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    The characteristics and impact of small and medium forest enterprises on sustainable forest management in Ghana

    The contributions of SMFEs to the local economy and developmentSMFEs are characterized by limited resources, hence their inability to employ more people however, the few being employed to aid in the operations of the businesses contribute to the reduction of the employment gap among the youth in the study areas. The employment opportunities provided by SMFEs supplement the central government’s efforts to offer employment to the people. Subsequently, the people in the area depend on it for their livelihood to improve their living standards. The study found a diverse number of SMFEs in terms of wood and non-wood-related activities (Fig. 3) that people engage in as primary or secondary jobs. Some evidence has proved that SMFE’s contribution to forest employment is above 50% in some countries like Brazil, Uganda, Guyana, and China, and almost 80 to 90% of all forest-based enterprises in most countries7. This may directly impact efforts to reduce poverty by improving the living standards of people who form and operate SMFEs as a livelihood.Zada et al.10 also reported that households who own SMFEs had a wealth index increase from 5.4 to 7.4 whereas those without SMFEs had an index of 4.9. SMFEs do have the potential to improve household income levels which can lead to reinvesting and expansion. This study found that the monthly expenses of SMFEs contribute to 46.2% of their monthly sales. Therefore, if SMFEs can increase significantly, their ability to reinvest while observing the best practices in operating their businesses then they will be able to maximize their turnovers. This can result in expansion and more employment opportunities for others hence, reducing the burden on the government to provide employment.There is a direct positive and significant relationship between SMFEs and local economic development11. SMFEs were reported to positively and significantly mediate the relationships between government support, entrepreneurship knowledge, and local economic development. SMFEs with informal or formal training can ensure government support is efficiently used in tapping into entrepreneurial knowledge to drive their impacts on local economies. This will also allow them to grow into sustainable businesses while also promoting the sustainability of forest resources which they depend on for raw materials.Operational characteristics and impacts of SMFEs on sustainabilityAround the globe and per the laws of Ghana, businesses are required to fulfill certain obligations to enable them to run smoothly12. Failure to undertake these tasks may attract severe penalties, including criminal charges that may carry significant jail terms. An example is failure to pay taxes and adhere to certain regulations. This section looks at certain characteristics of SMFEs in this study that project their impact on sustainable forest management.Firstly, the laws of Ghana make it mandatory for all business categories to pay tax and as such, SMFEs are not left out. However, the major challenge with taxes in Ghana and by extension, the world, is compliance. Mantey13 reported that 59.1% of small business owners did not understand the Ghanaian Tax System. The key lesson drawn from this observation is that, as SMFEs, one of their characteristics is that they generate a smaller income compared to larger companies or corporate bodies. This goes a long way in determining the amount they pay as taxes. In addition, by their nature, they can under-declare the revenue they make to influence the amount they will be taxed. This calls for the development and flawless implementation of mechanisms to monitor and audit these SMFEs to ensure that they comply with tax directives and regulations.Mantey13 further reported that 57.4% of the surveyed business owners are not aware of most tax laws and guidelines on the taxation of incomes for organizations. Some blamed their inability to pay taxes on the business being slow and others were unwilling to give a response to why they were unable to pay their taxes. In this study, majority (77.5%) indicated that they pay taxes. It was also established in this study that payment of taxes has a significantly weak correlation with the educational background of the respondents. Though the majority of the SMFEs paid taxes, it may not be directly linked to all respondents having some form of formal education and vice versa. However, this may be factored in when considering the training and mentoring of SMFEs to contribute to local development by paying their taxes. More SMFEs may endeavor to pay their taxes regularly if they understand what these taxes can do to improve their work environment.Governments in recent times have stepped up revenue mobilization efforts to capture more businesses into the tax bracket of the country. This has seen the revenue authorities recruit and train more revenue officers to reach businesses like SMFEs which are mostly not reachable due to their inability to register their businesses.Secondly, the majority (71.25%) of SMFEs in this study was not registered. This adds to the general belief that most businesses operate without the required licenses or have failed to renew their expired licenses. Some studies also made similar observations and arrived at the lack of enforcement of laws, as a key reason why many businesses in developing countries remained unregistered contrary to the requirements of the law14,15. Further analysis showed SMFEs who belong to associations are likely to register their businesses because it is a requirement to join them. The benefits of belonging to an association include access to loan facilities and other credit programs and therefore some SMFEs do not want to risk missing out through failure to get their business registered16.SMFEs need to get registered for them to be considered legitimate business entities however, this seems to be a challenge in most developing countries. Tomaselli et al.17 found this assertion relevant when investigating SMFEs access to microfinance. Registration of business is a key requirement to access loan facilities and so is belonging to a recognized association. Associations are known to serve as guarantors for members who want loan facilities from banks and other financial institutions to expand their businesses16. Unregistered, unregulated, and unmonitored SMFEs are those whose activities tend to compromise the sustainability of forest resources18. Therefore, registration of SMFEs does that only serve the interest of governments but also the interests of these SMFEs themselves.The third has to do with the sourcing of raw materials. Ghana being a tropical country is blessed abundantly with forest resources but over the decades, the overexploitation of these forests has brought to the brink of extinction, various species of both plant and animal life19. The dependence of SMFEs on the forests cannot be underestimated as literature, citing Osei Tutu et al.20, posits that SMFEs contribute to 95% of the income of some rural households. This study shows that 68.8% of SMFEs get their raw materials directly from the forest. Both woody and non-woody materials are in abundance and can be extracted with minimal cost.In sourcing raw materials from the forests in Ghana, SMFEs are required to obtain permits or licenses from the relevant authorities such as the forestry commission. This permit/license is what allows or gives this SMFEs access to otherwise inaccessible forest reserves to harvest raw materials20. Additionally, these documents can go as far as determining the type and quantity of materials to harvest. It can also determine the type of access granted as these accesses can vary or differ depending on the time or season of harvest18. The issuance of permits and licenses is meant to monitor and regulate resource harvesting with the primary goal of checking the overexploitation of these resources. However, this is not possible due to the high levels of non-compliance by SMFEs21. Evident in this study is the 78.2% of SMFEs who gather raw materials from the forest without permits/licenses.Osei Tutu et al.18 concluded that the neglect of the SMFEs sub-sector is responsible for the loss of state revenue because of their unwillingness to register and pay appropriate taxes and permit fees for their illegal and unsustainable business operations. The report further posits that “despite the numerous support channels (national and international) available to them, the roles played by SMFEs in poverty reduction are significantly unimpactful hence the need to intensify capitalizing on all opportunities to address challenges they present.” The government institutions in charge of these forest resources depend on these permits and license fees to supplement their already insufficient government subventions for the operations. Therefore, losing revenues may undermine their sustainability programs.Driving factors of SMFEsThe ability of a business to thrive highly depends on its ability to overcome certain challenges within its operating environment22. That alone, however, is not enough as certain factors ignite the ambition of a business. These factors decisively influence the success or the failure of the business hence, they are identified as determinants. The study sought to identify some determinants that drive the activities of SMFEs. Responses from the SMFEs concluded that economic and social factors such as resource availability, profits/revenue, employment, and labor are the key determinants that drive the SMFEs.Resource availability was the major driver of their activities cited by 91.3% of SMFEs. This is because, the numerous forests the nation is endowed with provide abundantly, the raw materials needed for them to use. Due to the favorable climatic conditions prevailing in the high forest zones, there is a constant supply of materials needed by SMFEs to produce their products for business23. In addition, availability means less competition for limited resources and therefore it boils down to the ability to process these raw materials into finished goods for market consumption hence, reducing the costs of production24.SMFEs also pointed to profits/revenue, as the factor driving their activities to engage in, and sustain their business. The abundance and readily availability of raw materials are very important to the growth of their business and in turn, help them maximize their returns. This is because the inputs they make to acquire the raw materials are relatively low in comparison to the total revenues they generate. This observation is also reflected in the captured expenditures they make as inputs or investments into their businesses.SMFEs that need technologically advanced mechanisms and equipment are those that are required or inclined to make heavy investments whereas those that need simple tools and equipment invest less. Whichever the case, the nature of SMFEs suggests that a business that requires raw materials with very minimal or no costs involved at all, yet yields very high profits, is how people can improve their living25. Badini et al.26 classified enabling environment of SMFEs into external and internal factors where financial capital, business management, and organizational capacities form internal factors. On the other hand, external factors include regulatory frameworks, forest law enforcement, and natural capital which refers to the stock of natural resources or environmental assets. The success of any SMFE is largely dependent on these factors.Finally, 8.75% of the SMFEs view labor and employment, as the determinants driving their existence. For them, compared to other labor-intensive ventures, their business does not require huge labor to get work done. The few hands needed means most of the revenues do not go to paying workers. They can dictate and bargain to their advantage because there are many people without jobs hence a job turned down, because of less encouraging benefits is gladly accepted by another25. Ultimately, the study finds that labor is cheap in some areas of the SMFEs’ environs primarily, due to unemployment.Sustainability challenges in forest management relative to SMFEs activitiesSince the United Nations Conference on Environment and Development (UNCED) in Rio de Janeiro, Brazil in 1992, key challenges of SFM have broadly covered the sustainability of forest resources through the reduction of deforestation and forest degradation, conservation and protection of biological diversity, genetic resources sustainability and improving forest goods and services valuation27. It is important to note that SMFEs have played an overlooked role in these challenges as it seems its contributions to poverty reduction have taken center stage in international discourses, with its negative impacts on the environment being relegated to the backseat when considering the causes of environmental degradation. Attempts to effectively manage the activities of SMFEs have witnessed the emergence of a lot of challenges that threaten the very sustainability the globe yearns for. Some reasons point to the source of the challenges that have plagued these efforts, some of which are highlighted below.First is the lack of resources to recruit and train the needed personnel to constantly monitor the activities of these SMFEs during the harvesting of raw materials. This makes it easier for them to enter restricted forest areas without the necessary documentation and proceed to harvest more than they are required to at any given time. Secondly, it is difficult to track their activities because many SMFEs currently, do not register their businesses as required by law.A typical example is the use of unapproved trails or routes and the use of inappropriate harvesting techniques such as burning. This leads to the destruction of various lifeforms that are critical to the regenerative capabilities of the forests28. The study also found that the supervision of the activities of SMFEs is very poor as only 12% of SMFEs had their activities supervised on certain occasions. This buttresses the assertion by Acheampong et al.29 who posited that the lack of supervision is a major issue that needs to be vigorously addressed if we need to achieve forest sustainability in developing countries.There is a need to educate SMFEs on the laws and regulations governing the use of forest resources. It was revealed that only 16% of the respondents have some knowledge of the regulations governing the harvest and use of both woody and non-woody forest resources. This knowledge gap is being exploited by SMFEs as an excuse for not doing what is expected of them. However, a study found that 69% of respondents claimed to have good knowledge of the regulations governing their activities14. This can be attributed to self-learning or the action of the supervising authorities who for one reason or another other can perform their mandate of educating the SMFEs. There is a need to properly equip the supervising agencies to carry out this mandate.The research, therefore, cites the non-registering of SMFEs as an underlying cause of the flouting of these regulations and laws. The research also suggests that some form of training can be done at the point of registering even before the certification is done. As observed in the area of training, there is not enough emphasis on the need to train SMFEs in sustainability issues in terms of harvesting raw materials. It was noted that the majority (67%) of SMFEs (Table 8) have no training on how to harvest, process, and adequately market their products to ensure maximum profits while sustaining the resources for future harvests. There is a need to institute training and capacity-building programs for SMFEs that will empower them to succeed and yet aim to ensure sustainable forest management.The role of sustainable forest management in climate change mitigationSustainable forest management (SFM) can play a significant role in climate change mitigation, as forests are an important sink for carbon dioxide and other greenhouse gases. By sequestering carbon in their biomass and soils, forests can help to remove carbon dioxide from the atmosphere, which can help to mitigate the impacts of climate change30.There are a number of ways in which SFM can support climate change mitigation, including through the conservation and expansion of forests, the sustainable management of forests, and the use of forest-based products and practices that reduce greenhouse gas emissions. Policymakers and stakeholders at local, national, and international levels are increasingly recognizing the role of forests in climate change mitigation, and there is growing interest in developing strategies and policies that support the use of forests for this purpose.However, there are challenges that impede the efficient leveraging of SFM for climate change mitigation and one of such challenges is the need to balance economic, social, and environmental considerations31. Forests provide a range of goods and services that are vital for human well-being and economic development, including timber, non-timber forest products, and ecosystem services such as carbon sequestration, water regulation, and habitat for wildlife32. However, these resources can be in high demand, and managing forests sustainably can be difficult, particularly in developing countries where there may be limited access to financial and technical resources33.Another challenge is the impact of external factors such as climate change on the health and productivity of forests34. Rising temperatures and changing weather patterns can affect the growth and survival of forests, and may also increase the risk of forest fires and pests35. Policymakers must consider the role of forests in mitigating and adapting to climate change, as well as the potential impacts on forest-dependent communities32.One way in which SMFEs can contribute to climate change mitigation is through the sustainable management of forests. By practicing sustainable forestry, SMFEs can help to maintain and enhance the carbon sequestration capacity of forests, which can help to remove carbon dioxide from the atmosphere and mitigate the impacts of climate change31. This can involve practices such as planting and reforestation, soil and water conservation, and the use of sustainable harvesting techniques32. However, this study revealed the majority of these SMFEs are unregistered and therefore not monitored. Meaning their activities cannot be regulated to ensure practices that promote climate change mitigation.SMFEs can also contribute to climate change mitigation by using forest-based products and practices that reduce greenhouse gas emissions. For example, the use of wood products as a substitute for fossil fuel-based products can help to reduce emissions, as wood products sequester carbon over their lifetime and do not release it into the atmosphere when they are used34. In addition, the use of biomass energy in place of fossil fuels can help to reduce emissions, provided that the biomass is sourced sustainably and the emissions associated with its transportation and use are accounted for35.Another way in which SMFEs can contribute to climate change mitigation is through the development of innovative solutions and technologies that support sustainable forestry practices and reduce greenhouse gas emissions. This could include the use of precision forestry techniques, which use advanced technology to improve the efficiency and sustainability of forestry operations34. It could also involve the development and commercialization of new forest-based products or practices that have a lower carbon footprint32.Policies can have a significant impact on the way in which forests are managed for climate change mitigation31. For example, policies that promote sustainable forestry practices, such as the use of certification schemes or incentive programs, can help to ensure that forests are managed in a way that meets the needs of current and future generations33. On the other hand, policies that do not adequately consider the needs and interests of all stakeholders, or that do not provide sufficient support for sustainable forestry practices, may have negative impacts on the ability of forests to contribute to climate change mitigation34.Overall, addressing the inter-challenges of SFM for climate change mitigation and the impact of policies is an important part of ensuring the sustainability and long-term viability of forests as a tool for mitigating climate change.Development of SMFEs within the forest-based economy of Ghana through policyDespite the global consensus on the sustainability of forest resources and their utmost importance regarding the sustenance of present and future generations, the situation remains unclear at the field level36. The application of criteria and indicators of sustainability provides support for a small but crucial clarification on achieving sustainable forest management (SFM). A meaningful basis for assessing SFM at operational levels will require clarification together with management prescriptions and performance standards while providing linkage to voluntary timber certification.Currently, many environment-based non-governmental organizations (ENGOs) like Global Footprint Network and Fauna & Flora International who are concerned about natural resource exploitation, are convinced by the international debate on criteria and indicators that timber harvesting and ecosystem services of the forests can be sustained37. Stakeholders of the forestry franchise agree that environmental conservation can be accommodated through a necessary and reasonable modification and adaptation of forest-harvesting practices. Therefore, multi-resource forest management as a new paradigm replaces the indigenous sustained-yield management approach that bases on growth-harvest equilibrium using policy as a vehicle38.Food and Agriculture Organization (FAO) is assisting countries through policy advice, technical assistance, capacity building, workshop, and hands-on training, to overcome the challenges of sustainable forest management39. The assistance is provided through the assessment of forest resources and the elements of SFM, as well as the monitoring of progress toward it. FAO also identifies, tests, and modern scientific SMF approaches and techniques to address climate change mitigation and adaptation challenges such as increasing demand for wood and non-wood forest products and services, pest, and diseases.The views held by the Forestry Commission and National Board for Small Scale Industries (NBSSI) during interviews are in line with the suggestions and actions by the World Bank and FOA that involve training and other support systems for managers of forest resources in tropical countries like Ghana that depends heavily on its natural forests. Despite the availability of some of the avenues needed to execute these strategies, the non-compliance by SMFEs makes it difficult for these targets to be met. The general thought is that, if all relevant authorities and stakeholders perform their roles effectively, the current challenges of maximizing the contributions of SMFEs to development and sustainable forest management can be realized.The impact of forest policies is evident in countries like Gabon, a country rich in forest resources, which regards forests as a critical economic resource. World Bank-supported reforms have helped make concessions awarding procedures more competitive and transparent40. Forest taxation recovery has been bolstered, with tax collection rates increasing from 40 to 80% between 2005 and 2010. Sustainable forest management is presently practiced in around 85% of productive forest areas and as a result of these reforms, the forestry sector’s contribution to Gabon’s GDP increased from 2.5% in 2004 to 4.7% in 200940.Support for small and medium forest-based firms raised actual cash income among forest user groups by 53% in India’s Andhra Pradesh throughout the project duration. Seasonal outmigration decreased by 23%, and the quality of thick forest cover in these places improved40,41.Ghana has made significant progress toward sustainable management of its forest resources via the adoption of different forest regulations like the Forest and Wildlife Policy of 1994, Timber Resources Management Act, of 2002, etc. The problem with most of the country’s forest resource policies is the lack of attention paid to the human component; the emphasis is on sustainable timber extraction, even if it is destructive to the livelihoods of forest-dependent populations. Forest policies have historically been determined by successive administrations’ economic interests, which essentially focused on the exploitation of wood resources for income production. This has been a significant impediment to the creation and development of non-timber forest products which the majority of SMFEs depend on in Ghana. This has allowed the number SMFEs rapidly increase due to the lack of coverage by forest policies42. The policy interventions in Gabon and India have yielded results that can provide the foundation needed for Ghana to formulate its policies for the development of SMFEs in a way that does not threaten sustainable forest management. More

