐type seeds. A controlled deterioration test showed that the mutant seeds were hypersensitive to unfavourable storage conditions. The results demonstrate that AtPARP3 is an important component of seed storability and viability.     

Relationships between intra‐specific variation in seed size and recruitment in four species in two contrasting habitats

Large seeds contain more stored resources, and seedlings germinating from large seeds generally cope better with environmental stresses such as shading, competition and thick litter layers, than seedlings germinating from small seeds. A pattern with small‐seeded species being associated with open habitats and large‐seeded species being associated with closed (shaded) habitats has been suggested and supported by comparative studies. However, few studies have assessed the intra‐specific relationship between seed size and recruitment, comparing plant communities differing in canopy cover. Here, seeds from four plant species commonly occurring in ecotones between open and closed habitats (Convallaria majalis, Frangula alnus, Prunus padus and Prunus spinosa) were weighed and sown individually (3200 seeds per species) in open and closed‐canopy sites, and seedling emergence and survival recorded over 3 years. Our results show a generally positive, albeit weak, relationship between seed size and recruitment. In only one of the species, C. majalis, was there an association between closed canopy habitat and a positive seed size effect on recruitment. We conclude that there is a weak selection gradient favouring larger seeds, but that this selection gradient is not clearly related to habitat.     

Protocols for Use of Potamogeton perfoliatus and Ruppia maritima Seeds in Large‐Scale Restoration

Restoration of submerged aquatic vegetation from seed has been hampered by a lack of information on the appropriate conditions for collecting, processing, and storing seeds prior to dispersal. Seeds must be processed and stored under conditions that maintain seed viability, meet dormancy requirements, and prevent premature germination. This study examined the effects of collection date, processing technique, aeration, storage and induction temperature and salinity, and storage period on seed germination of two mesohaline aquatic species, Potamogeton perfoliatus and Ruppia maritima. Collection date and processing technique were significant factors affecting seed yield from donor populations. Seeds of both species remained viable and germinated best when stored at 4°C, and then exposed to freshwater induction conditions. However, their responses to other factors differed. Aeration during storage was necessary in order to maintain viability of P. perfoliatus seeds, whereas it was unnecessary for R. maritima seeds. Storage in freshwater at 4°C prevented germination of P. perfoliatus seeds, while high salinity during cold storage was necessary to minimize premature germination of R. maritima. Mean germination time of P. perfoliatus was dependent on storage salinity; in contrast, mean germination time of R. maritima seeds was dependent on induction salinity. These differences indicate that the methods required to produce large quantities of underwater plant seed amenable to large‐scale restoration efforts must be tailored to the specific requirements of individual species and must consider the range of processes from initial harvest through seed testing prior to field establishment.     

Germination characteristics of Rhinanthus minor influence field emergence,competitiveness and potential use in restoration projects

• The facultative root hemi‐parasite Rhinanthus minor is often used in grassland habitat restoration projects to regulate ecosystem structure and function. Its impact on community productivity and diversity as a function of resource supply, sward composition and management has been widely investigated. However, there is a lack of information about the possible influence of seed quality on the efficacy of the hemi‐parasite.
• Ten seed lots from commercial sources were sown in the field and their germination characteristics investigated in the laboratory. Seeds from four lots were also germinated and sown in pots alongside plants of two host species, Lotus corniculatus and Holcus lanatus. Plant establishment, height and flowering density were evaluated for the hemi‐parasite, while plant biomass was measured for both R. minor and its host.
• Two aspects of seed quality influenced the field emergence of seed lots of R. minor, the radicle emergence (%) and the length of the lag period from the beginning of imbibition to germination (mean germination time), which indicates seed vigour. A longer lag period (lower vigour) was associated with higher levels of seedling mortality and lower plant vigour, in terms of plant height and biomass accumulation and was also reflected in the parasitic impact of the seed lots.
• Seed quality, specifically germination and vigour, can influence the establishment, survival, subsequent plant productivity and parasitic impact of R. minor in vegetation restoration projects. Seed quality is discussed as a key factor to consider when predicting the impact of the hemi‐parasite on community productivity and diversity.

