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.

Evolutionary game of life-cycle types in marine benthic invertebrates: Feeding larvae versus nonfeeding larvae versus direct development.

Many marine invertebrates have a benthic adult life with planktonic long feeding larval stages (planktotrophy). In other species, planktonic larvae do not eat, and after a rather short period, they settle and initiate their benthic stages (lecithotrophy). Still other species skip planktonic larval stages altogether, and adults produce benthic offspring (direct development). In this paper, we develop an evolutionary game among different life-cycle types and examine the conditions for each life-cycle type to win in a seasonal environment. The growth rate and mortality of benthic individuals are the same among all three life-cycle types, the local habitat (patches) for benthic individuals have a finite longevity, and adults may engage in a limited dispersal just before breeding. Planktotrophy evolves if the planktonic stages are more efficient in terms of biomass gain than benthic life. Otherwise, lecithotrophy or direct development should evolve. Among them, direct development is more advantageous than lecithotrophy if the cost of having planktonic larvae is large, the habitat for benthic individuals is stable, and adults engage in some dispersal.

Evolution of life cycle dimorphism: An example of sacoglossan sea slugs.

Many sea slugs of Sacoglossa (Mollusca: Heterobranchia) are sometimes called "solar-powered sea slugs" because they keep chloroplasts obtained from their food algae and receive photosynthetic products (termed kleptoplasty). Some species show life cycle dimorphism, in which a single species has some individuals with a complex life cycle (the mother produces planktotrophic larvae, which later settle in the adult habitat) and others with a simple life cycle (mothers produce benthic offspring by direct development or short-term nonfeeding larvae in which feeding planktonic stages are skipped). Life cycle dimorphism is not common among marine species. In this paper, we ask whether some aspects of the ecology of solar-powered sea slugs have promoted the evolution of life cycle dimorphism in them. We study the population dynamics of the two life-cycle types that differ in summer (one with planktonic life and the other with benthic life), but both have benthic life in other seasons. We obtain the conditions in which two types with different life cycles coexist stably or a single type generating offspring with different life cycles evolves. We conclude that the stable coexistence of two life cycles can evolve if benthic individuals in summer experience strongly density-dependent processes or if the between-year fluctuation of biomass growth in summer is very large. We discuss whether these results match the life cycles of solar-powered sea slugs with life cycle dimorphism.

Extreme autotomy and whole-body regeneration in photosynthetic sea slugs.

Autotomy, the voluntary shedding of a body part, is common to distantly-related animals such as arthropods, gastropods, asteroids, amphibians, and lizards1,2. Autotomy is generally followed by regeneration of shed terminal body parts, such as appendages or tails. Here, we identify a new type of extreme autotomy in two species of sacoglossan sea slug (Mollusca: Gastropoda). Surprisingly, they shed the main body, including the whole heart, and regenerated a new body. In contrast, the shed body did not regenerate the head. These sacoglossans can incorporate chloroplasts from algal food into their cells to utilise for photosynthesis (kleptoplasty3), and we propose that this unique characteristic may facilitate survival after autotomy and subsequent regeneration.

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.

Microsatellite DNA markers applicable to paternity inference in the androdioecious gooseneck barnacle Octolasmis warwickii (Lepadiformes: Poecilasmatidae).

The gooseneck barnacle Octolasmis warwickii has a rare sexual system called androdioecy, in which hermaphrodites and dwarf males co-occur. It has been hypothesized that dwarf males can coexist with conspecific hermaphrodites when dwarf males are capable of leaving more offspring than hermaphrodites via male reproduction. This hypothesis of reproductive superiority of dwarf males can be validated by comparing the reproductive success between dwarf males and hermaphrodites through DNA marker-based parentage testing. In the present study, we developed microsatellite DNA markers for O. warwickii, and evaluated the power of these markers to infer parentage based on simulation analysis. Using next generation sequencing, we obtained 344 microsatellite sequences suitable for designing primer sets for amplification in polymerase chain reaction (PCR). Of these, we examined the PCR amplification efficiency of 54 primer sets, of which 11 passed our primer screening in a population sample (n = 35). The developed markers exhibited moderate to high levels of polymorphisms, and met Hardy-Weinberg equilibrium with little evidence of significant allelic association to each other. Our simulated paternity inference suggested that the combinational use of the markers allows a high resolution of parentage (success rate of > 99.9%) if all candidate fathers are available.