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    Allelochemical run-off from the invasive terrestrial plant Impatiens glandulifera decreases defensibility in Daphnia

    Holt, R. D. Predation, apparent competition, and the structure of prey communities. Theor. Popul. Biol. 12, 197–229 (1977).Article 
    CAS 

    Google Scholar 
    Dugatkin, L. A. & Godin, J. G. J. Prey approaching predators: A cost-benefit perspective. Ann. Zool. Fennici 29, 233–252 (1992).
    Google Scholar 
    Portalier, S. M. J., Fussmann, G. F., Loreau, M. & Cherif, M. The mechanics of predator–prey interactions: First principles of physics predict predator–prey size ratios. Funct. Ecol. 33, 323–334 (2019).Article 

    Google Scholar 
    Achrai, B., Bar-On, B. & Wagner, H. D. Biological armors under impact—effect of keratin coating, and synthetic bio-inspired analogues. Bioinsp. Biomim. 10, 016009 (2015).Article 
    CAS 

    Google Scholar 
    Stankowich, T. & Campbell, L. A. Living in the danger zone: Exposure to predators and the evolution of spines and body armor in mammals. Evolution 70, 1501–1511 (2016).Article 

    Google Scholar 
    Tollrian, R. & Harvell, C. D. The ecology and evolution of inducible defenses. Q. Rev. Biol. 65, 323–340 (1990).Article 

    Google Scholar 
    Nordlund, D. A. & Lewis, W. J. Terminology of chemical releasing stimuli in intraspecific and interspecific interactions. J. Chem. Ecol. 2, 211–220 (1976).Article 

    Google Scholar 
    Poulin, R. X. et al. Chemical encoding of risk perception and predator detection among estuarine invertebrates. Proc. Natl. Acad. Sci. USA 115, 662–667 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Tollrian, R. & Dodson, S. I. Inducible defenses in Cladocera: Constraints, costs, and multipredator environments. Ecol. Evol. Inducible Defenses 177, 177–202 (1999).Article 

    Google Scholar 
    Von Elert, E. & Loose, C. J. Predator-induced diel vertical migration in Daphnia: Enrichment and preliminary chemical characterization of a kairomone exuded by fish. J. Chem. Ecol. 22, 885–895 (1996).Article 

    Google Scholar 
    Barry, M. J. Effects of endosulfan on Chaoborus-induced life-history shifts and morphological defenses in Daphnia pulex. J. Plankton Res. 22, 1705–1718 (2000).Article 
    ADS 
    CAS 

    Google Scholar 
    Riessen, H. P. & Gilbert, J. J. Divergent developmental patterns of induced morphological defenses in rotifers and Daphnia: Ecological and evolutionary context. Limnol. Oceanogr. 64, 541–557 (2019).Article 
    ADS 

    Google Scholar 
    Sperfeld, E., Nilssen, J. P., Rinehart, S., Schwenk, K. & Hessen, D. O. Ecology of predator-induced morphological defense traits in Daphnia longispina (Cladocera, Arthropoda). Oecologia 192, 687–698 (2020).Article 
    ADS 

    Google Scholar 
    Tollrian, R. Neckteeth formation in Daphnia pulex as an example of continuous phenotypic plasticity: Morphological effects of Chaoborus kairomone concentration and their quantification. J. Plankton Res. 15, 1309–1318 (1993).Article 

    Google Scholar 
    Laforsch, C. & Tollrian, R. Inducible defenses in multipredator environments: Cyclomorphosis in Daphnia cucullata. Ecology 85, 2302–2311 (2004).Article 

    Google Scholar 
    Petrusek, A., Tollrian, R., Schwenk, K., Haas, A. & Laforsch, C. A ‘crown of thorns’ is an inducible defense that protects Daphnia against an ancient predator. Proc. Natl. Acad. Sci. USA 106, 2248–2252 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Engel, K. & Tollrian, R. Inducible defences as key adaptations for the successful invasion of Daphnia lumholtzi in North America?. Proc. R. Soc. B Biol. Sci. 276, 1865–1873 (2009).Article 

    Google Scholar 
    Barry, M. J. & Bayly, I. A. E. Further studies on predator induction of crests in australian Daphnia and the effects of crests on predation. Mar. Freshw. Res. 36, 519–535 (1985).
    Google Scholar 
    Rabus, M. & Laforsch, C. Growing large and bulky in the presence of the enemy: Daphnia magna gradually switches the mode of inducible morphological defences. Funct. Ecol. 25, 1137–1143 (2011).Article 

    Google Scholar 
    Herzog, Q. & Laforsch, C. Modality matters for the expression of inducible defenses: Introducing a concept of predator modality. BMC Biol. 11, 113 (2013).Article 

    Google Scholar 
    Riessen, H. P. et al. Changes in water chemistry can disable plankton prey defenses. Proc. Natl. Acad. Sci. USA 109, 15377–15382 (2012).Article 
    ADS 
    CAS 

    Google Scholar 
    Tollrian, R., Duggen, S., Weiss, L. C., Laforsch, C. & Kopp, M. Density-dependent adjustment of inducible defenses. Sci. Rep. 5, 12736 (2015).Article 
    ADS 
    CAS 

    Google Scholar 
    Weiss, L. C. et al. Rising pCO2 in freshwater ecosystems has the potential to negatively affect predator-induced defenses in Daphnia. Curr. Biol. 28, 327-332.e3 (2018).Article 
    CAS 

    Google Scholar 
    Hanazato, T. Pesticide effects on freshwater zooplankton: An ecological perspective. Environ. Pollut. 112, 1–10 (2001).Article 
    CAS 

    Google Scholar 
    Coors, A. & DeMeester, L. Erratum: Synergistic, antagonistic and additive effects of multiple stressors: Predation threat, parasitism and pesticide exposure in Daphnia magna. J. Appl. Ecol. 46, 1138 (2009).
    Google Scholar 
    Schriever, C. A., von der Ohe, P. C. & Liess, M. Estimating pesticide runoff in small streams. Chemosphere 68, 2161–2171 (2007).Article 
    ADS 
    CAS 

    Google Scholar 
    Lobstein, A. et al. Quantitative determination of naphthoquinones of Impatiens species. Phytochem. Anal. 12, 202–205 (2001).Article 
    CAS 

    Google Scholar 
    Kisielius, V. et al. The invasive butterbur contaminates stream and seepage water in groundwater wells with toxic pyrrolizidine alkaloids. Sci. Rep. 10, 19784 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Yoneyama, K. & Natsume, M. 4.13 Allelochemicals for Plant—Plant and Plant—Microbe Interactions. Interactions (Elsevier Inc., 2010).Griffiths, M. R., Strobel, B. W., Hama, J. R. & Cedergreen, N. Toxicity and risk of plant-produced alkaloids to Daphnia magna. Environ. Sci. Eur. 33, 10 (2021).Article 
    CAS 

    Google Scholar 
    Callaway, R. M. & Ridenour, W. M. Novel weapons: Invasive success and the evolution of increased competitive ability. Front. Ecol. Environ. 2, 436–443 (2004).Article 

    Google Scholar 
    Beerling, D. J. & Perrins, J. M. Impatiens glandulifera Royle (Impatiens Roylei Walp.). J. Ecol. 81, 367–382 (1993).Article 

    Google Scholar 
    Roy, B., Popay, A.I., Champion, P.D., James, T.K. & Rahman, A. An Illustrated Guide to Common Weeds of New Zealand. 2nd Edn. (New Zealand Plant Protection Society, 2004). Ruckli, R., Hesse, K., Glauser, G., Rusterholz, H. P. & Baur, B. Inhibitory potential of naphthoquinones leached from leaves and exuded from roots of the invasive plant Impatiens glandulifera. J. Chem. Ecol. 40, 371–378 (2014).Article 
    CAS 

    Google Scholar 
    Gruntman, M., Pehl, A. K., Joshi, S. & Tielbörger, K. Competitive dominance of the invasive plant Impatiens glandulifera: Using competitive effect and response with a vigorous neighbour. Biol. Invasions 16, 141–151 (2014).Article 

    Google Scholar 
    Bieberich, J. et al. Species- and developmental stage-specific effects of allelopathy and competition of invasive Impatiens glandulifera on cooccurring plants. PLoS ONE 13, e0205843 (2018).Article 

    Google Scholar 
    Wright, D. A., Dawson, R., Cutler, S. J., Cutler, H. G. & Orano-Dawson, C. E. Screening of natural product biocides for control of non-indigenous species. Environ. Technol. 28, 309–319 (2007).Article 
    CAS 

    Google Scholar 
    Kayashima, T., Mori, M., Yoshida, H., Mizushina, Y. & Matsubara, K. 1,4-naphthoquinone is a potent inhibitor of human cancer cell growth and angiogenesis. Cancer Lett. 278, 34–40 (2009).Article 
    CAS 

    Google Scholar 
    Jentzsch, J. et al. New antiparasitic bis-naphthoquinone derivatives. Chem. Biodivers. 17, e1900597 (2020).Article 
    CAS 

    Google Scholar 
    Mitchell, M. J., Brescia, A. I., Smith, S. L. & Morgan, E. D. Effects of the compounds 2-methoxynaphthoquinone, 2-propoxynaphthoquinone, and 2-isopropoxynaphthoquinone on ecdysone 20-monooxygenase activity. Arch. Insect Biochem. Physiol. 66, 45–52 (2007).Article 
    CAS 

    Google Scholar 
    Westfall, B. A., Russell, R. L. & Auyong, T. K. Depressant agent from walnut hulls. Science 134, 1617 (1961).Article 
    ADS 
    CAS 

    Google Scholar 
    Diller, J. G. P. et al. The Beauty is a beast: Does leachate from the invasive terrestrial plant Impatiens glandulifera affect aquatic food webs?. Ecol. Evol. 12, e8781 (2022).Article 

    Google Scholar 
    Elendt, B. P. Selenium deficiency in Crustacea—an ultrastructural approach to antennal damage in Daphnia magna Straus. Protoplasma 154, 25–33 (1990).Article 
    CAS 

    Google Scholar 
    Ebert, D. The trade-off between offspring size and number in Daphnia magna: The influence of genetic, environmental and maternal effects. Arch. Fur Hydrobiol. 90, 453–473 (1993).
    Google Scholar 
    Trotter, B., Ramsperger, A. F. R. M., Raab, P., Haberstroh, J. & Laforsch, C. Plastic waste interferes with chemical communication in aquatic ecosystems. Sci. Rep. 9, 5889 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Laforsch, C., Beccara, L. & Tollrian, R. Inducible defenses: The relevance of chemical alarm cues in Daphnia. Limnol. Oceanogr. 51, 1466–1472 (2006).Article 
    ADS 

    Google Scholar 
    Miner, B. E., de Meester, L., Pfrender, M. E., Lampert, W. & Hairston, N. G. Linking genes to communities and ecosystems: Daphnia as an ecogenomic model. Proc. R. Soc. B Biol. Sci. 279, 1873–1882 (2012).Article 

    Google Scholar 
    Altshuler, I. et al. An integrated multi-disciplinary approach for studying multiple stressors in freshwater ecosystems: Daphnia as a model organism. Integr. Comp. Biol. 51, 623–633 (2011).Article 
    CAS 

    Google Scholar 
    Diel, P., Kiene, M., Martin-Creuzburg, D. & Laforsch, C. Knowing the enemy: Inducible defences in freshwater zooplankton. Diversity 12, 147 (2020).Article 
    CAS 

    Google Scholar 
    Pestana, J. L. T., Loureiro, S., Baird, D. J. & Soares, A. M. V. M. Pesticide exposure and inducible antipredator responses in the zooplankton grazer, Daphnia magna Straus. Chemosphere 78, 241–248 (2010).Article 
    ADS 
    CAS 

    Google Scholar 
    Grant, J. W. G. & Bayly, I. A. E. Predator induction of crests in morphs of the Daphnia carinata King complex. Limnol. Oceanogr. 26, 201–218 (1981).Article 
    ADS 

    Google Scholar 
    Dodson, S. I. Zooplankton competition and predation: An experimental test of the size-efficiency hypothesis. Ecology 55, 605–613 (1974).Article 

    Google Scholar 
    Klotz, L. O., Hou, X. & Jacob, C. 1,4-naphthoquinones: From oxidative damage to cellular and inter-cellular signaling. Molecules 19, 14902–14918 (2014).Article 

    Google Scholar 
    Subramoniam, T. Crustacean ecdysteriods in reproduction and embryogenesis. Comp. Biochem. C Physiol. Pharmacol. Toxicol. Endocrinol. 125, 135–156 (2000).Article 
    CAS 

    Google Scholar 
    De Coen, W. M. & Janssen, C. R. The missing biomarker link: Relationships between effects on the cellular energy allocation biomarker of toxicant-stressed Daphnia magna and corresponding population characteristics. Environ. Toxicol. Chem. 22, 1632–1641 (2003).Article 

    Google Scholar 
    Palma, P. et al. Effects of atrazine and endosulfan sulphate on the ecdysteroid system of Daphnia magna. Chemosphere 74, 676–681 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Mount, D. I. & Norberg, T. J. A seven-day life cycle Cladoceran toxicity test. Environ. Toxicol. Chem. 3, 425–434 (1984).Article 
    CAS 

    Google Scholar 
    Elnabarawy, M. T., Welter, A. N. & Robideau, R. R. Relative sensitivity of three daphnid species to selected organic and inorganic chemicals. Environ. Toxicol. Chem. 5, 393–398 (1986).Article 
    CAS 

    Google Scholar 
    Jaikumar, G., Baas, J., Brun, N. R., Vijver, M. G. & Bosker, T. Acute sensitivity of three Cladoceran species to different types of microplastics in combination with thermal stress. Environ. Pollut. 239, 733–740 (2018).Article 
    CAS 

