FY2020 Annual Report

Biodiversity and Biocomplexity Unit
Professor Evan Economo

 

Abstract

Our lab seeks to understand how ecological and evolutionary processes interact to generate and regulate biodiversity across spatiotemporal scales and levels of biological organization.  Living systems are diverse from gene sequences to organismal morphology to communities and ecosystems.  Our goal as biologists is not just to document and catalogue this diversity, but understand the complex interactions and dynamics that generate and sustain biological variation.  In FY2020, our research concentrated in five areas; our project on the evolution of the hyperdiverse ant radiations, our Global Ant Biodiversity Informatics (GABI) project which focuses on compiling analyzing global distributions of past and present ant biodiversity, and systematics, ecology, and evolution of Indo-Pacific ant faunas, the OKEON Churamori Project, and analyzing the evolution of organismal design using x-ray imaging.

1. Staff

  • Dr. Dan Warren, Staff Scientist
  • Dr. Francisco Hita Garcia, Staff Scientist
  • Dr. Nicholas Friedman, Postdoctoral scholar
  • Dr. Susan Kennedy, Postdoctoral Scholar
  • Dr. Alexandre Casadei Ferreira, Postdoctoral Scholar
  • Dr. Nao Takashina, JSPS Postdoctoral Fellow
  • Dr. Jamie Kass, JSPS Postdoctoral Fellow
  • Fumika Azuma, Research Unit Technician
  • Kenneth Dudley, Research Unit Technician
  • Dr. Kosmas Deligkaris, Research Unit Technician
  • Miyuki Suenaga, Research Unit Technician
  • Chisa Oshiro, Research Unit Administrator
  • Yuka Suzuki, Graduate Student
  • Yazmin Zurita-Gutierrez, Graduate Student
  • Julian Katzke, Graduate Student
  • Evropi Toulkeridou, Graduate Student
  • Aibekova Lazzat, Graduate Student
  • Gaurav Agavekar, Graduate Student
  • Shubham Gautam, Graduate Student

 

2. Activities and Findings

 

2.1 Global Ant Biodiversity Informatics (GABI) Project

Our understanding of large-scale biodiversity patterns has recently increased dramatically, but available information is strongly biased towards a few groups of vertebrates and plants. Biodiversity patterns in invertebrates, such as insects, are poorly documented despite representing the large majority of species. To address this gap in our knowledge, the Global Ant Biodiversity Informatics (GABI) project has compiled over 250 years of ant research into a single database providing distribution information for all ant species. These data can be used to support all kinds of research and are being used somehow in most of our ant projects. However, the two main analyses we are working on with these data are analyzing global ant diversification patterns across the globe, and a comparison of how global patterns of ant endemism compare with vertebrate groups.  In FY2019, we have continued to maintain and build the GABI dataset so it can be used for different research purposes.  We have published a number of manuscripts based on different aspects of ant biogeography (e.g. Guo et al 2020, Dias et al. 2020, Liu et al. 2020, Rosas-Mejia et al. 2021).  We continued and expanded a major georeferencing effort to increase the number of geolocated occurrence points available, and developed a range-mapping pipeline.  We are writing a manuscript that will introduce a new global dataset and models of global ant richness and rarity, to be submitted next fiscal year.

2.2 Evolution, Ecology, and Systematics of Hyperdiverse Ant Radiations

Over evolutionary time lineages evolve in and out of ecological niches, evolve through morphological spaces, and ranges expand and contract in geographic space. These transitions may not be independent, some phenotypes may be better suited to certain ecological habitats, some habitats may promote dispersal and colonization, and colonization of new geographic areas may lead to ecological niche shifts. These forces and constraints shape diversification on global and regional scales, but to understand them we need large scale integrated analyses of highly diverse groups.  We have projects analyzing the diversification of several hyperdiverse ant radiations, namely the genera Pheidole, Strumigenys, and Tetramorium.  Pheidole is a hyperdiverse and ecologically generalist group that dominates communities around the tropics.  We have analyzed their global diversification, morphological evolution, and community assembly on islands. Strumigenys is a leaf-litter predator that has evolved a complex trap-jaw mechanism, and we are examining the evolution of this trait in time and space.  In Tetramorium, we are analyzing biogeography, morphological evolution, and transitions between ecological generalism and specialism.  Specimen work and RAD-sequencing for phylogenomics reconstruction is ongoing for these groups.

