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    Author Correction: Climate change reshuffles northern species within their niches

    These authors contributed equally: Laura H. Antão, Benjamin Weigel.These authors jointly supervised this work: Tomas Roslin, Anna-Liisa Laine.Research Centre for Ecological Change, Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, FinlandLaura H. Antão, Benjamin Weigel, Giovanni Strona, Maria Hällfors, Elina Kaarlejärvi, Otso Ovaskainen, Marjo Saastamoinen, Jarno Vanhatalo, Tomas Roslin & Anna-Liisa LaineDepartment of Biological Sciences, University of South Carolina, Columbia, SC, USATad DallasDepartment of Biology, Lund University, Lund, SwedenØystein H. OpedalFinnish Environment Institute (SYKE), Helsinki, FinlandJanne Heliölä, Mikko Kuussaari, Juha Pöyry & Kristiina VuorioNatural Resources Institute Finland (Luke), Helsinki, FinlandHeikki Henttonen, Otso Huitu, Andreas Lindén, Päivi Merilä, Maija Salemaa & Tiina TonteriSection of Ecology, Department of Biology, University of Turku, Turku, FinlandErkki KorpimäkiFinnish Museum of Natural History, University of Helsinki, Helsinki, FinlandAleksi LehikoinenKainuu Centre for Economic Development, Transport and the Environment, Kajaani, FinlandReima LeinonenUniversity of Helsinki, Helsinki, FinlandHannu PietiäinenDepartment of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, FinlandOtso OvaskainenCentre for Biodiversity Dynamics, Department of Biology, Norwegian University of Science and Technology, Trondheim, NorwayOtso OvaskainenHelsinki Institute of Life Science, University of Helsinki, Helsinki, FinlandMarjo SaastamoinenDepartment of Mathematics and Statistics, Faculty of Science, University of Helsinki, Helsinki, FinlandJarno VanhataloSpatial Foodweb Ecology Group, Department of Agricultural Sciences, University of Helsinki, Helsinki, FinlandTomas RoslinSpatial Foodweb Ecology Group, Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, SwedenTomas RoslinDepartment of Evolutionary Biology and Environmental Studies, University of Zürich, Zürich, SwitzerlandAnna-Liisa Laine More

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    Influence of urbanisation on phytodiversity and some soil properties in riverine wetlands of Bamenda municipality, Cameroon

    Description of the study areaThe study covers urban, peri-urban and rural wetlands in the Bamenda Municipality of the North West Region of Cameroon that have evolved concomitantly with different stages of urbanization (Fig. 1). In this study, urbanisation is considered a loose term that is aimed at giving a geographical expression to the variation in the economic, social and cultural practices in the milieu. The central town with many economic activities is termed the urban, the fringe area with sprawls is termed peri-urban while the rural has typical peasant activities and make-shift structures. From the variation of human activities in the three sub-zones, a variety of chemical substances are discharged into drains, playing a substantial role in soil quality, and therefore plant macrophyte diversity. The Plants studied were ubiquitous in the area and verification of their IUCN conservation status in the red data book of plants of Cameroon confirmed their abundance14. Information on protected sites in Cameroon does not place the study area under conservation status. In line with that, permits are not required to undertake academic and research studies as well as do a responsible collection of plants in the study area. The urbanization rate of Bamenda is 42%, and the population grew from 48,111 inhabitants in 1976 to 488,883 inhabitants in 201015, with 150–200 inhabitants/km2.Figure 1Relief Map of Bamenda showing the Bamenda escarpment, topography and the location for quadrat sites.Full size imageThe study area is part of the Bamenda escarpment that is located between latitudes 5° 55″ N and 6° 30″ N and longitudes 10° 25″ E and 10° 67″ E. The town shows an altitudinal range of 1200–1700 m and is divided into two parts by escarpments—a low-lying and gently undulating part with altitudes ranging from 1200 to 1400 m, with many flat areas that are usually inundated for most parts of the year, and an elevated part that range from 1400 to 1700 m altitude. Most of the streams take their rise from this elevated part (Fig. 1).This area experiences two seasons—a rainy season (mid-March to mid-October) and a short dry season (mid-October to mid-March). The thermic and hyperthermic temperature regimes dominate in the area. The mean annual temperature stands at 19.9 °C. January and February are the hottest months with mean monthly temperatures of 29.1 and 29.7 °C, respectively. This area is dominated by the Ustic and Udic moisture regimes with the Udic extending to the south9. Annual rainfall ranges from 1300 to 3000 mm16. The area has a rich hydrographical network with intense human activities and a dense population along different water courses in the watershed. The area is bounded on the West, North and East by the Cameroon Volcanic Line (made up of basalts, trachytes, rhyolites and numerous salt springs). The geologic history of this area originates from the Precambrian era when there was a vast formation of geosynclinal complexes, which became filled with clay-calcareous, and sandstone sediments9. These materials, crossed by intrusions of crystalline rocks, were folded in a generally NE-SW direction and underwent variable metamorphism9. The Rocks in the area are thus of igneous (granitic and volcanic) and metamorphic (migmatites) origin17, which gives rise to ferralitic soils18.Agriculture is the principal human activity in and around this region18. The area equally harbours the commercial center that has factories ranging from soap production, and mechanic workshops to metallurgy, which may be potential sources of pollutants that can influence wetland Geochemistry. Raffia farinifera bush, which is largely limited to the wetlands, is an important vegetation type in this area. R. farinifera provides raffia wine, a vital economic resource to the inhabitants who are fighting against the cultivation of these wetlands by vegetable farmers.Methods of the studyMacrophyte diversity studyThe plant diversity of the wetlands was evaluated using quadrats in the dry season for accessibility reasons. For each of the three wetlands (the urban, peri-urban and rural areas), three transects were established on which representative quadrats, each measuring 10 m × 10 m, were mapped out in uncultivated areas for the determination of plant species cover-abundance and diversity. It is perceived that the different zones receive different mixtures of chemical substances and thus influence macrophyte diversity differently.According to a publication by14 on the vascular plants of Cameroon and a taxonomic checklist with IUCN assessment, the plants of the area are placed under the Least Concern Category(LC), and therefore not in the risky category. Diversity studies involved the identification of a specific area called “relevé” by progressively increasing test quadrat size and sampling for specific diversity until the smallest area with adequate species representation was reached. The relevé size determined here was 1 m2, making a total of 300 sub-quadrats (relevé) in the entire study ie. 100 in each main quadrat). For each site (main quadrat), 10 representative relevés were sampled and all plant species were enumerated. Most plant species in each of them were identified in the field by the Botanist, Dr Ndam Lawrence Monah using visual observation of the morphology of the leaves and flowers, a self-made field guide, the Flora of West Africa and the Flora of Cameroon. 10 unidentified plants were appropriately collected where there were in abundance, placed onto a conventional plant press and dried in the field. Voucher specimens were tagged and transported to the Limbe Botanic Gardens (SCA: Southern Cameroon, the code of the Limbe Botanic Gardens Herbarium) for identification. Mr Elias Ndive, the Taxonomist of the Limbe Botanic Gardens compared unidentified specimens with authentic herbarium specimens and other taxonomic guides and finally identified them. Voucher specimens of the 10 plants were given identification numbers and deposited in the Herbarium of the Limbe Botanic Gardens.The Braun–Banquet method was used19 for the assessment of species cover abundance. Relative abundance and abundance ratings were determined using the Braun–Banquet rating scheme (Table 1).Table 1 Braun-Blanquet rating scheme for vegetation cover-abundance, Source19.Full size tableSimpson’s diversity indexSpecies richness was evaluated using Simpson’s diversity index (D), which takes into account both species richness and the Braun-Blanquet rating scheme for vegetation cover abundance and evenness of abundance among the species present. In essence, D measures the probability that two individuals that are randomly selected from an area will belong to the same species. The formula for calculating D is presented as:$${text{D}} = frac{{sum {{text{n}}_{i} left( {{text{n}}_{i} – 1} right)} }}{{{text{N}}({text{N}} – 1)}}$$where ni = the total number of each species; N = the total number of individuals of all species.The value of D ranges from 0 to 1. With this index, 0 represents infinite diversity and 1 represents no diversity. That is, the larger the value the lower the diversity.Alternatively, Simpson’s Diversity Index, = 1–D,1-D was used as a measure of diversity because it is more logical and less likely to cause confusion. The scale then gives a score from 0 to 1 with higher scores showing higher diversity (instead of being associated with low scores).The Simpson index is a dominance index because it gives more weight to common or dominant species. In this case, a few rare species with only a few representatives will not affect the diversity.
    Soil sampling and analysisSoil sampling was done in and around the three quadrats laid in the urban, peri-urban and rural wetlands for macrophytes sampling. Twenty-one (21) composite samples (0–25 cm) were randomly collected (Fig. 2) and taken to the laboratory in black plastic bags. Each composite sample was a collection of 5 dried core soil samples. Due to the observed greater heterogeneity in the urban sector, the sampling density was intensified. The soil samples were air-dried and screened through a 2-mm sieve. They were analyzed in duplicate for their physicochemical properties in the Environmental and Analytical Chemistry Laboratory of the University of Dschang, Cameroon. Particle size distribution, cation exchange capacity (CEC), exchangeable bases, electrical conductivity (EC) and pH were determined by standard procedures20. Soil pH was measured both in water and KCl (1:2.5 soil/water mixture) using a glass electrode pH meter. Part of the soil was ball-milled for organic carbon (Walkley–Black method) and total nitrogen (Macro-Kjeldahl method) as largely described by20. Available phosphorus (P) was determined by Bray I method. Exchangeable cations were extracted using 1 N ammonium acetate at pH 7. Potassium (K) and sodium (Na) in the extract were determined using a flame photometer and magnesium (Mg) and calcium (Ca) were determined by complexiometric titration. Exchange acidity was extracted with 1 M KCl followed by quantification of Al and H by titration20. Effective cation exchange capacity (ECEC) was determined as the sum of bases and exchanged acidity.Figure 2Adapted from the 1980 land use map of the Bamenda City Area showing soil sampling points: Source Bamenda City Council.Map of the study area in freshwater wetlands of Bamenda Municipality.Full size imageApparent CEC (CEC at pH 7) was determined directly as outlined by20. Based on critical values of nutrients established for vegetables, nutrients were declared sufficient or deficient.
    Statistical analysisThe data were subjected to statistical analysis using Microsoft Excel 2007 and SPSS statistical package 20.0. Soil properties were assessed for their variability using the coefficient of variation (CV) and compared with variability classes (Table 2).$$CV=frac{Sd}{X}X 100$$where: Sd = standard deviation; = X arithmetic mean of soil properties.Table 2 Grouping coefficient of variation into variability classes.Full size tableThe hierarchical cluster analysis (HCA) was used to group the area under managing units. The main goal of the hierarchical agglomerative cluster analysis is to spontaneously classify the data into groups of similarity (clusters). This is done by searching objects in the n-dimensional space that is located in the closest neighborhood and separating a stable cluster from other clusters. The sampling sites were considered objects for classification. Each object was determined by a set of variables (chemical concentrations of the soils in this case). More