    Google Scholar 
    Gama-Flores, J. L., Salas, M. E. H., Sarma, S. S. S. & Nandini, S. Demographic responses of Cladocerans (Cladocera) in relation to different concentrations of humic substances. J. Environ. Sci. Heal. Part A Toxic/Hazardous Subst. Environ. Eng. 54, 1311–1317 (2019).CAS 

    Google Scholar 
    Cohen, J. E., Pimm, S. L., Yodzis, P. & Saldana, J. Body sizes of animal predators and animal prey in food webs. J. Anim. Ecol. 62, 67–78 (1993).Article 

    Google Scholar 
    Hunt, R. J. & Swift, M. Predation by larval damselflies on Cladocerans. J. Freshw. Ecol. 25, 345–351 (2010).Article 

    Google Scholar 
    Riessen, H. P. & Trevett-Smith, J. B. Turning inducible defenses on and off: Adaptive responses of Daphnia to a gape-limited predator. Ecology 90, 3455–3469 (2009).Article 

    Google Scholar 
    Pijanowska, J. Cyclomorphosis in Daphnia: An adaptation to avoid invertebrate predation. Hydrobiologia 198, 41–50 (1990).Article 

    Google Scholar 
    Gu, L. et al. Coping with antagonistic predation risks: Predator-dependent unique responses are dominant in Ceriodaphnia cornuta. Mol. Ecol. 31, 3951–3962 (2022).Article 
    CAS 

    Google Scholar 
    Jeziorski, A. et al. The jellification of north temperate lakes. Proc. R. Soc. B Biol. Sci. 2014, 282 (2014).
    Google Scholar 
    Ponti, B., Piscia, R., Bettinetti, R. & Manca, M. Long-term adaptation of Daphnia to toxic environment in Lake Orta: The effects of short-term exposure to copper and acidification. J. Limnol. 69, 217–224 (2010).Article 

    Google Scholar 
    Wright, D. A., Mitchelmore, C. L., Dawson, R. & Cutler, H. G. The influence of water quality on the toxicity and degradation of juglone (5-hydroxy 1,4-naphthoquinone). Environ. Technol. 28, 1091–1101 (2007).Article 
    CAS 

    Google Scholar  More

  • in

    Energetic and behavioral consequences of migration: an empirical evaluation in the context of the full annual cycle

    Alerstam, T., Hedenström, A. & Åkesson, S. Long-distance migration: Evolution and determinants. Oikos 103, 247–260. https://doi.org/10.1034/j.1600-0706.2003.12559.x (2003).Article 

    Google Scholar 
    Somveille, M., Rodrigues, A. S. L. & Manica, A. Why do birds migrate? A macroecological perspective. Glob. Ecol. Biogeogr. 24, 664–674. https://doi.org/10.1111/geb.12298 (2015).Article 

    Google Scholar 
    Tatner, P. & Bryant, D. M. Flight cost of a small passerine measured using doubly labeled water: Implications for energetics studies. Auk 103, 169–180. https://doi.org/10.2307/4086976 (1986).Article 

    Google Scholar 
    Boisclair, D. & Leggett, W. C. The importance of activity in bioenergetics models applied to actively foraging fishes. Can. J. Fish. Aquat. Sci. 46, 1859–1867. https://doi.org/10.1139/f89-234 (1989).Article 

    Google Scholar 
    Karasov, W. H. Daily energy expenditure and the cost of activity in mammals. Am. Zool. 32, 238–248. https://doi.org/10.1093/icb/32.2.238 (1992).Article 

    Google Scholar 
    Castro, G., Myers, J. P. & Ricklefs, R. E. Ecology and energetics of sandlerlings migrating to four latitudes. Ecology 73, 833–844. https://doi.org/10.2307/1940161 (1992).Article 

    Google Scholar 
    Fayet, A. L. et al. Ocean-wide drivers of migration strategies and their influence on population breeding performance in a declining seabird. Curr. Biol. 27, 3871-3878.e3. https://doi.org/10.1016/j.cub.2017.11.009 (2017).Article 
    CAS 

    Google Scholar 
    Alves, J. A. et al. Costs, benefits, and fitness consequences of different migratory strategies. Ecology 94, 11–17. https://doi.org/10.1890/12-0737.1 (2013).Article 

    Google Scholar 
    Carneiro, C., Gunnarsson, T. G., Méndez, V., Soares, A. M. & Alves, J. A. Linking range wide energetic tradeoffs to breeding performance in a long-distance migrant. Ecography 44, 521–524. https://doi.org/10.1111/ecog.05152 (2021).Article 

    Google Scholar 
    Fort, J. et al. Energetic consequences of contrasting winter migratory strategies in a sympatric Arctic seabird duet. J. Avian Biol. 44, 255–262. https://doi.org/10.1111/j.1600-048X.2012.00128.x (2013).Article 

    Google Scholar 
    Garthe, S. et al. Energy budgets reveal equal benefits of varied migration strategies in northern gannets. Mar. Biol. 159, 1907–1915 (2012).Article 

    Google Scholar 
    Pelletier, D. et al. So far, so good… Similar fitness consequences and overall energetic costs for short and long-distance migrants in a seabird. PLoS One 15, e0230262. https://doi.org/10.1371/journal.pone.0230262 (2020).Article 
    CAS 

    Google Scholar 
    Tinbergen, J. M. & Verhulst, S. A fixed energetic ceiling to parental effort in the great tit?. J. Anim. Ecol. 69, 323–334 (2000).Article 

    Google Scholar 
    Drent, R. H. & Daan, S. The prudent parent: Energetic adjustments in avian breeding 1. Ardea 68, 225–252 (1980).
    Google Scholar 
    Weiner, J. Physiological limits to sustainable energy budgets in birds and mammals: Ecological implications. Trends Ecol. Evol. 7, 384–388 (1992).Article 
    CAS 

    Google Scholar 
    Hammond, K. A. & Diamond, J. Maximal sustained energy budgets in humans and animals. Nature 386, 457–462 (1997).Article 
    ADS 
    CAS 

    Google Scholar 
    Speakman, J. R. & Król, E. Maximal heat dissipation capacity and hyperthermia risk: Neglected key factors in the ecology of endotherms. J. Anim. Ecol. 79, 726–746. https://doi.org/10.1111/j.1365-2656.2010.01689.x (2010).Article 

    Google Scholar 
    Deerenberg, C. et al. Parental energy expenditure in relation to manipulated brood size in the European kestrel. Zool. Anal. Complex Syst. 99, 38–47 (1995).
    Google Scholar 
    Daan, S., Deerenberg, C. & Dijkstra, C. Increased daily work precipitates natural death in the kestrel. J. Anim. Ecol. 65, 539–544. https://doi.org/10.2307/5734 (1996).Article 

    Google Scholar 
    Newton, I. Migration within the annual cycle: Species, sex and age differences. J. Ornithol. 152, 169–185 (2011).Article 

    Google Scholar 
    Wingfield, J. C. Organization of vertebrate annual cycles: Implications for control mechanisms. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 425–441. https://doi.org/10.1098/rstb.2007.2149 (2008).Article 

    Google Scholar 
    Barta, Z. et al. Optimal moult strategies in migratory birds. Philos. Trans. R. Soc. B Biol. Sci. 363, 211–229. https://doi.org/10.1098/rstb.2007.2136 (2008).Article 

    Google Scholar 
    Wingfield, J. C. Flexibility in annual cycles of birds: Implications for endocrine control mechanisms. J. Ornithol. 146, 291–304. https://doi.org/10.1007/s10336-005-0002-z (2005).Article 

    Google Scholar 
    Bryant, D. M. Energy expenditure in wild birds. Proc. Nutr. Soc. 56, 1025–1039. https://doi.org/10.1079/PNS19970107 (1997).Article 
    CAS 

    Google Scholar 
    Lustick, S. Energy requirements of molt in cowbirds. Auk 87, 742–746. https://doi.org/10.2307/4083708 (1970).Article 

    Google Scholar 
    Murphy, M. E. & King, J. R. Energy and nutrient use during moult by white-crowned sparrows Zonotrichia leucophrys gambelii. Ornis Scand. (Scand. J. Ornithol.) 23, 304–313. https://doi.org/10.2307/3676654 (1992).Article 

    Google Scholar 
    Lindström, Å., Visser, G. H. & Daan, S. The energetic cost of feather synthesis is proportional to basal metabolic rate. Physiol. Zool. 66, 490–510. https://doi.org/10.1086/physzool.66.4.30163805 (1993).Article 

    Google Scholar 
    Buttemer, W. A., Nicol, S. C. & Sharman, A. Thermoenergetics of pre-moulting and moulting kookaburras (Dacelo novaeguineae): They’re laughing. J. Comp. Physiol. B. 173, 223–230 (2003).Article 
    CAS 

    Google Scholar 
    Hedenström, A. & Sunada, S. On the aerodynamics of moult gaps in birds. J. Exp. Biol. 202, 67–76. https://doi.org/10.1242/jeb.202.1.67 (1999).Article 

    Google Scholar 
    Cherel, Y., Quillfeldt, P., Delord, K. & Weimerskirch, H. Combination of at-sea activity, geolocation and feather stable isotopes documents where and when seabirds molt. Front. Ecol. Evol. 4, 3. https://doi.org/10.3389/fevo.2016.00003 (2016).Article 

    Google Scholar 
    Rohwer, S., Butler, L. K., Froehlich, D. R., Greenberg, R. & Marra pp., Ecology and demography of east–west differences in molt scheduling of Neotropical migrant passerines. In Birds of Two Worlds: The Ecology and Evolution of Migration (eds Greenberg, R. & Marra, P. P.) 87–105 (Johns Hopkins University Press, 2005).
    Google Scholar 
    Norris, D. R., Marra, P. P., Kyser, T. K., Sherry, T. W. & Ratcliffe, L. M. Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird. Proc. R. Soc. Lond. B Biol. Sci. 271, 59–64. https://doi.org/10.1098/rspb.2003.2569 (2004).Article 

    Google Scholar 
    Ramenofsky, M. & Wingfield, J. C. Behavioral and physiological conflicts in migrants: The transition between migration and breeding. J. Ornithol. 147, 135 (2006).Article 

    Google Scholar 
    Kiat, Y., Izhaki, I. & Sapir, N. The effects of long-distance migration on the evolution of moult strategies in Western-Palearctic passerines. Biol. Rev. 94, 700–720. https://doi.org/10.1111/brv.12474 (2019).Article 

    Google Scholar 
    Newton, I. The Migration Ecology of Birds (Academic Press, 2008).
    Google Scholar 
    Klaassen, R. H. G., Ens, B. J., Shamoun-Baranes, J., Exo, K.-M. & Bairlein, F. Migration strategy of a flight generalist, the Lesser Black-backed Gull Larus fuscus. Behav. Ecol. 23, 58–68. https://doi.org/10.1093/beheco/arr150 (2012).Article 

    Google Scholar 
    Martín-Vélez, V. et al. Functional connectivity network between terrestrial and aquatic habitats by a generalist waterbird, and implications for biovectoring. Sci. Total Environ. 705, 135886. https://doi.org/10.1016/j.scitotenv.2019.135886 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Baert, J. M. et al. High-resolution GPS tracking reveals sex differences in migratory behaviour and stopover habitat use in the Lesser Black-backed Gull Larus fuscus. Sci. Rep. 8, 1–11. https://doi.org/10.1038/s41598-018-23605-x (2018).Article 
    CAS 

    Google Scholar 
    Spelt, A. et al. Habitat use of urban-nesting lesser black-backed gulls during the breeding season. Sci. Rep. 9, 1–11. https://doi.org/10.1038/s41598-019-46890-6 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Tyson, C., Shamoun-Baranes, J., Van Loon, E. E., Camphuysen, K. & Hintzen, N. T. Individual specialization on fishery discards by lesser black-backed gulls (Larus fuscus). ICES J. Mar. Sci. 72, 1882–1891. https://doi.org/10.1093/icesjms/fsv021 (2015).Article 

    Google Scholar 
    Shamoun-Baranes, J., Burant, J. B., Loon, E. E., Bouten, W. & Camphuysen, C. J. Short distance migrants travel as far as long distance migrants in lesser black-backed gulls Larus fuscus. J. Avian Biol. 48, 49–57. https://doi.org/10.1111/jav.01229 (2017).Article 

    Google Scholar 
    Brown, J. M. et al. Long-distance migrants vary migratory behaviour as much as short-distance migrants: An individual-level comparison from a seabird species with diverse migration strategies. J. Anim. Ecol. 90, 1058–1070. https://doi.org/10.1111/1365-2656.13431 (2021).Article 

    Google Scholar 
    Brown, J. M., Bouten, W., Camphuysen, K. C. J., Nolet, B. A. & Shamoun-Baranes, J. Acceleration as a proxy for energy expenditure in a facultative-soaring bird: Comparing dynamic body acceleration and time-energy budgets to heart rate. Funct. Ecol. 36, 1627–1638. https://doi.org/10.1111/1365-2435.14055 (2022).Article 

    Google Scholar 
    Somveille, M., Manica, A. & Rodrigues, A. S. L. Where the wild birds go: Explaining the differences in migratory destinations across terrestrial bird species. Ecography 42, 225–236. https://doi.org/10.1111/ecog.03531 (2019).Article 

    Google Scholar 
    Levin, S. A. The problem of pattern and scale in ecology: The Robert H MacArthur award lecture. Ecology 73, 1943–1967 (1992).Article 

    Google Scholar 
    Shepard, E. L. et al. Energy landscapes shape animal movement ecology. Am. Nat. 182, 298–312. https://doi.org/10.1086/671257 (2013).Article 

    Google Scholar 
    Sage, E., Bouten, W., Hoekstra, B., Camphuysen, K. C. & Shamoun-Baranes, J. Orographic lift shapes flight routes of gulls in virtually flat landscapes. Sci. Rep. 9, 1–10. https://doi.org/10.1038/s41598-019-46017-x (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Stephens, D. W. & Krebs, J. R. Foraging Theory (Princeton University Press, 2019).Book 

    Google Scholar 
    Piersma, T. Why marathon migrants get away with high metabolic ceilings: Towards an ecology of physiological restraint. J. Exp. Biol. 214, 295–302. https://doi.org/10.1242/jeb.046748 (2011).Article 

    Google Scholar 
    Shamoun-Baranes, J., Bouten, W., Camphuysen, C. J. & Baaij, E. Riding the tide: Intriguing observations of gulls resting at sea during breeding. Ibis 153, 411–415. https://doi.org/10.1111/j.1474-919X.2010.01096.x (2011).Article 

    Google Scholar 
    Kavelaars, M. M. et al. Simultaneous GPS-tracking of parents reveals a similar parental investment within pairs, but no immediate co-adjustment on a trip-to-trip basis. Mov. Ecol. 9, 42. https://doi.org/10.1186/s40462-021-00279-1 (2021).Article 

    Google Scholar 
    Humphreys, E. M., Wanless, S. & Bryant, D. M. Elevated metabolic costs while resting on water in a surface feeder: The Black-legged Kittiwake Rissa tridactyla. Ibis 149, 106–111. https://doi.org/10.1111/j.1474-919X.2006.00618.x (2007).Article 

    Google Scholar 
    Lustick, S., Battersby, B. & Kelty, M. Behavioral thermoregulation: Orientation toward the sun in herring gulls. Science 200, 81–83. https://doi.org/10.1126/science.635577 (1978).Article 
    ADS 

    Google Scholar 
    Green, J. A., Boyd, I. L., Woakes, A. J., Green, C. J. & Butler, P. J. Do seasonal changes in metabolic rate facilitate changes in diving behaviour?. J. Exp. Biol. 208, 2581–2593. https://doi.org/10.1242/jeb.01679 (2005).Article 
    CAS 

    Google Scholar 
    Green, J. A. et al. An increase in minimum metabolic rate and not activity explains field metabolic rate changes in a breeding seabird. J. Exp. Biol. 216, 1726–1735. https://doi.org/10.1242/jeb.085092 (2013).Article 
    CAS 