In FY2020, we made progress on all of the projects above, with phylogenies completed for Strumigenys, Tetramorium, and Pheidole.  We published a new global phylogeny of Strumigenys (Booher et al. 2021) as part of an analysis of the evolution of trap-jaw mandibles, in addition to systematic contributions (Sharaf et al. 2021, Sharaf et al. 2020, Casadei-Ferreira et al. 2020, Liu et al. 2020, Dias et al. 2020). We also analyzed the evolution of morphological integration and modularity within and across Pheidole castes (Friedman et al. 2020).

Figure 1:  In FY2020 we published an analysis of the global diversification of the ant genus Strumigenys.  We identified widespread convergent evolution of a biomechanical innovation, ultrafast trap-jaws (from Booher et al., PLoS Biology, 2021).

2.3 Analyzing evolution of organismal design with X-ray micro-CT

Since the earliest biological studies, description and quantification of biological structures has been a basic goal of biology as well as a first step toward deeper understanding of ecological and evolutionary processes.  In Entomology, the primary imaging tools have traditionally been optical microscopy and SEM, which are essential for certain tasks and allow us to see complex structures well. But these are limited in our ability to quantitatively characterize complex shapes, surfaces, and textures.  X-Ray CT has the potential to complement existing tools by providing a digital 3D image of the interior and exterior of the organism.  These images can be manipulated, dissected, measured, and quantified.  We have been developing imaging and post-processing techniques to better quantify the functional morphology of ants, including both external and internal structures.  This provides a basis for a research program analyzing the evolution of organismal design.

In FY2020, we analyzed the evolution of organism design using a variety of systems and techniques.  First, we published a major study on the evolution of trap-jaw mandibles in the genus Strumigenys (Booher et al. 2021), identifying 7-10 independent origins of the complex mandible mechanism.  Using comparative analysis of the 3D structure, we identified an anatomical pathway linking the simpler and more complex forms.

Figure 2: Using micro-CT, phylogenetic reconstruction, and comparative analysis, we analyzed the evolution of a group of social parasites in Madagascar in the genus Pheidole (from Fischer et al., Current Biology, 2020).

In another study, we examined morphological evolution in relation to social parasitism in the genus Pheidole.  We found that ants that parasitize other ants also evolve to mimic their morphology during a radiation in Madagascar (Fischer et al. 2020).  This surprising result may suggest that ants use morphological sensing to recognize nestmates, along with more well-known chemical markers. We also analyzed the evolution of Pheidole morphology across worker castes (Friedman et al. 2020).

We continued an expanding series of studies on functional morphology of ants, including studies of leg structures (Beutel et al. 2020), digestive traits (Casadei-Ferreira et al. 2020), the ant thorax (Peeters et al. 2020), and mandibles (Casadei-Ferreira et al. 2021).

In addition to evolutionary studies, we continued our work on integrating micro-CT and 3D imagery into systematic biology, with enhanced contributions on Pheidole (Casadei-Ferreira et al. 2020), Monomorium (Sharaf et al. 2021), and Lepisiota (Sharaf et al. 2020).

Figure 3:  In a recent study (Peeters et al., Frontiers in Zoology, 2020), we analyzed how the loss of flight enabled a remodeling of the ant thorax to make them efficient ground laborers.

2.4 OKEON Churamori Project

In collaboration with other researchers OIST, in FY2013 we initiated a major initiative called the OKEON Chura-Mori Project (OKEON stands for Okinawa Environmental Observation Network).  The goal is to develop an observation system to measure and monitor the environment of Okinawa, in collaboration with the people of Okinawa.  The primary scientific goal is to develop long-term space-time data series from sites across the island.

The field network is now fully operational and collecting data every 2 weeks.  We have also been broadening the activities and partners, we now have over 140 partners in the project.  See the OKEON website for more on our activities.  In FY20230, we have focused on analyzing 2-year dataset of biweekly ant community changes across our sampling network and are now preparing a manuscript.  We continued a Pacific-wide collaboration with colleagues in the US (Rosemary Gillespie, George Roderick, Haldre Rogers) and Germany (Henrik Krehenwinkel) to deploy metabarcoding methods in Okinawa and across the Pacific islands.   Field work was conducted in Okinawa, the Marianas, and Hawaii using the same protocol to test for biogeographic differences in disturbance responses.  Data is currently being analyzed to compare across systems. 

