Pub Date : 2024-09-02DOI: 10.1186/s40462-024-00499-1
Stefan Schoombie, Rory P Wilson, Yan Ropert-Coudert, Ben J Dilley, Peter G Ryan
Background: Recent technological advances have resulted in low-cost GPS loggers that are small enough to be used on a range of seabirds, producing accurate location estimates (± 5 m) at sampling intervals as low as 1 s. However, tradeoffs between battery life and sampling frequency result in studies using GPS loggers on flying seabirds yielding locational data at a wide range of sampling intervals. Metrics derived from these data are known to be scale-sensitive, but quantification of these errors is rarely available. Very frequent sampling, coupled with limited movement, can result in measurement error, overestimating movement, but a much more pervasive problem results from sampling at long intervals, which grossly underestimates path lengths.
Methods: We use fine-scale (1 Hz) GPS data from a range of albatrosses and petrels to study the effect of sampling interval on metrics derived from the data. The GPS paths were sub-sampled at increasing intervals to show the effect on path length (i.e. ground speed), turning angles, total distance travelled, as well as inferred behavioural states.
Results: We show that distances (and per implication ground speeds) are overestimated (4% on average, but up to 20%) at the shortest sampling intervals (1-5 s) and underestimated at longer intervals. The latter bias is greater for more sinuous flights (underestimated by on average 40% when sampling > 1-min intervals) as opposed to straight flight (11%). Although sample sizes were modest, the effect of the bias seemingly varied with species, where species with more sinuous flight modes had larger bias. Sampling intervals also played a large role when inferring behavioural states from path length and turning angles.
Conclusions: Location estimates from low-cost GPS loggers are appropriate to study the large-scale movements of seabirds when using coarse sampling intervals, but actual flight distances are underestimated. When inferring behavioural states from path lengths and turning angles, moderate sampling intervals (10-30 min) may provide more stable models, but the accuracy of the inferred behavioural states will depend on the time period associated with specific behaviours. Sampling rates have to be considered when comparing behaviours derived using varying sampling intervals and the use of bias-informed analyses are encouraged.
{"title":"The efficiency of detecting seabird behaviour from movement patterns: the effect of sampling frequency on inferring movement metrics in Procellariiformes.","authors":"Stefan Schoombie, Rory P Wilson, Yan Ropert-Coudert, Ben J Dilley, Peter G Ryan","doi":"10.1186/s40462-024-00499-1","DOIUrl":"10.1186/s40462-024-00499-1","url":null,"abstract":"<p><strong>Background: </strong>Recent technological advances have resulted in low-cost GPS loggers that are small enough to be used on a range of seabirds, producing accurate location estimates (± 5 m) at sampling intervals as low as 1 s. However, tradeoffs between battery life and sampling frequency result in studies using GPS loggers on flying seabirds yielding locational data at a wide range of sampling intervals. Metrics derived from these data are known to be scale-sensitive, but quantification of these errors is rarely available. Very frequent sampling, coupled with limited movement, can result in measurement error, overestimating movement, but a much more pervasive problem results from sampling at long intervals, which grossly underestimates path lengths.</p><p><strong>Methods: </strong>We use fine-scale (1 Hz) GPS data from a range of albatrosses and petrels to study the effect of sampling interval on metrics derived from the data. The GPS paths were sub-sampled at increasing intervals to show the effect on path length (i.e. ground speed), turning angles, total distance travelled, as well as inferred behavioural states.</p><p><strong>Results: </strong>We show that distances (and per implication ground speeds) are overestimated (4% on average, but up to 20%) at the shortest sampling intervals (1-5 s) and underestimated at longer intervals. The latter bias is greater for more sinuous flights (underestimated by on average 40% when sampling > 1-min intervals) as opposed to straight flight (11%). Although sample sizes were modest, the effect of the bias seemingly varied with species, where species with more sinuous flight modes had larger bias. Sampling intervals also played a large role when inferring behavioural states from path length and turning angles.</p><p><strong>Conclusions: </strong>Location estimates from low-cost GPS loggers are appropriate to study the large-scale movements of seabirds when using coarse sampling intervals, but actual flight distances are underestimated. When inferring behavioural states from path lengths and turning angles, moderate sampling intervals (10-30 min) may provide more stable models, but the accuracy of the inferred behavioural states will depend on the time period associated with specific behaviours. Sampling rates have to be considered when comparing behaviours derived using varying sampling intervals and the use of bias-informed analyses are encouraged.</p>","PeriodicalId":54288,"journal":{"name":"Movement Ecology","volume":"12 1","pages":"59"},"PeriodicalIF":3.4,"publicationDate":"2024-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11370088/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142121170","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-30DOI: 10.1186/s40462-024-00501-w
William F Fagan, Ananke Krishnan, Qianru Liao, Christen H Fleming, Daisy Liao, Clayton Lamb, Brent Patterson, Tyler Wheeldon, Ricardo Martinez-Garcia, Jorge F S Menezes, Michael J Noonan, Eliezer Gurarie, Justin M Calabrese
Direct encounters, in which two or more individuals are physically close to one another, are a topic of increasing interest as more and better movement data become available. Recent progress, including the development of statistical tools for estimating robust measures of changes in animals' space use over time, facilitates opportunities to link direct encounters between individuals with the long-term consequences of those encounters. Working with movement data for coyotes (Canis latrans) and grizzly bears (Ursus arctos horribilis), we investigate whether close intraspecific encounters were associated with spatial shifts in the animals' range distributions, as might be expected if one or both of the individuals involved in an encounter were seeking to reduce or avoid conflict over space. We analyze the movement data of a pair of coyotes in detail, identifying how a change in home range overlap resulting from altered movement behavior was apparently a consequence of a close intraspecific encounter. With grizzly bear movement data, we approach the problem as population-level hypothesis tests of the spatial consequences of encounters. We find support for the hypotheses that (1) close intraspecific encounters between bears are, under certain circumstances, associated with subsequent changes in overlap between range distributions and (2) encounters defined at finer spatial scales are followed by greater changes in space use. Our results suggest that animals can undertake long-term, large-scale spatial changes in response to close intraspecific encounters that have the potential for conflict. Overall, we find that analyses of movement data in a pairwise context can (1) identify distances at which individuals' proximity to one another may alter behavior and (2) facilitate testing of population-level hypotheses concerning the potential for direct encounters to alter individuals' space use.
