Impacts of the novel coronavirus SARS-CoV-2 on wildlife behaviour via human activities.

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) caused the pandemic of the coronavirus disease 2019 (COVID-19), resulting in a global lockdown in 2020. This stagnation in human activities ('anthropause') has been reported to affect the behaviour of wildlife in various ways. The sika deer Cervus nippon in Nara Park, central Japan, has had a unique relationship with humans, especially tourists, in which the deer bow to receive food and sometimes attack if they do not receive it. We investigated how a decrease and subsequent increase in the number of tourists visiting Nara Park affects the number of deer observed in the park and their behaviour (bows and attacks against humans). Compared with the pre-pandemic years, the number of deer in the study site decreased from an average of 167 deer in 2019 to 65 (39%) in 2020 during the pandemic period. Likewise, the number of deer bows decreased from 10.2 per deer in 2016-2017 to 6.4 (62%) in 2020-2021, whereas the proportion of deer showing aggressive behaviour did not change significantly. Moreover, the monthly numbers of deer and their bows both corresponded with the fluctuation in the number of tourists during the pandemic period of 2020 and 2021, whereas the number of attacks did not. Thus, the anthropause caused by the coronavirus altered the habitat use and behaviour of deer that have continuous interactions with humans.

Adaptive significance of light and food for a kleptoplastic sea slug: implications for photosynthesis.

Sacoglossan sea slugs can 'steal' chloroplasts from their algal food and use them for photosynthesis (kleptoplasty). Although it has been shown that light has positive effects on survival and body size retention of some sacoglossans likely through photosynthesis, it is unknown whether light affects their fitness components such as number of offspring or offspring size. Moreover, whether the effects of light extend over the sacoglossans' lifetime has been unexplored. To assess such long-term effects of light intensity and food availability on fitness components, we conducted a 15.9-week laboratory experiment using Elysia atroviridis under a combination of two light intensities (low or high) and two food conditions (with or without food). The total number of eggs laid was greater in the presence of both strong light and food than in other conditions, suggesting positive effects of both light intensity and food availability. The shell height at hatch was also largest in the presence of strong light and food. Larval rearing experiments showed that the size difference at hatch between conditions corresponded to a 1.19-1.93 days growth and 7.9-18.1% survival increase. Thus, positive effects of light and food on the fitness components extend over the lifetime of E. atroviridis.

Defensive chemicals of neighboring plants limit visits of herbivorous insects: Associational resistance within a plant population.

Despite our understanding of chemical defenses and their consequences for plant performance and herbivores, we know little about whether defensive chemicals in plant tissues, such as alkaloids, and their spatial variation within a population play unappreciated and critical roles in plant-herbivore interactions. Neighboring plants can decrease or increase attractiveness of a plant to herbivores, an example of a neighborhood effect. Chemical defensive traits may contribute to neighborhood effects in plant-herbivore interactions. We examined the effects of nicotine in leaves (a non-emitted defense chemical) on plant-herbivore interactions in a spatial context, using two varieties of Nicotiana tabacum with different nicotine levels. A common garden experiment demonstrated that visits by grasshoppers decreased with increasing density of neighboring plants with a greater nicotine level. In contrast, visits of leaf caterpillars were not affected by neighbors, irrespective of nicotine levels. Thus, our results clearly highlighted that the neighborhood effect caused by the nicotine in leaves depended on the insect identity, and it was mediated by plant-herbivore interactions, rather than plant-plant interactions. This study demonstrates that understanding of effects of plant defensive traits on plant-herbivore interactions requires careful consideration of the spatial distribution of plant defenses, and provides support for the importance of spatial context to accurately capture the ecological and evolutionary consequences of plant-herbivore interactions.

Roles of the seasonal dynamics of ecosystem components in fluctuating indirect interactions on a rocky shore.

