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To defend against predators, insects often modify their morphology, flexibly, to enhance survival and reproductive advantages. Here, we report that predation risks from either isolated predator or predator odor cues, induce a higher proportion of nymphs to developed into long-winged females among the parent generation, as well as among F1 generation offspring. Surprisingly, these previously threatened long-winged adults survived better when attacked by a predator owing to the enhanced agility level gained from risk experience. The long wing, and increased agility level, provide adaptive benefits for SBPHs to escape from predation and so are able to go on to reproduce.SBPHs responded more strongly to the caged predators (visual + odor risk cues) and predator odor cues, than just the visual cue of the predator. Different risk cues can elicit different levels of responses in prey33,34,35,36. For example, in the case of the Colorado potato beetle, volatile odor cues from the predator stronger reduced the beetle feeding on plants than predator visual and tactile cues35. But a visual cue has been shown to be crucial for insect pollinators detecting and avoiding flowers with predators37. Insect herbivores frequently communicate via chemical odors33,38. Exploiting the odor cue to perceive the presence of predators should have advantages, because the odor cue can be sensed from a long distance and penetrate the blocking effect of foliage or canopy structure39, enabling the prior detection of risks and the preparation of antipredation behaviors.In densely planted rice paddies, the active foraging behavior of rove beetle may serve as a selective pressure favouring the development in SBPHs of a chemical instead of visual pathway to detect the approach of a rove beetle. However, in the F1 generation, the influence of a predator odor cue on the proportion of winged forms was weaker than that of caged predators, indicating the combined effects of odor and visual cues might be stronger than only an odor cue, suggesting that visual cues cannot be ignored. In our experiments, sealed predator cadavers may have weakened the visual cue of the rove beetles, because the lack of motion did not fully represent the normal visual cue.SBPHs frequently exhibit wing plasticity in response to population density and food quality28,29. When nymph density is higher, or food has deteriorated, a higher proportion of macropters will arise28,29. The development of the winged form is thought to be a strategy for SBPHs to emigrate from inhospitable environments. However, we assumed, predation risks could also induce the occurrence of the winged form, because long wings might enable SBPHs to escape from predation. As expected, the results presented here show that a higher proportion of long-winged females and their offspring arose when nymphs or adults were previously exposed to predation risk, demonstrating that SBPHs can express morphologically plastic defenses in response to prior predation risk. Additionally, the higher proportion of wing forms was not only due to the increasing number of winged females (see Fig. 1, the number of winged females in “caged rove beetle” treatment was lower), but also the increasing proportion of winged females among female groups (the decreasing numbers and proportions of wingless females, Fig. 1). To date, similar patterns have only been shown in pea aphids, in which when predation risk (foot prints from lady beetles) is higher during the parent generation, a higher proportion of winged morphs arise in the offspring40,41. In our experiments, we tested the risk effects passing from nymphs to adults and from parents to their offspring with combined risk cues, an odor cue or a visual cue, which better reveals the capacity for flexible defense strategies within SBPHs and the nature of predation risks in the perpetual ‘arms race’ against predation. This is the first example of how insects can express both within- generational and transgenerational morphological plasticity as a defense strategy in response to prior predator threat, and we suggest that this phenomenon is likely to occur more widely.However, SBPHs do not only face a single lethal pressure from their environment as we discussed above. Nymph density, food quality, even the temperatures or photoperiods may play or interplay roles in the induction of wing plasticity in SBPHs28,29. In these situations, the responses of SBPHs may differ from present results, or opposite results can occur. As an example, the growth rates of snails vary depending on snail densities, food supply and the strength of predation risks. Growth rates were higher when snails were reared on high nutrients and in low densities, but decreased steeply as the predation risk increased. Conversely, the growth rate was lower at high densities and with high predation risk, but increased as nutrient availability increased42. As for SBPHs, the proportion of winged adults may be higher if we reared in higher densities combined with high predation risk, or may be lower if the nutrient condition of the rice plants increases (for example, higher fertilizer inputs benefit the development of planthoppers43) and predators are removed. This hypothesis needs to be tested. Further, the rice plant phenotypes (resistant or sensitive phenotypes) are important to the development of planthoppers or leafhoppers44,45,46, and tests of the interactive effects of plant phenotype, plant quality/quantity, nymph density and predation risk on the wing plasticity of SBPHs should provide insights into the evolution of insects within changing environments.Induced transgenerational defense plasticity as shown in SBPHs may be common in many organisms20,47. It allows parents to transfer their risk experience to offspring and promotes their evolutionary fitness20. When SBPH nymphs are exposed to predation risk, they are likely to develop into long-winged females, because it is an advantageous form for them in the current risk environment. However, such predation risk is variable in time and space, and SBPH parents cannot predict when or whether the predators will disappear. Thus, an appropriate strategy to enhance the survival rate of offspring in an unpredictable environment is to continue producing a higher proportion of long-winged forms. Within-generational and transgenerational plasticity of defense should be a successful adaptive defense strategy for SBPHs, given that rove beetle and other groups of predators such as predatory spiders are abundant all around the year in rice paddies.The higher mortality of SBPH nymphs when they experience predation risk, has been broadly addressed before24,48,49. Reduced food intake during risk periods may contribute to this poorer survival outcome, because insects are likely to alter their feeding behavior50,51, or shift from a high-risk host to a safer, but nutritionally inferior, one52, when they detect the presence of predators. However, we did not observe an apparent behavior change in threatened nymphs in our experiments, even those going on to be macropters, compared to the non-threatened