{"title":"Intraspecific encounters can lead to reduced range overlap.","authors":"William F Fagan, Ananke Krishnan, Qianru Liao, Christen H Fleming, Daisy Liao, Clayton Lamb, Brent Patterson, Tyler Wheeldon, Ricardo Martinez-Garcia, Jorge F S Menezes, Michael J Noonan, Eliezer Gurarie, Justin M Calabrese","doi":"10.1186/s40462-024-00501-w","DOIUrl":"https://doi.org/10.1186/s40462-024-00501-w","url":null,"abstract":"<p><p>Direct encounters, in which two or more individuals are physically close to one another, are a topic of increasing interest as more and better movement data become available. Recent progress, including the development of statistical tools for estimating robust measures of changes in animals' space use over time, facilitates opportunities to link direct encounters between individuals with the long-term consequences of those encounters. Working with movement data for coyotes (Canis latrans) and grizzly bears (Ursus arctos horribilis), we investigate whether close intraspecific encounters were associated with spatial shifts in the animals' range distributions, as might be expected if one or both of the individuals involved in an encounter were seeking to reduce or avoid conflict over space. We analyze the movement data of a pair of coyotes in detail, identifying how a change in home range overlap resulting from altered movement behavior was apparently a consequence of a close intraspecific encounter. With grizzly bear movement data, we approach the problem as population-level hypothesis tests of the spatial consequences of encounters. We find support for the hypotheses that (1) close intraspecific encounters between bears are, under certain circumstances, associated with subsequent changes in overlap between range distributions and (2) encounters defined at finer spatial scales are followed by greater changes in space use. Our results suggest that animals can undertake long-term, large-scale spatial changes in response to close intraspecific encounters that have the potential for conflict. Overall, we find that analyses of movement data in a pairwise context can (1) identify distances at which individuals' proximity to one another may alter behavior and (2) facilitate testing of population-level hypotheses concerning the potential for direct encounters to alter individuals' space use.</p>","PeriodicalId":54288,"journal":{"name":"Movement Ecology","volume":"12 1","pages":"58"},"PeriodicalIF":3.4,"publicationDate":"2024-08-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11365178/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142114778","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-26DOI: 10.1186/s40462-024-00489-3
Hans Linssen, Henrik J de Knegt, Jasper A J Eikelboom
Background: Animal movement arises from complex interactions between animals and their heterogeneous environment. To better understand the movement process, it can be divided into behavioural, temporal and spatial components. Although methods exist to address those various components, it remains challenging to integrate them in a single movement analysis.
Methods: We present an analytic workflow that integrates the behavioural, temporal and spatial components of the movement process and their interactions, which also allows for the assessment of the relative importance of those components. We construct a daily cyclic covariate to represent temporally cyclic movement patterns, such as diel variation in activity, and combine the three components in a multi-modal Hidden Markov Model framework using existing methods and R functions. We compare the trends and statistical fits of models that include or exclude any of the behavioural, spatial and temporal components, and perform variance partitioning on the model predictions that included all components to assess their relative importance to the movement process, both in isolation and in interaction.
Results: We apply our workflow to a case study on the movements of plains zebra, blue wildebeest and eland antelope in a South African reserve. Behavioural modes impacted movement the most, followed by diel rhythms and then the spatial environment (viz. tree cover and terrain slope). Interactions between the components often explained more of the movement variation than the marginal effect of the spatial environment did on its own. Omitting components from the analysis led either to the inability to detect relationships between input and response variables, resulting in overgeneralisations when drawing conclusions about the movement process, or to detections of questionable relationships that appeared to be spurious.
Conclusions: Our analytic workflow can be used to integrate the behavioural, temporal and spatial components of the movement process and quantify their relative contributions, thereby preventing incomplete or overly generic ecological interpretations. We demonstrate that understanding the drivers of animal movement, and ultimately the ecological phenomena that emerge from it, critically depends on considering the various components of the movement process, and especially the interactions between them.