Accurately evaluating the strengths of direct (i.e., consumptive and non-consumptive) effects and indirect (density- and trait-mediated) interactions is crucial for understanding the mechanisms of the maintenance and dynamics of an ecosystem. However, an in situ evaluation has not been conducted for a long enough period of time to fully consider the seasonality and life histories of the community components. We conducted a 9-month (from summer to spring) field experiment in an intertidal rocky shore ecosystem involving the carnivorous snail, Thais clavigera, its prey, the limpet Siphonaria sirius, and their resources, the cyanobacterium (blue-green alga) Lithoderma sp. and the green algae Ulva spp. From summer to autumn, the predation pressure was high, and the consumptive and non-consumptive effects of the predator had opposite (positive and negative, respectively) effects on the prey. Both the density- and trait-mediated indirect interactions decreased the coverage of Lithoderma and increased the coverage of Ulva. As the predation pressure decreased in autumn, the predator affected both the adults and the new recruits of the prey. The trait-mediated interactions still existed, but the density-mediated interactions were not detected. From winter to spring, no direct effects or indirect interactions were detected because of the low predation pressure. Our investigation highlights previously unnoticed processes-showing that the strengths of the direct effects and indirect interactions fluctuate greatly with the seasonality of the ecosystem components.

Early onset of spring increases the phenological mismatch between plants and pollinators.

Climate warming accelerates the timing of flowering and insect pollinator emergence, especially in spring. If these phenological shifts progress independently between species, features of plant-pollinator mutualisms may be modified. However, evidence of phenological mismatch in pollination systems is limited. We investigated the phenologies of a spring ephemeral, Corydalis ambigua, and its pollinators (bumble bees), and seed-set success over 10-14 years in three populations. Although both flowering onset and first detection of overwintered queen bees in the C. ambigua populations were closely related to snowmelt time and/or spring temperature, flowering tended to be ahead of first pollinator detection when spring came early, resulting in lower seed production owing to low pollination service. Relationships between flowering onset time, phenological mismatch, and seed-set success strongly suggest that phenological mismatch is a major limiting factor for reproduction of spring ephemerals. This report demonstrates the mechanism of phenological mismatch and its ecological impact on plant-pollinator interactions based on long-term monitoring. Frequent occurrence of mismatch can decrease seed production and may affect the population dynamics of spring ephemerals.

Demand-driven resource investment in annual seed production by a perennial angiosperm precludes resource limitation.

The limits on annual seed production have long been characterized as restriction by either pollination success or resource provision to seed development. This expected dichotomy between pollen and resource limitation is based on the assumption that reproductive resources are fixed, which is reasonable for semelparous species. In contrast, iteroparity can ease the constraints on reproductive output per breeding season, if resources can be either mobilized from past storage or borrowed against future performance. For perennial plants, these options allow enhanced reproductive investment in response to unusually good pollination, so that annual seed production may not be pollen or resource limited. We assessed demand-governed reproductive investment by manipulating both resource supply capacity (partial defoliation) and resource demand (pollination quality: fully self-pollination, fully cross-pollination, or combinations of partial self- and cross-pollination within the inflorescence) for a forest herb, Stenanthium occidentale, which is subject to strong pre-dispersal inbreeding depression. Insensitivity to partial defoliation indicated that reproductive output was not source regulated. Instead, demand by developing seeds governs resource distribution, as demonstrated by elevated photosynthate translocation to fruits on fully cross-pollinated plants and the ability of completely defoliated plants to produce seeds. Such contingent resource allocation eliminates a simple dichotomy between pollen receipt and resource availability as limits on annual seed production. Instead, such flexible reproductive investment allows iteroparous perennials to participate maximally in current reproduction (as determined by ovule production) following superior pollination, or to conserve resources for future reproduction following poor pollination.

Effects of defoliation and shading on the physiological cost of reproduction in silky locoweed Oxytropis sericea.