ones. For example, changing feeding location, non-feeding related motility, an increase in jump frequency, etc. did not occur in threatened nymphs. Thus, behavior plasticity seems not to be invoked to explain this phenomenon. However, considering the food consumption of sap-sucking SBPHs is difficult to determine, experiments employing electrical penetration graph (EPG) techniques should be conducted to quantify the amounts of sap consumption during risk periods53. This will help to explain whether the higher mortality is due to a change of feeding behavior (less food intake). Furthermore, some obscure internal physiological plasticity may also cause the higher mortality of SBPH nymphs at risk. For example, increased oxidative damage and decreased assimilation efficiency during the risk period may weaken the survival success of SBPH nymphs. Unfortunately, few studies have verified this assumption, although it has been shown that different assimilation efficiencies may arise under predation risk17, or oxidative damage may be induced by predation risk resulting in a slower growth rate54 and decreased escape performance55.SBPHs exhibit sexual differences in both with- and trans- generational morphological plasticity in relation to defense, i.e., threatened nymphs/parents are more likely to develop into long-winged females, due to the different vulnerability of females and males to predation. This predation difference is particularly acute between short-winged females and males, given that the proportion of short-winged females is lower than that seen in control settings (Fig. 1), and we assume the level of vulnerability may depend on their body size and reproductive role. The body sizes of short-winged females are larger than those of long-winged females or males, causing them to be more vulnerable to predation because they are more highly preferred targets for predator. Also, the short-winged female needs to stay and deposit eggs in the bare rice stem, which increases the time window of exposure to predators while, by contrast, long-winged males are slim and are not required to lay eggs, and so should be not be heavily predated. It follows that short-winged females should be more vulnerable to predation than long-winged females or males. Hence, in SHPBs, increasing the proportion of long-wing females in a population creates greater opportunities to migrate to predator-free habitats for reproduction, while at the same time reducing their vulnerability to predation. We hypothesize that the sexual difference in responses should be adaptive, and might be inheritable if predation pressure frequently favors the long-winged forms among populations over multiple generations.Results presented here also show that previously threatened long-winged offspring survived better than previosuly non-threatened ones when attacked by P. fuscipes. Studies suggest prey-altered morphology in response to predation risks should confer a survival advantage (fitness gained), i.e., a better-developed defensive structure13,24, or refuge in having a larger size that increase survival success57. However, wings themselves are without protective functions for SBPHs, as seen in pea aphids41. Thus, we setup behavioral experiments to reveal how threatened long-winged adults may increase their survival when attacked by a predator. Results show threatened long- winged offspring (but not parents) are more active, and respond more quickly, than unthreatened ones, i.e., a higher number of attacks are needed for P. fuscipes to capture a previously threatened long-winged offspring than one that has not been threatened before. We suggest the increased agility level is not because of the long wing itself, but due to the enhanced muscle strength in the legs of long-winged adults, because in our observation, long-winged adults avoid attack mainly by jumping but not by flight, probably because a jump needs less reaction time than flight.We only observed transgenerational plasticity of induced behavioral defense in SBPHs. This generational difference (within- and trans-generational) in behavioral defense in SBPHs may reflect potential carry-over effects from parents. To our knowledge, the generational difference in defense has rarely been shown in insects, though in pea aphids a fluctuating expression of transgenerational defensive traits (long wing) over generations when predation risk was present or absent has been reported58. We also expect there will be cumulative effects59 accumulated by SBPHs from the parent generation to the F1 generation. However, we are not certain whether these effects exist in our experiments. To determine this, experiments examining defensive traits across multigeneration should be conducted.However, if predation risk increases the number of agile, long-winged SBPH adults, which are of benefit in respect of dispersal, migration, and thus spreading rice viruses, the application of P. fuscipes in biological control appears ultimately to weaken the control effectiveness. Also, a study with field experiments found that predatory ladybugs increase the number of dispersed aphid nymphs, especially in plants with lower resistance. However, surprising results show that the higher number of dispersed aphid nymphs will not necessarily translate into population growth because dispersed aphids are weak (less food intake) and more easily predated by predators60. Thus, the benefits of anti-predator defense in aphids will, over time, translate into negative developmental costs that suppress the aphid population. As for SBPHs, threatened long-winged females perform well in dispersal and defense, but worse in development and reproduction. Recent experiments reveal that previously threatened long-winged females have a longevity that is three days shorter, and produces about 60 fewer eggs per female, than non-threatened long-winged females (unpublished data). Consequently, these negative effects would eventually translate into lower population growth rates within SBPHs. Thus, the introduction of the predation risk from P. fuscipes to control SBPHs is workable, since field experiments in controlling western flower thrips and grasshoppers by exposure to predation risk have been successful49,61, and the main purpose of biological control is to suppress the pest population beneath the relevant economic threshold, and reduce plant mass loss without necessarily eliminating the pest altogether.This study advances the importance of predation risk on the induction of flexible anti-predation defenses in insect parents and their offspring, uncovers the mediating mechanisms, shows how this anti-predation defense expresses differently between sexes, and further explores the adaptation significance of these defense traits for insects exposed to unpredictable environments. These findings should prove important for predicting SBPH migration or dispersal, conducting effective pest control, and better understanding prey-predator interactions. However, future work should examine the effects of predation risks from other groups of predators or parasites on the physiological and behavioral plasticity of SBPHs. More