We continued to participate in ant surveillance research in Japan, with the species arriving to many ports across the country.  We continued our OPG-funded project to use the OKEON system to monitor for fire ants and other introduced species.  We are working with community programs to use social network to identify fire ants, and use trapping methods at sensitive areas to identify the ant after it arrives.  We continue to work on our Ministry of Environment research grant for fire ant countermeasures, in collaboration with colleagues in Japan.  In FY2020 the focus was on setting up pipelines in our molecular lab, and we are fully engaged with experiments designing and testing metabarcoding methods.

2.5 Biodiversity Theory

Ecological and evolutionary processes often occur in a spatially complex environment, whether it is an archipelago of islands, patches of forest in a fragmented landscape, or a system of streams in a watershed.  This spatial structure appears on scales of meters to the sizes and arrangements of continents and interacts with biological processes on all of these scales.  Network theory offers a tool for representing the complex patterns of connectivity between ecosystems.  Our work is focused on how the structure of these networks interact with biodiversity dynamics, and how their widespread deconstruction by humans may affect biodiversity.  We also have interest in other areas of theoretical ecology and evolution, and have recently been focusing on increased connections of population genetic and ecological theory with regards to community dynamics.

In FY2020, PhD student Yuka Suzuki continued her investigations of metacommunity dynamics in spatial dispersal networks.  She published a paper about how network topology controls the transition from species sorting to mass effects (Suzuki & Economo 2021).  She is also working on an analysis of how spatial structure promotes or depresses metacommunity stability.  Postdoctoral fellow Nao Takashina also published a paper on theory for sampling biodiversity (Takashina & Economo 2021), and submitted another one on species range distribution dynamics.