背景:动物运动源于动物与其异质环境之间复杂的相互作用。为了更好地理解运动过程,可以将其分为行为、时间和空间三个部分。虽然已有方法可以解决这些不同的组成部分,但将它们整合到一个单一的运动分析中仍然具有挑战性:我们提出了一种分析工作流程,它整合了运动过程中的行为、时间和空间组成部分及其相互作用,还允许对这些组成部分的相对重要性进行评估。我们构建了一个日周期协变量来表示时间周期性的运动模式,如活动的日变化,并利用现有方法和 R 函数在多模态隐马尔可夫模型框架中将这三个组成部分结合起来。我们比较了包含或不包含任何行为、空间和时间成分的模型的趋势和统计拟合,并对包含所有成分的模型预测进行了方差分区,以评估它们在运动过程中的相对重要性,包括单独作用和相互作用:结果:我们将工作流程应用于南非一个保护区内平原斑马、蓝角马和伊兰羚羊运动的案例研究。行为模式对运动的影响最大,其次是昼夜节律,然后是空间环境(即树木覆盖和地形坡度)。这些因素之间的相互作用往往比空间环境本身的边际效应更能解释运动的变化。在分析中忽略成分会导致无法检测到输入变量与响应变量之间的关系,从而在得出运动过程的结论时过于笼统,或者检测到可疑的关系,而这些关系似乎是虚假的:我们的分析工作流程可用于整合运动过程的行为、时间和空间组成部分,并量化它们的相对贡献,从而防止不完整或过于笼统的生态解释。我们证明,理解动物运动的驱动因素以及最终由此产生的生态现象,关键在于考虑运动过程的各个组成部分,尤其是它们之间的相互作用。
{"title":"Unveiling the roles of temporal periodicity, the spatial environment and behavioural modes in terrestrial animal movement.","authors":"Hans Linssen, Henrik J de Knegt, Jasper A J Eikelboom","doi":"10.1186/s40462-024-00489-3","DOIUrl":"10.1186/s40462-024-00489-3","url":null,"abstract":"<p><strong>Background: </strong>Animal movement arises from complex interactions between animals and their heterogeneous environment. To better understand the movement process, it can be divided into behavioural, temporal and spatial components. Although methods exist to address those various components, it remains challenging to integrate them in a single movement analysis.</p><p><strong>Methods: </strong>We present an analytic workflow that integrates the behavioural, temporal and spatial components of the movement process and their interactions, which also allows for the assessment of the relative importance of those components. We construct a daily cyclic covariate to represent temporally cyclic movement patterns, such as diel variation in activity, and combine the three components in a multi-modal Hidden Markov Model framework using existing methods and R functions. We compare the trends and statistical fits of models that include or exclude any of the behavioural, spatial and temporal components, and perform variance partitioning on the model predictions that included all components to assess their relative importance to the movement process, both in isolation and in interaction.</p><p><strong>Results: </strong>We apply our workflow to a case study on the movements of plains zebra, blue wildebeest and eland antelope in a South African reserve. Behavioural modes impacted movement the most, followed by diel rhythms and then the spatial environment (viz. tree cover and terrain slope). Interactions between the components often explained more of the movement variation than the marginal effect of the spatial environment did on its own. Omitting components from the analysis led either to the inability to detect relationships between input and response variables, resulting in overgeneralisations when drawing conclusions about the movement process, or to detections of questionable relationships that appeared to be spurious.</p><p><strong>Conclusions: </strong>Our analytic workflow can be used to integrate the behavioural, temporal and spatial components of the movement process and quantify their relative contributions, thereby preventing incomplete or overly generic ecological interpretations. We demonstrate that understanding the drivers of animal movement, and ultimately the ecological phenomena that emerge from it, critically depends on considering the various components of the movement process, and especially the interactions between them.</p>","PeriodicalId":54288,"journal":{"name":"Movement Ecology","volume":"12 1","pages":"57"},"PeriodicalIF":3.4,"publicationDate":"2024-08-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11348775/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142074461","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-20DOI: 10.1186/s40462-024-00496-4
Coralie Moccetti, Nicola Sperlich, Grégoire Saboret, Hanna Ten Brink, Jakob Brodersen
Background: Seasonal movements of animals often result in the transfer of large amounts of energy and nutrients across ecosystem boundaries, which may have large consequences on local food webs through various pathways. While this is known for both terrestrial- and aquatic organisms, quantitative estimates on its effects on food web structure and identification of key pathways are scarce, due to the difficulty in obtaining replication on ecosystem level with negative control, i.e. comparable systems without migration.
Methods: In this study, we estimate the impact of Arctic charr (Salvelinus alpinus) migration on riverine ecosystem structure, by comparing multiple streams with strictly resident populations above natural migration barriers with streams below those barriers harboring partially migratory populations. We compared density estimates and size structure between above and below populations. Diet differences were examined through the analysis of stomach contents, changes in trophic position were examined by using stable isotopes. To infer growth rate of resident individuals, back-growth calculation was performed using otoliths.
Results: We find higher densities of small juveniles in partially migratory populations, where juvenile Arctic charr show initially lower growth, likely due to higher intraspecific competition. After reaching a size, where they can start feeding on eggs and smaller juveniles, which are both more frequent in partially migratory populations, growth surpasses that of resident populations. Cannibalism induced by high juvenile densities occurred almost exclusively in populations with migration and represents an altered energy pathway to the food web. The presence of large cannibalistic charr feeding on smaller ones that have a similar trophic level as charr from strictly resident populations (based on stomach content) coupled with steeper δ15N-size regression slopes illustrate the general increase of food chain length in systems with migration.
Conclusions: Our results thus suggest that the consumption of migration-derived resources may result in longer food chains through middle-up rather than bottom-up effects. Furthermore, by occupying the apex of the food chain and feeding on juvenile conspecifics, resident individuals experience reduced competition with their young counterparts, which potentially balances their fitness with migratory individuals.