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    High-yield dairy cattle breeds improve farmer incomes, curtail greenhouse gas emissions and reduce dairy import dependency in Tanzania

    Meat, Milk and More: Policy Innovations to Shepherd Inclusive and Sustainable Livestock Systems in Africa (Malabo Montpellier Panel, 2020).Value of Agricultural Production (FAO, accessed August 25, 2022); https://www.fao.org/faostat/en/#data/QVJayne, T. & Sanchez, P. A. Agricultural productivity must improve in sub-Saharan Africa. Science 372, 1045–1047 (2021).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Dangal, S. R. S. et al. Methane emission from global livestock sector during 1890–2014: magnitude, trends and spatiotemporal patterns. Glob. Change Biol. 23, 4147–4161 (2017).Article 
    ADS 

    Google Scholar 
    Mottet, A. et al. Climate change mitigation and productivity gains in livestock supply chains: insights from regional case studies. Reg. Env. Change 17, 129–141 (2016).Article 

    Google Scholar 
    Valin, H. et al. Agricultural productivity and greenhouse gas emissions: trade-offs or synergies between mitigation and food security? Environ. Res. Lett. 8, 035019 (2013).Article 
    ADS 
    CAS 

    Google Scholar 
    González-Quintero, R. et al. Yield gap analysis to identify attainable milk and meat productivities and the potential for greenhouse gas emissions mitigation in cattle systems of Colombia. Agric. Syst. 195, 103303 (2022).Article 

    Google Scholar 
    Crops and Livestock Products (FAO, accessed August 17,2022); https://www.fao.org/faostat/en/#data/QCLLedo, J. et al. Persistent challenges in safety and hygiene control practices in emerging dairy chains: the case of Tanzania. Food Control 105, 164–173 (2019).Article 

    Google Scholar 
    Häsler, B. et al. Integrated food safety and nutrition assessments in the dairy cattle value chain in Tanzania. Glob. Food Sec. 18, 102–113 (2018).Article 

    Google Scholar 
    Supply Utilization Accounts (FAO, accessed August 26, 2022); https://www.fao.org/faostat/en/#data/SCLMichael, S. et al. Tanzania Livestock Master Plan (International Livestock Research Institute, 2018).Tanzania Livestock Sector Analysis (2016/2017–2030/2031) (United Republic of Tanzania Ministry of Livestock and Fisheries, 2017); https://www.mifugouvuvi.go.tz/uploads/projects/1553602287-LIVESTOCK%20SECTOR%20ANALYSIS.pdfNicholson, C. et al. Assessment of Investment Priorities for Tanzania’s Dairy Sector: Report on Activities and Accomplishments (International Livestock Research Institute, 2021).Chagunda, M. G. C., Romer, D. A. M. & Roberts, D. J. Effect of genotype and feeding regime on enteric methane, non-milk nitrogen and performance of dairy cows during the winter feeding period. Livest. Sci. 122, 323–332 (2009).Article 

    Google Scholar 
    Notenbaert, A. et al. Towards environmentally sound intensification pathways for dairy development in the Tanga region of Tanzania. Reg. Environ. Change 20, 138 (2020).Yesuf, G. A. et al. Embedding stakeholders’ priorities into the low-emission development of the East African dairy sector. Env. Res. Lett. 16, 064032 (2021).Article 
    CAS 

    Google Scholar 
    GLS (Greening Livestock Survey) (International Livestock Research Institute, 2019); https://data.ilri.org/portal/dataset/greeninglivestockIntended Nationally Determined Contributions (United Republic of Tanzania, 2021); https://unfccc.int/sites/default/files/NDC/2022-06/TANZANIA_NDC_SUBMISSION_30%20JULY%202021.pdfNdung’u, P. W. et al. Farm-level emission intensities of smallholder cattle (Bos indicus; B. indicus–B. taurus crosses) production systems in highlands and semi-arid regions. Animal 16, 100445 (2022).Article 
    PubMed 

    Google Scholar 
    Goopy, J. P. et al. Severe below-maintenance feed intake increases methane yield from enteric fermentation in cattle. Br. J. Nutr. 123, 1239–1246 (2020).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Goopy, J. P. et al. A new approach for improving emission factors for enteric methane emissions of cattle in smallholder systems of East Africa—results for Nyando, Western Kenya. Agric. Syst. 161, 72–80 (2018).Article 

    Google Scholar 
    Supporting Low Emissions Development in the Tanzanian Dairy Cattle Sector—Reducing Enteric Methane for Food Security and Livelihoods (FAO, 2019).Gerssen-Gondelach, S. J. et al. Intensification pathways for beef and dairy cattle production systems: impacts on GHG emissions, land occupation and land use change. Agric. Ecosyst. Environ. 240, 135–147 (2017).Article 

    Google Scholar 
    Havlik, P. et al. Climate change mitigation through livestock system transitions. Proc. Natl Acad. Sci. USA 111, 3709–3714 (2014).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Herrero, M. et al. Greenhouse gas mitigation potentials in the livestock sector. Nat. Clim. Change 6, 452–461 (2016).Article 
    ADS 

    Google Scholar 
    Dizyee, K., Baker, D. & Omore, A. Upgrading the smallholder dairy value chain: a system dynamics ex-ante impact assessment in Tanzania’s Kilosa district. J. Dairy Res. 86, 440–449 (2019).Article 
    CAS 
    PubMed 

    Google Scholar 
    Simões, A. R. P., Nicholson, C. F., Novakovicc, A. M. & Protil, R. M. Dynamic impacts of farm-level technology adoption on the Brazilian dairy supply chain. Int. Food Agribus. Manag. Rev. 23, 71–84 (2020).Article 

    Google Scholar 
    Rahimi, J. et al. Heat stress will detrimentally impact future livestock production in East Africa. Nat. Food. 2, 88–96 (2021).Article 

    Google Scholar 
    Mbululo, Y. & Nyihirani, F. Climate characteristics over southern highlands Tanzania. Atmos. Clim. Sci. 2, 454–463 (2012).
    Google Scholar 
    Kihoro, E. M., Schoneveld, G. C. & Crane, T. A. Pathways toward inclusive low-emission dairy development in Tanzania: producer heterogeneity and implications for intervention design. Agric. Syst. 190, 103073 (2021).Mruttu, H. et al. Animal Genetics Strategy and Vision for Tanzania (Tanzania Ministry of Agriculture, Livestock and Fisheries and ILRI, 2016).Agricultural Sample Survey 2018/19 Report on Livestock and Livestock Characteristics (Private Peasant Holdings) (Central Statistical Agency, 2019).2019/20 National Sample Census of Agriculture Main Report (Tanzania National Bureau of Statistics, 2022).Robinson, T. P. et al. Global Livestock Production Systems (FAO, 2011).Herrero, M. et al. Biomass use, production, feed efficiencies and greenhouse gas emissions from global livestock systems. Proc. Natl Acad. Sci. USA 110, 20888–20893 (2013).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Baseline Study of the Tanzania Dairy Value Chain (United Republic of Tanzania Ministry of Agriculture, Livestock and Fisheries, 2016).Mbwambo, N., Nandonde, S., Ndomba, C. & Desta, S. Assessment of Animal Feed Resources in Tanzania (Tanzania Ministry of Agriculture, Livestock and Fisheries and ILRI, 2016).Hartung, C., Lerer, A., Anokwa, Y., Tseng, C., Brunette, W., & Borriello, G. Open data kit: tools to build information services for developing regions. Proc. 4th ACM/IEEE International Conference on Information and Communication Technologies and Development (Association for Computing Machinery, 2010).R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2022).https://www.r-project.orgRufino, M. C. et al. Lifetime productivity of dairy cows in smallholder farming systems of the central highlands of Kenya. Animal 3, 1044–1056 (2009).Article 
    CAS 
    PubMed 