Different effects of mating group size as male and as female on sex allocation in a simultaneous hermaphrodite.

Sex allocation theory predicts that the optimal sexual resource allocation of simultaneous hermaphrodites is affected by mating group size (MGS). Although the original concept assumes that the MGS does not differ between male and female functions, the MGS in the male function (MGSm; i.e., the number of sperm recipients the focal individual can deliver its sperm to plus one) and that in the female function (MGSf; the number of sperm donors plus one) do not always coincide and may differently affect the optimal sex allocation. Moreover, reproductive costs can be split into "variable" (e.g., sperm and eggs) and "fixed" (e.g., genitalia) costs, but these have been seldom distinguished in empirical studies. We examined the effects of MGSm and MGSf on the fixed and variable reproductive investments in the sessilian barnacle Balanus rostratus. The results showed that MGSm had a positive effect on sex allocation, whereas MGSf had a nearly significant negative effect. Moreover, the "fixed" cost varied with body size and both aspects of MGS. We argue that the two aspects of MGS should be distinguished for organisms with unilateral mating.

Evidence of oligogenic sex determination in the apple snail Pomacea canaliculata.

A small number of genes may interact to determine sex, but few such examples have been demonstrated in animals, especially through comprehensive mating experiments. The highly invasive apple snail Pomacea canaliculata is gonochoristic and shows a large variation in brood sex ratio, and the involvement of multiple genes has been suggested for this phenomenon. We conducted mating experiments to determine whether their sex determination involves a few or many genes (i.e., oligogenic or polygenic sex determination, respectively). Full-sib females or males that were born from the same parents were mated to an adult of the opposite sex, and the brood sex ratios of the parents and their offspring were investigated. Analysis of a total of 4288 offspring showed that the sex ratios of offspring from the full-sib females were variable but clustered into only a few values. Similar patterns were observed for the full-sib males, although the effect was less clear because fewer offspring were used (n = 747). Notably, the offspring sex ratios of all full-sib females in some families were nearly 0.5 (proportion of males) with little variation. These results indicate that the number of genotypes of the full-sibs, and hence genes involved in sex determination, is small in this snail. Such oligogenic systems may be a major sex-determining system among animals, especially those with variable sex ratios.

Direct Growth Measurements of Two Deep-sea Scalpellid Barnacles, Scalpellum stearnsii and Graviscalpellum pedunculatum.

Yoichi Yusa, Natsumi Yasuda, Tomoko Yamamoto, Hiromi Kayama Watanabe, Takuo Higashiji, Atsushi Kaneko, Kazuki Nishida, and Jens T. Høeg (2018) Little is known about the growth rates of invertebrates living in ordinary deep-sea habitats such as continental slopes. Thus, the growth rates of two species of the deep-sea scalpellid barnacles, Scalpellum stearnsii and Graviscalpellum pedunculatum, were studied in two aquaria (at Nara and Okinawa Churaumi, Japan). In addition, growth of an S. stearnsii individual after 1 year of deployment was measured in the field. Overall, adult individuals of both species showed slow growths over 8 months (at Nara) and 2 years (at Okinawa) of rearing (e.g., at Nara: 2.0 ± 3.6 µm d-1 for S. stearnsii and 5.9 ± 2.7 µm d-1 for G. pedunculatum; mean ± SD). In contrast, growth rates of juvenile S. stearnsii at Nara were greater (15 ± 7.7 µm d-1). The in situ growth rate of the adult S. stearnsii (3.4 µm d-1) was greater than the average, but within the range of the rates of similar-sized individuals recorded in aquaria. Compared with other pedunculate barnacles, both species show small growth rates typical for deep-sea animals.