3. Publications

3.1 Journals

  1. Casadei-Ferreira, A., Friedman, N.R., Economo, E.P., Pie, M.R., Feitosa, R.M. (In Press) Head and mandible shapes are highly integrated yet represent two distinct modules within and among worker sub-castes of the ant genus Pheidole. Ecology & Evolution.
  2. Booher, D., Gibson, J., Liu, C., Longino, J.T., Fisher, B.L., Janda, M., Narula, N., Mikheyev, A.S., Suarez, A., Economo, E.P. (In Press) An anatomical pathway facilitated the repeated evolution and diversification of an ultrafast trap-jaw mechanism in ants. PLoS Biology.
  3. Suzuki, Y., Economo, E.P. (In Press) From species sorting to mass effects: spatial network structure mediates the transition between metacommunity archetypes. Ecography.
  4. Ross, S.R.P-J., Friedman, N.R., Yoshimura, M., Yoshida, T., Donohue, I.*, Economo, E.P.* (2021) Utility of acoustic indices for ecological monitoring in complex sonic environments. Ecological Indicators. 121: 107114. *joint supervision
  5. Rosas-Mejia, M., Guénard, B., Aguilar-Méndez, M.J., Ghilardi, A., Vásquez-Bolaños, M., Economo, E.P., Janda, M. (2021) Introduced ants (Formicidae: Hymenoptera) in Mexico – the first database of records. Biological Invasions.
  6. Sharaf​, M. R., Mohamed, A. A., Boudinot, B. E., Wetterer, J. K., Hita Garcia, F., Al Dhafer, H. Am., Aldawood, A. S. (2021) Monomorium (Hymenoptera: Formicidae) of the Arabian Peninsula with description of two new species, M. heggyi sp. n. and M. khalidi sp. n. PeerJ 9:e10726.
  7. Ryo, M., Angelov, B., Mammola, S., Kass, J. M., Benito, B. M., Hartig, F. (2020) Explainable artificial intelligence enhances the ecological interpretability of black‐box species distribution models. Ecography 44: 199–205.
  8. Zhang, Z., Kass, J. M., Mammola, S., Koizumi, I., Li, X., Tanaka, K., Ikeda, K., Suzuki, T., Yokota, M., Usio, N. (2021) Lineage-level distribution models lead to more realistic climate change predictions for a threatened crayfish. Diversity and Distributions.
  9. Arribas, P. et al., (24 others including Kennedy, S.) (2021). Connecting high‐throughput biodiversity inventories: Opportunities for a site‐based genomic framework for global integration and synthesis. Molecular Ecology.
  10. Warren, D. L., Matzke, N. J., Cardillo, M., Baumgartner, J. B., Beaumont, L. J., Turelli, M., Glor, R. E., Huron, N. A., Simões, M., Iglesias, T. L. Piquet, J. C., Dinnage, R. (2021). ENMTools 1.0: an R package for comparative ecological biogeography. Ecography.
  11. Takashina, N., Economo, E.P. (2020) Developing generalized sampling schemes with known error properties: the case of a moving observer. Ecography 44: 293–306.
  12. Kass , J. M., Anderson, R. P., Espinosa-Lucas, A., Juárez-Jaimes, V., Martínez-Salas, E., Botello, F., Tavera, G., Flores-Martínez, J. J., Sánchez-Cordero, V. (2020) Biotic predictors with phenological information improve range estimates for migrating monarch butterflies in Mexico. Ecography 43: 341-352. Editor’s Choice. (should I remove “Editor’s Choice” from the publication pages?)
  13. Sharaf, M. R., Aldawood, A. S., Mohamed, A. A., Hita Garcia, F. (2020) The genus Lepisiota Santschi, 1926 of the Arabian Peninsula with the description of a new species, Lepisiota elbazi sp. nov. from Oman, an updated species identification key, and assessment of zoogeographic affinities. Journal of Hymenoptera Research 76: 127-152.
  14. Casadei-Ferreira, A., Economo, E.P., Feitosa, R.M. (2020) Additions to the taxonomy of Pheidole (Hymenoptera: Formicidae) from the southern grasslands of Brazil. Revista Brasileira de Entomologia 64:e20200068.
  15. Peeters, C., Keller, R.A., Khalife, A., Fischer, G., Katzke, J., Blanke, A., Economo, E.P. (2020) The loss of flight in ant workers enabled an evolutionary redesign of the thorax for ground labour. Frontiers in Zoology 17: 33.
  16. Liu, C., Fischer, G., Hita Garcia, F., Yamane, S., Liu, Q., Peng, Y.Q., Economo, E.P., Guénard, B., Pierce, N. E. (2020) Ants of the Hengduan mountains: a new altitudinal survey and updated checklist for Yunnan Province highlight an understudied insect biodiversity hotspot. ZooKeys 978: 1-171.
  17. Dinets, V., Friedman, N.R., Yoshimura, M., Ogasawara, M., Economo, E.P. (In Press) Acoustic detection of an unknown bat species in Okinawa. Mammal Study 45: 1-4.
  18. Kass, J. M., Meenan, S. I., Tinoco, N., Burneo, S. F., Anderson, R. P. (2020) Improving area of occupancy estimates for parapatric species using distribution models and support vector machines. Ecological Applications 31: e02228.