    Google Scholar 
    Hawkins, J. et al. Feeding efficiency gains can increase the greenhouse gas mitigation potential of the Tanzanian dairy sector. Sci. Rep. 11, 4190 (2021).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Python Software Foundation (Python Software Foundation, 2019); https://www.python.org/psf/Kashoma, I. P. B. et al. Predicting body weight of Tanzania shorthorn zebu cattle using heart girth measurements. Livest. Res. Rural. Dev. 23, Table 1 (2011).Galukande, E. B., Mahadevan, P. & Black, J. G. Milk production in East African zebu cattle. Anim. Sci. 4, 329–336 (1962).Article 

    Google Scholar 
    Gillah, K. A., Kifaro, G. C. & Madsen, J. Effects of pre partum supplementation on milk yield, reproduction and milk quality of crossbred dairy cows raised in a peri urban farm of Morogoro town Tanzania. Livest. Res. Rural. Dev. 26 (2014).Njau, F. B. C., Lwelamira, J. & Hyandye, C. Ruminant livestock production and quality of pastures in the communal grazing land of semi-arid central Tanzania. Livest. Res. Rural. Dev. 8, Table 4 (2013).Mwambene, P. L. et al. Selecting indigenous cattle populations for improving dairy production in the Southern Highlands and Eastern Tanzania. Livest. Res. Rural. Dev. 26 (2014).Rege, J. E. O. et al. Cattle of Kenya: Uses, Performance, Farmer Preferences, Measures of Genetic Diversity and Options for Improved Use (International Livestock Research Institute, 2001).Beffa, L. M. Genotype × Environment Interaction in Afrikaner Cattle. PhD thesis, Univ. of the Free State (2005).Meaker, H. J., Coetsee, T. P. N. & Lishman, A. W. The effects of age at 1st calving on the productive and reproductive-performance of beef-cows. S. Afr. J. Anim. Sci. 10, 105–113 (1980).
    Google Scholar 
    Chenyambuga, S. W. & Mseleko, K. F. Reproductive and lactation performances of Ayrshire and Boran crossbred cattle kept in smallholder farms in Mufindi district, Tanzania. Livest. Res. Rural. Dev. 21, 100 (2009).
    Google Scholar 
    Ojango, J. M. K. et al. Dairy production systems and the adoption of genetic and breeding technologies in Tanzania, Kenya, India and Nicaragua. Anim. Genet. Resour. 59, 81–95 (2016).Article 

    Google Scholar 
    Feedipedia—Animal Feed Resources Information System (FAO, accessed 2021); https://www.feedipedia.org/Lukuyu, B. et al. (eds) Feeding Dairy Cattle in East Africa (East Africa Dairy Development Project, 2012).Rubanza, C. D. K. et al. Biomass production and nutritive potential of conserved forages in silvopastoral traditional fodder banks (Ngitiri) of Meatu District of Tanzania. Asian-Aust. J. Anim. Sci. 19, 978–983 (2006).Article 

    Google Scholar 
    Food Balances (2010-) (FAO, accessed September 29, 2021); http://www.fao.org/faostat/en/#data/FBSCrop Data for the United Republic of Tanzania (FAO, accessed September 22, 2021); http://www.fao.org/faost at/en/#data/QCGilbert, M. et al. Global distribution data for cattle, buffaloes, horses, sheep, goats, pigs, chickens and ducks in 2010. Sci. Data. 5, 180227 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    2014/15 Annual Agricultural Sample Survey Report (The United Republic of Tanzania, 2016).Basic Data for Livestock and Fisheries (The United Republic of Tanzania Ministry of Livestock and Fisheries, 2013).IPCC Guidelines for National Greenhouse Gas Inventories Vol. 4 Agriculture, Forestry and Other Land Use (IPCC, 2006).2019 Refinement to the IPCC Climate Change 2014: Synthesis Report (eds Core Writing Team, Pachauri, R. K. & Meyer L. A.) (IPCC, 2019).Fertilizers by Nutrient (FAO, accessed July 6, 2022); https://www.fao.org/faostat/en/#data/RFNHutton, M. O. et al. Toward a nitrogen footprint calculator for Tanzania. Env. Res. Lett. 12, 034016 (2017).Article 

    Google Scholar 
    Tanzania Fertilizer Assessment (International Fertilizer Development Center, 2012); http://tanzania.countrystat.org/fileadmin/user_upload/countrystat_fenix/congo/docs/Tanzania%20Fertilizer%20Assessment%202012.pdfA Common Carbon Footprint Approach for the Dairy Sector: The IDF Guide to Standard Life Cycle Methodology (International Dairy Federation, 2015); https://www.fil-idf.org/wp-content/uploads/2016/09/Bulletin479-2015_A-common-carbon-footprint-approach-for-the-dairy-sector.CAT.pdfBruzzone, L., Bovolo, F. & Arino, O. European Space Agency land cover climate change initiative. ESA LC CCI data: high resolution land cover data via Centre for Environmental Data Analysis; https://climate.esa.int/en/projects/high-resolution-land-cover/ (2021)Characteristics of Markets for Animal Feeds Raw Materials in the East African Community: Focus on Maize Bran and Sunflower Seed Cake (Kilimo Trust, 2017).Ngunga, D. & Mwendia, S. Forage Seed System in Tanzania: A Review Report (Alliance of Biodiversity and CIAT, 2020).Nkombe, B.M. Investigation of the Potential for Forage Species to Enhance the Sustainability of Degraded Rangeland and Cropland Soils. MSc thesis, Ohio State Univ. (2016).Producer Prices (FAO, accessed 2021); http://www.fao.org/faostat/en/#data/PP More

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    Tidal effects on periodical variations in the occurrence of singing humpback whales in coastal waters of Chichijima Island, Ogasawara, Japan

    Morrison, M. A., Francis, M. P., Hartill, B. W. & Parkinson, D. M. Diurnal and tidal variation in the abundance of the fish fauna of a temperate tidal mudflat. Estuar. Coast. Shelf Sci. 54, 793–807 (2002).Article 
    ADS 

    Google Scholar 
    Ribeiro, J. et al. Seasonal, tidal and diurnal changes in fish assemblages in the Ria Formosa lagoon (Portugal). Estuar. Coast. Shelf Sci. 67, 461–474 (2006).Article 
    ADS 

    Google Scholar 
    Takemura, A., Rahman, M. S. & Park, Y. J. External and internal controls of lunar-related reproductive rhythms in fishes. J. Fish Biol. 76, 7–26 (2010).Article 
    CAS 
    PubMed 

    Google Scholar 
    Mendes, S., Turrell, W., Lütkebohle, T. & Thompson, P. Influence of the tidal cycle and a tidal intrusion front on the spatio-temporal distribution of coastal bottlenose dolphins. Mar. Ecol. Prog. Ser. 239, 221–229 (2002).Article 
    ADS 

    Google Scholar 
    Johnston, D. W., Thorne, L. H. & Read, A. J. Fin whales Balaenoptera physalus and minke whales Balaenoptera acutorostrata exploit a tidally driven island wake ecosystem in the Bay of Fundy. Mar. Ecol. Prog. Ser. 305, 287–295 (2005).Article 
    ADS 

    Google Scholar 
    Ichikawa, K. et al. Dugong (Dugong dugon) vocalization patterns recorded by automatic underwater sound monitoring systems. J. Acoust. Soc. Am. 119, 3726–3733 (2006).Article 
    ADS 
    PubMed 

    Google Scholar 
    Akamatsu, T. et al. Seasonal and diurnal presence of finless porpoises at a corridor to the ocean from their habitat. Mar. Biol. 157, 1879–1887 (2010).Article 

    Google Scholar 
    Li, S. et al. Seasonal, lunar and tidal influences on habitat use of indo-pacific humpback dolphins in Beibu gulf, China. Zool. Stud. https://doi.org/10.6620/ZS.2018.57-01 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zamon, J. E. Seal predation on salmon and forage fish schools as a function of tidal currents in the San Juan Islands, Washington, USA. Fish. Oceanogr. 10, 353–366 (2001).Article 

    Google Scholar 
    Van Parijs, S. M., Hastie, G. D. & Thompson, P. M. Geographical variation in temporal and spatial vocalization patterns of male harbour seals in the mating season. Anim. Behav. 58, 1231–1239 (1999).Article 
    PubMed 

    Google Scholar 
    Bortolotto, G. A., Danilewicz, D., Hammond, P. S., Thomas, L. & Zerbini, A. N. Whale distribution in a breeding area: Spatial models of habitat use and abundance of western South Atlantic humpback whales. Mar. Ecol. Prog. Ser. 585, 213–227 (2017).Article 
    ADS 