{"title":"Migratory-derived resources induce elongated food chains through middle-up food web effects.","authors":"Coralie Moccetti, Nicola Sperlich, Grégoire Saboret, Hanna Ten Brink, Jakob Brodersen","doi":"10.1186/s40462-024-00496-4","DOIUrl":"10.1186/s40462-024-00496-4","url":null,"abstract":"<p><strong>Background: </strong>Seasonal movements of animals often result in the transfer of large amounts of energy and nutrients across ecosystem boundaries, which may have large consequences on local food webs through various pathways. While this is known for both terrestrial- and aquatic organisms, quantitative estimates on its effects on food web structure and identification of key pathways are scarce, due to the difficulty in obtaining replication on ecosystem level with negative control, i.e. comparable systems without migration.</p><p><strong>Methods: </strong>In this study, we estimate the impact of Arctic charr (Salvelinus alpinus) migration on riverine ecosystem structure, by comparing multiple streams with strictly resident populations above natural migration barriers with streams below those barriers harboring partially migratory populations. We compared density estimates and size structure between above and below populations. Diet differences were examined through the analysis of stomach contents, changes in trophic position were examined by using stable isotopes. To infer growth rate of resident individuals, back-growth calculation was performed using otoliths.</p><p><strong>Results: </strong>We find higher densities of small juveniles in partially migratory populations, where juvenile Arctic charr show initially lower growth, likely due to higher intraspecific competition. After reaching a size, where they can start feeding on eggs and smaller juveniles, which are both more frequent in partially migratory populations, growth surpasses that of resident populations. Cannibalism induced by high juvenile densities occurred almost exclusively in populations with migration and represents an altered energy pathway to the food web. The presence of large cannibalistic charr feeding on smaller ones that have a similar trophic level as charr from strictly resident populations (based on stomach content) coupled with steeper δ<sup>15</sup>N-size regression slopes illustrate the general increase of food chain length in systems with migration.</p><p><strong>Conclusions: </strong>Our results thus suggest that the consumption of migration-derived resources may result in longer food chains through middle-up rather than bottom-up effects. Furthermore, by occupying the apex of the food chain and feeding on juvenile conspecifics, resident individuals experience reduced competition with their young counterparts, which potentially balances their fitness with migratory individuals.</p>","PeriodicalId":54288,"journal":{"name":"Movement Ecology","volume":"12 1","pages":"56"},"PeriodicalIF":3.4,"publicationDate":"2024-08-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11337878/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142009947","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-06DOI: 10.1186/s40462-024-00494-6
Prabhleen Kaur, Simone Ciuti, Federico Ossi, Francesca Cagnacci, Nicolas Morellet, Anne Loison, Kamal Atmeh, Philip McLoughlin, Adele K Reinking, Jeffrey L Beck, Anna C Ortega, Matthew Kauffman, Mark S Boyce, Amy Haigh, Anna David, Laura L Griffin, Kimberly Conteddu, Jane Faull, Michael Salter-Townshend
Background: Social network analysis of animal societies allows scientists to test hypotheses about social evolution, behaviour, and dynamic processes. However, the accuracy of estimated metrics depends on data characteristics like sample proportion, sample size, and frequency. A protocol is needed to assess for bias and robustness of social network metrics estimated for the animal populations especially when a limited number of individuals are monitored.
Methods: We used GPS telemetry datasets of five ungulate species to combine known social network approaches with novel ones into a comprehensive five-step protocol. To quantify the bias and uncertainty in the network metrics obtained from a partial population, we presented novel statistical methods which are particularly suited for autocorrelated data, such as telemetry relocations. The protocol was validated using a sixth species, the fallow deer, with a known population size where of the individuals have been directly monitored.
Results: Through the protocol, we demonstrated how pre-network data permutations allow researchers to assess non-random aspects of interactions within a population. The protocol assesses bias in global network metrics, obtains confidence intervals, and quantifies uncertainty of global and node-level network metrics based on the number of nodes in the network. We found that global network metrics like density remained robust even with a lowered sample size, while local network metrics like eigenvector centrality were unreliable for four of the species. The fallow deer network showed low uncertainty and bias even at lower sampling proportions, indicating the importance of a thoroughly sampled population while demonstrating the accuracy of our evaluation methods for smaller samples.
Conclusions: The protocol allows researchers to analyse GPS-based radio-telemetry or other data to determine the reliability of social network metrics. The estimates enable the statistical comparison of networks under different conditions, such as analysing daily and seasonal changes in the density of a network. The methods can also guide methodological decisions in animal social network research, such as sampling design and allow more accurate ecological inferences from the available data. The R package aniSNA enables researchers to implement this workflow on their dataset, generating reliable inferences and guiding methodological decisions.