BACKGROUND: The production of flowers, fruits and seeds demands considerable energy and nutrients, which can limit the allocation of these resources to other plant functions and, thereby, influence survival and future reproduction. The magnitude of the physiological costs of reproduction depends on both the factors limiting seed production (pollen, ovules or resources) and the capacity of plants to compensate for high resource demand. METHODS: To assess the magnitude and consequences of reproductive costs, we used shading and defoliation to reduce photosynthate production by fully pollinated plants of a perennial legume, Oxytropis sericea (Fabaceae), and examined the resulting impact on photosynthate allocation, and nectar, fruit and seed production. KEY RESULTS: Although these leaf manipulations reduced photosynthesis and nectar production, they did not alter photosynthate allocation, as revealed by (13)C tracing, or fruit or seed production. That photosynthate allocation to reproductive organs increased >190 % and taproot mass declined by 29 % between flowering and fruiting indicates that reproduction was physiologically costly. CONCLUSIONS: The insensitivity of fruit and seed production to leaf manipulation is consistent with either compensatory mobilization of stored resources or ovule limitation. Seed production differed considerably between the two years of the study in association with contrasting precipitation prior to flowering, perhaps reflecting contrasting limits on reproductive performance.

Comparison of light harvesting and resource allocation strategies between two rhizomatous herbaceous species inhabiting deciduous forests.

Light conditions on the floor of deciduous forests are determined by the leaf dynamics of canopy trees and gap formation. Such spatiotemporal variations of light availability should affect the resource partitioning strategies of understory herbs. Although rhizomatous species are common in understory, relationships between rhizome structure, vegetative growth, and sexual reproduction are unclear in terms of carbon allocation. We compared the photosynthetic characteristics and carbon translocation patterns in the under-canopy and light-gap sites between two summer-green perennial species: Cardamine leucantha with an annual long rhizome, and Smilacina japonica with a perennial short rhizome system. Flowering of both species occurs in early summer under decreasing light availability. In the light-gap, C. leucantha maintained high photosynthetic activity due to continuous leaf production, resulting in higher seed production than in the under-canopy. In contrast, the photosynthetic rate of S. japonica, producing leaves simultaneously, decreased with time irrespective of light conditions, resulting in stable seed production in both sites. Although seasonally decreasing light availability commonly restricts carbon assimilation of understory herbs, the responses of resource partitioning to variations in light availability depend greatly on the belowground structure of individual species.

Linkages between phenology, pollination, photosynthesis, and reproduction in deciduous forest understory plants.

Light availability in the understory of deciduous forests changes drastically within the growing season due to the foliage dynamics of canopy trees. Because flowering phenology, photosynthetic characteristics, and fruiting success respond to such strong seasonality in light availability, we hypothesized that understory plants in such ecosystems should describe distinct phenological groups or syndromes where "syndrome" is defined only as a set of characteristics that co-occur. To identify these phenological syndromes, we studied the flowering phenology, fruit or seed set, and photosynthetic characteristics for 18 perennial understory herbaceous species that differed in reproductive strategy over eight years in a deciduous forest in northern Japan. Three phenological groups emerged from this study: (1) spring bloomers, flowering and fruiting before the completion of canopy closure; (2) early-summer bloomers, flowering during the progress of canopy closure and fruiting after canopy closure; and (3) late-summer bloomers, flowering and fruiting after canopy closure. The spring bloomers had high photosynthetic rates and high fruiting abilities, but the flowering time varied considerably among years due to yearly fluctuations of snowmelt date. Bumble bee-pollinated species of spring bloomers showed variable seed-set success, while fly-pollinated species showed relatively stable seed sets over the years. The early-summer bloomers showed low fruiting abilities irrespective of pollination success, reflecting severe resource limitation with decelerating light availability during fruit development. Although the late-summer bloomers showed low photosynthetic rates under low-light conditions, high fruit-set success was attained if pollination was sufficient. These results support our hypothesis that phenological syndromes may be found in deciduous forest understory plants. Given that reproductive success of bee-pollinated spring bloomers is highly susceptible to seasonal fluctuation, climate change may have its strongest impacts on this group.

Timing of canopy closure influences carbon translocation and seed production of an understorey herb, Trillium apetalon (Trilliaceae).