    Google Scholar 
    Johnson, J. H. & Wolman, A. A. The humpback whale, Megaptera novaeangliae. Mar. Fish. Rev. 46, 30–37 (1984).
    Google Scholar 
    Kobayashi, N. et al. Spatial distribution and habitat use patterns of humpback whales in Okinawa, Japan. Mammal Study 41, 207–214 (2016).Article 

    Google Scholar 
    Mori, K., Sata, F., Yamaguchi, M., Suganuma, H. & Ueyanagi, S. Distribution, migration and local movements of humpback whale (Megaptera novaeangliae) in the adjacent waters of the Ogasawara (Bonin) Islands Japan. J. Fac. Mar. Sci. Technol. Tokai Univ. 45, 197–213 (1998).
    Google Scholar 
    Rasmussen, K., Calambokidis, J. & Steiger, G. H. Distribution and migratory destinations of humpback whales off the Pacific coast of Central America during the boreal winters of 1996–2003. Mar. Mammal Sci. 28, 1–13 (2012).Article 

    Google Scholar 
    Calambokidis, J. et al. SPLASH: structure of populations, levels of abuncance and status of humpback whales in the North Pacific. Final report for Contract AB133F-03-RP-00078, to U.S. Dept. of Comm. Western Administrative Center, Seattle, WA. https://cascadiaresearch.org/files/SPLASH-contract-Report-May08.pdf (2008).Hill, M. et al. Found: A missing breeding ground for endangered western North Pacific humpback whales in the Mariana Archipelago. Endanger. Species Res. 41, 91–103 (2020).Article 

    Google Scholar 
    Payne, R. S. & McVay, S. Songs of humpback whales. Science 173, 585–597 (1971).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Winn, H. E. & Winn, L. The song of the humpback whale Megaptera novaeangliae in the West Indies. Mar. Biol. 47, 97–114 (1978).Article 

    Google Scholar 
    Tyack, P. Interactions between singing Hawaiian humpback whales and conspecifics nearby. Behav. Ecol. Sociobiol. 8, 105–116 (1981).Article 

    Google Scholar 
    Herman, L. M. The multiple functions of male song within the humpback whale (Megaptera novaeangliae) mating system: Review, evaluation, and synthesis. Biol. Rev. 92, 1795–1818 (2017).Article 
    PubMed 

    Google Scholar 
    Au, W. W. L., Mobley, J., Burgess, W. C., Lammers, M. O. & Nachtigall, P. E. Seasonal and diurnal trends of chorusing humpback whales wintering in waters off western Maui. Mar. Mammal Sci. 16, 530–544 (2000).Article 

    Google Scholar 
    Cerchio, S., Collins, T., Strindberg, S., Bennett, C. & Rosenbaum, H. Humpback whale singing activity off northern Angola: An indication of the migratory cycle, breeding habitat and impact of seismic surveys on singer number in Breeding. Int. Whal. Comm. P. SC/62/SH12 (2010).Kobayashi, N., Okabe, H., Higashi, N., Miyahara, H. & Uchida, S. Diel patterns in singing activity of humpback whales in a winter breeding area in Okinawan (Ryukyuan) waters. Mar. Mammal Sci. 37, 982–992 (2021).Article 

    Google Scholar 
    Munger, L. M., Lammers, M. O., Fisher-Pool, P. & Wong, K. Humpback whale (Megaptera novaeangliae) song occurrence at American Samoa in long-term passive acoustic recordings, 2008–2009. J. Acoust. Soc. Am. 132, 2265–2272 (2012).Article 
    ADS 
    PubMed 

    Google Scholar 
    Barlow, D. R., Fournet, M. & Sharpe, F. Incorporating tides into the acoustic ecology of humpback whales. Mar. Mammal Sci. 35, 234–251 (2019).Article 

    Google Scholar 
    Chenoweth, E., Gabriele, C. & Hill, D. Tidal influences on humpback whale habitat selection near headlands. Mar. Ecol. Prog. Ser. 423, 279–289 (2011).Article 
    ADS 

    Google Scholar 
    Sousa-Lima, R. S., Clark, C. W. & Road, S. W. Modeling the effect of boat traffic on singing activity of humpback whales (Megaptera novaeangliae) in the abrolhos national marine park, Brazil. Can. Acoust 36, 174–181 (2008).
    Google Scholar 
    Cerchio, S., Strindberg, S., Collins, T., Bennett, C. & Rosenbaum, H. Seismic surveys negatively affect humpback whale singing activity off Northern Angola. PLoS ONE 9, e86464. https://doi.org/10.1371/journal.pone.0086464 (2014).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Darling, J. D. & Mori, K. Recent observations of humpback whales (Megaptera novaeangliae) in Japanese waters off Ogasawara and Okinawa. Can. J. Zool. 71, 325–333 (1993).Article 

    Google Scholar 
    Calambokidis, J. et al. Movements and population structure of humpback whales in the North Pacific. Mar. Mammal Sci. 17, 769–794 (2001).Article 

    Google Scholar 
    Wessel, P., Smith, W. H. F., Scharroo, R., Luis, J. & Wobbe, F. Generic mapping tools: Improved version released. Eos Trans. Am. Geophys. Union 94, 409–410 (2013).Article 
    ADS 

    Google Scholar 
    Helweg, D. A. & Herman, L. M. Diurnal patterns of behaviour and group membership of humpback whales (Megaptera novaeangliae) wintering in Hawaiian waters. Ethology 98, 298–311 (1994).Article 

    Google Scholar 
    Darling, J. D. & Berube, M. Interactions of singing humpback whales with other males. Mar. Mammal Sci. 17, 570–584 (2001).Article 

    Google Scholar 
    Whitlow, W. L. et al. Acoustic properties of humpback whale songs. J. Acoust. Soc. Am. 120, 1103–1110 (2006).Article 

    Google Scholar 
    Japan Coast Guard. Sailing Directions for South and East Coasts of Honshu. (1981).Tsujii, K. et al. Change in singing behavior of humpback whales caused by shipping noise. PLoS ONE 13, e0204112. https://doi.org/10.1371/journal.pone.0204112 (2018).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ryan, J. P. et al. Humpback whale song occurrence reflects ecosystem variability in feeding and migratory habitat of the northeast Pacific. PLoS ONE 14, e0222456. https://doi.org/10.1371/journal.pone.0222456 (2019).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing. 4.0.0 version. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ (2020).Wood, S.N. Generalized Additive Models: An Introduction with R 2nd edn, (Chapman and Hall/CRC, 2017). More

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    The control of malaria vectors in rice fields: a systematic review and meta-analysis