  19. Dias, R.K.S., Guénard, B., Economo, E.P., Akbar, S.A., Udayakantha, W.S., Wachkoo, A.A.A. (2020) The Ants (Hymenoptera: Formicidae) of Sri Lanka: A summary of taxonomic research and updated checklist. ZooKeys 967: 1-142.
  20. Casadei-Ferreira, A., Fischer, G., Economo, E.P. (2020) Evidence for a thoracic crop in the workers of some Pheidole species (Formicidae: Myrmicinae). Arthropod Structure & Development 59: 100977.
  21. Wepfer, P., Nakajima, Y., Radice, V., Toonen, R., Richards, Z., Ang, P., Sutthacheep, M., Chen, A., Sudek, M., Fujimura, A., Mikheyev, A.S., Economo, E.P.*, Mitarai, S.* (2020) Evolutionary biogeography of the coral genus Galaxea. Molecular Phylogenetics and Evolution 151: 1060905. *joint supervision
  22. Fischer, G., Friedman, N.R., Huang, J.P., Knowles, L.L., Fisher, B.L., Mikheyev, A.S., Economo, E.P. (2020) Socially parasitic ants evolve a mosaic of host-matching and parasitic morphological traits. Current Biology 30: 1-8.
  23. Kennedy, S. R., Krehenwinkel, H. (2020) DNA barcoding and community assembly—A simple solution to a complex problem. Molecular Ecology 29: 2318-2320.
  24. Friedman, N.R., Lecroq-Bennett, B., Fischer, G., Sarnat, E.M., Huang, J.P., Knowles, L.L., Economo, E.P. (2020) Macroevolutionary integration and modularity of phenotypes within and across ant worker castes. Ecology and Evolution 10: 9371-9383.
  25. Aoyama, Y., Yoshimura, M., Ogasawara, M., Suwabe, M., Economo, E.P. (2020) Potential economic impacts of invasion of the red imported fire ant in Okinawa, Japan. Japanese Journal of Ecology 70: 3-14. [in Japanese, original citation: 青山 夕貴子, 吉村 正志, 小笠原 昌子, 諏訪部 真友子, エコノモ P. エヴァン (2020) 沖縄県におけるヒアリの侵入・蔓延時に推定される経済的損失. 日本生態学会誌 70: 3-14.]
  26. Li, S., Huang, J., Darwell, C.T., Peng, Y. (2020) Development of 19 universal microsatellite loci for three closely related Ficus species (Moraceae) by high-throughput sequencing. Genes & Genetic Systems 95: 21-27.
  27. Miao, B.G., Peng, Y.Q., Yang, D.R., Kubota, Y., Economo, E.P., Liu, C. (2020) Climate and land-use interactively shape butterfly diversity in tropical rainforest and savanna ecosystems of southwestern China. Insect Science.
  28. Richter, A., Keller, R.A., Hita Garcia, F., Billen, J., Economo, E.P.*, Beutel, R.G.* (2020) Comparative analysis of worker head anatomy of Formica and Brachyponera (Hymenoptera: Formicidae). Arthropod Systematics & Phylogeny 78: 133-170. *joint supervision
  29. Beutel, R.G., Richter, A., Keller, R., Hita Garcia, F., Matsumura, Y., Economo, E.P., Gorb, S.N. (2020) Distal leg structures of the Aculeata (Hymenoptera): a comparative evolutionary study of Sceliphron (Sphecidae) and Formica (Formicidae). Journal of Morphology 281: 737-753.
  30. Liu, C., Friedman, N.R., Hita Garcia, F., Darwell, C., Booher, D., Mikheyev, A., Economo, E.P. (2020) Colonize, radiate, decline: unraveling the dynamics of island community assembly with Fijian trap-jaw ants. Evolution 74: 1082-1097.
  31. Cicconardi, F., Gamisch, A., Krapf, P., Wagner, H.C., Nguyen, A.D., Economo, E.P., Mikheyev, A.S., Guenard, B., Grabherr, R., Arthofer, W., di Marino, D., Steiner, F.M., Schlick-Steiner, B.C. (2020) Strong diversifying and relaxed purifying selection are shifting the evolutionary equilibrium of the alpine ant Tetramorium alpestre (Insecta: Hymenoptera) genome. Molecular Biology & Evolution 37: 2211-2227.
  32. Kass, J. M., Tingley, M. W.,  Tetsuya, T., Koike, F. (2020) Co-occurrence of invasive and native carnivorans affects occupancy patterns across environmental gradients. Biological Invasions 22: 2251–2266.
  33. Yoshimura, M., Suwabe, M., Ikeda, T., Ogasawara, M., Economo, E.P.. (2020) Development and Implementation of a workshop on alien species and Red Imported Fire Ants (RIFA) for elementary school students. Japanese Journal of Science Communication 26: 39-56 (in Japanese, original citation: 吉村正志, 諏訪部真友子, 池田貴子, 小笠原昌子, エヴァン・エコノモ (2020) 小学生向け外来種＆ヒアリ学習ワークショップの開発と実践. 科学技術コミュニケーション, 26: 39-56.)
  34. Mao, Y., Qian, H., Economo, E.P. (2020) TREEasy: an automated workflow for the inference of gene trees, species trees, and phylonetworks from molecular sequences. Molecular Ecology Resources 20: 832–840.
  35. Guo, F., Guénard, B., Economo, E.P., Deutsch, C., Bonebrake, T. (2020). Activity niches outperform thermal physiological limits in predicting global ant distributions. Journal of Biogeography 47: 829-842.