    Google Scholar 
    White, C. R., Grémillet, D., Green, J. A., Martin, G. R. & Butler, P. J. Metabolic rate throughout the annual cycle reveals the demands of an Arctic existence in Great Cormorants. Ecology 92, 475–486 (2011).Article 

    Google Scholar 
    Guillemette, M. & Butler, P. J. Seasonal variation in energy expenditure is not related to activity level or water temperature in a large diving bird. J. Exp. Biol. 215, 3161–3168. https://doi.org/10.1242/jeb.061119 (2012).Article 

    Google Scholar 
    Dunn, R. E., Wanless, S., Daunt, F., Harris, M. P. & Green, J. A. A year in the life of a North Atlantic seabird: Behavioural and energetic adjustments during the annual cycle. Sci. Rep. 10, 1–11. https://doi.org/10.1038/s41598-020-62842-x (2020).Article 
    CAS 

    Google Scholar 
    Camphuysen, C. J. Lesser Black-backed gulls nesting at Texel. Final report (Royal Netherlands Institute for Sea Research, 2011).
    Google Scholar 
    Camphuysen, C. J., Shamoun-Baranes, J., van Loon, E. E. & Bouten, W. Sexually distinct foraging strategies in an omnivorous seabird. Mar. Biol. 162, 1417–1428. https://doi.org/10.1007/s00227-015-2678-9 (2015).Article 

    Google Scholar 
    Dunn, R. E., White, C. R. & Green, J. A. A model to estimate seabird field metabolic rates. Biol. Lett. 14, 20180190. https://doi.org/10.1098/rsbl.2018.0190 (2018).Article 

    Google Scholar 
    Catry, P., Dias, M. P., Phillips, R. A. & Granadeiro, J. P. Carry-over effects from breeding modulate the annual cycle of a long-distance migrant: An experimental demonstration. Ecology 94, 1230–1235. https://doi.org/10.1890/12-2177.1 (2013).Article 

    Google Scholar 
    Gutowsky, S. E. et al. Daily activity budgets reveal a quasi-flightless stage during non-breeding in Hawaiian albatrosses. Mov. Ecol. 2, 23. https://doi.org/10.1186/s40462-014-0023-4 (2014).Article 

    Google Scholar 
    Harris, M. P. Ecological adaptations of moult in some British gulls. Bird Study 18, 113–118 (1971).Article 

    Google Scholar 
    Verbeek, N. A. Timing of primary moult in adult herring gulls and lesser black-backed gulls. J. Ornithol. 118, 87–92 (1977).Article 

    Google Scholar 
    Sorensen, M. C., Hipfner, J. M., Kyser, T. K. & Norris, D. R. Carry-over effects in a Pacific seabird: Stable isotope evidence that pre-breeding diet quality influences reproductive success. J. Anim. Ecol. 78, 460–467. https://doi.org/10.1111/j.1365-2656.2008.01492.x (2009).Article 

    Google Scholar 
    Lok, T., Overdijk, O., Tinbergen, J. M. & Piersma, T. The paradox of spoonbill migration: Most birds travel to where survival rates are lowest. Anim. Behav. 82, 837–844 (2011).Article 

    Google Scholar 
    Reneerkens, J. et al. Low fitness at low latitudes: Wintering in the tropics increases migratory delays and mortality rates in an Arctic breeding shorebird. J. Anim. Ecol. 89, 691–703. https://doi.org/10.1111/1365-2656.13118 (2020).Article 

    Google Scholar 
    Bouten, W., Baaij, E. W., Shamoun-Baranes, J. & Camphuysen, K. C. A flexible GPS tracking system for studying bird behaviour at multiple scales. J. Ornithol. 154, 571–580. https://doi.org/10.1007/s10336-012-0908-1 (2013).Article 

    Google Scholar 
    Thaxter, C. B. et al. A trial of three harness attachment methods and their suitability for long-term use on Lesser Black-backed Gulls and Great Skuas. Ring. Migr. 29, 65–76. https://doi.org/10.1080/03078698.2014.995546 (2014).Article 

    Google Scholar 
    Shamoun-Baranes, J., Bouten, W., van Loon, E. E., Meijer, C. & Camphuysen, C. J. Flap or soar? How a flight generalist responds to its aerial environment. Philos. Trans. R. Soc. B 371, 20150395. https://doi.org/10.1098/rstb.2015.0395 (2016).Article 

    Google Scholar 
    Buchhorn, M., Smets, B., Bertels, L., Lesiv, M., Masiliunas, D., Linlin, L., Herold, M. & Fritz S. Copernicus Global Land Service: Land Cover 100m: Collection 3: epoch 2016–2019: Globe (2020).Wilson, R. P. et al. Estimates for energy expenditure in free-living animals using acceleration proxies: A reappraisal. J. Anim. Ecol. 89, 161–172. https://doi.org/10.1111/1365-2656.13040 (2019).Article 

    Google Scholar 
    Cartar, R. V. & Morrison, R. G. Estimating metabolic costs for homeotherms from weather data and morphology: An example using calidridine sandpipers. Can. J. Zool. 75, 94–101 (1997).Article 

    Google Scholar 
    Baveco, J. M., Kuipers, H. & Nolet, B. A. A large-scale multi-species spatial depletion model for overwintering waterfowl. Ecol. Model. 222, 3773–3784 (2011).Article 

    Google Scholar 
    Hersbach H et al. ERA5 hourly data on single levels from 1979 to present. Copernicus Climate Change Service (C3S) Climate Data Store (CDS). https://doi.org/10.24381/cds.adbb2d47 (2018).Bevan, R. M., Butler, P. J., Woakes, A. J. & Prince, P. A. The energy expenditure of free-ranging black-browed albatrosses. Philos. Trans. R. Soc. Lond. B Biol. Sci. 350, 119–131. https://doi.org/10.1098/rstb.1995.0146 (1995).Article 
    ADS 

    Google Scholar 
    Bevan, R. M. & Butler, P. J. The effects of temperature on the oxygen consumption, heart rate and deep body temperature during diving in the tufted duck Aythya fuligula. J. Exp. Biol. 163, 139–151. https://doi.org/10.1242/jeb.163.1.139 (1992).Article 

    Google Scholar 
    Stahel, C. D. & Nicol, S. C. Temperature regulation in the little penguin, Eudyptula minor, in air and water. J. Comp. Physiol. 148, 93–100 (1982).Article 

    Google Scholar 
    Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. https://doi.org/10.18637/jss.v067.i01 (2015).Article 

    Google Scholar 
    Wood, S. mgcv: Mixed GAM Computation Vehicle with Automatic Smoothness Estimation (2021).Zuur, A. F. Beginner’s Guide to Spatial, Temporal, and Spatial-Temporal Ecological Data Analysis with R-INLA (Highland Statistics Ltd., 2017).
    Google Scholar 
    Brown, J. M., Bouten, W., Camphuysen, K., Nolet, B. A. & Shamoun-Baranes, J. Z. Data and code archive for ‘Energetic and behavioral consequences of migration: An empirical evaluation in the context of the full annual cycle’. https://doi.org/10.21942/uva.21583926.v1 (2022).Wickham, H. ggplot2: Elegant Graphics for Data Analysis. https://ggplot2.tidyverse.org (Springer, 2016).South, A. rworldmap: Mapping Global Data. http://cran.r-project.org/web/packages/rworldmap (2016).Natural Earth. V 1.4.0. Free vector and raster map data at 1:10m, 1:50m, and 1:110m scales. https://www.naturalearthdata.com/downloads/. More

  • in

    Significant changes in soil microbial community structure and metabolic function after Mikania micrantha invasion

    Runyon, J. B., Butler, J. L., Friggens, M. M., Meyer, S. E. & Sing, S. E. Invasive species and climate change. USDA For. Serv. 285, 97–115 (2012).
    Google Scholar 
    Murphy, G. E. & Romanuk, T. N. A meta-analysis of declines in local species richness from human disturbances. Ecol. Evol. 4, 91–103 (2014).Article 

    Google Scholar 
    Mollot, G., Pantel, J. H. & Romanuk, T. N. The effects of invasive species on the decline in species richness: a global meta-analysis. Adv. Ecol. Res. 56, 61–83 (2017).Article 

    Google Scholar 
    Gaertner, M., Den Breeyen, A., Hui, C. & Richardson, D. M. Impacts of alien plant invasions on species richness in Mediterranean-type ecosystems: A meta-analysis. Prog. Phys. Geog. 33, 319–338 (2009).Article 

    Google Scholar 
    Vilà, M. et al. Local and regional assessments of the impacts of plant invaders on vegetation structure and soil properties of Mediterranean islands. J. Biogeogr. 33, 853–861 (2010).Article 

    Google Scholar 
    Hejda, M., Pysek, P. & Jarosik, V. Impact of invasive plants on the species richness, diversity and composition of invaded communities. J. Ecol. 97, 393–403 (2009).Article 

    Google Scholar 
    Powell, K. I., Chase, J. M. & Knight, T. M. A synthesis of plant invasion effects on biodiversity across spatial scales. Am. J. Bot. 98, 539–548 (2011).Article 

    Google Scholar 
    Ehrenfeld, J. G. Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6, 503–523 (2003).Article 
    CAS 

    Google Scholar 
    Liao, C. et al. Altered ecosystem carbon and nitrogen cycles by plant invasion: A meta-analysis. New Phytol. 177, 706–714 (2008).Article 
    CAS 

    Google Scholar 
    Chabrerie, O., Laval, K., Puget, P., Desaire, S. & Alard, D. Relationship between plant and soil microbial communities along a successional gradient in a chalk grassland in north-western France. Appl. Soil Ecol. 24, 43–56 (2003).Article 

    Google Scholar 
    Harris, J. Soil microbial communities and restoration ecology: Facilitators or followers?. Science 325, 573–574 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Dawson, W. & Schrama, M. Identifying the role of soil microbes in plant invasions. J. Ecol. 104, 1211–1218 (2016).Article 

    Google Scholar 
    Lankau, R. Soil microbial communities alter allelopathic competition between Alliaria petiolata and a native species. Biol. Invasions 12, 2059–2068 (2010).Article 

    Google Scholar 
    Siefert, A., Zillig, K. W., Friesen, M. L. & Strauss, S. Y. Soil microbial communities alter conspecific and congeneric competition consistent with patterns of field coexistence in three Trifolium congeners. J. Ecol. 106, 1876–1891 (2018).Article 
    CAS 

    Google Scholar 
    Kourtev, P. S., Ehrenfeld, J. G. & Haggblom, M. Exotic plant species alter the microbial community structure and function in the soil. Ecology 83, 3152–3166 (2002).Article 

    Google Scholar 
    Li, W. H., Zhang, C. B., Jiang, H. B., Xin, G. R. & Yang, Z. Y. Changes in soil microbial community associated with invasion of the exotic weed, Mikania micrantha H.B.K. Plant Soil 281, 309–324 (2006).Article 
    CAS 

    Google Scholar 
    Li, W. H., Zhang, C., Gao, G., Zan, Q. & Yang, Z. Relationship between Mikania micrantha invasion and soil microbial biomass, respiration and functional diversity. Plant Soil 296, 197–207 (2007).Article 
    CAS 

    Google Scholar 
    Chen, X. P. et al. Exotic plant Alnus trabeculosa alters the composition and diversity of native rhizosphere bacterial communities of Phragmites australis. Pedosphere 26, 108–119 (2016).Article 

    Google Scholar 
    Yin, L., Liu, B., Wang, H., Zhang, Y. & Fan, W. The rhizosphere microbiome of Mikania micrantha provides insight into adaptation and invasion. Front. Microbiol. 11, 1462 (2020).Article 

    Google Scholar 
    Griffiths, B. S., Ritz, K. & Wheatley, R. E. Relationship between functional diversity and genetic diversity in complex microbial communities. In Microbial Communities (eds Insam, H. & Rangger, A.) 1–9 (Springer, 1997). https://doi.org/10.1007/978-3-642-60694-6_1.Chapter 

    Google Scholar 
    Pérez-Piqueres, A., Edel-Hermann, V., Alabouvette, C. & Steinberg, C. Response of soil microbial communities to compost amendments. Soil Biol. Biochem. 38, 460–470 (2006).Article 

    Google Scholar 
    Grime, J. P. Plant strategies and vegetation processes. Biol. Plant 23, 254–254 (1979).
    Google Scholar 
    Goldberg, D. & Novoplansky, A. On the relative importance of competition in unproductive environments. J. Ecol. 85, 409–418 (1997).Article 

    Google Scholar 
    Goldberg, D. E., Martina, J. P., Elgersma, K. J. & Currie, W. S. Plant size and competitive dynamics along nutrient gradients. Am. Nat. 190, 229–243 (2017).Article 

    Google Scholar 
    Castro-Díez, P., Godoy, O., Alonso, A., Gallardo, A. & Saldaña, A. What explains variation in the impacts of exotic plant invasions on the nitrogen cycle? A meta-analysis. Ecol. Lett. 17, 1–12 (2014).Article 

    Google Scholar 
    Chapuis-Lardy, L., Vanderhoeven, S., Dassonville, N., Koutika, L. S. & Meerts, P. Effect of the exotic invasive plant Solidago gigantea on soil phosphorus status. Biol. Fertil. Soils 42, 481–489 (2006).Article 

    Google Scholar 
    Thorpe, A. S., Archer, V. & DeLuca, T. H. The invasive forb, Centaurea maculosa, increases phosphorus availability in Montana grasslands. Appl. Soil Ecol. 32, 118–122 (2006).Article 

    Google Scholar 
    Hawkes, C. V., Wren, I. F., Herman, D. J. & Firestone, M. K. Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol. Lett. 8, 976–985 (2005).Article 

    Google Scholar 
    Zhang, A. M., Chen, Z. H., Zhang, G. N., Chen, L. J. & Wu, Z. J. Soil phosphorus composition determined by 31P NMR spectroscopy and relative phosphatase activities influenced by land use. Eur. J. Soil Biol. 52, 73–77 (2012).Article 

    Google Scholar 
    Souza-Alonso, P., Novoa, A. & Gonzalez, L. Soil biochemical alterations and microbial community responses under Acacia dealbata Link invasion. Soil Biol. Biochem. 79, 100–108 (2014).Article 
    CAS 

    Google Scholar 
    Callaway, M. et al. Exotic invasive plants increase productivity, abundance of ammonia-oxidizing bacteria and nitrogen availability in intermountain grasslands. J. Ecol. 104, 994–1002 (2016).Article 

    Google Scholar 
    Zhao, M. et al. Ageratina adenophora invasions are associated with microbially mediated differences in biogeochemical cycles. Sci. Total Environ. 677, 47–56 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Litton, C. M., Sandquist, D. R. & Cordell, S. Effects of non-native grass invasion on aboveground carbon pools and tree population structure in a tropical dry forest of Hawaii. For. Ecol. Manag. 231, 105–113 (2006).Article 

    Google Scholar 
    Wolkovich, E. M., Lipson, D. A., Virginia, R. A., Cottingham, K. L. & Bolger, D. T. Grass invasion causes rapid increases in ecosystem carbon and nitrogen storage in a semiarid shrubland. Glob. Chang. Biol. 16, 1351–1365 (2010).Article 
    ADS 

    Google Scholar 
    Sardans, J. et al. Plant invasion is associated with higher plant-soil nutrient concentrations in nutrient-poor environments. Glob. Chang. Biol. 23, 1282–1291 (2017).Article 
    ADS 

    Google Scholar 
    Yu, H. et al. Soil nitrogen dynamics and competition during plant invasion: insights from Mikania micrantha invasions in China. New Phytol. 229, 3440–3452 (2021).Article 
    CAS 

    Google Scholar 
    Day, M. D. et al. Biology and impacts of pacific islands invasive species. 13. Mikania micrantha Kunth (Asteraceae). Pac. Sci. 70, 257–285 (2016).Article 