WORLD VIEW
18 August 2021

Great Barrier Reef: accept ‘in danger’ status, there’s more to gain than lose

The Australian government must embrace UNESCO’s assessment to marshal the resources needed to protect the unique coral ecosystem.

Tiffany H. Morrison

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Tiffany H. Morrison

Tiffany H. Morrison is a political geographer specializing in marine interventions at James Cook University in Townsville, Australia.

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No one denies the cascade of climate-induced coral bleaching that devastated huge portions of the Great Barrier Reef in 2016, nor the subsequent bleaching. No one questions the Queensland government’s 2019 report (see go.nature.com/3ckg) that the reef’s condition near the shore is poor.Yet last month, the World Heritage Committee of the United Nations organization UNESCO caved to lobbying from the Australian government — pressured by fossil-fuel, agricultural and mining interests — and kept the Great Barrier Reef off its list of ecosystems ‘in danger’. In my view, this decision is wrong, factually and strategically. It leaves both UNESCO and Australia weaker against the climate crisis.I study the governance of approximately 250 ecosystems with World Heritage status because of their outstanding value to humanity — including attempts to curtail runaway industrial development of Vietnam’s Ha Long Bay and overzealous urbanization along Florida’s Everglades wetlands.There are benefits to an in-danger listing: the Belize Barrier Reef Reserve System was placed on the list in 2009. The World Heritage Fund then provided technical and financial assistance for its restoration. By 2018, mangrove coverage was restored nearly to 1996 levels, with clearing in protected areas almost entirely curtailed. The whole maritime zone was under a moratorium on oil and gas production. Restoration work is ongoing, but the Belize reef is no longer on the list.
Save reefs to rescue all ecosystems
This July, UNESCO proposed to list the Great Barrier Reef as in danger owing to severe coral bleaching, poor water quality and inaction on climate change.In arguing against the listing, the Australian government did not directly deny the reef’s parlous state, but did play down its condition. The government also argued that the listing would decrease tourism revenues, that Australia had too little time to respond and should not be held responsible for global change, and that UNESCO should not supersede national sovereignty on climate-change policy.Australian environment minister Sussan Ley lobbied committee members from more than a dozen countries to override UNESCO’s recommendation. Australia avoided an in-danger listing in 2015 using similar tactics and by touting a sustainability plan. The following year saw the worst coral bleaching in the world’s history.But changes are in the wind. After back-to-back coral bleaching in 2016–17 and the tragic 2020 bush fires, more Australian voters, industries and even conservative politicians are calling for strong efforts against climate change.Accepting an in-danger listing for the reef could tip the balance past gridlock. More than 70% of Australians think that formally acknowledging the reef’s endangered state would spur action. In 1993, former US president Bill Clinton’s administration requested that UNESCO certify Florida’s Everglades as in danger. This helped to bring industry opponents on board to better manage coastal development. Had the Great Barrier Reef been listed as in danger in 2015, fossil-fuel developments in the catchment areas draining into the reef would have struggled to get approval.Australia’s most conservative politicians will argue that avoiding an in-danger listing in 2022 is necessary to boost economic development. But this will embarrass Australia later. As more marine heating occurs globally, Australia will struggle to defend its inaction on climate to the UN climate-change conference in November and to the World Heritage Committee next year. Even the Queensland Tourism Industry Council has said keeping the reef’s status under the spotlight is a “call to the world to do more on climate change”.
Fevers are plaguing the oceans — and climate change is making them worse
And undercutting the listing undermines the purpose of the World Heritage Committee. Since 1972, 41 ecosystems have been considered for the in-danger list — 27 of them more than once — but not officially inscribed, even though UNESCO and its advisory body had assessed these ecosystems as threatened, or more threatened than those already listed. The number of sites on the list has declined by almost one-third since 2001, although threats continue to grow and there are more ecosystems on the overall World Heritage List.However, destabilizing strategies are mainly due to a small group of nations — including countries in the Organisation for Economic Co-operation and Development, such as Australia and Spain. World Heritage status and in-danger listings often work as intended: the managers of 73% of sites do comply with their responsibilities.Concerned observers are helping the World Heritage Committee to protect itself from political manipulation. In February 2020, a consortium of 76 organizations and individuals petitioned UNESCO to consider climate change in its World Heritage decisions. A nascent international network known as World Heritage Watch hopes to provide more oversight and monitoring of self-interested states. Ecologists and non-profit organizations are using remote sensing and citizen science to track and expose degradation of protected areas (see go.nature.com/2xn1) and hold governments accountable.UNESCO and its World Heritage Committee grasp the stakes. A new draft policy clearly states that climate-related degradation of a World Heritage Area can be used as the basis for in-danger listing; it will probably be ratified later this year at the UNESCO General Assembly. This policy will shine a harsh light on the intensifying geopolitics of climate change. Advanced economies, such as Australia, with high per-capita emissions but limited climate action, will need to find alternative ways to protect resources and jobs.