3.2 Oral and Poster Presentations

  1. Kass, J. M., Donohue, I., Economo, E. P. (2021, March 17). 土地被覆と季節性が特徴づける沖縄アリ群集の時間変動 [Land cover and seasonality characterize temporal variability of Okinawan ant communities]. The 68th Annual Meeting of the Ecological Society of Japan (Online).
  2. Casadei-Ferreira, A. (2021, February 3). Ferramentas modernas para o estudo dos insetos: O papel da morfologia no século XX [Modern tools for the study of insects: The role of morphology in the 21st century]. X Curso de Verão em Entomologia UFPR [X UFPR Entomology Summer Course]. Brazil (Online).
  3. Casadei-Ferreira, A. (2021, January 21). Comunidade LGBTQIA+ na STEM [LGBTQIA+ people in STEM]. I Seminário Integrador de Ensino, Pesquisa e Extensão (I SIEPEX) da UFDPar [I Seminar Integrator of Teaching, Research and Extension (I SIEPEX) of UFDPar]. Brazil (Online).
  4. Kennedy, S., Calaor, J., Gillespie, R., Krehenwinkel, H., Roderick, G., Rogers, H., Economo, E. (2020, December 9). Rapid characterization of island arthropod communities using DNA metabarcoding: A cross-Pacific comparison. Trends in Biodiversity and Evolution (TiBE) 2020 - Metabarcoding and Metagenomics (Online).
  5. Friedman, N. (2020, September 7). Macroevolutionary patterns of dorsoventral color patterning in birds. The 22nd Annual Meeting of the Society of Evolutionary Studies, Japan (Online).
  6. Kass, J. M., Guenard, B., Jenkins, C. N., Dudley, K., Azuma, F., Chao, A., Dunn, R. R., Fisher, B. L., Gibb, H., Parr, C., Sanders, N. J., Weiser, M. D., Economo, E. P. (2020, August 3-6). Global patterns of ant diversity and congruence with other taxa. The 105th Annual Meeting of the Ecological Society of America, USA (Online).
  7. Kennedy, S., Tsau, S., Gillespie, R., Krehenwinkel, H. (2020, August 5). A transient, diet-driven gut microbiome in the gray house spider Badumna longinqua. Model Systems for Microbiome Research, Joint Berkeley Initiative for Microbiome Sciences (Online).
  8. Friedman, N, Miller, E., Ball, J., Kasuga, H., Remeš, V., Economo, E. (2020, July 31). Beak shape in honeyeaters is a multifunctional trait linked to foraging, thermoregulation, and song. 2020 ABS Virtual Conference. USA (Online).
  9. Kennedy,S., Tsau, S., Gillespie, R., Krehenwinkel, H. (2020, June 29). A transient, diet-driven gut microbiome in the gray house spider Badumna longinqua. American Arachnological Society 2020 Virtual Summer Symposium (Online).
  10. Kennedy, S., Calaor, J., Gillespie, R., Krehenwinkel, H., Roderick, G., Rogers, H., Economo, E. (2020, May 15). Using bulk-community and gut content metabarcoding to characterize arthropod diversity across Pacific islands. Virtual Genomic Social Hour, California Academy of Sciences (Online).
  11. Toulkeridou, E., Baum, D., Doya, K., Economo, E. (2020, January 15-17). Automated Tissue Segmentation of Micro-CT images using Machine Learning Techniques and its applications to Comparative Morphology. MLM2020, the 1st International Conference on Big Data and Machine Learning in Microscopy. Kanazawa, Japan.

3.3 Seminars

  1. Deligkaris, K. (2021, January 14). Project management tools for academic teams. OIST Online Webinar: "Project management tools for academic teams". Japan (Online).
  2. Warren, D. (2021, January 14). Building Better Species Distribution Models by Modeling Nonsense and Imaginary Creatures. Max Planck - Yale Center for Biodiversity Movement and Global Change, USA (Online).
  3. Kass, J. M. (2020). ENM2020 - W13T2 - Data Subsetting. The Ecological Niche Modeling 2020 (Online).
  4. Kass, J. M. (2020). ENM2020 - W19T2 - Wallace. The Ecological Niche Modeling 2020 (Online).

3.4 Software

  1. Kass, J. M. ENMeval. Version 1.9.0. Software. (2020, December). GitHub, https://github.com/jamiemkass/ENMeval.

3.5 Blog posts for scientific journals

  1. Kass, J. M., Meenan, S. I., Tinoco, N., Burneo, S. F., & Anderson, R. P. (2021, January 13). Improving Area of Occupancy Estimates for Parapatric Species Using Distribution Models and Support Vector Machines. Bulletin of the Ecological Society of America, 102:e01813. https://doi.org/10.1002/bes2.1813
  2. Kass, J. M., Juárez-Jaimes, Flores-Martínez, J. J., Sánchez-Cordero, V. (2020, June 30). New range estimates for migrating monarch butterflies in Mexico: implementing and interpreting biotic variables and future conservation applications [Blog post]. https://www.ecography.org/blog/new-range-estimates-migrating-monarch-butterflies-mexico-implementing-and-interpreting-biotic