    Google Scholar 
    Lowe, S., Browne, M., Boudjelas, S. & De Poorter, M. (eds) 100 of the World’s Worst Invasive Alien Species: A Selection from the Global Invasive Species Database. CID: 20.500.12592/drpzmz. (Auckland: Invasive Species Specialist Group, 2000).Zhang, L. Y., Ye, W. H., Cao, H. L. & Feng, H. L. Mikania micrantha H.B.K. in China: An overview. Weed Res. 44, 42–49 (2004).Article 

    Google Scholar 
    Manrique, V., Diaz, R., Cuda, J. P. & Overholt, W. A. Suitability of a new plant invader as a target for biological control in Florida. Invas. Plant Sci. Manag. 4, 1–10 (2011).Article 

    Google Scholar 
    Macanawai, A., Day, M., Tumaneng-Diete, T., Adkins, S. & Nausori, F. Impact of Mikania micrantha on crop production systems in Viti Levu, Fiji. Pak. J. Weed Sci. Res. 18, 357–365 (2012).
    Google Scholar 
    Carter, M. R. & Gregorich, E. G. (eds) Soil Sampling and Methods of Analysis 2nd edn. (CRC Press, 2007). https://doi.org/10.1201/9781420005271.Book 

    Google Scholar 
    Liu, X. et al. Will nitrogen deposition mitigate warming-increased soil respiration in a young subtropical plantation?. Agric. For. Meteorol. 246, 78–85 (2017).Article 
    ADS 

    Google Scholar 
    Turner, B. L. & Wright, S. J. The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117, 115–130 (2014).Article 
    CAS 

    Google Scholar 
    Sun, S. & Badgley, B. D. Changes in microbial functional genes within the soil metagenome during forest ecosystem restoration. Soil Biol. Biochem. 135, 163–172 (2019).Article 
    CAS 

    Google Scholar 
    Saiya-Cork, K. R., Sinsabaugh, R. L. & Zak, D. R. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol. Biochem. 34, 1309–1315 (2002).Article 
    CAS 

    Google Scholar 
    Dawkins, K. & Esiobu, N. The invasive brazilian pepper tree (Schinus terebinthifolius) is colonized by a root microbiome enriched with Alphaproteobacteria and unclassified Spartobacteria. Front. Microbiol. 9, 876 (2018).Article 

    Google Scholar 
    Carey, C. J., Beman, J. M., Eviner, V. T., Malmstrom, C. M. & Hart, S. C. Soil microbial community structure is unaltered by plant invasion, vegetation clipping, and nitrogen fertilization in experimental semi-arid grasslands. Front. Microbiol. 6, 466 (2015).Article 

    Google Scholar 
    Strickland, M. S., Osburn, E., Lauber, C., Fierer, N. & Bradford, M. A. Litter quality is in the eye of the beholder: Initial decomposition rates as a function of inoculum characteristics. Funct. Ecol. 23, 627–636 (2009).Article 

    Google Scholar 
    Kanokratana, P. et al. Insights into the phylogeny and metabolic potential of a primary tropical peat swamp forest microbial community by metagenomic analysis. Microb. Ecol. 61, 518–528 (2011).Article 

    Google Scholar 
    Margesin, R., Jud, M., Tscherko, D. & Schinner, F. Microbial communities and activities in alpine and subalpine soils. FEMS Microbiol. Ecol. 67, 208–218 (2009).Article 
    CAS 

    Google Scholar 
    Xu, Z. W. et al. Soil enzyme activity and stoichiometry in forest ecosystems along the North-South Transect in eastern China (NSTEC). Soil Biol. Biochem. 104, 152–163 (2017).Article 
    CAS 

    Google Scholar 
    Zhou, X. et al. Warming and increased precipitation have differential effects on soil extracellular enzyme activities in a temperate grassland. Sci. Total Environ. 444, 552–558 (2013).Article 
    ADS 
    CAS 

    Google Scholar 
    Mao, T. & Minoru, K. Using the KEGG database resource. Curr. Protoc. Bioinform. 38, 1121–11243. https://doi.org/10.1002/0471250953.bi0112s38 (2012).Article 

    Google Scholar 
    Grayston, S. J., Griffith, G. S., Mawdsley, J. L., Campbell, C. D. & Bardgett, R. D. Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol. Biochem. 33, 533–551 (2001).Article 
    CAS 

    Google Scholar 
    Chen, W. B. & Chen, B. M. Considering the preferences for nitrogen forms by invasive plants: a case study from a hydroponic culture experiment. Weed Res. 59, 49–57 (2019).CAS 

    Google Scholar 
    Christian, J. M. & Wilson, S. D. Long-term ecosystem impacts of an introduced grass in the northern Great Plains. Ecology 80, 2397–2407 (1999).Article 

    Google Scholar 
    Strickland, M. S., Devore, J. L., Maerz, J. C. & Bradford, M. A. Grass invasion of a hardwood forest is associated with declines in belowground carbon pools. Glob. Chang. Biol. 16, 1338–1350 (2010).Article 
    ADS 

    Google Scholar 
    Bradley, B. A., Houghtonw, R. A., Mustard, J. F. & Hamburg, S. P. Invasive grass reduces aboveground carbon stocks in shrublands of the Western US. Glob. Chang. Biol. 12, 1815–1822 (2006).Article 
    ADS 

    Google Scholar 
    Ogle, S. M., Ojima, D. & Reiners, W. A. Modeling the impact of exotic annual brome grasses on soil organic carbon storage in a northern mixed-grass prairie. Biol. Invasions 6, 365–377 (2004).Article 

    Google Scholar 
    Ni, G. Y. et al. Mikania micrantha invasion enhances the carbon (C) transfer from plant to soil and mediates the soil C utilization through altering microbial community. Sci. Total Environ. 711, 135020. https://doi.org/10.1016/j.scitotenv.2019.135020 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Callaway, R. M., Thelen, G. C., Rodriguez, A. & Holben, W. E. Soil biota and exotic plant invasion. Nature 427, 731–733 (2004).Article 
    ADS 
    CAS 

    Google Scholar 
    Klironomos, J. N. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417, 67–70 (2002).Article 
    ADS 
    CAS 

    Google Scholar 
    Kourtev, P. S., Ehrenfeld, J. G. & Haggblom, M. Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol. Biochem. 35, 895–905 (2003).Article 
    CAS 

    Google Scholar 
    Jansson, J. K. & Hofmockel, K. S. Soil microbiomes and climate change. Nat. Rev. Microbiol. 18, 35–46 (2020).Article 
    CAS 

    Google Scholar 
    Ehrenfeld, J. G., Kourtev, P. & Huang, W. Z. Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol. Appl. 11, 1287–1300 (2001).Article 

    Google Scholar 
    Allison, S. D. & Vitousek, P. M. Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141, 612–619 (2004).Article 
    ADS 

    Google Scholar 
    Harner, M. J. et al. Decomposition of leaf litter from a native tree and an actinorhizal invasive across riparian habitats. Ecol. Appl. 19, 1135–1146 (2009).Article 

    Google Scholar 
    Wolkovich, E. M. Nonnative grass litter enhances grazing arthropod assemblages by increasing native shrub growth. Ecology 91, 756–766 (2010).Article 

    Google Scholar 
    Yan, J. et al. Conversion of organic carbon from decayed native and invasive plant litter in Jiuduansha wetland and its implications for SOC formation and sequestration. J. Soils Sediments 20, 675–689 (2020).Article 
    CAS 

    Google Scholar 
    Aerts, R. & de Caluwe, H. Nitrogen deposition effects on carbon dioxide and methane emissions from temperate peatland soils. Oikos 84, 44–54 (1999).Article 

    Google Scholar 
    Shen, C. C. et al. Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol. Biochem. 57, 204–211 (2013).Article 
    CAS 

    Google Scholar 
    Kuypers, M. M. M., Marchant, H. K. & Kartal, B. The microbial nitrogen-cycling network. Nat. Rev. Microbiol. 16, 263–276 (2018).Article 
    CAS 

    Google Scholar 
    Mothé, G. P. B., Quintanilha-Peixoto, G., Souza, G. R. D., Ramos, A. C. & Intorne, A. C. Overview of the role of nitrogen in copper pollution and bioremediation mediated by plant–microbe interactions. In Soil Nitrogen Ecology (eds Cruz, C. et al.) 249–264. https://doi.org/10.1007/978-3-030-71206-8_12 (Springer, 2021).Chapter 

    Google Scholar 
    Chen, B. M., Peng, S. L. & Ni, G. Y. Effects of the invasive plant Mikania micrantha H.B.K. on soil nitrogen availability through allelopathy in South China. Biol. Invasions 11, 1291–1299 (2009).Article 

    Google Scholar 
    Fan, Y. X. et al. Decreased soil organic P fraction associated with ectomycorrhizal fungal activity to meet increased P demand under N application in a subtropical forest ecosystem. Biol. Fertil. Soils 54, 149–161 (2018).Article 
    CAS 

    Google Scholar 
    Walker, T. W. & Syers, J. K. The fate of phosphorus during pedogenesis. Geoderma 15, 1–19 (1976).Article 
    ADS 
    CAS 

    Google Scholar 
    Khan, M. S., Zaidi, A., Ahemad, M. & Oves, M. Plant growth promotion by phosphate solubilizing fungi: Current perspective. Arch. Agron. Soil Sci. 56, 73–98 (2010).Article 
    CAS 

    Google Scholar 
    Kouas, S., Labidi, N., Debez, A. & Abdelly, C. Effect of P on nodule formation and N fixation in bean. Agron. Sustain. Dev. 25, 389–393 (2005).Article 
    CAS 

    Google Scholar 
    Bolan, N. S. et al. Dissolved organic matter: biogeochemistry, dynamics, and environmental significance in soils. Adv. Agron. 110, 1–75 (2011).Article 
    CAS 

    Google Scholar 
    Dail, D. B., Davidson, E. A. & Chorover, J. Rapid abiotic transformation of nitrate in an acid forest soil. Biogeochemistry 54, 131–146 (2001).Article 
    CAS 

    Google Scholar 
    Fitzhugh, R. D., Lovett, G. M. & Venterea, R. T. Biotic and abiotic immobilization of ammonium, nitrite, and nitrate in soils developed under different tree species in the Catskill Mountains, New York, USA. Glob. Chang. Biol. 9, 1591–1601 (2003).Article 
    ADS 

    Google Scholar  More

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    The influence of task difficulty, social tolerance and model success on social learning in Barbary macaques

    Heyes, B. Y. C. M. Social learning in animals: Categories and mechanisms. Biol. Rev. 69(2), 207–231. https://doi.org/10.1111/j.1469-185X.1994.tb01506.x (1994).Article 
    CAS 

    Google Scholar 
    Hoppitt, W. & Laland, K. N. Social processes influencing learning in animals: A review of the evidence. Adv. Study Behav. 38, 105–165. https://doi.org/10.1016/S0065-3454(08)00003-X (2008).Article 

    Google Scholar 
    Kendal, R. L., Coolen, I. & Laland, K. N. Adaptive trade-offs in the use of social and personal information. In Cognitive Ecology II (eds Dukas, R. & Ratcliffe, J. M.) 249–271 (University of Chicago Press, 2009).Chapter 

    Google Scholar 
    Marshall-Pescini, S. & Whiten, A. Social learning of nut-cracking behavior in East African sanctuary-living chimpanzees (Pan troglodytes schweinfurthii). J. Comp. Psychol. 122(2), 186. https://doi.org/10.1037/0735-7036.122.2.186 (2008).Article 

    Google Scholar 
    Hobaiter, C., Poisot, T., Zuberbühler, K., Hoppitt, W. & Gruber, T. Social network analysis shows direct evidence for social transmission of tool use in wild chimpanzees. PLoS Biol. 12(9), e1001960. https://doi.org/10.1371/journal.pbio.1001960 (2014).Article 
    CAS 

    Google Scholar 
    Coelho, C. G. et al. Social learning strategies for nut-cracking by tufted capuchin monkeys (Sapajus spp.). Anim. Cogn. 18(4), 911–919. https://doi.org/10.1007/s10071-015-0861-5 (2015).Article 
    CAS 

    Google Scholar 
    Boyd, R. & Richerson, P. J. Culture and the evolutionary process (University of Chicago press, 1985).
    Google Scholar 
    Laland, K. N. Social learning strategies. Anim. Learn. Behav. 32(1), 4–14. https://doi.org/10.3758/BF03196002 (2004).Article 

    Google Scholar 
    Kendal, R. L. Animal ‘culture wars’: Evidence from the Wild?. Psychologist 21(4), 312–315 (2008).
    Google Scholar 
    Kendal, R. L., Kendal, J. R., Hoppitt, W. & Laland, K. N. Identifying social learning in animal populations: A new ‘option-bias’ method. PLoS ONE 4(8), e6541. https://doi.org/10.1371/journal.pone.0006541 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Giraldeau, L. A., Valone, T. J. & Templeton, J. J. Potential disadvantages of using socially acquired information. Philos. Trans. R. Soc. Lond. Series B. 357(1427), 1559–1566. https://doi.org/10.1098/rstb.2002.1065 (2002).Article 

    Google Scholar 
    Kendal, R. L., Coolen, I., van Bergen, Y. & Laland, K. N. Trade-offs in the adaptive use of social and asocial learning. Adv. Study Behav. 35, 333–379. https://doi.org/10.1016/S0065-3454(05)35008-X (2005).Article 

    Google Scholar 
    Galef, B. G. Jr. Why behaviour patterns that animals learn socially are locally adaptive. Anim. Behav. 49(5), 1325–1334. https://doi.org/10.1006/anbe.1995.0164 (1995).Article 

    Google Scholar 
    Kendal, R. L. et al. Social learning strategies: Bridge-building between fields. Trends Cogn. Sci. 22(7), 651–665. https://doi.org/10.1016/j.tics.2018.04.003 (2018).Article 

    Google Scholar 
    Rendell, L. et al. Cognitive culture: Theoretical and empirical insights into social learning strategies. Trends Cogn. Sci. 15(2), 68–76. https://doi.org/10.1016/j.tics.2010.12.002 (2011).Article 

    Google Scholar 
    Dindo, M., Thierry, B. & Whiten, A. Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella). Proc. R. Soc. B 275(1631), 187–193. https://doi.org/10.1098/rspb.2007.1318 (2008).Article 

    Google Scholar 
    Reader, S. M. & Biro, D. Experimental identification of social learning in wild animals. Learn. Behav. 38(3), 265–283. https://doi.org/10.3758/LB.38.3.265 (2010).Article 

    Google Scholar 
    Hoppitt, W. & Laland, K. N. Social Learning: An Introduction to Mechanisms, Methods, and Models (Princeton University Press, 2013).Book 

    Google Scholar 
    Byrne, R. W. & Russon, A. E. Learning by imitation: A hierarchical approach. Behav. Brain Sci. 21(5), 667–684. https://doi.org/10.1017/S0140525X9833174X (1998).Article 
    CAS 

    Google Scholar 
    Kendal, R. L. et al. Evidence for social learning in wild lemurs (Lemur catta). Learn. Behav. 38(3), 220–234. https://doi.org/10.3758/LB.38.3.220 (2010).Article 

    Google Scholar 
    Lonsdorf, E. V. & Bonnie, K. E. Opportunities and constraints when studying social learning: Developmental approaches and social factors. Learn. Behav. 38(3), 195–205. https://doi.org/10.3758/LB.38.3.195 (2010).Article 

    Google Scholar 
    Coussi-korbel, S. & Fragaszy, M. On the relation between social dynamics and social learning. Anim. Behav. 50(6), 1441–1453. https://doi.org/10.1016/0003-3472(95)80001-8 (1995).Article 

    Google Scholar 
    Franz, M. & Nunn, C. L. Network-based diffusion analysis: A new method for detecting social learning. Proc. R. Soc. Lond B 276(1663), 1829–1836. https://doi.org/10.1098/rspb.2008.1824 (2009).Article 

    Google Scholar 
    Hoppitt, W., Boogert, N. J. & Laland, K. N. Detecting social transmission in networks. J. Theor. Biol. 263(4), 544–555. https://doi.org/10.1016/j.jtbi.2010.01.004 (2010).Article 
    ADS 
    MATH 