    We investigated whether ricefield mosquito larval control and/or rice cultivation practices are associated with malaria vector densities through a systematic review and meta-analysis. Forty-seven experimental studies were eligible for inclusion in the qualitative analysis and thirty-three studies were eligible for the meta-analysis. It was demonstrated that the use of fish, chemical and biological larvicides in rice fields were effective in controlling larval malaria vector densities at all developmental stages. Intermittent irrigation, however, could only significantly reduce late-stage larvae. Based on a limited number of studies, meta-analyses on other forms of larval control such as monomolecular surface films (MSFs), neem, copepods and Azolla failed to demonstrate any consistent reduction in anopheline numbers. Similarly, rice cultivation practices such as plant variety and density, type of levelling and pesticide application were not generally associated with reduced malaria vectors. Nonetheless, in one study, minimal tillage was observed to reduce average numbers of larvae throughout a cropping season. In another study, herbicide application increased larval abundance over a 4-week period, as did one-time drainage in a third study.
    Despite their different modes of action, the use of chemical and bacterial larvicides and MSFs were all relatively effective measures of larval control in rice fields, varying between a 57% to 76% reduction in vector abundance compared to no larviciding. Their effects were highest (often reaching 100% reduction) only shortly following application but did not persist for longer than two weeks. These larvicides mostly had short residual half-lives because they were applied to paddy water which was naturally not completely stagnant: there was a small but constant process of water loss (through drainage, evapotranspiration and percolation) and replacement through irrigation. Hence, even with a residual formulation, weekly re-application would be needed for sustained control47,40,41,50. This would be very labour- and cost-intensive to scale-up, to ensure that larvicides are evenly distributed across vast areas (even at plot/sub-plot level) throughout at least one 5-month long rice-growing season per year42,51. Aerial application (including unmanned aerial vehicles), although widely used in the US and Europe, is unlikely to be a feasible delivery system for smallholders in SSA, even in large irrigation schemes26,27,48,49. Furthermore, if synthetic organic chemicals were to be considered for riceland malaria vector control, their management in the current landscape of insecticide resistance across Africa must be considered.Biological control using fish was found to be, in general, slightly more effective than (chemical, bacterial and MSF) larviciding. The degree of effectiveness was dependent on the fish species and their feeding preferences: surface-feeding, larvivorous species provided better anopheline control than bottom-feeding selective feeders4,43. Selecting the most suitable fish for local rice fields is not straightforward; many criteria need to be considered4,52,53. Generally, fish were well-received by rice farmers, perceived to contribute to increased yield by reducing weeds and pests and providing fertiliser through excrement43,44. This was reportedly also observed in Guangxi, China, where a certain proportion of the field had to be deepened into a side-trench where the fish could take shelter when the fields were drained. Even with this reduction in rice production area, carp rearing still increased yields by 10% and farmer’s income per hectare by 70%53. Unfortunately, none of the eligible studies in this review had included yield or water use as an outcome. Future entomological studies need to measure these critical agronomic variables so that studies of vector control in rice can be understood by, and transferred to, agronomists. In SSA, irrigated rice-fish farming can be scaled up provided that an inventory of fish species suitable for specific locations is available and that water is consistently available in fields (an important limiting factor in African irrigation schemes)54. Lessons can be learnt from successful large-scale rice-fish systems in Asia, where they have served as win–win solutions for sustainable food production and malaria control16,55.Overall, there was only limited evidence that intermittent irrigation is effective at reducing late-instar anopheline larvae in rice fields. This finding contrasts with prior reviews, which found mixed results (regardless of larval stage) but emphasised that success was site-specific4,17,56. This contrast is presumably due to the inclusion criteria of our systematic review. These reviews excluded studies in various geographical settings and some older studies that reported successful anopheline control with intermittent irrigation but lacked either a contemporaneous control arm, adequate replication or adequate differentiation between culicines and anophelines16,57,50,51,52,61. It seems, from our review, that intermittent irrigation does not prevent the recruitment of early instars (and in one case, may have encouraged oviposition31) but tends to prevent their development into late-stage immatures. This important conclusion is, however, based only on four studies; more evidence is urgently needed where future trials should consider the basic principles of modern trials with adequate replication, controls and differentiation between larval instars and species.Generally, it is observed that drainage, passive or active, did not reliably reduce overall numbers of mosquito immatures. In India and Kenya, closer inspection revealed that soils were not drying sufficiently, so any stranded larvae were not killed31,46. Highlighted by van der Hoek et al.29 and Keiser et al.17, water management in rice fields is very dependent on the physical characteristics of the soil and the climate and is most suited to places that not only favour rapid drying, but also have a good control of water supply17,56. Moreover, repeated drainage, although directed against mosquitoes, can also kill their aquatic predators62. Since mosquitoes can re-establish themselves in a newly flooded rice field more quickly than their predators, intermittent irrigation with more than a week between successive drying periods can permit repeated cycles of mosquito breeding without any predation pressure. Its efficacy against malaria vectors is therefore highly reliant on the timing of the wetting and drying periods. Further site-specific research on timing, especially with regards to predator–prey interactions within the rice agroecosystem, is required to find the perfect balance.Another limitation in intermittent irrigation is that it cannot be applied during the first two to three weeks following transplanting, because rice plants must remain flooded to recover from transplanting shock. Unfortunately, this time coincides with peak vector breeding. Thus, other methods of larval control would be required to fill this gap. To agronomists, intermittent irrigation provides benefits to farmers, as it does not penalise yield but significantly reduces water consumption. Nonetheless, farmer compliance seems to be variable, especially in areas where water availability is inconsistent and intermittent irrigation would potentially require more labour31,32,39. Importantly, rice farmers doubted their ability to coordinate water distribution evenly amongst themselves, suggesting that there may be sharing issues, as in the “tragedy of the commons”63. Instead, they said that they preferred to have an agreed authority to regulate water46.No general conclusions could be made on the effect on malaria vectors of other rice cultivation practices (apart from water management) because only one study was eligible for each practice. Nevertheless, these experiments on pesticide application, tillage and weed control, as well as another study on plant spacing (not eligible since glass rods were used to simulate rice plants), do illustrate that small changes in agronomic inputs and conditions can have considerable effects on mosquito densities, not just rice yield36,38,64. Moreover, in partially- or shallowly-flooded plots, the larvae are often concentrated in depressions (usually footprints), suggesting that rice operations which leave or remove footprints (e.g. hand-weeding, drum seeders, levelling) will influence vector breeding4.Our study has some important limitations. First, in most trials, the units of intervention were replicate plots of rice, and success was measured as a reduction in larval densities within treated plots. This design focuses on the identification of effective and easy-to-implement ways of growing rice without growing mosquitoes, on the assumption that higher vector densities are harmful. However, from a public health perspective, the need for epidemiological outcomes is often, and reasonably, stressed22,65. Nonetheless, from a farmers’ perspective, it is also important to consider whether the vectors emerging from their rice fields significantly contribute to the local burden of malaria and to determine how this contribution can be minimised. There is evidence that riceland vectors do increase malaria transmission, since human biting rates are much higher in communities living next to rice schemes than their non-rice counterparts66 and that additional riceland vectors may intensify transmission and malaria prevalence in rice communities15. Hence, when investigating how rice-attributed malaria risk can be minimised, mosquito abundance as measured in the experimental rice trials is a useful indicator of potential impact on epidemiological outcomes.Second, larval density was not always separated into larval developmental stages. This can be misleading because some interventions work by reducing larval survival (but not by preventing oviposition) and development to late instars and pupae. Therefore, an intervention could completely eliminate late-stage larvae and pupae but have little effect on the total number of immatures. This was illustrated in our meta-analyses of intermittent irrigation in Table 3 and Supplementary Table 5, and could have been the case for some studies that failed to demonstrate consistent reductions in overall anopheline numbers but did not differentiate between larval instars34,45,67,60,69. We infer that when monitoring mosquito immatures in rice trials, it is important to distinguish between larval instars and pupae. Pupae should always be counted separately since its abundance is the most direct indicator of adult productivity70.Third, experimental trials rarely reported the timing of intervention application or accounted for different rice-growing phases, or “days after transplantation”, in the outcome. Both aspects are important to consider since an intervention may be suited to control larvae during certain growth phases but not others. This is illustrated by Djegbe et al.38, where, compared to deep tillage, minimal tillage could significantly reduce larvae during the early stages of rice cultivation but not during tillering and maturation38. In contrast, other interventions, such as Azolla and predatory copepods, took time to grow and accumulate, and were more effective during the later stages of a rice season45,67,71. This differentiation is important because it can identify components that could potentially form a complementary set of interventions against riceland malaria vectors, each component being effective at different parts of the season. Since rice fields, and hence the dynamics of riceland mosquito populations, vary from place to place, this set of interventions must also be robust. Special attention must be paid to the early stages of rice cultivation, particularly the first few weeks after transplanting (or sowing), since, with many vector species, a large proportion of adult mosquitoes are produced during this time.Fourth, the analysis of entomological counts is often inadequate. Many studies failed to provide the standard deviation (or any other measure of error) for larval counts and could not be included in the quantitative analysis. Often, due to the extreme (and not unexpected) variability of larval numbers, sample sizes were insufficient to calculate statistically significant differences between treatments. Fifth, a high risk of bias was found across both CTS and CITS studies, including high heterogeneity and some publication bias. Study quality was, in general, a shortcoming and limited the number of eligible studies for certain interventions, including intermittent irrigation. Moreover, there are conspicuous a priori reasons for bias in such experimental trials: trial locations are frequently chosen to maximise the probability of success.Finally, few studies were conducted in African countries, where the relationship between rice and malaria is most important because of the efficiency, and the “rice-philic” nature, of the vector An. gambiae s.l.15. In particular, there was a lack of studies on the effectiveness and scalability of biological control and rice cultivation practices. There is also very little information (particularly social science studies) on the views and perspectives of African rice farmers on mosquitoes in rice and interventions to control them72,73.In the future, as malaria declines (particularly across SSA), the contribution of rice production to increased malaria transmission is likely to become more conspicuous15. Unless this problem is addressed, rice growing will probably become an obstacle to malaria elimination. Current default methods of rice production provide near-perfect conditions for the larvae of African malaria vectors. Therefore, we need to develop modified rice-growing methods that are unfavourable to mosquitoes but still favourable for the rice. Although larviciding and biological control may be appropriate, their unsustainable costs remain the biggest barrier to uptake amongst smallholder farmers. Future investigations into riceland vector control should pay more attention to interventions that may be useful to farmers.Supported by medical entomologists, agronomists should lead the research task of identifying cultivation methods that achieve high rice productivity whilst suppressing vector productivity. Rice fields are a major global source of greenhouse gases, and agronomists have responded by successfully developing novel cultivation methods that minimise these emissions while maintaining yield. We need the same kind of response from agronomists, to achieve malaria control co-benefits within rice cultivation. At present, only a few aspects of rice cultivation have been investigated for their effects on mosquitoes, and the potential of many other practices for reducing anopheline numbers are awaiting study. Due to the spatial and temporal heterogeneity of rice agroecosystems, it is likely that no single control method can reduce mosquito numbers throughout an entire cropping season and in all soil types and irrigation methods. Thus, effective overall control is likely to come from a combination of local, site-specific set of complementary methods, each of which is active and effective during a different phase of the rice-growing season. More

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    Pathogen spillover driven by rapid changes in bat ecology