{"title":"A protocol for assessing bias and robustness of social network metrics using GPS based radio-telemetry data.","authors":"Prabhleen Kaur, Simone Ciuti, Federico Ossi, Francesca Cagnacci, Nicolas Morellet, Anne Loison, Kamal Atmeh, Philip McLoughlin, Adele K Reinking, Jeffrey L Beck, Anna C Ortega, Matthew Kauffman, Mark S Boyce, Amy Haigh, Anna David, Laura L Griffin, Kimberly Conteddu, Jane Faull, Michael Salter-Townshend","doi":"10.1186/s40462-024-00494-6","DOIUrl":"10.1186/s40462-024-00494-6","url":null,"abstract":"<p><strong>Background: </strong>Social network analysis of animal societies allows scientists to test hypotheses about social evolution, behaviour, and dynamic processes. However, the accuracy of estimated metrics depends on data characteristics like sample proportion, sample size, and frequency. A protocol is needed to assess for bias and robustness of social network metrics estimated for the animal populations especially when a limited number of individuals are monitored.</p><p><strong>Methods: </strong>We used GPS telemetry datasets of five ungulate species to combine known social network approaches with novel ones into a comprehensive five-step protocol. To quantify the bias and uncertainty in the network metrics obtained from a partial population, we presented novel statistical methods which are particularly suited for autocorrelated data, such as telemetry relocations. The protocol was validated using a sixth species, the fallow deer, with a known population size where <math><mrow><mo>∼</mo> <mn>85</mn> <mo>%</mo></mrow> </math> of the individuals have been directly monitored.</p><p><strong>Results: </strong>Through the protocol, we demonstrated how pre-network data permutations allow researchers to assess non-random aspects of interactions within a population. The protocol assesses bias in global network metrics, obtains confidence intervals, and quantifies uncertainty of global and node-level network metrics based on the number of nodes in the network. We found that global network metrics like density remained robust even with a lowered sample size, while local network metrics like eigenvector centrality were unreliable for four of the species. The fallow deer network showed low uncertainty and bias even at lower sampling proportions, indicating the importance of a thoroughly sampled population while demonstrating the accuracy of our evaluation methods for smaller samples.</p><p><strong>Conclusions: </strong>The protocol allows researchers to analyse GPS-based radio-telemetry or other data to determine the reliability of social network metrics. The estimates enable the statistical comparison of networks under different conditions, such as analysing daily and seasonal changes in the density of a network. The methods can also guide methodological decisions in animal social network research, such as sampling design and allow more accurate ecological inferences from the available data. The R package aniSNA enables researchers to implement this workflow on their dataset, generating reliable inferences and guiding methodological decisions.</p>","PeriodicalId":54288,"journal":{"name":"Movement Ecology","volume":"12 1","pages":"55"},"PeriodicalIF":3.4,"publicationDate":"2024-08-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11304672/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141898884","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-01DOI: 10.1186/s40462-024-00495-5
Tianhao Zhao, Wieland Heim, Raphaël Nussbaumer, Mariëlle van Toor, Guoming Zhang, Arne Andersson, Johan Bäckman, Zongzhuang Liu, Gang Song, Magnus Hellström, Jacob Roved, Yang Liu, Staffan Bensch, Bregje Wertheim, Fumin Lei, Barbara Helm
Background: Small songbirds respond and adapt to various geographical barriers during their annual migration. Global flyways reveal the diverse migration strategies in response to different geographical barriers, among which are high-elevation plateaus. However, few studies have been focused on the largest and highest plateau in the world, the Qinghai-Tibet Plateau (QTP) which poses a significant barrier to migratory passerines. The present study explored the annual migration routes and strategies of a population of Siberian Rubythroats (Calliope calliope) that breed on the north-eastern edge of the QTP.
Methods: Over the period from 2021 to 2023, we applied light-level geolocators (13 deployed, seven recollected), archival GPS tags (45 deployed, 17 recollected), and CAnMove multi-sensor loggers (with barometer, accelerometer, thermometer, and light sensor, 20 deployed, six recollected) to adult males from the breeding population of Siberian Rubythroat on the QTP. Here we describe the migratory routes and phenology extracted or inferred from the GPS and multi-sensor logger data, and used a combination of accelerometric and barometric data to describe the elevational migration pattern, flight altitude, and flight duration. All light-level geolocators failed to collect suitable data.
Results: Both GPS locations and positions derived from pressure-based inference revealed that during autumn, the migration route detoured from the bee-line between breeding and wintering grounds, leading to a gradual elevational decrease. The spring route was more direct, with more flights over mountainous areas in western China. This different migration route during spring probably reflects a strategy for faster migration, which corresponds with more frequent long nocturnal migration flights and shorter stopovers during spring migration than in autumn. The average flight altitude (1856 ± 781 m above sea level) was correlated with ground elevation but did not differ between the seasons.
Conclusions: Our finding indicates strong, season-dependent impact of the Qinghai-Tibet Plateau on shaping passerine migration strategies. We hereby call for more attention to the unexplored central-China flyway to extend our knowledge on the environment-migration interaction among small passerines.
{"title":"Seasonal migration patterns of Siberian Rubythroat (Calliope calliope) facing the Qinghai-Tibet Plateau.","authors":"Tianhao Zhao, Wieland Heim, Raphaël Nussbaumer, Mariëlle van Toor, Guoming Zhang, Arne Andersson, Johan Bäckman, Zongzhuang Liu, Gang Song, Magnus Hellström, Jacob Roved, Yang Liu, Staffan Bensch, Bregje Wertheim, Fumin Lei, Barbara Helm","doi":"10.1186/s40462-024-00495-5","DOIUrl":"10.1186/s40462-024-00495-5","url":null,"abstract":"<p><strong>Background: </strong>Small songbirds respond and adapt to various geographical barriers during their annual migration. Global flyways reveal the diverse migration strategies in response to different geographical barriers, among which are high-elevation plateaus. However, few studies have been focused on the largest and highest plateau in the world, the Qinghai-Tibet Plateau (QTP) which poses a significant barrier to migratory passerines. The present study explored the annual migration routes and strategies of a population of Siberian Rubythroats (Calliope calliope) that breed on the north-eastern edge of the QTP.</p><p><strong>Methods: </strong>Over the period from 2021 to 2023, we applied light-level geolocators (13 deployed, seven recollected), archival GPS tags (45 deployed, 17 recollected), and CAnMove multi-sensor loggers (with barometer, accelerometer, thermometer, and light sensor, 20 deployed, six recollected) to adult males from the breeding population of Siberian Rubythroat on the QTP. Here we describe the migratory routes and phenology extracted or inferred from the GPS and multi-sensor logger data, and used a combination of accelerometric and barometric data to describe the elevational migration pattern, flight altitude, and flight duration. All light-level geolocators failed to collect suitable data.</p><p><strong>Results: </strong>Both GPS locations and positions derived from pressure-based inference revealed that during autumn, the migration route detoured from the bee-line between breeding and wintering grounds, leading to a gradual elevational decrease. The spring route was more direct, with more flights over mountainous areas in western China. This different migration route during spring probably reflects a strategy for faster migration, which corresponds with more frequent long nocturnal migration flights and shorter stopovers during spring migration than in autumn. The average flight altitude (1856 ± 781 m above sea level) was correlated with ground elevation but did not differ between the seasons.</p><p><strong>Conclusions: </strong>Our finding indicates strong, season-dependent impact of the Qinghai-Tibet Plateau on shaping passerine migration strategies. We hereby call for more attention to the unexplored central-China flyway to extend our knowledge on the environment-migration interaction among small passerines.</p>","PeriodicalId":54288,"journal":{"name":"Movement Ecology","volume":"12 1","pages":"54"},"PeriodicalIF":3.4,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11295652/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141876680","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-31DOI: 10.1186/s40462-024-00490-w
Martinique J Chavez, Phaedra Budy, Casey A Pennock, Thomas P Archdeacon, Peter D MacKinnon
Background: Unfettered movement among habitats is crucial for fish to access patchily distributed resources and complete their life cycle, but many riverscapes in the American Southwest are fragmented by dams and dewatering. The endangered Rio Grande silvery minnow (Hybognathus amarus, RGSM) persists in a fragmented remnant of its former range (ca. 5%), and its movement ecology is understudied.