    Google Scholar 
    Hoppitt, W. & Laland, K. N. Detecting social learning using networks: A users guide. Am. J. Primatol. 73(8), 834–844. https://doi.org/10.1002/ajp.20920 (2011).Article 

    Google Scholar 
    Hasenjager, M. J., Leadbeater, E. & Hoppitt, W. Detecting and quantifying social transmission using network-based diffusion analysis. J. Anim. Ecol. 90(1), 8–26. https://doi.org/10.1111/1365-2656.13307 (2021).Article 

    Google Scholar 
    Schnoell, A. V. & Fichtel, C. Wild red-fronted lemurs (Eulemur rufifrons) use social information to learn new foraging techniques. Anim. Cogn. 15(4), 505–516. https://doi.org/10.1007/s10071-012-0477-y (2012).Article 

    Google Scholar 
    Coelho, C. Social Dynamics and Diffusion of Novel Behaviour Patterns in Wild Capuchin Monkeys (Sapajus libidinosus) Inhabiting the Serra da Capivara National Park. (Unpublished Doctoral Dissertation) (Durham University, 2015).
    Google Scholar 
    Claidière, N., Messer, E. J., Hoppitt, W. & Whiten, A. Diffusion dynamics of socially learned foraging techniques in squirrel monkeys. Curr. Biol. 23(13), 1251–1255. https://doi.org/10.1016/j.cub.2013.05.036 (2013).Article 
    CAS 

    Google Scholar 
    van Leeuwen, E. J., Staes, N., Verspeek, J., Hoppitt, W. J. & Stevens, J. M. Social culture in bonobos. Curr. Biol. 30(6), R261–R262. https://doi.org/10.1016/j.cub.2020.02.038 (2020).Article 
    CAS 

    Google Scholar 
    Canteloup, C., Hoppitt, W. & van de Waal, E. Wild primates copy higher-ranked individuals in a social transmission experiment. Nat. Commun. 11(1), 1–10. https://doi.org/10.1038/s41467-019-14209-8 (2020).Article 
    CAS 

    Google Scholar 
    Kawai, M. Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima Islet. Primates 6(1), 1–30. https://doi.org/10.1007/BF01794457 (1965).Article 

    Google Scholar 
    Huffman, M. A., Leca, J. B. & Nahallage, C. A. Cultured Japanese macaques: A multidisciplinary approach to stone handling behavior and its implications for the evolution of behavioral tradition in nonhuman primates. In The Japanese Macaques (eds Nakagawa, N. et al.) 191–219 (Springer, 2010). https://doi.org/10.1007/978-4-431-53886-8_9.Chapter 

    Google Scholar 
    Drapier, M. & Thierry, B. Social transmission of feeding techniques in Tonkean macaques?. Int. J. Primatol. 23(1), 105–122. https://doi.org/10.1023/A:1013201924975 (2002).Article 

    Google Scholar 
    Ducoing, A. M. & Thierry, B. Tool-use learning in Tonkean macaques (Macaca tonkeana). Anim. Cogn. 8(2), 103–113. https://doi.org/10.1007/s10071-004-0240-0 (2005).Article 

    Google Scholar 
    Ferrari, P. F. et al. Neonatal imitation in rhesus macaques. PLoS Biol. 4(9), e302. https://doi.org/10.1371/journal.pbio.0040302 (2006).Article 
    CAS 

    Google Scholar 
    Leca, J. B., Gunst, N. & Huffman, M. A. The first case of dental flossing by a Japanese macaque (Macaca fuscata): Implications for the determinants of behavioral innovation and the constraints on social transmission. Primates 51(1), 13. https://doi.org/10.1007/s10329-009-0159-9 (2010).Article 

    Google Scholar 
    Macellini, S. et al. Individual and social learning processes involved in the acquisition and generalization of tool use in macaques. Philos. Trans. R. Soc. B 367(1585), 24–36. https://doi.org/10.1098/rstb.2011.0125 (2012).Article 
    CAS 

    Google Scholar 
    Redshaw, J. Re-analysis of data reveals no evidence for neonatal imitation in rhesus macaques. Biol. Let. 15(7), 20190342. https://doi.org/10.1098/rsbl.2019.0342 (2019).Article 

    Google Scholar 
    Hook, M. A. et al. Inter-group variation in abnormal behavior in chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). Appl. Anim. Behav. Sci. 76(2), 165–176. https://doi.org/10.1016/S0168-1591(02)00005-9 (2002).Article 

    Google Scholar 
    Watanabe, K., Urasopon, N. & Malaivijitnond, S. Long-tailed macaques use human hair as dental floss. Am. J. Primatol. 69(8), 940–944. https://doi.org/10.1002/ajp.20403 (2007).Article 

    Google Scholar 
    Gumert, M. D., Kluck, M. & Malaivijitnond, S. The physical characteristics and usage patterns of stone axe and pounding hammers used by long-tailed macaques in the Andaman Sea region of Thailand. Am. J. Primatol. 71(7), 594–608. https://doi.org/10.1002/ajp.20694 (2009).Article 

    Google Scholar 
    Tan, A. W., Hemelrijk, C. K., Malaivijitnond, S. & Gumert, M. D. Young macaques (Macaca fascicularis) preferentially bias attention towards closer, older, and better tool users. Anim. Cogn. 21(4), 551–563. https://doi.org/10.1007/s10071-018-1188-9 (2018).Article 

    Google Scholar 
    Bandini, E. & Tennie, C. Exploring the role of individual learning in animal tool-use. PeerJ 8, e9877. https://doi.org/10.7717/peerj.9877 (2020).Article 

    Google Scholar 
    Leca, J. B., Gunst, N., & Huffman, M. A. Japanese macaque cultures: Inter-and intra-troop behavioural variability of stone handling patterns across 10 troops. Behaviour, 251–281. https://www.jstor.org/stable/4536445 (2007).Tanaka, I. Matrilineal distribution of louse egg-handling techniques during grooming in free-ranging Japanese macaques. Am. J. Phys. Anthropol. 98(2), 197–201. https://doi.org/10.1002/ajpa.1330980208 (1995).Article 
    CAS 

    Google Scholar 
    Tanaka, I. Social diffusion of modified louse egg-handling techniques during grooming in free-ranging Japanese macaques. Anim. Behav. 56(5), 1229–1236. https://doi.org/10.1006/anbe.1998.0891 (1998).Article 
    CAS 

    Google Scholar 
    Whiten, A. & van de Waal, E. The pervasive role of social learning in primate lifetime development. Behav. Ecol. Sociobiol. 72(5), 1–16. https://doi.org/10.1007/s00265-018-2489-3 (2018).Article 

    Google Scholar 
    Widdig, A., Streich, W. J. & Tembrock, G. Coalition formation among male Barbary macaques (Macaca sylvanus). Am. J. Primatol. 50(1), 37–51. https://doi.org/10.1002/(SICI)1098-2345(200001)50:1%3c37::AID-AJP4%3e3.0.CO;2-3 (2000).Article 
    CAS 

    Google Scholar 
    Thierry, B. Unity in diversity: Lessons from macaque societies. Evol. Anthropol. 16(6), 224–238. https://doi.org/10.1002/evan.20147 (2007).Article 

    Google Scholar 
    Berghänel, A., Ostner, J., Schröder, U. & Schülke, O. Social bonds predict future cooperation in male Barbary macaques, Macaca sylvanus. Anim. Behav. 81(6), 1109–1116. https://doi.org/10.1016/j.anbehav.2011.02.009 (2011).Article 

    Google Scholar 
    Carne, C., Wiper, S. & Semple, S. Reciprocation and interchange of grooming, agonistic support, feeding tolerance, and aggression in semi-free-ranging Barbary macaques. Am. J. Primatol. 73(11), 1127–1133. https://doi.org/10.1002/ajp.20979 (2011).Article 

    Google Scholar 
    Molesti, S. & Majolo, B. Cooperation in wild Barbary macaques: Factors affecting free partner choice. Anim. Cogn. 19(1), 133–146. https://doi.org/10.1007/s10071-015-0919-4 (2016).Article 

    Google Scholar 
    Rebout, N., Desportes, C. & Thierry, B. Resource partitioning in tolerant and intolerant macaques. Aggress. Behav. 43(5), 513–520. https://doi.org/10.1002/ab.21709 (2017).Article 

    Google Scholar 
    Amici, F., Caicoya, A. L., Majolo, B. & Widdig, A. Innovation in wild Barbary macaques (Macaca sylvanus). Sci. Rep. 10(1), 1–12. https://doi.org/10.1038/s41598-020-61558-2 (2020).Article 
    CAS 

    Google Scholar 
    Fischer, J. Emergence of individual recognition in young macaques. Anim. Behav. 67(4), 655–661. https://doi.org/10.1016/j.anbehav.2003.08.006 (2004).Article 

    Google Scholar 
    Seyfarth, R. M. & Cheney, D. L. Production, usage, and comprehension in animal vocalizations. Brain Lang. 115(1), 92–100. https://doi.org/10.1016/j.bandl.2009.10.003 (2010).Article 

    Google Scholar 
    Garcia-Nisa, I. Communication and cultural transmission in populations of semi free-ranging Barbary macaques (Macaca sylvanus). (Doctoral dissertation). Durham University, United Kingdom. http://etheses.dur.ac.uk/14140/ (2021).Hoppitt, W. The conceptual foundations of network-based diffusion analysis: Choosing networks and interpreting results. Philos. Trans. R. Soc. B 372(1735), 20160418. https://doi.org/10.1098/rstb.2016.0418 (2017).Article 

    Google Scholar 
    Hikami, K., Hasegawa, Y. & Matsuzawa, T. Social transmission of food preferences in Japanese monkeys (Macaca fuscata) after mere exposure or aversion training. J. Comp. Psychol. 104(3), 233. https://doi.org/10.1037/0735-7036.104.3.233 (1990).Article 
    CAS 

    Google Scholar 
    Deaner, R. O., Khera, A. V. & Platt, M. L. Monkeys pay per view: Adaptive valuation of social images by rhesus macaques. Curr. Biol. 15(6), 543–548. https://doi.org/10.1016/j.cub.2005.01.044 (2005).Article 
    CAS 

    Google Scholar 
    Gariépy, J. F. et al. Social learning in humans and other animals. Front. Neurosci. 8, 58. https://doi.org/10.3389/fnins.2014.00058 (2014).Article 

    Google Scholar 
    Barrett, B. J., McElreath, R. L. & Perry, S. E. Pay-off-biased social learning underlies the diffusion of novel extractive foraging traditions in a wild primate. Proc. R. Soc. B 284(1856), 20170358. https://doi.org/10.1098/rspb.2017.0358 (2017).Article 

    Google Scholar 
    Kuester, J. & Paul, A. Group fission in Barbary macaques (Macaca sylvanus) at Affenberg Salem. Int. J. Primatol. 18(6), 941–966. https://doi.org/10.1023/A:1026396113830 (1997).Article 

    Google Scholar 
    Whitehead, H. Analyzing Animal Societies: Quantitative Methods for Vertebrate Social Analysis (University of Chicago Press, 2008).Book 

    Google Scholar 
    Hoppitt, W. (2011). NBDA User Guide V1.2. https://lalandlab.st-andrews.ac.uk/freeware/ 28 Sept 2016.Fleiss, J. L., Levin, B. & Paik, M. C. Statistical Methods for Rates and Proportions 3rd edn. (Wiley, 2003).Book 
    MATH 

    Google Scholar 
    McHugh, M. L. Interrater reliability: the kappa statistic. Biochemia medica: Biochemia medica, 22(3), 276–282. https://hrcak.srce.hr/89395 (2012).Hair, J. F., Anderson, R. E., Babin, B. J. & Black, W. C. Multivariate Data Analysis: A Global Perspective Vol. 7 (Pearson Education, 2010).
    Google Scholar 
    Campbell, L. A., Tkaczynski, P. J., Lehmann, J., Mouna, M. & Majolo, B. Social thermoregulation as a potential mechanism linking sociality and fitness: Barbary macaques with more social partners form larger huddles. Sci. Rep. 8(1), 1–8. https://doi.org/10.1038/s41598-018-24373-4 (2018).Article 
    CAS 

    Google Scholar 
    Barrett, L., Henzi, S. P., Weingrill, T., Lycett, J. E. & Hill, R. A. Market forces predict grooming reciprocity in female baboons. Proc. R. Soc. Lond. Ser. B 266(1420), 665–670. https://doi.org/10.1098/rspb.1999.0687 (1999).Article 

    Google Scholar 
    Henzi, S. P. et al. Effect of resource competition on the long-term allocation of grooming by female baboons: Evaluating Seyfarth’s model. Anim. Behav. 66(5), 931–938. https://doi.org/10.1006/anbe.2003.2244 (2003).Article 

    Google Scholar 
    Ueno, M. & Nakamichi, M. Grooming facilitates huddling formation in Japanese macaques. Behav. Ecol. Sociobiol. 72(6), 1–10. https://doi.org/10.1007/s00265-018-2514-6 (2018).Article 

    Google Scholar 
    Carter, A. J., Tico, M. T. & Cowlishaw, G. Sequential phenotypic constraints on social information use in wild baboons. Elife 5, e13125. https://doi.org/10.7554/eLife.13125.001 (2016).Article 

    Google Scholar 
    Barelli, C., Reichard, U. H. & Mundry, R. Is grooming used as a commodity in wild white-handed gibbons, Hylobates lar?. Anim. Behav. 82(4), 801–809. https://doi.org/10.1016/j.anbehav.2011.07.012 (2011).Article 

    Google Scholar 
    Schülke, O., Dumdey, N. & Ostner, J. Selective attention for affiliative and agonistic interactions of dominants and close affiliates in macaques. Sci. Rep. 10(1), 1–8. https://doi.org/10.1038/s41598-020-62772-8 (2020).Article 
    CAS 

    Google Scholar 
    Heesen, M., Macdonald, S., Ostner, J. & Schülke, O. Ecological and social determinants of group cohesiveness and within-group spatial position in wild Assamese macaques. Ethology 121(3), 270–283. https://doi.org/10.1111/eth.12336 (2015).Article 

    Google Scholar 
    Ortiz, K. M. Female feeding competition in a folivorous primate (Propithecus verreauxi) with formalized dominance hierarchies: contest or scramble? (Doctoral dissertation). University of Texas, USA. https://repositories.lib.utexas.edu/handle/2152/34120 (2015).Jurczyk, V., Fröber, K. & Dreisbach, G. Increasing reward prospect motivates switching to the more difficult task. Mot. Sci. 5(4), 295–313. https://doi.org/10.1037/mot0000119 (2019).Article 

    Google Scholar 
    Rathke, E. M. & Fischer, J. Differential ageing trajectories in motivation, inhibitory control and cognitive flexibility in Barbary macaques (Macaca sylvanus). Philos. Trans. R. Soc. B 375(1811), 20190617. https://doi.org/10.1098/rstb.2019.0617 (2020).Article 

    Google Scholar 
    Kendal, R. et al. Chimpanzees copy dominant and knowledgeable individuals: Implications for cultural diversity. Evol. Hum. Behav. 36(1), 65–72. https://doi.org/10.1016/j.evolhumbehav.2014.09.002 (2015).Article 

    Google Scholar 
    van de Waal, E., Claidière, N. & Whiten, A. Social learning and spread of alternative means of opening an artificial fruit in four groups of vervet monkeys. Anim. Behav. 85(1), 71–76. https://doi.org/10.1016/j.anbehav.2012.10.008 (2013).Article 

    Google Scholar 
    Luncz, L. V. & Boesch, C. Tradition over trend: Neighboring chimpanzee communities maintain differences in cultural behavior despite frequent immigration of adult females. Am. J. Primatol. 76(7), 649–657. https://doi.org/10.1002/ajp.22259 (2014).Article 