Nature 596, 319 (2021)
doi: https://doi.org/10.1038/d41586-021-02220-3

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When introducing ARs as a fisheries management tool to Senegal, the Japanese management had the mindset of Japanese stakeholders, i.e., introducing fishing rights. However, after discussions with Senegalese stakeholders, it was decided that no-take areas would be delineated around ARs because the establishment of a strong fishing rights regime was not socially acceptable to the Senegalese fishing community. Japanese governance is based on the acceptance and respect of fishers towards individual, private AR concessions. In contrast, fishers in Senegal, and more widely in West Africa, are characterized by high mobility, particularly in the context of climate change and overexploitation18,19. Consequently, respect for local management regulations is lower, with open access being generally assumed. The basic concept of implementing a no-take area on the AR was not easily accepted by fishers. The immersion of AR concrete blocks was set as a top priority by managers at the expense of more complex socio-economic considerations, such as consciousness-raising activities and self-sustaining participative monitoring of the AR.The clear contradiction between the ecological knowledge of fishers and their behavior was explained by the well-known effects of open access resources on individual behavior. This phenomenon was also observed in our mathematical model. The processes in the mathematical model are in accordance with those perceived by the fishers, so that the results are also those expected by fisher’s local ecological knowledge. It is interesting to notice that the theoretical results presented here are the mathematical solutions of the model at equilibrium between fishing effort and fish population growth, i.e. after an oscillation period. It is obvious that short-term effect of fishing on the AR is always to increase the catch, but many fishers did perceive the longer-term effect of decreasing catches. The potential negative effect of the AR on catch when there is high fish attraction combined with high fishing pressure on the AR might explain the reluctance of a part of the fishers community to AR deployment (Fig. 2). In particular, the model illustrates that the AR attraction effect strongly determines the impact of the management. In general, fish attraction is the most immediate effect perceived after AR deployment11, as was true for our study16. Though the AR volume was relatively small (70 m3), the empty space between the higher blocks also contributes approximately 280 to 570 m3 of good habitat/refuge for schooling fish; therefore, it is actually difficult to accurately describe the volume that affects fish. Thus, it is difficult to say whether this AR is below or above the forecasted optimal volume in absence of fishing (120m3 with model parameters). The existence of an optimal volume for AR was also suggested by field studies as a trade off between food supply and refuge20, in line with our results. For management purposes, it is interesting to determine whether the AR is above or below this optimal level because if the volume is too small, the model predicted that any level of fishing on the AR would, in the long term, decrease the catch in the considered area. On the other hand, if the volume is above the optimal level, a small fishing effort on the AR could be authorized and would increase the total catch in the area.Field observation showed that the fish attraction effect was strong16 but precise estimation of this parameter cannot be inferred, as this would need, ideally, individual fish trajectories. Future field research on the attraction effect may permit estimating the AR attraction parameters. The model sensitivity test showed that the stronger the attraction parameter, the better the impact of the AR for the fisheries in case of no or small fishing effort on the AR (Fig. 3). But at the same time, the attraction is a strong incentive for fishers to fish on the AR, and the predicted benefit for fisheries in the fishing area rapidly vanishes when fishing effort on AR increases. This in turn provides further incentive for fishers to fish the AR, challenging the surveillance capacity. If fish attractiveness is strong and too many fishers fish on the AR, catch in the area will be concentrated on the AR, while the adjacent fishing area will be depleted, with catch levels lower than those prior to AR deployment.Specifically, in the context of generalized overfishing in Senegal21, deciding not to fish on the AR represents significant individual loss, despite being recognized as beneficial, globally22. It has been argued that this situation would rarely occur in small-scale fisheries, due to existing arrangements between individuals23. However, in the context of the highly mobile Senegalese artisanal fishing fleet and its overcapacity, as soon as the AR in Yenne was no longer subject to surveillance, it rapidly attracted fishers from other villages. Also, pre-existing arrangements between fishers might be overruled when new ARs are created, changing the structure of existing fishing grounds.At the time of the survey, the surveillance system set up by the co-management entities was not operational in our case study, because it was dependent on temporally limited external financing. These limitations are typical of short-term projects that focus on a single restricted area for a pre-determined duration, usually up to two years (e.g., NGOs, World Bank). Local fishers perceptions were globally in line with the model prediction that this AR fails to improve fisheries yield when surveillance is not in place to ensure AR regulations are observed, despite effective fish attraction and production existing in the AR.The model predicted that enhanced production on ARs could not keep pace with unrestricted access, which might be particularly true in Senegal where fishing effort rapidly reorganizes itself according to local yields24. Enhanced production due to the AR largely increases the catch if the fishing pressure on the AR remains null or very low, but it has no effect on the catch for higher fishing pressures on the AR (Fig. 3). These results were stable even if fish population growth, fish catchability, mobility and economic parameters could modulate the predicted amplitude of the catch and AR optimal volume. These results are consistent with existing theoretical studies of the impact of fisher movement to high production areas in and around MPAs25. Taking into account several species and their interactions (predation, competition) would lead to a very complex ecosystem model specific to the area (e.g. 26), with necessarily more assumptions. This model would necessarily be more difficult to share with fishers and other stakeholders. Both to simplify model structure and facilitate communication of results to stakeholders, we assumed in our model that the balance of entries exits and is in equilibrium, so that the migratory species did not affect the long-term equilibrium between fishing effort and fish abundance.The design of ARs could be adjusted to reduce the effect of illegal fishing by passively preventing both industrial and artisanal fishing activity. Complex structures are more effective for fish production and attraction27. We showed that, although production might have a limited effect on total catch, attraction can largely increase AR efficiency (total catch) if the rate of illegal fishing rate is very low or absent. Complex structures protect fish more effectively from small scale fishing gear28, including divers (Pers. Comm., Mamadou Sarr, Ouakam fishers committee). Thus, ARs should be appropriately designed to help mitigate potential issues28. Such designs might be more costly, and do not exclude the need for surveillance, but would enhance fisheries management, especially when surveillance cannot capture low levels of illegal fishing.Finally, if socio-economic and governance conditions are not met, well-intentioned AR projects will likely disturb the existing equilibrium among fishers that have different levels of access to the AR. Poor governance of marine resources has previously been described in West Africa, particularly in Senegal29, as has the failure of AR projects in a number of other developing countries9, which further deteriorate fishers trust and management plans efficiency30. In order to avoid that, NGO and governmental agencies driving ARs projects must consider that AR management induces collective costs before providing potentially collective gains. Thus, co-management that involves governmental institutions and fisher communities is required. Future management and adaptation plans for fishers, particularly in developing countries, should, therefore, focus efforts on raising long-term awareness of actors in both government institutions and fishing communities. At the level of institutional or development partners, long-term management costs should be included in the set-up of AR projects. For example, the local fishers committee of Yenne recently reported the establishment of a collective ship chandler whose profits are used to finance AR surveillance during the daytime. Subsequently, fishers noted an improvement in catches around the AR, even though illegal fishing likely continues on the AR at night (Pers. Comm. chair of local fishers committee). These observations support model predictions that low levels of illegal fishing might not disturb the positive impact of the AR. Alternatively surveillance effort could be supported by the community if benefits were managed according to ancestral traditions. Indeed, “no take area” regime on the AR would be in line with some past West African tribal laws, applied before the colonization era, which set marine area where fishing activities were restricted for occasional community celebrations. Collective processes where fishers and other stakeholders can design temporary no-take zones around the AR could increase fishers trust and compliance to the rules, fostering a positive socio-ecological feedback loop30.Hybridization of local and scientific knowledge, through the integration of natural sciences and social sciences, is key point for governance setting31,32,33. Indeed, the communication of the resulting hybrid knowledge in specific events gathering local stakeholders helps strengthen fisheries co-management for the establishment of surveillance and regulatory frameworks. This phenomenon was experienced during the public restitution of the present study with the community, fishers, children’s from local schools and governmental stakeholders. Science popularization of the study results was in French and local language (Wolof) retransmitted on national news (available at https://www.youtube.com/watch?v=yQqFU2P4XZU). Posters were exposed during the event, including pictures of local fishers interviewed and statements reflecting their own perception of how the artificial reef interacts with ecological processes and fisheries dynamics. Straightaway, stakeholders and local promoters of AR publicly expressed their concern and willingness to prioritize the setting up an efficient AR surveillance independent from external resources prior to increase AR deployments. Knowledge hybridization could produce more specific models that could be used for warning and advice, for example by considering potential impacts of ARs on species compositions3,34,35, environmental parameters36, and cascade effects on the trophic food web37. However this approach would need to be adapted to local social-ecological governance, which might require dedicated political-anthropological studies (see concept of adaptive co-management32).In summary, best practices should involve all stakeholders, consider local specificities, such as site configuration, governance, ecosystem, availability of ad hoc human and financial resources for AR surveillance, and define AR volume and design accordingly to these parameters. Thus, if plans exist to deploy ARs at large scales we recommend that legislation is strengthened, with detailed Environmental and social Impact Assessments38 to implement ARs, including considerations of long-term governance. More