    During recent decades, pathogens that originated in bats have become an increasing public health concern. A major challenge is to identify how those pathogens spill over into human populations to generate a pandemic threat1. Many correlational studies associate spillover with changes in land use or other anthropogenic stressors2,3, although the mechanisms underlying the observed correlations have not been identified4. One limitation is the lack of spatially and temporally explicit data on multiple spillovers, and on the connections among spillovers, reservoir host ecology and behavior, and viral dynamics. We present 25 years of data on land-use change, bat behavior, and spillover of Hendra virus from Pteropodid bats to horses in subtropical Australia. These data show that bats are responding to environmental change by persistently adopting behaviors that were previously transient responses to nutritional stress. Interactions between land-use change and climate now lead to persistent bat residency in agricultural areas, where periodic food shortages drive clusters of spillovers. Pulses of winter flowering of trees in remnant forests appeared to prevent spillover. We developed integrative Bayesian network models based on these phenomena that accurately predicted the presence or absence of clusters of spillovers in each of 25 years. Our long-term study identifies the mechanistic connections among habitat loss, climate, and increased spillover risk. It provides a framework for examining causes of bat virus spillover and for developing ecological countermeasures to prevent pandemics. More

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    The study of aggression and affiliation motifs in bottlenose dolphins’ social networks

    Subjects and facilityWe observed two groups of Atlantic bottlenose dolphins (six different individuals in total) housed at the marine zoo “Marineland Mallorca”. One of the groups was composed of four individuals (G1) and the other was constituted by five individuals (G2). The two adult males and one of the females were the same in both groups (Table 1). Group composition changed due to the transfer of individuals to another pool of the zoo and due to the arrival of new individuals from another aquatic park.Table 1 Age, sex, group, and identification number in the network of the subject dolphins. M male, F female.Full size tableThe dolphins were kept in three outdoor interconnecting pools: the main performance pool (1.6 million liters of water), a medical pool (37.8 thousand liters of water) and a small pool (636.8 thousand liters of water). During the observational periods, the dolphins had free access to all the pools. Underwater viewing at the main and the small pool was available through the transparent walls around the rim of the pools.Ethics statementThis study was approved by the UIB Committee of Research Ethics and Marineland Mallorca. This research was conducted in compliance with the standards of the European Association of Zoos and Aquaria (EAZA). All subjects tested in this study were housed in Marineland Mallorca following the Directive 1999/22/EC on the keeping of animals in zoos. This study was strictly non-invasive and did not affect the welfare of dolphins.Behavioral observations and data collectionBehavioral data were collected in situ by APM from May to November 2016 for G1 and from November 2017 to February 2018 for G2. All observational periods were also recorded using two waterproof cameras SJCAM SJ4000. Observations were conducted at the main pool between 8:00 a.m. and 11:00 a.m. Due to the schedules and dynamics of the zoo, we were unable to collect data outside this period. Dolphin social behavior was registered and videotaped for 30 min–2 h each day. Only data from sessions that lasted at least 30 min were included in the analysis. We did not collect any data during training or medical procedures and resumed the observational session a few minutes after the end of these events.We recorded all occurrences of affiliative and aggressive interactions, the identities of the involved individuals and the identity of the dolphin initiating the contact. Aggressive contacts were defined by the occurrence of chasing, biting, and hitting, as established in previous studies37,38,39,40,41. Affiliative contacts were defined as contact swimming, synchronous breathing and swimming (at least 30″ of continuous swimming) or flipper-rubbing, as established in previous studies37,39,40,41,43.To assess the strength of the affiliative bonds in both groups, we calculated the index of affiliative relationships (IA) between dolphins following the procedure described in Yamamoto et al. For calculating the IA we recorded the relative frequencies of synchronous swimming since it is a well-defined affiliative behavior in dolphins. Data of synchronous swimming were recorded using group 0–1 sampling44 at 3-min intervals. This method consists of the observation of individuals during short periods and the recording of the occurrence (assigning to that period a 1) or non-occurrence (assigning to that period a 0) of a well-defined behavior44. For calculating the IA for each couple, the number of sampling periods in which synchronous swimming between individuals A and B occurred (XAB) was divided by the number of sampling periods in which individuals A and B were observed (YAB): (IA=frac{{X}_{AB}}{{Y}_{AB}})39,45. Therefore, the IA reflects the level of affiliation for each dolphin dyad based on the pattern of synchronous swimming. This index served to construct the general affiliative social networks of both groups of dolphins.Temporal network constructionTemporal networks can provide insight into social events such as conflicts and post-conflict interactions in which the order of interactions and the timing is crucial. Furthermore, they allow us to calculate the probabilities of the different affiliative and aggressive interactions occurring in the group.We used behavioral observations to construct temporal networks for each group. Each dolphin was treated as a node (N) with their aggressive and affiliative interactions supplying the network links. We divided the daily observations into periods of 3 min. In each period, we assigned a positive (+ 1), negative (− 1) or neutral (0) interaction to each pair of dolphins. That is, if during the period a pair of dolphins displayed affiliative interactions, we assigned a + 1 to the link between that pair of nodes, if they were involved in a conflict, we assigned a − 1, and if the pair did not engage in any interaction, we assigned to that link a 0. If during the same period, the pair displayed both aggressive and affiliative interactions we considered the last observed interaction. Therefore, we obtained an adjacency matrix (an N × N matrix describing the links in the network) for each group of dolphins. Thus, for each day we had a series of different signed networks of the group, each network representing a 3-min period.Social network analysis: time-aggregated networks and network motifsWe collapsed the temporal networks of each day in time-aggregated networks. This procedure consists in aggregating the data collected over time within specific intervals to create weighted networks. The sign and the weight of the links characterize these networks, indicating the valence and duration of the interaction respectively. Thus, they are static representations of the social structure of the group of dolphins. To obtain these time-aggregated networks we proceeded as follows:First, for each day we aggregated the values of each interaction of the temporal networks until one link qualitatively changed. We considered a qualitative change if one interaction passed from being negative (− 1) to positive (+ 1) meaning that the pair of dolphins reconciled after the conflict or vice versa, or if a new affiliation (+ 1) or aggression (− 1) took place, that is the link changed from being neutral (0) to positive or negative. If a link changed from being negative or positive to being neutral, we did not consider that this interaction has changed qualitatively. For example, if dolphins interacted positively during two periods of time, then they ceased to interact (neutral) and finally they engaged in an aggressive interaction, the total weight of the interaction in the resulting time-aggregated network would be of + 2. Therefore, a conflict or an affiliation may extend over multiple periods containing several contacts, and is considered finished when the interaction changes its valence. In this way, we obtained a series of time-aggregated networks for each day, which retain the information on the duration, timing, and ordering of the affiliative and aggressive events in the group.We examined the local-scale structure of the affiliative-aggressive social networks using motif analysis. Thus, for each group, we analyzed the network motif representation of the temporal and time-aggregated networks, identifying and recording the number of occurrences of each motif.Model of affiliative and aggressive interactionsWe built two models (a simple and a complex one) that aim to simulate the dynamics of aggressive and affiliative interactions of a group of four dolphins. These models were created using the observed probabilities of each affiliative or aggressive interaction between individuals in group G1. We only used the data of G1 since we had more hours of video recordings and, thus, more statistics of the pattern of dolphins’ interactions. Both models return affiliative/aggressive temporal networks constituted by four nodes and different aggressive, affiliative, or neutral interactions between the six possible pairs of individuals in the network. We simulated data for 20 periods of 3 min per day for a total of 80 days to mimic the empirical data time structure. We obtained one temporal network for each period (1600 temporal networks in total) and ran 100 realizations of each model.Our models work as follows: At the beginning of the simulations, all the interactions between the four nodes are neutral (0). In each period, we select a pair of nodes randomly and assign to that link a positive (+ 1) or a negative (− 1) interaction with probability p (calculated previously for each type of interaction). These interactions correspond to spontaneous aggressions and affiliations. In the complex model, if in the previous period a conflict took place, before assessing spontaneous interactions we first evaluated the different possible post-conflict contacts that could occur (reconciliation, new aggressions, and affiliations). Therefore, for reconciliations, we change the valence of the interaction from negative to positive with a certain probability. Then, we also randomly choose a pair of nodes including one of the former opponents and assign to that link a positive or negative interaction with the observed probabilities to simulate the occurrence of new affiliations (third party-affiliation) or redirected aggressions arising from the previous conflict. We keep on doing this procedure period by period. Lastly, we obtained the time-aggregated networks for the two models.The simpler model only includes the probability of aggression and affiliation between group members, whereas the complex one also includes the patterns of conflict resolution previously observed. In this way, the complex model serves to assess the influence of post-conflict management mechanisms on the observed pattern of aggressive/affiliative networks. That is, the complex model also keeps track of past actions. Thus, depending on the interaction of the previous step, the probability of the following interaction changes based on the observed pattern of conflict resolution strategies.Calculation of the observed probabilities of affiliative and aggressive interactionsFor the simple model, we calculated the probability of general aggression and affiliation per day without distinguishing between types of positive and negative interactions. Thus, we obtained the number of periods in which an aggressive or affiliative contact took place per day and divided it by the total number of periods of that day (probability of general aggression or affiliation per 3-min period). With these probabilities, we calculated the mean probability of general aggression and affiliation per period.For the complex model, we calculated the probabilities of reconciliation, new affiliations/aggressions, and spontaneous affiliations/aggressions per day. That is, the probability that former opponents exchange affiliative contacts after an aggressive encounter (reconciliation), the probabilities that a conflict may promote new affiliations (third-party affiliation) or new conflicts (redirected aggression) between one of the opponents and a bystander in the same day, and the probability of affiliative or aggressive interactions not derived from a previous conflict (spontaneous interactions). To classify affiliations and aggressions in these categories we used the temporal networks, examining the interactions that took place after a conflict between opponents and between them and bystanders. If the opponents reconciled or affiliated with a bystander after a fight, we assumed that the following affiliative or aggressive interactions were spontaneous and were not a consequence of that conflict. Thus, to calculate the number of spontaneous affiliations, we subtracted the number of reconciliations and new affiliations from the total number of affiliations per day. For spontaneous aggressions, we subtracted the number of new aggressions to the total number of aggressions per day. Then, we obtained the probability of spontaneous affiliation and aggression per period.Using the previous probabilities, we obtained the rate (r) of reconciliation, new aggression and new affiliation per minute with the following formula:({p=1-e}^{-rDelta t}). Using the same formula, we finally calculated the probability of reconciliation, new aggression and affiliation per 3-min period used in the complex model (Supplementary Table 1 for details of probabilities calculation).Network-motif analysisWe also carried out a network-motif analysis. As we did not consider the identities or sex of the nodes in these models, we grouped the obtained motifs into equivalent categories considering the pattern of interactions between nodes. We also classified the motifs obtained from the real data of G1 into those equivalent categories. Finally, we compared the pattern of equivalent network motifs of the observed social network of dolphins and the ones of the two models. To do so we calculated the Spearman’s rank correlation coefficient (rs), defined as a nonparametric measure of the statistical dependence between the rankings of two variables: ({r}_{s}=frac{covleft({rg}_{X}{rg}_{Y}right)}{{sigma }_{{rg}_{X}}}{sigma }_{{rg}_{Y}}); rgX and rgY are the rank variables; cov (rgX rgY) is the covariance of the rank variables, and σrgX and σrgY are the standard deviations of the rank variables. Therefore, this coefficient allows us to assess the statistical dependence between the motif ranking of the real data and the one of each model.Computational implementationsAll the models, network construction, visualization and motif analysis were generated and implemented using MATLAB R2018b. More