BACKGROUND AND AIMS: The light availability on a temperate, deciduous-forest floor varies greatly, reflecting the seasonal leaf dynamics of the canopy trees. The growth and/or reproductive activity of understorey plants should be influenced by the length of the high-irradiance period from snowmelt to canopy closure. The aim of the present study was to clarify how spring-blooming species regulate the translocation of photosynthetic products to current reproduction and storage organs during a growing season in accordance with the changing light conditions. METHODS: Growth pattern, net photosynthetic rate, seed production, and shoot and flower production in the next year of Trillium apetalon were compared between natural and experimentally shaded conditions. Furthermore, translocation of current photosynthetic products within plants was assessed by a labelled carbon-chase experiment. KEY RESULTS: During the high-irradiance period, plants showed high photosynthetic ability, in which current products were initially used for shoot growth, then reserved in the rhizome. Carbon translocation to developing fruit occurred after canopy closure, but this was very small due to low photosynthetic rates under the darker conditions. The shading treatment in the early season advanced the time of carbon translocation to fruit, but reduced seed production in the current year and flower production of the next year. CONCLUSIONS: Carbon translocation to the storage organ had priority over seed production under high-irradiance conditions. A shortened bright period due to early canopy closure effectively restricts carbon assimilation, which greatly reduces subsequent reproductive output owing to low photosynthetic products for fruit development and small carbon storage for future reproduction. As populations of this species are maintained by seedling recruitment, acceleration of canopy closure timing may influence the maintenance and dynamics of populations.

A test of the effect of floral color change on pollination effectiveness using artificial inflorescences visited by bumblebees.

Floral color change has been recognized as a pollination strategy, but its relative effectiveness has been evaluated insufficiently with respect to other floral traits. In this study, effects of floral color change on the visitation pattern of bumblebees were empirically assessed using artificial flowers. Four inflorescence types were postulated as strategies of flowering behavior: type 1 has no retention of old flowers, resulting in a small display size; type 2 retains old flowers without nectar production; type 3 retains old flowers with nectar; and type 4 retains color-changed old flowers without nectar. Effects of these treatments varied depending on both the total display size (single versus multiple inflorescences) and the pattern of flower-opening. In the single inflorescence experiment, a large floral display due to the retention of old flowers (types 2-4) enhanced pollinator attraction, and the number of flower visits per stay decreased with color change (type 4), suggesting a decrease in geitonogamous pollination. Type-4 plants also reduced the foraging time of bees in comparison with type-2 plants. In the multiple inflorescence experiment, the retention of old flowers did not contribute to pollinator attraction. When flowering occurred sequentially within inflorescences, type-4 plants successfully decreased the number of visits and the foraging time in comparison with type-2 plants. In contrast, floral color change did not influence the number of visits, and it extended the foraging time when flowering occurred simultaneously within inflorescences but the opening of inflorescences progressed sequentially within a plant. Therefore, the effectiveness of floral color change is highly susceptible to the display size and flowering pattern within plants, and this may limit the versatility of the color change strategy in nature.

Floral color change in Weigela middendorffiana (Caprifoliaceae): reduction of geitonogamous pollination by bumble bees.

We examined the significance of retaining color-changed flowers in pollination success of Weigela middendorffiana through a single visit of bumble bees. Inner parts of flowers changed color with age from yellow to red. In an investigation of the mating system, duration of each color phase, reproductive ability of each of the color-phase flowers, and the effects of color-changed flowers on bumble bee behavior (1) flowers of this species were self-incompatible, (2) color-changed flowers provided little reward to pollinators and little residual reproductive ability, (3) the timing of floral color change was delayed with the progress of flowering season within individual plants, while the duration of the red phase shortened with the progress of flowering season, and (4) red-phase flowers did not attract bumble bees at a distance but did contribute to reducing the number of successive flower visits during a single stay within the plants. Red-phase flowers seemed to indicate the low reward level of old flowers and functioned as a cue to discourage pollinators from staying longer on the same plant. Our results predict that the retention of color-changed flowers without sexual function can enhance the pollination success of a whole plant through male function by reducing successive flower visits during a single stay of pollinators, i.e., geitonogamous pollination.