Bagworm walking method using a ladder-like silk footholdWhen bagworms are reared in a plastic or glass cage, they walk not only on the floor but also on the walls or ceiling using only their three pairs of thoracic legs. The method by which they achieve this was clarified by placing a bagworm on black paper. Where the bagworm had walked, a ladder-like silk trace was observed on the black paper (Fig. 2a). Scanning electron microscopy (SEM) observation of one of the steps (or rungs) of the ladder-like trace revealed that each step was made up of a zigzag pattern of silk threads (Fig. 2b). Further magnified SEM observations revealed that the folded parts of the zigzag-spun thread were glued selectively to the substrate with adhesive whereas the remaining straight parts (hereafter, termed ‘bridges’ or ‘bridge threads’) were unglued (Fig. 2c–e).Figure 2Architecture of the ladder-like foothold. (a) A typical ladder-like foothold constructed by a bagworm on black paper, (b) an enlarged image showing one of the steps in the foothold and (c) a scanning electron microscopy image of the step shown in (b). The unglued bridge threads and a glued turn in the step shown in (c) are magnified in (d) and (e), respectively. (f) An enlarged image of four continuous steps in the foothold shown in (a). The neighbouring steps are connected via a single thread indicated by the arrows. (g) A schematic depiction of the basic architecture of the foothold; blue lines and green circles correspond to the silk thread and glued parts, respectively. (h) A photograph of a bagworm constructing a foothold on a transparent plastic board.Full size imageNotably, the steps of the foothold were not independent but rather always connected with neighbouring steps via a single thread (Fig. 2f). The overall basic construction of the foothold is schematically depicted in Fig. 2g. We found that the foothold was constructed in one continuous movement and always made of a single thread regardless of walking distance or time; therefore, a continuous thread exceeding a length of 100 m could be collected from one foothold14. We also observed bagworm climbing behaviour on a transparent plastic board, which clarified the important role of the silk trace as a foothold (Fig. 2h). During this behaviour, the bagworm used its sickle claws (Fig. 1e) to hook its second and third pairs of thoracic legs onto the first and second newest steps, respectively, and constructed the next step by spinning silk with a zigzag motion of the head and the skilful use of the first pair of thoracic legs. When the bagworm advanced one step, it always first shifted its third pair of thoracic legs to the next step before then shifting its second pair of thoracic legs to the newest step to avoid overloading this step, which may not yet be fully adhered to the surface (see Supplementary Movie S1). Because of this construction method, the interval distance between neighbouring steps is automatically determined by the interval between the thoracic legs. By repeating this process, the bagworm can advance forward slowly but steadily. This walking method was commonly observed on a horizontal floor surface, vertical wall, or horizontal ceiling. Although we have mainly described and shown observations from E. variegate here, with the exception of Supplementary Fig. S4 and Movie S1, we also observed instances of walking behaviour in other species, namely Eumeta minuscula, Mahasena aurea, Nipponopsyche fuscescens and Bambalina sp. (for a movie on E. minuscula walking behaviour, wherein it climbs a vertical wall, see Supplementary Movie S2). For at least 100 individuals of these bagworm species, we observed essentially identical walking behaviour to that described in the present study without exceptions for locomotion on substrates with slippery surfaces.Based on our observations, we asked the following question: how do bagworms selectively glue the folded parts of the foothold onto the substrate? Real-time observation of the tip of the spinneret (i.e. the spigot) through a transparent plastic board during the construction of the foothold revealed that adhesive was selectively discharged to attach the folded parts to the substrate; this process could be distinguished from the continuous spinning of the silk thread (for a movie showing construction behaviour, see Supplementary Movie S3). Figure 3a–g shows a time-sequence of foothold construction with enlarged images in the vicinity of the spinneret provided, whereas Fig. 3h depicts a schematic trace of the construction process. It was clearly noted that the bagworm discharged the adhesive only at the folded parts (shown in Fig. 3a–c,e,f; termed the ‘glued turn’) and not at the straight bridge parts (shown in Fig. 3d,g; termed the ‘unglued bridge thread’). From these time-sequence observations, we concluded that the bagworm controls the discharge of adhesive in an ‘on and off’ manner as necessary (essentially the same construction behaviours were confirmed for at least 20 individuals).Figure 3Foothold construction. (a–g) (left side) Time-sequence images taken during foothold construction and (right side) enlarged images of the vicinity of the spinneret (corresponding to the yellow rectangular area in each left-side image). The time-sequence images correspond to the parts of the schematic trace of foothold construction depicted by the red line in (h). In each right-side image and the schematic trace, the part of silk thread at which the adhesive was discharged is traced with a light-blue line. Green arrows in the right-side images show the direction of travel of the spinneret.Full size imagePassages of fibroin brins and adhesiveWe next investigated the spinning mechanism that enables continuous spinning of silk thread together with the selective discharge of adhesive via a single spigot. To this end, we observed the morphology of the bagworm from the silk gland to the spigot. Figure 4a shows the area in the vicinity of the