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.

Plastic Sexual Expression in the Androdioecious Barnacle Octolasmis warwickii (Cirripedia: Pedunculata).

Most barnacles are simultaneous hermaphrodites, but dwarf males are also found attached to hermaphrodites in several species. This biologically rare phenomenon of the coexistence of males and hermaphrodites is termed androdioecy. To test whether the hermaphrodite and male sexes are fixed or plastic in the androdioecious pedunculate barnacle Octolasmis warwickii, we conducted a series of 22-day-long transplanting experiments to evaluate the effects of a) the original site (attached to the conspecific vs. attached directly to the substrate) and b) the transplanting site (conspecific-attached vs. substrate-attached). Penis length (as an index of male function), the presence or absence of egg mass (female function), and growth rate were investigated. As with natural dwarf males, individuals that were transplanted onto conspecifics developed longer penises than did those that were transplanted onto the substrate. The original site of attachment also affected penis length. However, no significant effects of the original site or the transplanting were detected in egg-laying activities, as only one experimental individual laid eggs. Individuals that were transplanted onto conspecifics grew less than those that were attached to the substrate. These results indicate that individual sexual expression is affected by the environment in O. warwickii.

Host Relation, Size and Reproduction in the Burrowing Barnacle Trypetesa lampas (Hancock) (Crustacea Cirripedia Acrothoracica).

Sofie K. D. Nielsen, Jens T. Høeg, and Yoichi Yusa (2016) The aim of this study is to investigate the population biology of the burrowing barnacle Trypetesa lampas, a symbiont of hermit crabs and representing the little known cirripede group Acrothoracica. We put special emphasis on the host-barnacle relation and reproduction. A total of 341 hermit crabs from the west coast of Sweden was captured in November 2009 and August 2010, and examined for the associated burrowing barnacles. We found a mean load of 1.4 T. lampas per host and an average prevalence of 31.4% with no seasonal variation. Male hermit crabs also carried T. lampas, indicating that T. lampas does not rely on egg-predation to any substantial degree. The T. lampas load was positively related to host size, but otherwise their frequency distribution did not differ from random. The position of the burrow in the columella of the shell was positively associated with T. lampas size. Reproduction seems to occur throughout the year. We found ovigerous females also in winter, although less frequently than in summer, and no difference in the number of dwarf males between the summer and winter samples. The data from the present study site deviates in many respects (prevalence, female and male load, reproductive cycle, host relation) from previous studies on this and closely related acrothoracican species. This emphasizes that a basic lack of knowledge still exists concerning most aspects of acrothoracican reproduction, life cycles and host relation.

The origins and evolution of dwarf males and habitat use in thoracican barnacles.

Barnacles are exceptional in having various sexual systems (androdioecy, hermaphroditism, dioecy) and with a high morphological diversity of males, though these are always minute (dwarf) compared to their female or hermaphrodite partners. For the first time, we use a multiple DNA marker-based phylogeny to elucidate the ancestral states and evolution of (1) dwarf males, (2) their morphology when present, (3) their attachment site on the partner, and (4) habitat use in thoracican barnacles. Our taxon sampling was especially rich in rare deep-sea Scalpelliformes and comprised species with diverse sexual systems and dwarf male morphologies. Within the thoracican barnacles dwarf male evolution is subject to extensive convergence, but always correlated to similar ecological conditions. Males evolved convergently at least four times from purely hermaphroditic ancestors, in each case correlated with the invasion into habitats with low mating group sizes. The independent evolution of dwarf males in these lineages dovetails with the males having different morphologies and occurring in several different locations on their sexual partner.

Dwarf males and hermaphrodites can coexist in marine sedentary species if the opportunity to become a dwarf male is limited.

