Secondary Seed Ingestion in Snakes: Germination Frequency and Rate, Seedling Viability, and Implications for Dispersal in Nature

The importance of vertebrate animals as seed dispersers (zoochory) has received increasing attention from researchers over the past 20 years, yet one category in particular, diploendozoochory, remains understudied. As the term implies, this is a two-phase seed dispersal system whereby a secondary seed predator (carnivorous vertebrate) consumes a primary seed predator or granivore (rodent and bird) with undamaged seeds in their digestive tract (mouth, cheek pouch, crop, stomach, or other organ), which are subsequently eliminated with feces. Surprisingly, although snakes are among the most abundant predators of granivorous vertebrates, they are the least studied group insofar as our knowledge of seed rescue and secondary dispersal in a diploendozoochorous system. Here, using live snake subjects of the Sonoran Desert (one viperid and two colubrid species) and seeds of the Foothill Palo Verde (Parkinsonia microphylla), a dominant tree of the same region, we experimentally tested germination frequency and rate, and seedling viability. Specifically, to mimic rodents with seed-laden cheek pouches, we tested whether wild-collected P. microphylla seeds placed in the abdomen of thawed laboratory mice and ingested by the snakes would retain their germination viability. Second, we examined whether seeds exposed to gut transit germinated at a greater frequency and rate than the controls. While we found strong statistical support for our first hypothesis, both aspects of the second one were not significant. Accordingly, we provide an explanation for these results based on specific life-history traits (dormant and non-dormant seeds) of P. microphylla. Our study provides support for the role of snakes as important agents of seed rescue and dispersal in nature, their potential as ecosystem engineers, and crucial evidence for the investment of field-based studies on diploendozoochorous systems in deserts and other ecosystems.

Annual variability in sound acorn production was regulated by a generalist seed predator weevil in Quercus serrata

Highly variable and synchronous seed production within a population (‘masting’) could be from either synchronised high annual variability in floral initiation (‘flower masting’) or synchronised floral abortion until maturity (‘fruit maturation masting’). We investigated the demographic processes of the female organs from flowering to seed maturity, including each type of insect damage identified, in Quercus serrata in six individuals within a stand from 2014 to 2020, western Japan. Although the annual production of sound acorns was significantly correlated with that of female flowers, the annual variability in sound acorn production within an individual was significantly higher and their synchrony increased, compared to those of female flowers. The annual production of female flowers was positively correlated with the temperature difference in April between the previous and flowering years. However, their fluctuation was low, which was neither affected by seed and flower production in the previous year nor contributed to predator starvation. Key-factor analyses revealed that reproductive loss due to oviposition and sap suction by Mechoris ursulus , a generalist seed predator weevil for oak species, was the largest and most important factor that contributed to the annual variation in the total pre-dispersal loss of Q. serrata . The survival rate from female flowers to sound acorns was strongly predicted by the temperature in June, corresponding to the emergence of adult M. ursulus . This study suggests that highly variable and synchronous sound seed production can be proximately regulated by seed predation when the main predator is a generalist.

Unexpected parasitism of Douglas-fir seed chalcid limits biocontrol options for invasive Douglas-fir in New Zealand

Douglas-fir seed chalcid (DFSC) Megastigmus spermotrophus, a small (3 mm long) host-specific seed-predatory wasp, was accidentally introduced into New Zealand in the 1920s. Concern over DFSC reducing Douglas-fir seed production in New Zealand led to an attempt at biocontrol in 1955 with the release, but failed establishment, of the small (2.5 mm long) parasitoid wasp, Mesopolobus spermotrophus. We investigated why DFSC causes little destruction of Douglas-fir seed in New Zealand (usually <20%) despite the apparent absence of major natural enemies. Douglas-fir seed collections from 13 New Zealand sites yielded the seed predator (DFSC) but also potential parasitoids, which were identified using morphology and partial COI DNA sequencing. DFSC destroyed only 0.15% of Douglas-fir seed. All parasitoids were identified as the pteromalid wasp, Mes. spermotrophus, the host-specific biocontrol agent released in 1955. Total parasitism was 48.5%, but levels at some sites approached 90%, with some evidence of density-dependence. The discovery of the parasitoid Mes. spermotrophus could indicate that the biocontrol agent released in 1955 did establish after all. Alternatively, Mes. spermotrophus could have arrived accidentally in more recent importations of Douglas-fir seed. The high level of parasitism of DFSC by Mes. spermotrophus is consistent with DFSC being under successful biological control in New Zealand. Suppression of DFSC populations will benefit commercial Douglas-fir seed production in New Zealand, but it also represents the likely loss of a potential biological control agent for wilding Douglas-fir.