     

Toucans (Ramphastos ambiguus) facilitate resilience against seed dispersal limitation to a large‐seeded tree (Virola surinamensis) in a human‐modified landscape

Large‐seeded plants may suffer seed dispersal limitation in human‐modified landscapes if seed dispersers are absent or unable to disperse their seeds. We investigated dispersal limitation for the large‐seeded tree Virola surinamensis in a human‐modified landscape in southern Costa Rica. During two fruiting seasons, we monitored crop size, seed removal rates, the number of fruiting conspecifics within 100 m, and feeding visitation rates by frugivores at trees located in high and low forest disturbance conditions. Seed removal rates and the total number of seeds removed were high regardless of the disturbance level, but these parameters increased with tree crop size and decreased with the number of fruiting V. surinamensis trees within a 100 m radius. Trees at low disturbance levels were more likely to be visited by seed dispersers. Black mandibled toucans (Ramphastos ambiguus) and spider monkeys (Ateles geoffroyi) were the most important seed dispersers, based on visitation patterns and seed removal rates. Spider monkey feeding visits were more frequent at high disturbance levels, but the monkeys preferentially visited isolated trees with large yields and surrounded by a low number of fruiting Virola trees within 100 m. Toucan visitation patterns were not constrained by any of the predictors and they visited trees equally across the landscape. We suggest that isolated and highly fecund Virola trees are an important food resource for spider monkeys in human‐modified landscapes and that toucans can provide resilience against seed dispersal limitations for large‐seeded plants in human‐modified landscapes in the absence of hunting.     

Comparative germination ecology of two altitudinal vicariant Saxifraga species endemic to the north of Spain

Seeds of high‐mountain species are thought to germinate rapidly, synchronously and at high percentages after a cold period, with limited dependence on the external environment; yet, empirical evidence only partially supports this behaviour. We performed a comparative study of the germination response of two closely related taxa along an altitude gradient in northern Spain. Seeds from several maternal families of six populations of Saxifraga trifurcata (lowland species) and S. canaliculata (highland species) were subjected to temperature and stratification treatments. Germination percentages and germination rates were analysed using generalised linear mixed modelling and accelerated failure‐time modelling. We found that germination percentages and germination rates were high and dependent on incubation temperature in both species. Within species, seeds from higher altitudes had higher germination percentages under all conditions. Cold–wet stratification negatively affected germination success, particularly in the lowland species. Overall, the highland species was less responsive to the experimental treatments and showed more synchronous germination patterns. We conclude that seeds from these two Saxifraga species germinate as efficiently as species from other habitats, but have a narrower germination response, probably due to the stronger selective pressures in their harsh environments. Finally, a cold, wet stratification period is not a prerequisite for the germination of high‐mountain S. canaliculata, and its strong negative effect on the germination of its lowland relative S. trifurcata may contribute to the altitudinal segregation of these two species.     

Heteromorphic seeds of wheat wild relatives show germination niche differentiation

• Crop wild relatives are fundamental genetic resources for crop improvement. Wheat wild relatives often produce heteromorphic seeds that differ in morphological and physiological traits. Several Aegilops and Triticum species possess, within the same spikelet, a dimorphic seed pair, with one seed being larger than the other. A comprehensive analysis is needed to understand which traits are involved in seed dimorphism and if these aspects of variation in dimorphic pairs are functionally related.
• To this end, dispersal units of Triticum urartu and five Aegilops species were X‐rayed and the different seed morphs weighed. Germination tests were carried out on seeds, both dehulled and left in their dispersal units. Controlled ageing tests were performed to detect differences in seed longevity among seed morphs, and the antioxidant profile was assessed in terms of antioxidant compounds equipment and expression of selected antioxidant genes. We used PCA to group seed morphs sharing similar patterns of germination traits, longevity estimates and antioxidant profile.
• Different seed morphs differed significantly in terms of mass, final germination, germination timing, longevity estimates and antioxidant profile in most of the tested species. Small seeds germinated slower, had lower germination when left in their dispersal units, a higher antioxidant potential and were longer‐lived than large seeds. The antioxidant gene expression varied between morphs, with different patterns across species but not clearly reflecting the phenotypic observations.
• The results highlight different trait trade‐offs in dimorphic seeds of Aegilops and T. urartu, affecting their germination phenology and longevity, thereby resulting in recruitment niche differentiation.