Methods: We tracked movements of hatchery-reared RGSM, tagged with passive integrated transponder tags, using stationary and mobile antennas from 2019 to 2022. We quantified probability of movement and total distance moved by RGSM released above and below a dam. We then assessed how well two prevailing riverine movement theories (i.e., restricted movement paradigm [RMP] and colonization cycle hypothesis [CCH]) explained RGSM movement patterns.
Results: We detected 36.8% of released RGSM (n = 37,215) making at least one movement. Movements were leptokurtic and substantially greater than expected based on the RMP for both stationary (1.7-5.9 m) and mobile (30.3-77.8 m) individuals. On average, RGSM were detected at large for 75 days and moved a total of 12.2 rkm within a year. The maximum total distance moved by RGSM was 103 rkm. Similarly, we observed a multimodal distribution of detected range sizes with a mean detected range of 2.4 rkm and a maximum detected range of 78.2 rkm. We found little support for an upstream movement bias, as expected under the CCH, and most movements (74%) were directed downstream.
Conclusions: Our data suggest RGSM are highly mobile, with the ability to make long-distance movements. Neither movement theory adequately described movement patterns of RGSM; instead, our findings support a nomadic movement pattern and an apparent drift paradox matching recent studies of other pelagic-broadcast spawning minnows where populations persist upstream despite experiencing downstream drift as larvae. Resolution of the drift paradox may be achieved through further, targeted studies into different aspects of the species' life history. Quantification of RGSM movement provides crucial insights into the species' movement ecology and may help define the appropriate scale of recovery efforts.
{"title":"Movement patterns of a small-bodied minnow suggest nomadism in a fragmented, desert river.","authors":"Martinique J Chavez, Phaedra Budy, Casey A Pennock, Thomas P Archdeacon, Peter D MacKinnon","doi":"10.1186/s40462-024-00490-w","DOIUrl":"10.1186/s40462-024-00490-w","url":null,"abstract":"<p><strong>Background: </strong>Unfettered movement among habitats is crucial for fish to access patchily distributed resources and complete their life cycle, but many riverscapes in the American Southwest are fragmented by dams and dewatering. The endangered Rio Grande silvery minnow (Hybognathus amarus, RGSM) persists in a fragmented remnant of its former range (ca. 5%), and its movement ecology is understudied.</p><p><strong>Methods: </strong>We tracked movements of hatchery-reared RGSM, tagged with passive integrated transponder tags, using stationary and mobile antennas from 2019 to 2022. We quantified probability of movement and total distance moved by RGSM released above and below a dam. We then assessed how well two prevailing riverine movement theories (i.e., restricted movement paradigm [RMP] and colonization cycle hypothesis [CCH]) explained RGSM movement patterns.</p><p><strong>Results: </strong>We detected 36.8% of released RGSM (n = 37,215) making at least one movement. Movements were leptokurtic and substantially greater than expected based on the RMP for both stationary (1.7-5.9 m) and mobile (30.3-77.8 m) individuals. On average, RGSM were detected at large for 75 days and moved a total of 12.2 rkm within a year. The maximum total distance moved by RGSM was 103 rkm. Similarly, we observed a multimodal distribution of detected range sizes with a mean detected range of 2.4 rkm and a maximum detected range of 78.2 rkm. We found little support for an upstream movement bias, as expected under the CCH, and most movements (74%) were directed downstream.</p><p><strong>Conclusions: </strong>Our data suggest RGSM are highly mobile, with the ability to make long-distance movements. Neither movement theory adequately described movement patterns of RGSM; instead, our findings support a nomadic movement pattern and an apparent drift paradox matching recent studies of other pelagic-broadcast spawning minnows where populations persist upstream despite experiencing downstream drift as larvae. Resolution of the drift paradox may be achieved through further, targeted studies into different aspects of the species' life history. Quantification of RGSM movement provides crucial insights into the species' movement ecology and may help define the appropriate scale of recovery efforts.</p>","PeriodicalId":54288,"journal":{"name":"Movement Ecology","volume":"12 1","pages":"52"},"PeriodicalIF":3.4,"publicationDate":"2024-07-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11293174/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141861615","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-31DOI: 10.1186/s40462-024-00488-4
Kendall L Calhoun, Thomas Connor, Kaitlyn M Gaynor, Amy Van Scoyoc, Alex McInturff, Samantha E S Kreling, Justin S Brashares
Background: Movement plays a key role in allowing animal species to adapt to sudden environmental shifts. Anthropogenic climate and land use change have accelerated the frequency of some of these extreme disturbances, including megafire. These megafires dramatically alter ecosystems and challenge the capacity of several species to adjust to a rapidly changing landscape. Ungulates and their movement behaviors play a central role in the ecosystem functions of fire-prone ecosystems around the world. Previous work has shown behavioral plasticity is an important mechanism underlying whether large ungulates are able to adjust to recent changes in their environments effectively. Ungulates may respond to the immediate effects of megafire by adjusting their movement and behavior, but how these responses persist or change over time following disturbance is poorly understood.