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    The effects of visitors and social isolation from a peer on the behavior of a mixed-species pair of captive gibbons

    Kazarov, E. The Role of Zoos in Creating a Conservation Ethic in Visitors. SIT Digital Collections (2022). at https://digitalcollections.sit.edu/isp_collection/584.Hosey, G. How does the zoo environment affect the behaviour of captive primates?. Appl. Anim. Behav. Sci. 90, 107–129 (2005).
    Google Scholar 
    Morgan, K. & Tromborg, C. Sources of stress in captivity. Appl. Anim. Behav. Sci. 102, 262–302 (2007).
    Google Scholar 
    Sherwen, S. & Hemsworth, P. The visitor effect on zoo animals: Implications and opportunities for zoo animal welfare. Animals 9, 366 (2019).PubMed Central 

    Google Scholar 
    Chamove, A., Hosey, G. & Schaetzel, P. Visitors excite primates in zoos. Zoo Biol. 7, 359–369 (1988).
    Google Scholar 
    Tetley, C. L. & O’Hara, S. J. Ratings of animal personality as a tool for improving the breeding, management and welfare of zoo mammals. Anim. Welf. UFAW J. 21(4), 463 (2012).CAS 

    Google Scholar 
    Stoinski, T. S., Jaicks, H. F. & Drayton, L. A. Visitor effects on the behavior of captive western lowland gorillas: The importance of individual differences in examining welfare. Zoo Biol. 31(5), 586–599 (2012).PubMed 

    Google Scholar 
    Queiroz, M. B. & Young, R. J. The different physical and behavioural characteristics of zoo mammals that influence their response to visitors. Animals 8(8), 139 (2018).PubMed Central 

    Google Scholar 
    Fanson, K. V. & Wielebnowski, N. C. Effect of housing and husbandry practices on adrenocortical activity in captive Canada lynx (Lynx canadensis). Anim. Welf. 22, 159–165 (2013).CAS 

    Google Scholar 
    Pirovino, M. et al. Fecal glucocorticoid measurements and their relation to rearing, behavior, and environmental factors in the population of pileated gibbons (Hylobates pileatus) held in European zoos. Int. J. Primatol. 32(5), 1161–1178 (2011).
    Google Scholar 
    Williams, I., Hoppitt, W. & Grant, R. The effect of auditory enrichment, rearing method and social environment on the behavior of zoo-housed psittacines (Aves: Psittaciformes); implications for welfare. Appl. Anim. Behav. Sci. 186, 85–92 (2017).
    Google Scholar 
    Fernandez, E., Tamborski, M., Pickens, S. & Timberlake, W. Animal–visitor interactions in the modern zoo: Conflicts and interventions. Appl. Anim. Behav. Sci. 120, 1–8 (2009).
    Google Scholar 
    Hosey, G. & Skyner, L. Self-injurious behavior in zoo primates. Int. J. Primatol. 28, 1431–1437 (2007).
    Google Scholar 
    Mallapur, A., Sinha, A. & Waran, N. Influence of visitor presence on the behaviour of captive lion-tailed macaques (Macaca silenus) housed in Indian zoos. Appl. Anim. Behav. Sci. 94, 341–352 (2005).
    Google Scholar 
    Davey, G. Visitors’ Effects on the Welfare of Animals in the Zoo: A Review. J. Appl. Anim. Welf. Sci. 10, 169–183 (2007).CAS 
    PubMed 

    Google Scholar 
    Jones, H., McGregor, P., Farmer, H. & Baker, K. The influence of visitor interaction on the behavior of captive crowned lemurs (Eulemur coronatus) and implications for welfare. Zoo Biol. 35, 222–227 (2016).CAS 
    PubMed 

    Google Scholar 
    Cook, S. & Hosey, G. R. Interaction sequences between chimpanzees and human visitors at the zoo. Zoo Biol. 14(5), 431–440 (1995).
    Google Scholar 
    Baker, K. C. Benefits of positive human interaction for socially-housed chimpanzees. Anim. Welf. (South Mimms, Engl.nd) 13(2), 239 (2004).CAS 

    Google Scholar 
    Carder, G. & Semple, S. Visitor effects on anxiety in two captive groups of western lowland gorillas. Appl. Anim. Behav. Sci. 115, 211–220 (2008).
    Google Scholar 
    Wood, W. Interactions among environmental enrichment, viewing crowds, and zoo chimpanzees (Pantroglodytes). Zoo Biol. 17, 211–230 (1998).
    Google Scholar 
    Todd, P., Macdonald, C. & Coleman, D. Visitor-associated variation in captive Diana monkey (Cercopithecus diana diana) behaviour. Appl. Anim. Behav. Sci. 107, 162–165 (2007).
    Google Scholar 
    Davis, N., Schaffner, C. & Smith, T. Evidence that zoo visitors influence HPA activity in spider monkeys (Ateles geoffroyii rufiventris). Appl. Anim. Behav. Sci. 90, 131–141 (2005).
    Google Scholar 
    Sherwen, S. L. et al. Effects of visual contact with zoo visitors on black-capped capuchin welfare. Appl. Anim. Behav. Sci. 167, 65–73 (2015).
    Google Scholar 
    Choo, Y., Todd, P. & Li, D. Visitor effects on zoo orangutans in two novel, naturalistic enclosures. Appl. Anim. Behav. Sci. 133, 78–86 (2011).
    Google Scholar 
    Sherwen, S., Magrath, M., Butler, K., Phillips, C. & Hemsworth, P. A multi-enclosure study investigating the behavioural response of meerkats to zoo visitors. Appl. Anim. Behav. Sci. 156, 70–77 (2014).
    Google Scholar 
    Hosey, G. & Druck, P. The influence of zoo visitors on the behaviour of captive primates. Appl. Anim. Behav. Sci. 18, 19–29 (1987).
    Google Scholar 
    Mitchell, G. et al. More on the ‘influence’of zoo visitors on the behaviour of captive primates. Appl. Anim. Behav. Sci. 35(2), 189–198 (1992).
    Google Scholar 
    Sellinger, R. & Ha, J. The effects of visitor density and intensity on the behavior of two captive jaguars (Panthera onca). J. Appl. Anim. Welfare Sci. 8, 233–244 (2005).CAS 

    Google Scholar 
    Azevedo, C., Lima, M., Silva, V., Young, R. & Rodrigues, M. Visitor Influence on the Behavior of Captive Greater Rheas (Rhea americana, Rheidae Aves). J. Appl. Anim. Welfare Sci. 15, 113–125 (2012).
    Google Scholar 
    Das Gupta, M., Das, A., Sumy, M. C. & Islam, M. M. An explorative study on visitor’s behaviour and their effect on the behaviour of primates at Chittagong zoo. Bangladesh J. Vet. Anim. Sci. 5(2), 24–32 (2017).
    Google Scholar 
    Hemsworth, P. Human–animal interactions in livestock production. Appl. Anim. Behav. Sci. 81, 185–198 (2003).
    Google Scholar 
    Stoinski, T., Czekala, N., Lukas, K. & Maple, T. Urinary androgen and corticoid levels in captive, male Western lowland gorillas (Gorilla g. gorilla): Age- and social group-related differences. Am. J. Primatol. 56, 73–87 (2002).CAS 
    PubMed 