    Google Scholar 
    van Leeuwen, E. J., Acerbi, A., Kendal, R. L., Tennie, C. & Haun, D. B. A reappreciation of ‘conformity’. Anim. Behav. 122, e5–e10. https://doi.org/10.1016/j.anbehav.2016.09.010 (2016).Article 

    Google Scholar 
    Horner, V. & Whiten, A. Causal knowledge and imitation/emulation switching in chimpanzees (Pan troglodytes) and children (Homo sapiens). Anim. Cogn. 8(3), 164–181. https://doi.org/10.1007/s10071-004-0239-6 (2005).Article 

    Google Scholar 
    Wood, L. The influence of model-based biases and observer prior experience on social learning mechanisms and strategies. (Doctoral dissertation). Durham University, United Kingdom. http://etheses.dur.ac.uk/7274/ (2013).van Leeuwen, E. J., Cronin, K. A., Schütte, S., Call, J. & Haun, D. B. Chimpanzees (Pan troglodytes) flexibly adjust their behaviour in order to maximize payoffs, not to conform to majorities. PLoS ONE 8(11), e80945. https://doi.org/10.1371/journal.pone.0080945 (2013).Article 
    CAS 

    Google Scholar 
    Vale, G. L., Flynn, E. G., Lambeth, S. P., Schapiro, S. J. & Kendal, R. L. Public information use in chimpanzees (Pan troglodytes) and children (Homo sapiens). J. Comp. Psychol. 128(2), 215–223. https://doi.org/10.1037/a0034420 (2014).Article 

    Google Scholar 
    Canteloup, C., Cera, M. B., Barrett, B. J. & van de Waal, E. Processing of novel food reveals payoff and rank-biased social learning in a wild primate. Sci. Rep. 11(1), 1–13. https://doi.org/10.1038/s41598-021-88857-6 (2021).Article 
    CAS 

    Google Scholar 
    Boccaletti, S. et al. The structure and dynamics of multilayer networks. Phys. Rep. 544(1), 1–122. https://doi.org/10.1016/j.physrep.2014.07.001 (2014).Article 
    ADS 
    CAS 

    Google Scholar 
    Kivela, M. et al. Multilayer networks. J. Complex Netw. 2(3), 203e271. https://doi.org/10.1093/comnet/cnu016 (2014).Article 

    Google Scholar 
    Snijders, L. & Naguib, M. Communication in animal social networks: A missing link. Adv. Study Behav. 49, 297–359. https://doi.org/10.1016/bs.asb.2017.02.004 (2017).Article 

    Google Scholar 
    Finn, K. R., Silk, M. J., Porter, M. A. & Pinter-Wollman, N. The use of multilayer network analysis in animal behaviour. Anim. Behav. 149, 7–22. https://doi.org/10.1016/j.anbehav.2018.12.016 (2019).Article 

    Google Scholar  More

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    Nudibranch predation boosts sponge silicon cycling

    Tréguer, P. J. et al. Reviews and syntheses: The biogeochemical cycle of silicon in the modern ocean. Biogeosciences 18, 1269–1289 (2021).Article 
    ADS 

    Google Scholar 
    Tréguer, P. et al. Influence of diatom diversity on the ocean biological carbon pump. Nat. Geosci. 11, 27–37 (2018).Article 
    ADS 

    Google Scholar 
    Benoiston, A.-S. et al. The evolution of diatoms and their biogeochemical functions. Phil. Trans. R. Soc. B 372, 20160397 (2017).Article 

    Google Scholar 
    de Goeij, J. M. et al. Surviving in a marine desert: The sponge loop retains resources within coral reefs. Science 342, 108–110 (2013).Article 
    ADS 

    Google Scholar 
    Folkers, M. & Rombouts, T. Sponges revealed: a synthesis of their overlooked ecological functions within aquatic ecosystems. In YOUMARES 9—The Oceans: Our Research, Our Future (eds. Jungblut, S. et al.) 181–193 (Springer International Publishing, 2020).Kristiansen, S. & Hoell, E. E. The importance of silicon for marine production. Hydrobiologia 484, 21–31 (2002).Article 
    CAS 

    Google Scholar 
    Henderson, M. J., Huff, D. D. & Yoklavich, M. M. Deep-sea coral and sponge taxa increase demersal fish diversity and the probability of fish presence. Front. Mar. Sci. 7, 593844 (2020).Article 

    Google Scholar 
    McGrath, E. C., Woods, L., Jompa, J., Haris, A. & Bell, J. J. Growth and longevity in giant barrel sponges: Redwoods of the reef or pines in the Indo-Pacific?. Sci. Rep. 8, 15317 (2018).Article 
    ADS 

    Google Scholar 
    Jochum, K. P., Wang, X. H., Vennemann, T. W., Sinha, B. & Muller, W. E. G. Siliceous deep-sea sponge Monorhaphis chuni: A potential paleoclimate archive in ancient animals. Chem. Geol. 300, 143–151 (2012).Article 
    ADS 

    Google Scholar 
    Maldonado, M. et al. Sponge grounds as key marine habitats: A synthetic review of types, structure, functional roles, and conservation concerns. In Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots (eds. Rossi, S. et al.) vol. 1 145–184 (Springer International Publishing, 2017).Maldonado, M. et al. Sponge skeletons as an important sink of silicon in the global oceans. Nat. Geosci. 12, 815–822 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Maldonado, M. et al. Siliceous sponges as a silicon sink: An overlooked aspect of benthopelagic coupling in the marine silicon cycle. Limnol. Oceanogr. 50, 799–809 (2005).Article 
    ADS 
    CAS 

    Google Scholar 
    López-Acosta, M. et al. Sponge contribution to the silicon cycle of a diatom-rich shallow bay. Limnol. Oceanogr. 67, 2431–2447 (2022).Article 
    ADS 

    Google Scholar 
    Maldonado, M. et al. Massive silicon utilization facilitated by a benthic-pelagic coupled feedback sustains deep-sea sponge aggregations. Limnol. Oceanogr. 66, 366–391 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Wulff, J. L. Ecological interactions of marine sponges. Can. J. Zool. 84, 146–166 (2006).Article 

    Google Scholar 
    Pawlik, J. R., Loh, T.-L. & McMurray, S. E. A review of bottom-up vs. top-down control of sponges on Caribbean fore-reefs: What’s old, what’s new, and future directions. PeerJ 6, 4343 (2018).Article 

    Google Scholar 
    Dayton, P. K., Robilliard, G. A., Paine, R. T. & Dayton, L. B. Biological Accommodation in the Benthic Community at McMurdo Sound, Antartica. Ecol. Monogr. 44, 105–128 (1974).Article 

    Google Scholar 
    Meylan, A. Spongivory in hawksbill turtles: A diet of glass. Science 239, 393–395 (1988).Article 
    ADS 
    CAS 

    Google Scholar 
    Wulff, J. Sponge-feeding by Caribbean angelfishes, trunk-fishes, and filefishes. In Sponges in time and space 265–271 (A. A. Balkema, 1994).Santos, C. P., Coutinho, A. B. & Hajdu, E. Spongivory by Eucidaris tribuloides from Salvador, Bahia (Echinodermata: Echinoidea). J. Mar. Biol. Ass. 82, 295–297 (2002).Article 

    Google Scholar 
    Chu, J. W. F. & Leys, S. P. The dorid nudibranchs Peltodoris lentiginosa and Archidoris odhneri as predators of glass sponges. Invertebr. Biol. 131, 75–81 (2012).Article 

    Google Scholar 
    Maschette, D. et al. Characteristics and implications of spongivory in the Knifejaw Oplegnathus woodwardi (Waite) in temperate mesophotic waters. J. Sea Res. 157, 101847 (2020).Article 

    Google Scholar 
    Knowlton, A. L. & Highsmith, R. C. Nudibranch-sponge feeding dynamics: Benefits of symbiont-containing sponge to Archidoris montereyensis (Cooper, 1862) and recovery of nudibranch feeding scars by Halichondria panicea (Pallas, 1766). J. Exp. Mar. Biol. Ecol. 327, 36–46 (2005).Article 

    Google Scholar 
    Bloom, S. A. Morphological correlations between dorid nudibranch predators and sponge prey. Veliger 18, 289–301 (1976).
    Google Scholar 
    Faulkner, D. & Ghiselin, M. Chemical defense and evolutionary ecology of dorid nudibranchs and some other opisthobranch gastropods. Mar. Ecol. Prog. Ser. 13, 295–301 (1983).Article 
    ADS 

    Google Scholar 
    Bloom, S. A. Specialization and noncompetitive resource partitioning among sponge-eating dorid nudibranchs. Oecologia 49, 305–315 (1981).Article 
    ADS 

    Google Scholar 
    Clark, K. B. Nudibranch life cycles in the Northwest Atlantic and their relationship to the ecology of fouling communities. Helgolander Wiss. Meeresunters 27, 28–69 (1975).Article 
    ADS 

    Google Scholar 
    Wulff, J. Regeneration of sponges in ecological context: Is regeneration an integral part of life history and morphological strategies?. Integr. Comp. Biol. 50, 494–505 (2010).Article 

    Google Scholar 
    Wu, Y.-C., Franzenburg, S., Ribes, M. & Pita, L. Wounding response in Porifera (sponges) activates ancestral signaling cascades involved in animal healing, regeneration, and cancer. Sci. Rep. 12, 1307 (2022).Article 
    ADS 
    CAS 

    Google Scholar 
    Turner, T. The marine sponge Hymeniacidon perlevis is a globally-distributed exotic species. Aquat. Invasions 15, 542–561 (2020).Article 

    Google Scholar 
    Ackers, R. G., Moss, D. & Picton, B. E. In Sponges of the British Isles (‘Sponge V’). vol. A Colour Guide and Working Document (Marine Conservation Society, 1992).Lima, P. O. V. & Simone, L. R. L. Anatomical review of Doris verrucosa and redescription of Doris januarii (Gastropoda, Nudibranchia) based on comparative morphology. J. Mar. Biol. Ass. 95, 1203–1220 (2015).Article 

    Google Scholar 
    Avila, C. et al. Biosynthetic origin and anatomical distribution of the main secondary metabolites in the nudibranch mollusc Doris verrucosa. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 97, 363–368 (1990).Article 

    Google Scholar 
    Urgorri, V. & Besteiro, C. The feeding habits of the nudibranchs of Galicia. Iberus 4, 51–58 (1984).
    Google Scholar 
    Aminot, A. & Kerouel, R. In Dosage automatique des nutriments dans les eaux marines: Méthodes en flux continu. Méthodes d’analyse en milieu marin, Ed. Ifremer 188 (2007).Hydes, D. J. & Liss, P. S. Fluorimetric method for the determination of low concentrations of dissolved aluminium in natural waters. Analyst 101, 922 (1976).Article 
    ADS 
    CAS 

    Google Scholar 
    López-Acosta, M., Leynaert, A., Coquille, V. & Maldonado, M. Silicon utilization by sponges: An assessment of seasonal changes. Mar. Ecol. Prog. Ser. 605, 111–123 (2018).Article 
    ADS 

    Google Scholar 
    Grall, J., Le-Loch, F., Guyonnet, B. & Riera, P. Community structure and food web based on stable isotopes (δ15N and δ13C) analysis of a North Eastern Atlantic maerl bed. J. Exp. Mar. Biol. Ecol. 338, 1–15 (2006).Article 
    CAS 

    Google Scholar 
    Cebrian, E., Uriz, M. J., Garrabou, J. & Ballesteros, E. Sponge Mass Mortalities in a warming Mediterranean sea: Are cyanobacteria-harboring species worse off?. PLoS ONE 6, e20211 (2011).Article 
    ADS 
    CAS 

    Google Scholar 
    McClintock, J. B. Investigation of the relationship between invertebrate predation and biochemical composition, energy content, spicule armament and toxicity of benthic sponges at McMurdo Sound, Antartica. Mar. Biol. 94, 479–487 (1987).Article 
    CAS 

    Google Scholar 
    Cockburn, T. C. & Reid, R. G. B. Digestive tract enzymes in two Aeolid nudibranchs (opisthobranchia: Gastropoda). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 65, 275–281 (1980).Article 

    Google Scholar 
    De Caralt, S., Uriz, M. & Wijffels, R. Grazing, differential size-class dynamics and survival of the Mediterranean sponge Corticium candelabrum. Mar. Ecol. Prog. Ser. 360, 97–106 (2008).Article 
    ADS 

    Google Scholar 
    Ragueneau, O., De-Blas-Varela, E., Tréguer, P., Quéguiner, B. & Del Amo, Y. Phytoplankton dynamics in relation to the biogeochemical cycle of silicon in a coastal ecosystem of western Europe. Mar. Ecol. Prog. Ser. 106, 157–172 (1994).Article 
    ADS 

    Google Scholar 
    Turon, X., Tarjuelo, I. & Uriz, M. J. Growth dynamics and mortality of the encrusting sponge Crambe crambe (Poecilosclerida) in contrasting habitats: Correlation with population structure and investment in defence: Growth and mortality of encrusting sponges. Funct. Ecol. 12, 631–639 (1998).Article 

    Google Scholar 
    Hoppe, W. F. Growth, regeneration and predation in three species of large coral reef sponges. Mar. Ecol. Prog. Ser. 50, 117–125 (1988).Article 
    ADS 

    Google Scholar 
    Ayling, A. L. Growth and regeneration rates in thinly encrusting Demospongiae from temperate waters. Biol. Bull. 165, 343–352 (1983).Article 

    Google Scholar 
    Fillinger, L., Janussen, D., Lundälv, T. & Richter, C. Rapid glass sponge expansion after climate-induced Antarctic ice shelf collapse. Curr. Biol. 23, 1330–1334 (2013).Article 
    CAS 

    Google Scholar 
    Dayton, P. K. et al. Benthic responses to an Antarctic regime shift: Food particle size and recruitment biology. Ecol. Appl. 29, 1 (2019).Article 

    Google Scholar 
    Guy, G. & Metaxas, A. Recruitment of deep-water corals and sponges in the Northwest Atlantic Ocean: Implications for habitat distribution and population connectivity. Mar. Biol. 169, 107 (2022).Article 

    Google Scholar 
    Beucher, C., Treguer, P., Corvaisier, R., Hapette, A. M. & Elskens, M. Production and dissolution of biosilica, and changing microphytoplankton dominance in the Bay of Brest (France). Mar. Ecol. Prog. Ser. 267, 57–69 (2004).Article 
    ADS 

    Google Scholar 
    López-Acosta, M., Leynaert, A. & Maldonado, M. Silicon consumption in two shallow-water sponges with contrasting biological features. Limnol. Oceanogr. 61, 2139–2150 (2016).Article 
    ADS 

    Google Scholar 
    Ellwood, M. J., Wille, M. & Maher, W. Glacial silicic acid concentrations in the Southern Ocean. Science 330, 1088–1091 (2010).Article 
    ADS 
    CAS 

    Google Scholar 
    Maldonado, M. et al. Cooperation between passive and active silicon transporters clarifies the ecophysiology and evolution of biosilicification in sponges. Sci. Adv. 6, eaba9322 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Palumbi, S. R. Tactics of acclimation: morphological changes of sponges in an unpredictable environment. Science 225, 1478–1480 (1984).Article 
    ADS 
    CAS 

    Google Scholar 
    Broadribb, M., Bell, J. J. & Rovellini, A. Rapid acclimation in sponges: Seasonal variation in the organic content of two intertidal sponge species. J. Mar. Biol. Ass. 101, 983–989 (2021).Article 
    CAS 

    Google Scholar 
    Schönberg, C. H. L. & Barthel, D. Inorganic skeleton of the demosponge Halichondria panacea. Seasonality in spicule production in the Baltic Sea. Mar. Biol. 130, 133–140 (1997).Article 

    Google Scholar 
    Sheild, C. J. & Witman, J. D. The impact of Henricia sanguinolenta (O. F. Müller) (Echinodermata: Asteroidea) predation on the finger sponges, Isodictya spp.. J. Exp. Mar. Biol. Ecol. 166, 107–133 (1993).Article 

    Google Scholar 
    Lewis, J. R., Bowman, R. S., Kendall, M. A. & Williamson, P. Some geographical components in population dynamics: Possibilities and realities in some littoral species. Neth. J. Sea Res. 16, 18–28 (1982).Article 

    Google Scholar 
    Ashton, G. V. et al. Predator control of marine communities increases with temperature across 115 degrees of latitude. Science 376, 1215–1219 (2022).Article 
    ADS 
    CAS 

    Google Scholar 
    Knowlton, A. & Highsmith, R. Convergence in the time-space continuum: A predator-prey interaction. Mar. Ecol. Prog. Ser. 197, 285–291 (2000).Article 
    ADS 

    Google Scholar  More

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    Unspoilt forests fall to feed the global supply chain

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    Agricultural expansion can plunder forests, but it is not the only human activity to do so. Researchers have found that more than one-third of the loss of Earth’s large, intact forests is driven by production for export — especially of wood, minerals and energy1.