Delayed fertilization facilitates flowering time diversity in Fagaceae

Fagaceae includes typical masting species that exhibit highly synchronized and fluctuating acorn production. Fagaceae shows an interesting feature in that fertilization is delayed by several weeks to more than 1 year after pollination. Although delayed fertilization was recorded over a century ago, the evolutionary advantage of delayed fertilization is still poorly understood. Here, we present a new hypothesis that delayed fertilization facilitates temporal niche differentiation via non-overlapping flowering times among species. Comparing flowering and fruiting times in 228 species from five genera in Fagaceae, we first show that there is a close association between a wider spread of flowering times and the likelihood of a 2-year fruiting habit in which there is a long delay from pollination to fertilization. To study the coevolution of flowering time and delayed fertilization, we developed a mathematical model that incorporates the effects of competition for pollinators, seed predator satiation and unfavourable season for reproduction on fitness. The model shows that delayed fertilization facilitates the diversification of flowering time in a population, which is advantageous for animal-pollinated trees that compete over pollinators. Our new hypothesis about the coevolution of delayed fertilization and flowering time will provide new insight into the evolution of masting. This article is part of the theme issue ‘The ecology and evolution of synchronized seed production in plants’.

Cone characteristics and insect predation levels vary across years in mast seeding white spruce

Populations of many tree species exhibit synchronous and highly temporally variable seed crops across years. This is called mast seeding, and there are two predominant hypotheses for this pattern of reproduction, pollination efficiency and seed-predator satiation. Mast seeding studies typically involve records of population-level reproduction, with less information on the characteristics of reproductive structures. Here, we use data across six years (2012-2017), spanning a range of population-level cone conditions, to characterize i) white spruce (Picea glauca) cone lengths and seeds per cone, and ii) levels of seed predation. We quantified population-level cone production and collected 1,399 cones from a total of 38 trees in the Huron Mountains, Michigan, USA. Linear mixed models showed that mean and minimum cone lengths varied significantly across years; both being longest during the greatest cone production year. Larger cones had more seeds and the slopes of the relationships as well as the intercepts varied significantly across years. Generalized linear mixed models and AIC model selection showed that cones with insect predation damage was greatest when population-level reproduction was the lowest, with a mean proportion of cones damaged 0.82 in that year. Our findings show that white spruce cone characteristics and losses to insect seed predation vary temporally, and follow expectations based on mast seeding hypotheses.

A new species of Mesopolobus (Hymenoptera, Pteromalidae) from black locust crops

A new species of the genus Mesopolobus Westwood, 1833, Mesopolobus robiniae Lakatos &#38; László sp. nov., is described and illustrated from east-central Europe (Romania and Hungary). The species was reared from black locust (Robinia pseudoacacia) seedpod samples, where it most likely parasitizes the black locust’s seed predator Bruchophagus robiniae Zerova, 1970. Here we present the new species and report on its ecological relationships within the European seed predator community of black locust. We also give details regarding type material and type locality, a detailed description with images, a differential diagnosis of the new species, and a modification to the identification key published by Graham (1969), that distinguishes this new species from closely related species. In addition, we provide information on the distribution, biology and results of barcoding analysis. We also provide the DNA sequence data to complement the morphological taxonomy.

Present and Future Distribution of Two Non-Indigenous Orchids and Their Acquired Enemy in Puerto Rico

Establishment of new populations is contingent on overcoming abiotic and biotic barriers. While this applies to all species, these hurdles are at the forefront of invasion biology where prediction, prevention, eradication, and control strategies depend on an understanding of these processes. Arundina graminifolia and Dendrobium crumenatum are two non-indigenous orchids spreading throughout Puerto Rico. The two species have acquired a native herbivore & seed predator, the orchid-specialist weevil, Stethobaris polita. With recently acquired presence records of the three species, land cover data and BioClim variables, we modeled their potential distributions under current conditions and also those projected under the least and most extreme climate scenarios for 2050 and 2070. We show that D. crumenatum flourishes in urban environments which also provide refugia from S. polita, whereas there is currently limited refugia for A. graminifolia from S. polita attack, as this orchid is sensitive to the same climatic variables as the weevil. Projections into all climate scenarios suggest range retractions for all species, with an equal to or greater proportion of both orchid populations subject to S. polita attack. Thus, we illustrate for island invasions how climate change will likely alter the distribution of acquired biotic interactions.