    Google Scholar 
    Stoinski, T., Lukas, K., Kuhar, C. & Maple, T. Factors influencing the formation and maintenance of all-male gorilla groups in captivity. Zoo Biol. 23, 189–203 (2004).
    Google Scholar 
    Olsson, I. & Westlund, K. More than numbers matter: The effect of social factors on behaviour and welfare of laboratory rodents and non-human primates. Appl. Anim. Behav. Sci. 103, 229–254 (2007).
    Google Scholar 
    Martin, J. E. Early life experiences: Activity levels and abnormal behaviours in resocialised chimpanzees. Anim Welf. 11(4), 419–436 (2002).CAS 

    Google Scholar 
    Birkett, L. P. & Newton-Fisher, N. E. How abnormal is the behaviour of captive, zoo-living chimpanzees?. PLoS ONE 6(6), e20101 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ballen, C., Shine, R. & Olsson, M. Effects of early social isolation on the behaviour and performance of juvenile lizards Chamaeleo calyptratus. Anim. Behav. 88, 1–6 (2014).
    Google Scholar 
    Coe, C., Mendoza, S., Smotherman, W. & Levine, S. Mother-infant attachment in the squirrel monkey: Adrenal response to separation. Behav. Biol. 22, 256–263 (1978).CAS 
    PubMed 

    Google Scholar 
    Mendoza, S., Smotherman, W., Miner, M., Kaplan, J. & Levine, S. Pituitary-adrenal response to separation in mother and infant squirrel monkeys. Dev. Psychobiol. 11, 169–175 (1978).CAS 
    PubMed 

    Google Scholar 
    Gilbert, M. & Baker, K. Social buffering in adult male rhesus macaques (Macaca mulatta): Effects of stressful events in single vs. pair housing. J. Med. Primatol. 40, 71–78 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    Schapiro, S. Effects of social manipulations and environmental enrichment on behavior and cell-mediated immune responses in rhesus macaques. Pharmacol. Biochem. Behav. 73, 271–278 (2002).CAS 
    PubMed 

    Google Scholar 
    Chen, W. et al. Effects of social isolation and re-socialization on cognition and ADAR1 (p110) expression in mice. PeerJ 4, e2306 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Glatston, A., Geilvoet-Soeteman, E., Hora-Pecek, E. & Van Hooff, J. The influence of the zoo environment on social behavior of groups of cotton-topped tamarins Saguinus oedipus oedipus. Zoo Biol. 3, 241–253 (1984).
    Google Scholar 
    Mitchell, G. et al. Effects of visitors and cage changes on the behaviors of mangabeys. Zoo Biol. 10, 417–423 (1991).
    Google Scholar 
    Geissmann, T. & Orgeldinger, M. The relationship between duet songs and pair bonds in siamangs Hylobates syndactylus. Anim. Behav. 60, 805–809 (2000).CAS 
    PubMed 

    Google Scholar 
    Palombit, R. Pair bonds in monogamous apes: A comparison of the siamang hylobates syndactylus and the white-handed gibbon hylobates lar. Behaviour 133, 321–356 (1996).
    Google Scholar 
    Rutberg, A. The evolution of monogamy in primates. J. Theor. Biol. 104, 93–112 (1983).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Giorgi, A., Montebovi, G., Vitale, A. & Alleva, E. A behavioural case study of early social isolation of a subadult white-handed gibbon (Hylobates lar). Folia Primatol. 89, 287–294 (2018).
    Google Scholar 
    Skynner, L. A., Amory, J. R. & Hosey, G. The effect of visitors on the self-injurious behaviour of a male pileated gibbon (Hylobates pileatus). Zool. Garten 74(1), 38–41 (2004).
    Google Scholar 
    Smith, K. & Kuhar, C. Siamangs (Hylobates syndactylus) and white-cheeked gibbons (Hylobates leucogenys) show few behavioral differences related to zoo attendance. J. Appl. Anim. Welfare Sci. 13, 154–163 (2010).CAS 

    Google Scholar 
    Lukas, K. E. et al. Longitudinal study of delayed reproductive success in a pair of white-cheeked gibbons (Hylobates leucogenys). Zoo Biol. 21, 413–434 (2002).
    Google Scholar 
    Cooke, C. & Schillaci, M. Behavioral responses to the zoo environment by white handed gibbons. Appl. Anim. Behav. Sci. 106, 125–133 (2007).
    Google Scholar 
    Mootnick, A. & Baker, E. Masturbation in captiveHylobates (gibbons). Zoo Biol. 13, 345–353 (1994).
    Google Scholar 
    Geissmann, T. Reassessment of age of sexual maturity in gibbons (hylobates spp.). American Journal of Primatology 23, 11–22 (1991).Altmann, J. Observational study of behavior: Sampling methods. Behaviour 49(3–4), 227–266 (1974).CAS 
    PubMed 

    Google Scholar 
    Pomerantz, O. & Terkel, J. Effects of positive reinforcement training techniques on the psychological welfare of zoo-housed chimpanzees (Pan troglodytes). Am. J. Primatol. 71, 687–695 (2009).PubMed 

    Google Scholar 
    Orgeldinger, M. Protective and territorial behavior in captive siamangs (Hylobates syndactylus). Zoo Biol. 16, 309–325 (1997).
    Google Scholar 
    Fox, J. et al. Package ‘car’. Vienna: R Foundation for Statistical Computing, 16 https://cran.uni-muenster.de/web/packages/car/car.pdf (2012).Magnusson, A., Skaug, H., Nielsen, A., Berg, C., Kristensen, K., Maechler, M., van Bentham, K., Bolker, B., Brooks, M. & Brooks, M. M. Package ‘glmmtmb’. R Package Version 0.2. 0 (2017).Hartig, F., & Hartig, M. F. Package ‘DHARMa’. Vienna, Austria: R Development Core Team (2017).Troisi, A. Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects. Stress 5, 47–54 (2002).PubMed 

    Google Scholar 
    Baker, K. & Aureli, F. Behavioural indicators of anxiety: An empirical test in chimpanzees. Behaviour 134, 1031–1050 (1997).
    Google Scholar 
    Vick, S. J. & Paukner, A. Variation and context of yawns in captive chimpanzees (Pan troglodytes). Am. J. Primatol. Off. J. Am. Soc. Primatol. 72(3), 262–269 (2010).
    Google Scholar 
    Norscia, I. & Palagi, E. When play is a family business: Adult play, hierarchy, and possible stress reduction in common marmosets. Primates 52, 101–104 (2010).PubMed 

    Google Scholar 
    Held, S. & Špinka, M. Animal play and animal welfare. Anim. Behav. 81, 891–899 (2011).
    Google Scholar 
    Davey, G. Visitor behavior in zoos: A review. Anthrozoös 19, 143–157 (2006).
    Google Scholar 
    Nimon, A. & Dalziel, F. Cross-species interaction and communication: a study method applied to captive siamang (Hylobates syndactylus) and long-billed corella (Cacatua tenuirostris) contacts with humans. Appl. Anim. Behav. Sci. 33, 261–272 (1992).
    Google Scholar 
    Suomi, S. Early determinants of behaviour: Evidence from primate studies. Br. Med. Bull. 53, 170–184 (1997).CAS 
    PubMed 

    Google Scholar 
    Anderson, J. & Chamove, A. Self-aggression and social aggression in laboratory-reared macaques. J. Abnorm. Psychol. 89, 539–550 (1980).CAS 
    PubMed 

    Google Scholar 
    Mallapur, A. & Choudhury, B. Behavioral abnormalities in captive nonhuman primates. J. Appl. Anim. Welfare Sci. 6, 275–284 (2003).CAS 

    Google Scholar 
    Barlow, C., Caldwell, C. & Lee, P. Individual differences and response to visitors in zoo-housed diana monkeys (Cercopithecus diana diana). Cabdirect.org (2022). at https://www.cabdirect.org/cabdirect/abstract/20123180753.Gartner, M. & Weiss, A. Studying primate personality in zoos: Implications for the management, welfare and conservation of great apes. International Zoo Yearbook 52, 79–91 (2018).
    Google Scholar 
    Mitchell, G., Raymond, E., Ruppenthal, G. & Harlow, H. Long-term effects of total social isolation upon behavior of rhesus monkeys. Psychol. Rep. 18, 567–580 (1966).
    Google Scholar 
    Martín, O., Vinyoles, D., García-Galea, E. & Maté, C. Improving the welfare of a zoo-housed male drill (Mandrillus leucophaeus poensis) aggressive toward visitors. J. Appl. Anim. Welfare Sci. 19, 323–334 (2016).
    Google Scholar 
    Ross, S., Melber, L., Gillespie, K. & Lukas, K. The impact of a modern, naturalistic exhibit design on visitor behavior: A cross-facility comparison. Visitor Stud. 15, 3–15 (2012).
    Google Scholar 
    Quadros, S., Goulart, V., Passos, L., Vecci, M. & Young, R. Zoo visitor effect on mammal behaviour: Does noise matter?. Appl. Anim. Behav. Sci. 156, 78–84 (2014).
    Google Scholar 
    Bonnie, K., Ang, M. & Ross, S. Effects of crowd size on exhibit use by and behavior of chimpanzees (Pan troglodytes) and Western lowland gorillas (Gorilla gorilla) at a zoo. Appl. Anim. Behav. Sci. 178, 102–110 (2016).
    Google Scholar  More