Methods: We examined how an ecologically dominant ungulate with strong site fidelity, Columbian black-tailed deer (Odocoileus hemionus columbianus), adjusted its movement and behavior in response to an altered landscape following a megafire. To do so, we collected GPS data from 21 individual female deer over the course of a year to compare changes in home range size over time and used resource selection functions (RSFs) and hidden Markov movement models (HMMs) to assess changes in behavior and habitat selection.
Results: We found compelling evidence of adaptive capacity across individual deer in response to megafire. Deer avoided exposed and severely burned areas that lack forage and could be riskier for predation immediately following megafire, but they later altered these behaviors to select areas that burned at higher severities, potentially to take advantage of enhanced forage.
Conclusions: These results suggest that despite their high site fidelity, deer can navigate altered landscapes to track rapid shifts in encounter risk with predators and resource availability. This successful adjustment of movement and behavior following extreme disturbance could help facilitate resilience at broader ecological scales.
{"title":"Movement behavior in a dominant ungulate underlies successful adjustment to a rapidly changing landscape following megafire.","authors":"Kendall L Calhoun, Thomas Connor, Kaitlyn M Gaynor, Amy Van Scoyoc, Alex McInturff, Samantha E S Kreling, Justin S Brashares","doi":"10.1186/s40462-024-00488-4","DOIUrl":"10.1186/s40462-024-00488-4","url":null,"abstract":"<p><strong>Background: </strong>Movement plays a key role in allowing animal species to adapt to sudden environmental shifts. Anthropogenic climate and land use change have accelerated the frequency of some of these extreme disturbances, including megafire. These megafires dramatically alter ecosystems and challenge the capacity of several species to adjust to a rapidly changing landscape. Ungulates and their movement behaviors play a central role in the ecosystem functions of fire-prone ecosystems around the world. Previous work has shown behavioral plasticity is an important mechanism underlying whether large ungulates are able to adjust to recent changes in their environments effectively. Ungulates may respond to the immediate effects of megafire by adjusting their movement and behavior, but how these responses persist or change over time following disturbance is poorly understood.</p><p><strong>Methods: </strong>We examined how an ecologically dominant ungulate with strong site fidelity, Columbian black-tailed deer (Odocoileus hemionus columbianus), adjusted its movement and behavior in response to an altered landscape following a megafire. To do so, we collected GPS data from 21 individual female deer over the course of a year to compare changes in home range size over time and used resource selection functions (RSFs) and hidden Markov movement models (HMMs) to assess changes in behavior and habitat selection.</p><p><strong>Results: </strong>We found compelling evidence of adaptive capacity across individual deer in response to megafire. Deer avoided exposed and severely burned areas that lack forage and could be riskier for predation immediately following megafire, but they later altered these behaviors to select areas that burned at higher severities, potentially to take advantage of enhanced forage.</p><p><strong>Conclusions: </strong>These results suggest that despite their high site fidelity, deer can navigate altered landscapes to track rapid shifts in encounter risk with predators and resource availability. This successful adjustment of movement and behavior following extreme disturbance could help facilitate resilience at broader ecological scales.</p>","PeriodicalId":54288,"journal":{"name":"Movement Ecology","volume":"12 1","pages":"53"},"PeriodicalIF":3.4,"publicationDate":"2024-07-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11293098/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141861614","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-13DOI: 10.1186/s40462-024-00491-9
Andrea Cardini, Giulio Melone, Paul O'Higgins, Diego Fontaneto
Background: Movement is a defining aspect of animals, but it is rarely studied using quantitative methods in microscopic invertebrates. Bdelloid rotifers are a cosmopolitan class of aquatic invertebrates of great scientific interest because of their ability to survive in very harsh environment and also because they represent a rare example of an ancient lineage that only includes asexually reproducing species. In this class, Adineta ricciae has become a model species as it is unusually easy to culture. Yet, relatively little is known of its ethology and almost nothing on how it behaves during feeding.
Methods: To explore feeding behaviour in A. ricciae, as well as to provide an example of application of computational ethology in a microscopic invertebrate, we apply Procrustes motion analysis in combination with ordination and clustering methods to a laboratory bred sample of individuals recorded during feeding.
Results: We demonstrate that movement during feeding can be accurately described in a simple two-dimensional shape space with three main 'modes' of motion. Foot telescoping, with the body kept straight, is the most frequent 'mode', but it is accompanied by periodic rotations of the foot together with bending while the foot is mostly retracted.
Conclusions: Procrustes motion analysis is a relatively simple but effective tool for describing motion during feeding in A. ricciae. The application of this method generates quantitative data that could be analysed in relation to genetic and ecological differences in a variety of experimental settings. The study provides an example that is easy to replicate in other invertebrates, including other microscopic animals whose behavioural ecology is often poorly known.