spinneret, dissected and isolated from an E. variegata bagworm, which included a pair of silk glands and plural adhesive glands. As we previously reported21, the exterior shape of the silk gland in E. variegata (see Supplementary Fig. S1) is almost the same shape as that in the silkworm Bombyx mori and it is subdivided into three parts: the anterior (ASG), middle (MSG) and posterior (PSG) silk glands. We also previously confirmed that fibroin heavy chain (h-fib), fibroin light chain (l-fib) and fiboinhexamerin genes are expressed dominantly in the PSG, while sericin is expressed in the MSG, which strongly suggests that division-selective production of each protein exists in E. variegata (as has been shown in B. mori22). Figure 4b shows a magnified image of the spinneret including the end of the ASG. Beyond the pair of ASGs, which are merged into a common tube, a silk press and spinning tube appear before the spigot. This basic passage of silk fibroin from the ASG to the spigot is essentially the same as the passage observed in B. mori23. However, more detailed morphological observations of the inner structure of the passage revealed several obvious differences between E. variegata and B. mori.Figure 4Structural examination of the passages of fibroin brins and adhesive. (a) An optical microscope image of the area in the vicinity of a spinneret isolated from a female bagworm in the final instar stage. Indicated by arrows is a pair of silk glands (SG), one of the adhesive glands (ADG) and the spinneret (SP). (b) An optical microscope image of the passage including the (1) end of the anterior SGs (ASGs), (2) common tube, (3) silk press, (4) spinning tube and (5) spigot. (c–j) Optical microscope images showing cross-sections of the passage of fibroin brins obtained from the corresponding positions (c–j) in image (b). To focus on the fibroin brins and its passage, the surrounding outer part was removed so that a pair of fibroin brins was revealed in each image (except for image (c), which shows only one side of the ASG). Unmagnified images of (f–j), including the outer part, are shown in Supplementary Fig. S2. (k–n) 3D X-ray CT images of the spinneret: (k) overview, (l) cross-sectional top view, (m) cross-sectional side view and (n) passage of the fibroin brins and corresponding cross-sectional images at various positions. In the cross-sectional side view (m), the sheath and core parts are coloured blue and pink, respectively. (o) Image of the tip of a spigot from which adhesive is overflowing and a silk thread is emerging.Full size imageCross-sectional images along the spinneret are shown in Fig. 4c–j; these focus on the silk brins and their passage (unmagnified versions of the images in Fig. 4f–j are shown in Supplementary Fig. S2). The fibroin brins have an approximately round cross-sectional shape at the end of the ASG (Fig. 4c) and are merged at a common tube, which deforms their round shape slightly (Fig. 4d). The fibroin brins seem to be coated with a thin layer of sericin after the MSG, similar to B. mori; however, we omit the presence of the sericin layer here for convenience. The paired brins are gradually pressed between the ventral and dorsal hard cuticle plates at the silk press, and a gradual diameter decrease and shape deformation follows (Fig. 4e,f). At the exit of the silk press, each brin becomes elliptic and the diameter in the major axis decreases. Interestingly, the elliptical shape and 1.7-axial ratio for the major and minor axes of the fibroin brin cross-section in bagworm silk, which we previously reported14, are already determined at this stage in the silk press; afterwards, the diameter decreases without any change in the axial ratio of the elliptical cross-section. Notably, the two elliptical fibroin brins are aligned side-by-side so that their major axes are in line horizontally (to resemble a figure of ‘∞’) at the spinning press, and these are followed by the spinning tube (Fig. 4e–h). However, the alignment is twisted by 90° in one direction (to resemble a figure of ‘8’) before the brins are spun from the spigot (Fig. 4i,j).We found that the spinning tube was surrounded by a hard exoskeleton. Using 3D-X-ray CT observations, we produced clear images of the exterior and interior morphologies of the spinning tube enveloped by exoskeleton (Fig. 4k–m; the exterior shape observed from the dorsal-, ventral- and lateral-sides by optical microscopy is provided in Supplementary Fig. S3). The spigot was not cut perpendicularly to the spinning tube but rather with a slope of around 20°; consequently, it was elliptic. X-ray CT clearly showed the core-sheath structure of the spinneret and a wide expanse of sheath parts (Fig. 4m) between the exterior shell and interior spinning tube (Fig. 4l,m). Using optical microscope observations of the cross-sections, we found that at least three pairs of adhesive ducts were running in the sheath space (Supplementary Fig. S2E). Therefore, while the silk brins pass through the central narrow spinning tube, the plural adhesive ducts pass through the outer space independently of the silk thread. Finally, the adhesive enters a ladle-like reservoir located at the spigot and is released together with the silk thread (Fig. 4o). The presence of definitive routes connecting the adhesive passage and the spigot were not clearly observed in our X-ray CT images, probably due to the small structural scale relative to the space resolution used in our analysis (i.e. 0.31 μm). We speculate that the adhesive merges into the spigot via a fine, porous sponge-like structure, and we indicate assumed routes in Fig. 4l,m. X-ray CT observations also revealed a sophisticated structural design involving gradual twists in the silk brins by 90° from ‘∞’ to ‘8’ (Fig. 4n and Supplementary Movie S4). Essentially identical spinneret structures were observed by X-ray CT images for all of eight observed individuals from the third to final instars of E. variegata. More