In many marine sedentary species, dwarf males coexist with large individuals who are either hermaphrodites or females. Simple models of the evolutionary game of sex allocation and life history choice predict that stable coexistence of dwarf males and hermaphrodites is rather difficult. In many of these models, however, newly settled larvae are assumed to choose freely between becoming a dwarf male or an immature fast growing individual. In this paper, we consider a new model in which the opportunity for a newly settled individual to become a dwarf male is limited, for example by the scarcity of large individuals near its settlement site. In the evolutionarily stable strategy, the stationary population is either (1) dominated by hermaphrodites, with dwarf males scarce or absent, if immature individuals are fast-growing, (2) a mixture of dwarf males and large females, if larval growth is slow and the opportunity to become dwarf males is high, (3) a mixture of dwarf males and hermaphrodites, if larval growth is slow and the opportunity to become dwarf males is limited. We also examine the case in which the opportunity to be a growing individual is spatially limited.

Diverse, continuous, and plastic sexual systems in barnacles.

Barnacles (Crustacea: Thoracica) show diverse sexual systems, including simultaneous hermaphroditism, androdioecy (hermaphrodites + males), and dioecy (females + males). When males occur, they are always much smaller (called dwarf males) than conspecific hermaphrodites or females. Ever since Darwin made this discovery, many scientists have been fascinated by such diversity. In this study, we provide an overview of (1) the diversity of sexual systems in barnacles, (2) the continuity between different sexual systems in some genera or species, and (3) the plasticity in sexual expression in several species. First, although most barnacles are hermaphroditic, both theoretical and empirical studies suggest that females and dwarf males tend to occur in species with small mating groups. Low sperm competition among hermaphrodites and little chance to act as a male are both associated with small group sizes and identified as the forces promoting the evolution of dwarf males and pure females, respectively. Second, in some groups of barnacles, the distinction between hermaphrodites and dwarf males is unclear because of the potential of dwarf males to become hermaphrodites. As many barnacle species tend toward protandric simultaneous hermaphroditism (develop male function first and then add female function without discarding male function), the dwarf males in such cases are best described as potential hermaphrodites that arrest growth and emphasize male function much earlier because of attachment to conspecifics. This is presumably advantageous in fertilizing the eggs of the host individuals. The distinction between hermaphrodites and females may also be obscured in some species. Third, sex allocation and penial morphology are plastic in some species. We also report the results of a transplanting experiment on small individuals of the pedunculate barnacle Octolasmis angulata, which suggests that individuals transplanted onto conspecifics developed longer and broader penises than did control individuals. Overall, the diversity, continuity, and plasticity in the sexual systems of barnacles are sources of important insights into the evolution and maintenance of the diversity of sexual systems.

Population genetics of sex determination in Mytilus mussels: reanalyses and a model.

Large variations in offspring sex ratio have been reported in Mytilus mussels, which show doubly uniparental inheritance of mitochondria (DUI). Here, we reanalyzed the published sex ratio data, using simple population genetics concepts and logistic regression. Contrary to previous studies that detected only maternal effects, we found both paternal and maternal effects on the offspring sex ratio. We propose that sex in Mytilus is controlled by a pair of nuclear sex ratio alleles expressed in the mother and by minor sex-determining genes inherited from the father and also possibly from the mother.

Postembryonic development of the bone-eating worm Osedax japonicus.

Bone-eating worms of the genus Osedax exclusively inhabit sunken vertebrate bones on the seafloor. The unique lifestyle and morphology of Osedax spp. have received much scientific attention, but the whole process of their development has not been observed. We herein report the postembryonic development and settlement of Osedax japonicus Fujikura et al. (Zool Sci 23:733-740, 2006). Fertilised eggs were spawned into the mucus of a female, and the larvae swam out from the mucus at the trochophore stage. Larvae survived for 10 days under laboratory conditions. The larvae settled on bones, elongated their bodies and crawled around on the bones. Then they secreted mucus to create a tube and the palps started to develop. The palps of O. japonicus arose from the prostomium, whereas the anterior appendages of other siboglinids arose from the peristomium. The recruitment of dwarf males was induced by rearing larvae with adult females. Females started to spawn eggs 6 weeks after settlement.