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    doi: https://doi.org/10.1038/d41586-023-00119-9

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    Conservation biology More

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    Plastic responses lead to increased neurotoxin production in the diatom Pseudo-nitzschia under ocean warming and acidification

    Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, et al. Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol. 2019;17:569–86.Article 
    CAS 

    Google Scholar 
    Myers SS, Smith MR, Guth S, Golden CD, Vaitla B, Mueller ND, et al. Climate Change and Global Food Systems: Potential Impacts on Food Security and Undernutrition. Annu Rev Pub Health. 2017;38:259–77.Article 

    Google Scholar 
    Brown AR, Lilley M, Shutler J, Lowe C, Artioli Y, Torres R, et al. Assessing risks and mitigating impacts of harmful algal blooms on mariculture and marine fisheries. Rev Aquac. 2020;12:1663–88.
    Google Scholar 
    Bates SS, Hubbard KA, Lundholm N, Montresor M, Leaw CP. Pseudo-nitzschia, Nitzschia, and domoic acid: New research since 2011. Harmful Algae. 2018;79:3–43.Article 

    Google Scholar 
    Silver MW, Bargu S, Coale SL. Toxic diatoms and domoic acid in natural and iron enriched waters of the oceanic pacific. Proc Natl Acad Sci. 2010;107:20762–67.Article 
    CAS 

    Google Scholar 
    Trick CG, Bill BD, Cochlan WP, Wells ML, Trainer VL, Pickell LD. Iron enrichment stimulates toxic diatom production in high-nitrate, low-chlorophyll areas. Proc Natl Acad Sci. 2010;107:5887–92.Article 
    CAS 

    Google Scholar 
    Hallegraeff G, Enevoldsen H, Zingone A. Global harmful algal bloom status reporting. Harmful Algae. 2021;102:101992.Article 

    Google Scholar 
    McKibben SM, Peterson W, Wood AM, Trainer VL, Hunter M, White AE. Climatic regulation of the neurotoxin domoic acid. Proc Natl Acad Sci. 2017;114:239–44.Article 
    CAS 

    Google Scholar 
    Clark S, Hubbard KA, Ralston DK, McGillicuddy DJ, Stocke C, Alexander MA, et al. Projected effects of climate change on Pseudo-nitzschia bloom dynamics in the Gulf of Maine. J Mar Syst. 2022;230:103737.Article 

    Google Scholar 
    Trainer VL, Kudela RM, Hunter MV, Adams NG, McCabe RM. Climate extreme seeds a new domoic ccid hotspot on the US West Coast. Front Clim. 2020;2:1–11.Article 

    Google Scholar 
    Hinder SL, Hays GC, Edwards M, Roberts EC, Walne AW, Gravenor MB. Changes in marine dinoflagellate and diatom abundance under climate change. Nat Clim Change. 2012;2:271–75.Article 

    Google Scholar 
    Sun J, Hutchins DA, Feng Y, Seubert EL, Caron DA, Fu FX. Effects of changing pCO2 and phosphate availability on domoic acid production and physiology of the marine harmful bloom diatom Pseudo-nitzschia multiseries. Limnol Oceanogr. 2011;56:829–40.Article 
    CAS 

    Google Scholar 
    Zhu Z, Qu P, Fu F, Tennenbaum N, Tatters AO, Hutchins DA. Understanding the blob bloom: warming increases toxicity and abundance of the harmful bloom diatom Pseudo-nitzschia in California coastal waters. Harmful Algae. 2017;67:36–43.Article 
    CAS 

    Google Scholar 
    Radan RL, Cochlan WP. Differential toxin response of Pseudo-nitzschia multiseries as a function of nitrogen speciation in batch and continuous cultures, and during a natural assemblage experiment. Harmful Algae. 2018;73:12–29.Article 
    CAS 

    Google Scholar 
    Wingert CJ, Cochlan WP. Effects of ocean acidification on the growth, photosynthetic performance, and domoic acid production of the diatom Pseudo-nitzschia australis from the California Current System. Harmful Algae. 2021;107:102030.Article 
    CAS 

    Google Scholar 
    Auro ME, Cochlan WP. Nitrogen utilization and toxin production by two diatoms of the Pseudo-nitzschia pseudodelicatissima complex: P. cuspidate and P. fryxelliana. J Phycol. 2013;49:156–69.Article 
    CAS 

    Google Scholar 
    Lundholm N, Clarke A, Ellegaard M. A 100-year record of changing Pseudo-nitzschia species in a sill-fjord in Denmark related to nitrogen loading and temperature. Harmful Algae. 2010;9:449–57.Article 

    Google Scholar 
    Ryan JP, Kudela RM, Birch JM, Blum M, Bower HA, Chavez FP, et al. Causality of an extreme harmful algal bloom in Monterey Bay, California, during the 2014–2016 northeast Pacific warm anomaly. Geophys Res Lett. 2017;44:5571–79.Article 

    Google Scholar 
    McCabe RM, Hickey BM, Kudela RM, Lefebvre KA, Adams NG, Bill BD, et al. An unprecedented coastwide toxic algal bloom linked to anomalous ocean conditions. Geophys Res Lett. 2016;43:10,366–76.Article 

    Google Scholar 
    Tatters AO, Fu FX, Hutchins DA. High CO2 and silicate limitation synergistically increase the toxicity of Pseudo-nitzschia fraudulenta. PLoS One. 2012;7:e32116.Article 
    CAS 

    Google Scholar 
    Lundholm N, Hansen PJ, Kotaki Y. Effect of pH on growth and domoic acid production by potentially toxic diatoms of the genera Pseudo-nitzschia and Nitzschia. Mar Ecol Prog Ser. 2004;273:1–15.Article 
    CAS 

    Google Scholar 
    Trimborn S, Lundholm N, Thoms S, Richter KW, Krock B, Hansen P, et al. Inorganic carbon acquisition in potentially toxic and non-toxic diatoms: the effect of pH-induced changes in seawater carbonate chemistry. Physiol Plant. 2008;133:92–105.Article 
    CAS 

    Google Scholar 
    Brunson JK, McKinnie SMK, Chekan JR, McCrow JP, Miles ZD, Bertrand EM, et al. Biosynthesis of the neurotoxin domoic acid in a bloom-forming diatom. Science. 2018;361:1356–58.Article 
    CAS 

    Google Scholar 
    Boissonneault KR, Henningsen BM, Bates SS, Robertson DL, Milton S, Pelletier J, et al. Gene expression studies for the analysis of domoic acid production in the marine diatom Pseudo-nitzschia multiseries. BMC Mole Biol. 2013;14:1–19.
    Google Scholar 
    Pierrot DE, Lewis E, Wallace DWR MS Excel program developed for CO2 system calculations. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of. Energy, Oak Ridge, TN. 2006; Retrieved from https://doi.org/10.3334/CDIAC/otg.CO2SYS_XLS_CDIAC105a.Brzezinski MA, Nelson DM. The annual silica cycle in the Sargasso Sea near Bermuda. Deep-Sea Res Pt I Oceanogr Res Papers. 1995;42:1215–37.Article 
    CAS 

    Google Scholar 
    Schlüter L, Lohbeck KT, Gutowska MA, Gröger JP, Riebesell U, Reusch TBH. Adaptation of a globally important coccolithophore to ocean warming and acidification. Nat Clim Change. 2014;4:1024–30.Article 

    Google Scholar 
    Schaum CE, Barton S, Bestion E, Buckling A, Garcia-Carreras B, Lopez P, et al. Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis. Nat Ecol Evol. 2017;1:0094.Article 

    Google Scholar 
    Wang Z, Maucher-Fuquay J, Fire SE, Mikulski CM, Haynes B, Doucette GJ, et al. Optimization of solid-phase extraction and liquid chromatography–tandem mass spectrometry for the determination of domoic acid in seawater, phytoplankton, and mammalian fluids and tissues. Anal Chim Acta. 2012;715:71–9.Article 
    CAS 

    Google Scholar 
    Brandenburg KM, Velthuis M, Van de Waal DB. Meta-analysis reveals enhanced growth of marine harmful algae from temperate regions with warming and elevated CO2 levels. Glob Change Biol. 2019;25:2607–18.Article 

    Google Scholar 
    Wohlrab S, John U, Klemm K, Rberlein T, Grivogiannis AMF, Krock B, et al. Ocean acidification increases domoic acid contents during a spring to summer succession of coastal phytoplankton. Harmful Algae. 2020;92:101697.Article 
    CAS 

    Google Scholar 
    Zhong J, Guo Y, Liang Z, Huang Q, Lu H, Pan J, et al. Adaptation of a marine diatom to ocean acidification and warming reveals constraints and trade-offs. Sci Total Environ. 2021;771:145167.Article 
    CAS 

    Google Scholar 
    Trainer VL, Bates SS, Lundholm N, Thessen AE, Cochlan WP, Adams NG, et al. Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health. Harmful Algae. 2012;14:271–300.Article 

    Google Scholar 
    Zhu Z, Qu P, Gale J, Fu F, Hutchins DA. Individual and interactive effects of warming and CO2 on Pseudo-nitzschia subcurvata and Phaeocystis antarctica, two dominant phytoplankton from the Ross Sea, Antarctica. Biogeosciences. 2017;14:5281–95.Article 
    CAS 

    Google Scholar 
    Hutchins DA, Walworth NG, Webb EA, Saito MA, Moran D, McIlvin MR, et al. Irreversibly increased N2 fixation in Trichodesmium experimentally adapted to high CO2. Nat Commun. 2015;6:8155.Article 

    Google Scholar 
    Walworth NG, Lee MD, Fu FX, Hutchins DA, Webb EA. Molecular and physiological evidence of genetic assimilation to high CO2 in the marine nitrogen fixer Trichodesmium. P Natl Acad Sci. 2016;113:E7367–74.Article 
    CAS 

    Google Scholar 
    Schaum CE, Buckling A, Smirnoff N, Studholme DJ, Yvon-Durocher G. Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom. Nat Commun. 2018;9:1719.Article 

    Google Scholar 
    Hutchins DA, Capone DG. The ocean nitrogen cycle: New developments and global change. Nat Rev Microbiol. 2022;20:401–14.Article 
    CAS 

    Google Scholar 
    Xu D, Tong S, Wang B, Zhang X, Wang W, Zhang X, et al. Ocean acidification stimulation of phytoplankton growth depends on the extent of departure from the optimal growth temperature. Mar Pollut Bull. 2022;177:113510.Article 
    CAS 

    Google Scholar 
    Hennon GMM, Sefbom J, Schaum E, Dyhrman ST, Godhe A Studying the acclimation and adaptation of HAB species to changing environmental conditions. In: Wells ML, et al. (eds.). GlobalHAB. 2021. Guidelines for the Study of Climate Change Effects on HABs. Paris: UNESCO-IOC/SCOR, 2021. pp 64–78.Collins S, Bell G. Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature. 2004;431:566–9.Article 
    CAS 

    Google Scholar 
    Kremp A, Godhe A, Egardt J, Dupont S, Suikkanen S, Casabianca S, et al. Intraspecific variability in the response of bloom-forming marine microalgae to changed climate conditions. Ecol Evol. 2012;2:1195–207.Article 

    Google Scholar 
    Tatters AO, Schnetzer A, Fu F, Lie AY, Caron DA, Hutchins DA. Short‐versus long‐term responses to changing CO2 in a coastal dinoflagellate bloom: Implications for interspecific competitive interactions and community structure. Evolution. 2013;67:1879–91.Article 

    Google Scholar 
    Schaum CE, Collins S. Plasticity predicts evolution in a marine alga. P Roy Soc B-Biol Sci. 2014;281:20141486.
    Google Scholar 
    Moran XAG, Lopez-Urrutia Á, Calvo-Díaz A, Li WKW. Increasing importance of small phytoplankton in a warmer ocean. Glob Change Biol. 2010;16:1137–44.Article 

    Google Scholar 
    Thomas MK, Kremer CT, Klausmeier CA, Litchman EA. Global pattern of thermal adaptation in marine phytoplankton. Science. 2012;338:1085–88.Article 
    CAS 

    Google Scholar 
    Toseland ADSJ, Daines SJ, Clark JR, Kirkham A, Strauss J, Uhlig C, et al. The impact of temperature on marine phytoplankton resource allocation and metabolism. Nat Clim Change. 2013;3:979–84.Article 
    CAS 

    Google Scholar 
    Collins S. Many Possible Worlds: Expanding the Ecological Scenarios in Experimental Evolution. Evol Biol. 2011;38:3–14.Article 

    Google Scholar 
    Qu PP, Fu F, Wang XW, Kling JD, Elghazzawy M, Huh M, et al. Two co‐dominant nitrogen‐fixing cyanobacteria demonstrate distinct acclimation and adaptation responses to cope with ocean warming. Env Microbiol Rep. 2022;14:203–17.Article 
    CAS 

    Google Scholar 
    Lande R. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol. 2009;22:1435–46.Article 

    Google Scholar 
    Draghi J, Whitlock MC. Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution 2012;66:2891–902.Article 

    Google Scholar 
    Collins S, Rost B, Rynearson TA. Evolutionary potential of marine phytoplankton under ocean acidification. Evol Appl. 2014;7:140–55.Article 
    CAS 

    Google Scholar 
    Kim H, Spivack AJ, Menden-Deuer S. pH alters the swimming behaviors of the raphidophyte Heterosigma akashiwo: Implications for bloom formation in an acidified ocean. Harmful Algae. 2013;26:1–11.Article 
    CAS 

    Google Scholar 
    Hennon GMM, Quay P, Morales RL, Swanson LM, Armbrust EV. Acclimation conditions modify physiological response of the diatom Thalassiosira pseudonana to elevated CO2 concentrations in a nitrate-limited chemostat. J Phycol. 2014;50:243–53.Article 
    CAS 

    Google Scholar 
    Daufresne M, Lengfellner K, Sommer U. Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci. 2009;106:12788–93.Article 
    CAS 

    Google Scholar 
    Atkinson D, Ciotti BJ, Montagnes DJS. Protists decrease in size linearly with temperature: ca. 2.5% °C-1. Proc R Soc Lond B 2003;270:2605–11.Article 

    Google Scholar 
    Tong S, Gao K, Hutchins DA. Adaptive evolution in the coccolithophore Gephyrocapsa oceanica following 1,000 generations of selection under elevated CO2. Glob Chang Biol 2018;24:3055–64.Article 

    Google Scholar 
    Kelly KJ, Fu FX, Jiang X, Li H, Xu D, Yang N, et al. Interactions between ultraviolet B radiation, warming, and changing nitrogen source may reduce the accumulation of toxic Pseudo-nitzschia multiseries biomass in future coastal oceans. Front Mar Sci. 2021;8:433.Article 

    Google Scholar 
    Sterner R, Elser, J Ecological stoichiometry. In: Levin SA, et al. (eds) The Princeton Guide to Ecology. Princeton Univ. Press, 2009. pp 376–85.Petrou K, Baker KG, Nielsen DA, Hancock AM, Schulz KG, Davidson AT. Acidification diminishes diatom silica production in the Southern Ocean. Nat Clim Change 2019;9:781–86.Article 
    CAS 

    Google Scholar  More