NEWS
17 August 2021

Brazilian road proposal threatens famed biodiversity hotspot

Scientists and environmentalists say the road, slated to pass through Iguaçu National Park, could harm research projects and precious ecosystems.

Meghie Rodrigues

Meghie Rodrigues

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Protesters oppose the Caminho do Colono at Iguaçu Falls.Credit: Marcos Labanca

Brazil’s National Congress could soon vote on a bill proposing to construct a road through the country’s Iguaçu National Park. If the proposal moves ahead, researchers fear that it will threaten the park’s lush forest, a biodiversity hotspot that is home to almost 1,600 animal species, including endangered animals such as the purple-winged ground dove.Environmentalists and researchers have fought off construction of the 17.5-kilometre road for years, arguing that it will not only bring pollution to the park, but also poachers, who would threaten animals such as jaguars and tapirs. Even research in the park could be affected. In a portion of the park that dips into Argentina, for example, “poachers often steal our cameras”, says Julia Pardo, a mammal conservation and ecology researcher at the Subtropical Biology Institute in Misiones, Argentina.
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Under the leadership of President Jair Bolsonaro, Brazil’s government has weakened protection of the country’s forests in favour of industries such as mining, logging and ranching. The lower house of Brazil’s Congress, the Chamber of Deputies, put the bill on a fast track in June, allowing it to skip regular debate among its committees and head straight for a vote — a move that has researchers worried.If passed, the legislation would establish a dangerous precedent that could weaken environmental law in Brazil, says Sylvia Torrecilha, a biologist at the Secretariat of Environment, Economic Development, Production and Family Agriculture in Mato Grosso do Sul. In addition to cutting Iguaçu Park in two with a road that will connect towns to its north and south (see ‘Contested route’), the bill seeks to create a new type of protected area — the estrada-parque, or park road — within Brazil’s System of Natural Conservation Units, which regulates environmentally protected areas. Approving the construction of the ‘Caminho do Colono’ (the Settler’s Road) in Iguaçu could literally pave the way for creating through-ways in other parks and conservation areas in Brazil, says Torrecilha.Normally, the idea of a park road is to preserve the green areas along an already-existing scenic route, she says, not to bring commercial or economic advancement to a state — the argument lawmakers have made in favour of the road. The proposal, from its very beginning, is “inappropriate”, she adds.A historical routeEstablished in 1939, Iguaçu National Park is famous for the waterfall — one of the world’s largest — on the border with Argentina along its southwestern tip. But it is also notable because it contains the largest remaining patch of Atlantic Forest in southern Brazil. Although less well-known than the Amazon rainforest, the Atlantic Forest is rich in plant and animal species, and originally stretched along the coast of southeastern Brazil and down to Argentina and Paraguay. However, the forest is rapidly disappearing: it has lost almost 90% of its tree cover, accelerated by deforestation from urbanization, and agricultural and industrial activities in the twentieth century. Because of these attributes, the park was designated as a World Heritage site by the United Nations cultural organization UNESCO in 1986.