Dwarf males, large hermaphrodites and females in marine species: a dynamic optimization model of sex allocation and growth.

In this study, we investigate the evolutionarily stable schedule of growth and sex allocation for marine benthic species that contain dwarf males. We consider a population in an ephemeral microhabitat that receives a constant supply of larvae. Small individuals can immediately reproduce as a dwarf male or remain immature and grow. Large individuals allocate reproductive resources between male and female functions. The fraction c of newly settled individuals who remain immature and the sex allocation of large individuals m are quantities to evolve. In the stationary ESS, if the relative reproductive success of dwarf males is greater than the survivorship of immature individuals until they reach a mature size, then the population is a mixture of females and dwarf males. If the opposite inequality holds, the population is dominated by hermaphrodites and lacks dwarf males. There is no case in which a mixture of hermaphrodites and dwarf males to be the ESS in the stationary solution. The ESS can be solved by dynamic programming when the strategies depend on the age of the microhabitat (c(t) and m(t)). Typically, the ESS schedule begins with a population composed only of hermaphrodites, which is replaced by a mixture of dwarf males and hermaphrodites and then by a mixture of dwarf males and pure females. The relative importance of these three phases depends on multiple parameters.

Sexual systems and dwarf males in barnacles: integrating life history and sex allocation theories.

Barnacles, which are sedentary marine crustaceans, have diverse sexual systems that include simultaneous hermaphroditism, androdioecy (coexistence of hermaphrodites and males) and dioecy (females and males). In dioecious and androdioecious species, the males are very small and are thus called dwarf males. These sexual systems are defined by two factors: sex allocation of non-dwarf individuals and the presence or absence of dwarf males. We constructed an ESS model treating sex allocation and life history simultaneously to explain sexual systems in barnacles. We analyzed the evolutionarily stable size-dependent resource allocation strategy to male reproductive function, female reproductive function and growth in non-dwarf barnacles, and the ESS proportion of dwarf males, under conditions of varying mortality and food availability. Sex allocation in non-dwarf individuals (hermaphrodites or females) is affected by mate availability and the proportion of dwarf males. When hermaphrodites appear, all hermaphrodites become protandric simultaneous hermaphrodites. Furthermore, high mortality and poor resource availability favor dwarf males because of their early maturation and weakened sperm competition. In conclusion, we showed that combining sex allocation and life history theories is a useful way to understand various sexual systems in barnacles and perhaps in other organisms as well.

Changes in algal community structure via density- and trait-mediated indirect interactions in a marine ecosystem.

In various terrestrial and aquatic ecosystems, predators affect resources indirectly via intermediate prey. Such indirect interactions involve reducing the density of the prey (density-mediated indirect interactions, DMIIs) or changing the behavioral, morphological, or life history traits of the prey (trait-mediated indirect interactions, TMIIs). Although the importance of TMIIs has been highlighted recently, the strengths of both DMIIs and TMIIs under natural conditions have rarely been evaluated, especially in the context of resource community structure. We studied a three-level marine food chain involving the carnivorous snail Thais clavigera, its limpet prey Siphonaria sirius, and the limpet's food sources, the algae Lithoderma sp. and Ulva sp. We measured the strengths of DMIIs and TMIIs and observed how the algal community changes under the pressure of natural predation by T. clavigera on S. sirius. Neither DMIIs nor TMIIs affected the total algal cover or chlorophyll content per unit area. However, both types of indirect interactions caused similar changes in algal composition by increasing the cover of Ulva and decreasing the cover of Lithoderma. This change in the algal community was caused by a reduction in the limpet's preferential consumption of the competitively dominant Ulva over Lithoderma. These results suggest that both DMIIs and TMIIs have similar effects on the changes in resource community structure under natural conditions.