{"title":"Exploring motion using geometric morphometrics in microscopic aquatic invertebrates: 'modes' and movement patterns during feeding in a bdelloid rotifer model species.","authors":"Andrea Cardini, Giulio Melone, Paul O'Higgins, Diego Fontaneto","doi":"10.1186/s40462-024-00491-9","DOIUrl":"10.1186/s40462-024-00491-9","url":null,"abstract":"<p><strong>Background: </strong>Movement is a defining aspect of animals, but it is rarely studied using quantitative methods in microscopic invertebrates. Bdelloid rotifers are a cosmopolitan class of aquatic invertebrates of great scientific interest because of their ability to survive in very harsh environment and also because they represent a rare example of an ancient lineage that only includes asexually reproducing species. In this class, Adineta ricciae has become a model species as it is unusually easy to culture. Yet, relatively little is known of its ethology and almost nothing on how it behaves during feeding.</p><p><strong>Methods: </strong>To explore feeding behaviour in A. ricciae, as well as to provide an example of application of computational ethology in a microscopic invertebrate, we apply Procrustes motion analysis in combination with ordination and clustering methods to a laboratory bred sample of individuals recorded during feeding.</p><p><strong>Results: </strong>We demonstrate that movement during feeding can be accurately described in a simple two-dimensional shape space with three main 'modes' of motion. Foot telescoping, with the body kept straight, is the most frequent 'mode', but it is accompanied by periodic rotations of the foot together with bending while the foot is mostly retracted.</p><p><strong>Conclusions: </strong>Procrustes motion analysis is a relatively simple but effective tool for describing motion during feeding in A. ricciae. The application of this method generates quantitative data that could be analysed in relation to genetic and ecological differences in a variety of experimental settings. The study provides an example that is easy to replicate in other invertebrates, including other microscopic animals whose behavioural ecology is often poorly known.</p>","PeriodicalId":54288,"journal":{"name":"Movement Ecology","volume":"12 1","pages":"50"},"PeriodicalIF":3.4,"publicationDate":"2024-07-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11245788/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141604505","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-06DOI: 10.1186/s40462-024-00487-5
Lucretia E Olson, Joel D Sauder, Patrick A Fekety, Jessie D Golding, Carly W Lewis, Rema B Sadak, Michael K Schwartz
Background: Studies of animal habitat selection are important to identify and preserve the resources species depend on, yet often little attention is paid to how habitat needs vary depending on behavioral state. Fishers (Pekania pennanti) are known to be dependent on large, mature trees for resting and denning, but less is known about their habitat use when foraging or moving within a home range.
Methods: We used GPS locations collected during the energetically costly pre-denning season from 12 female fishers to determine fisher habitat selection during two critical behavioral activities: foraging (moving) or resting, with a focus on response to forest structure related to past forest management actions since this is a primary driver of fisher habitat configuration. We characterized behavior based on high-resolution GPS and collar accelerometer data and modeled fisher selection for these two behaviors within a home range (third-order selection). Additionally, we investigated whether fisher use of elements of forest structure or other important environmental characteristics changed as their availability changed, i.e., a functional response, for each behavior type.
Results: We found that fishers exhibited specialist selection when resting and generalist selection when moving, with resting habitat characterized by riparian drainages with dense canopy cover and moving habitat primarily influenced by the presence of mesic montane mixed conifer forest. Fishers were more tolerant of forest openings and other early succession elements when moving than resting.
Conclusions: Our results emphasize the importance of considering the differing habitat needs of animals based on their movement behavior when performing habitat selection analyses. We found that resting fishers are more specialist in their habitat needs, while foraging fishers are more generalist and will tolerate greater forest heterogeneity from past disturbance.
{"title":"Fishers (Pekania pennanti) are forest structure specialists when resting and generalists when moving: behavior influences resource selection in a northern Rocky Mountain fisher population.","authors":"Lucretia E Olson, Joel D Sauder, Patrick A Fekety, Jessie D Golding, Carly W Lewis, Rema B Sadak, Michael K Schwartz","doi":"10.1186/s40462-024-00487-5","DOIUrl":"10.1186/s40462-024-00487-5","url":null,"abstract":"<p><strong>Background: </strong>Studies of animal habitat selection are important to identify and preserve the resources species depend on, yet often little attention is paid to how habitat needs vary depending on behavioral state. Fishers (Pekania pennanti) are known to be dependent on large, mature trees for resting and denning, but less is known about their habitat use when foraging or moving within a home range.</p><p><strong>Methods: </strong>We used GPS locations collected during the energetically costly pre-denning season from 12 female fishers to determine fisher habitat selection during two critical behavioral activities: foraging (moving) or resting, with a focus on response to forest structure related to past forest management actions since this is a primary driver of fisher habitat configuration. We characterized behavior based on high-resolution GPS and collar accelerometer data and modeled fisher selection for these two behaviors within a home range (third-order selection). Additionally, we investigated whether fisher use of elements of forest structure or other important environmental characteristics changed as their availability changed, i.e., a functional response, for each behavior type.</p><p><strong>Results: </strong>We found that fishers exhibited specialist selection when resting and generalist selection when moving, with resting habitat characterized by riparian drainages with dense canopy cover and moving habitat primarily influenced by the presence of mesic montane mixed conifer forest. Fishers were more tolerant of forest openings and other early succession elements when moving than resting.</p><p><strong>Conclusions: </strong>Our results emphasize the importance of considering the differing habitat needs of animals based on their movement behavior when performing habitat selection analyses. We found that resting fishers are more specialist in their habitat needs, while foraging fishers are more generalist and will tolerate greater forest heterogeneity from past disturbance.</p>","PeriodicalId":54288,"journal":{"name":"Movement Ecology","volume":"12 1","pages":"49"},"PeriodicalIF":3.4,"publicationDate":"2024-07-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11227722/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141545550","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}