If the legislation is successful, it would actually enable the creation of the Caminho do Colono for the second time. The government of Paraná, the state where Iguaçu National Park is located, transformed an existing walking path into an unpaved version of the road during the 1950s. “Nobody cared much at the time because there wasn’t much difference between the inside and the outside of the park, as the Atlantic Forest stretched all over the place,” says former park chief Ivan Baptiston. “With all the deforestation of the last decades, nowadays, the scenario is a lot different.”In 1986 — the same year the park received its UNESCO World Heritage Site designation — Brazil’s Federal Prosecutor’s Office filed a civil suit to close the road, and the following year, a federal judge officially closed it. Since then, vegetation has overtaken the route, and some local residents have tried and failed to force it back open, claiming economic hardships associated with not being able to travel efficiently through the area.
‘We are being ignored’: Brazil’s researchers blame anti-science government for devastating COVID surge
The new bill states that re-establishing the road would offer a “solution to a logistical problem in Paraná state”. Sponsored by Nelsi Coguetto Maria, a member of the Chamber of Deputies, the proposal also says it “answers a decades-old outcry of Paraná inhabitants, salvaging the region’s history and its socioeconomic, environmental and tourism relations.”Environmentalists have criticized Coguetto Maria for backing the bill. And local media outlets have reported that his family stands to potentially gain from the Caminho do Colono; two of his sons are partners in construction companies that could pave the road. Coguetto Maria’s office did not respond to Nature’s queries about this, or about researchers’ concerns over the road. When the Chamber of Deputies approved fast-tracking of the bill, he argued that the Brazil of today is “responsible”, and has the “competence and capacity to build an ecologically correct road”, pointing out that the road existed as a walking path before the park was even created.Research interruptedFor many conservationists and researchers, the economic argument to open the road doesn’t hold water. The damage caused to the park’s highly valued Atlantic Forest would far outweigh the potential economic gains for the surrounding towns1, they say. Furthermore, the species protected by the park are irreplaceable, they add. Iguaçu is the only location in the world where the jaguar population is increasing instead of declining. If the road opens, says Pardo, pressure on the animals will skyrocket. “Easy access is the main enabler for poachers,” she says.

Iguaçu Falls is located along the border of Argentina and Brazil, on the Iguaçu River.Credit: Thiago Trevisan/Alamy

Cars using the road will also cause air, soil, water and even sound pollution, says Victor Prasniewski, a conservation biologist at the Federal University of Mato Grosso in Brazil. Sound pollution, in particular, changes communication patterns among a number of species. “Birds that attract females by singing will be forced to sing louder or longer to get noticed,” says Prasniewski, who published a paper last year2 listing the potential negative impacts of the Caminho do Colono.“These changes can affect the reproduction and even the evolution of some birds,” says Carlos Araújo, a bioacoustics ecologist at Argentina’s Subtropical Biology Institute. “The building of a road would be catastrophic to research in my field,” he says.He works on a large-scale monitoring project looking for the purple-winged ground-dove, the last confirmed sighting of which was more than three decades ago. “It’s a rare animal, and we leave recorders spread over the forest to try and catch her singing. We often capture helicopter noise, which disturbs our work.” Cars and trucks on the road would create similar low-frequency noise, he says. “It will be a lot harder to find birds like this dove.”
Brazil’s lawmakers renew push to weaken environmental rules
For some, the argument that the road will enhance tourism in Paraná doesn’t make sense either. Reopening the road, says Carmel Croukamp Davies, chief executive of Parque das Aves, a private bird sanctuary and shelter near the park, could threaten Iguaçu’s UNESCO World Heritage title if it damages the park’s biodiversity and severs the Atlantic Forest. Visitors come because they want to experience nature, she adds: “Whoever doesn’t understand the impact of a proposal like this doesn’t understand an inch of tourism nor biodiversity.”With Brazil’s Congress having returned from holiday earlier this month, the bill could soon be put to a vote. And when it is, environmentalists worry it will be passed, given how many representatives within the Chamber of Deputies currently align with Bolsonaro. Then it would face the Senate, and finally, Bolsonaro, who is expected to ultimately approve it.

doi: https://doi.org/10.1038/d41586-021-02199-x

References1.Ortiz, R. A. Ambientalia 1, 141–160 (2009).
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2.Prasniewski, V. M. et al. Ambio 49, 2061–2067 (2020).
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