     

Mating system,population growth,and management scenario for Kalanchoe pinnata in an invaded seasonally dry tropical forest

Ecological invasions are a major issue worldwide, where successful invasion depends on traits that facilitate dispersion, establishment, and population growth. The nonnative succulent plant Kalanchoe pinnata, reported as invasive in some countries, is widespread in remnants of seasonally dry tropical forest on a volcanic outcrop with high conservation value in east‐central Mexico where we assessed its mating system and demographic growth and identified management strategies. To understand its local mating system, we conducted hand‐pollination treatments, germination, and survival experiments. Based on the experimental data, we constructed a life‐stage population matrix, identified the key traits for population growth, weighted the contributions of vegetative and sexual reproduction, and evaluated management scenarios. Hand‐pollination treatments had slight effects on fruit and seed setting, as well as on germination. With natural pollination treatment, the successful germination of seeds from only 2/39 fruit suggests occasional effective natural cross‐pollination. The ratios of the metrics for self‐ and cross‐pollinated flowers suggest that K. pinnata is partially self‐compatible. Most of the pollinated flowers developed into fruit, but the seed germination and seedling survival rates were low. Thus, vegetative propagation and juvenile survival are the main drivers of population growth. Simulations of a virtual K. pinnata population suggest that an intense and sustained weeding campaign will reduce the population within at least 10 years. Synthesis and applications. The study population is partially self‐compatible, but sexual reproduction by K. pinnata is limited at the study site, and population growth is supported by vegetative propagation and juvenile survival. Demographic modeling provides key insights and realistic forecasts on invasion process and therefore is useful to design management strategies.     

Opposing forces of seed dispersal and seed predation by mammals for an invasive cactus in central Kenya

The invasive erect prickly pear cactus (Opuntia stricta) has reduced rangeland quality and altered plant communities throughout much of the globe. In central Kenya's Laikipia County, olive baboons (Papio anubis) frequently consume O. stricta fruits and subsequently disperse the seeds via defecation. Animal‐mediated seed dispersal can increase germination and subsequent survival of plants. However, consumption of seeds (seed predation) by rodents may offset the potential benefits of seed dispersal for cactus establishment by reducing the number of viable seeds. We investigated foraging preferences of a common and widely distributed small mammal—the fringe‐tailed gerbil (Gerbilliscus robustus), between O. stricta seeds deposited in baboon faeces versus control O. stricta seeds. In addition to providing evidence of seed predation on O. stricta by G. robustus, our data show that seed removal was higher (shorter time to use) for seeds within faeces than for control seeds. G. robustus clearly prefers seeds within faeces compared to control seeds. These results suggest that high abundances of rodents may limit successful establishment of O. stricta seeds, possibly disrupting seed dispersal via endozoochory by baboons.     

A histone methyltransferase inhibits seed germination by increasing PIF1 mRNA expression in imbibed seeds

Phytochrome‐interacting factor 1 (PIF1) inhibits light‐dependent seed germination. The specific function of PIF1 in seed germination is partly due to its high level of expression in imbibed seeds, but the associated regulatory factors have not been identified. Here we show that mutation of the early flowering in short days (EFS) gene, encoding an H3K4 and H3K36 methyltransferase, decreases the level of H3K36me2 and H3K36me3 but not H3K4me3 at the PIF1 locus, reduces the targeting of RNA polymerase II to the PIF1 locus, and reduces mRNA expression of PIF1 in imbibed seeds. Consistently, the efs mutant geminated even under the phyB_off condition, and had an expression profile of PIF1 target genes similar to that of the pif1 mutant. Introduction of an EFS transgene into the efs mutant restored the level of H3K36me2 and H3K36me3 at the PIF1 locus, the high‐level expression of PIF1 mRNA, the expression pattern of PIF1 target genes, and the light‐dependent germination of these seeds. Introduction of a PIF1 transgene into the efs mutant also restored the expression pattern of PIF1 target genes and light‐dependent germination in imbibed seeds, but did not restore the flowering phenotype. Taken together, our results indicate that EFS is necessary for high‐level expression of PIF1 mRNA in imbibed seeds.