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Oecologia Australis 19(1): 16-31, 2015 10.4257/oeco.2015.1901.02

PUBLICATION TRENDS IN DISTRIBUTION MODELING AND THE PIONEER CONTRIBUTION OF DR. RUI CERQUEIRA TO ECOLOGICAL AND DISTRIBUTION MODELING IN BRAZIL

Maria Lucia Lorini1* and Mariana M. Vale2

1 Universidade Federal do Estado do Rio de Janeiro, Instituto de Biociências, Departamento de Ciências Naturais, Av. Pasteur, 458, Sala 411, Urca, Rio de Janeiro, RJ, Brasil. CEP: 22290-255. 2 Universidade Federal do Rio de Janeiro, Instituto de Biologia, Departamento de Ecologia, Laboratório de Vertebrados, Ilha do Fundão, Caixa Postal 68020, Rio de Janeiro, RJ, Brasil. CEP: 21941-590. E-mails: [email protected], [email protected]

ABSTRACT The quantification of species-environment relationship represents the core of predictive geographical modeling in and the root of contemporary model- ing. The correlative approaches that link known occurrences of species with environmental variation across landscapes to estimate ecological niches and geographic distributions are generally termed modeling (ENM) or species distribution modeling (SDM). The theoretical basis of these models is that each organism is adapted to specific tolerance zones or ‘‘niches’’ which, in a Grinellian sense, can be considered as the set of abiotic require- ments in which a species can maintain itself. Here we provided an overview of the publication trends on ENM/SDM, both globally and in Brazil, through a scientometric approach. We also review the most important contributions of Dr. Rui Cerqueira’s pioneer scientific research program on biogeography and distribution modeling in Brazil. The global production in the ENM/SDM field showed a growing trend in publication from 1990s on, with peaks on global production output occurring five times from 2005 to 2012. After 2009, more than a hundred articles were published yearly. In Brazil, although the production has also increased in the last decade, especially from 2006 on, the increase did not follow the magnitude of the global trend. Only after 2009 the number of articles published yearly surpassed ten. Cerqueira figures among the top ten authors in Brazil, being the only author to publish on the topic before 2002. Cerqueira has also made few, but quite important contributions to the understanding of biogeographical patterns in the Neotropics. These results highlight the pioneer contribution of Dr. Rui Cerqueira to the fields of ecological niche modeling / species distribution modeling and biogeography in Brazil, which we present and discuss here. Keywords: ecological niche modelling; Neotropical biogeography; scientometrics; Restinga; South American mammalogy.

INTRODUCTION widely distributed? What determines the limit of species distribution? Why species are distributed as they These questions have always been are? Why are there so geographically inspirational for biogeographers and restricted species while others are ecologists. Throughout the centuries Lorini & Vale 17 humans have observed and recorded more common in the 1980s, and (iii) consistent relationships between spatially explicit statistical and empirical species distributions and the physical modeling of species distribution, that environment (Elith and Leathwick 2009) began in the late 1970s, experienced and the importance of climate and terrain a massive growing since, and is characteristics to explain distributions currently the most common approach was recognized early on the scientific to quantitative modeling and mapping of writings (Humboldt and Bonpland 1807, species distributions. One of the earliest de Candolle 1855, Grinnell 1904). The ENM/SDM attempt is the niche-based quantification of species-environment spatial predictions of crop species by relationship represents the core of Henry Nix and collaborators in Australia predictive geographical modeling in (Nix et al. 1977, Guisan and Thuiller ecology and the root of contemporary 2005). This and some of the earliest species distribution modeling (Guisan numerical SDMs used environmental and Zimmermann 2000, Elith and envelope and similarity models to Leathwick 2009). The correlative describe the species’ distribution in approaches that link known occurrences relation to a set of predictors (Box 1981, of species with environmental variation Nix 1986, Elith and Leathwick 2009), across landscapes to estimate ecological sometimes combined with discriminant niches and geographic distributions function analyses. are generally termed ecological niche Logistic regression and generalized modeling (ENM) or species distribution linear models expanded on envelope and modeling (SDM) (see Peterson and similarity approaches, allowing to select Soberón 2012a,b for further terminology predictors according to their observed discussion). The theoretical basis of importance to species occurrence, and these models is that each organism is generalized additive models provided adapted to specific tolerance zones or flexibility to deal with nonlinear species’ ‘‘niches’’ which, in a Grinellian sense, responses to environment (Elith and can be considered as the set of abiotic Leathwick 2009). Next, ENM/SDM requirements in which a species can also started to use methods developed maintain a net positive rate of towards prediction, including machine increase without immigration (Soberón learning and data mining algorithms 2007, 2010, Colwell and Rangel 2009, (Elith and Leathwick 2009), such as: Soberón and Nakamura 2009). ANNs (Olden et al. 2008), multivariate The history of ENM/SDM can be adaptive regression splines (Moisen divided in three phases (Guisan and and Frescino 2002), classification and Thuiller 2005): (i) non-spatial statistical regression trees (Prasad et al. 2006, quantification of species-environment Elith et al. 2008), genetic algorithms relationship based on empirical data, (Stockwell and Peters 1999), support that peaked in the 1970s, (ii) expert- vector machines (Drake et al. 2006), based (non-statistical, non-empirical) and maximum entropy models (Phillips spatial modeling of species distribution, et al. 2006).

Oecol. Aust., 19(1): 16-31, 2015 18 Publication Trends in SDM and the Contribution of Rui Cerqueira

Comparisons among the results conservation biogeography (Franklin from the wide range of ENM/SDM 2013) and to address the Wallacean methods available revealed that many shortfall. methodological decisions taken during The purpose of this paper is two-fold. the modeling process may lead to great First, we provided an overview of the variability in the predictions (Araújo publication trends on Ecological Niche and Guisan 2006, Dormann et al. 2008). and Species Distribution Modeling, Also, as many ENM/SDM applications both globally and in Brazil, through demand extrapolation, i.e., need to a scientometric analysis. Second, project models in temporal and/or spatial we reviewed the most important domains different from which the model contributions of Dr. Rui Cerqueira, is fitted (for example, climate change Professor at the Ecology Department or biological invasion), researchers of the Federal University of Rio de developed methods that could generate Janeiro (UFRJ), in his pioneer scientific more robust predictions and minimize research program on biogeography and variation around model projections. A distribution modeling in Brazil. growing concern has recently emerged Dr. Rui Cerqueira is one of the for ensemble forecasting approaches most influential mammalogists in to improve reliability and characterize South America. In 1982 he created uncertainty (Araújo and New 2007, the Vertebrate Laboratory (LabVert) Marmion et al. 2009, Diniz-Filho et al. at the UFRJ, which develops scientific 2009, 2010, Buisson et al. 2010, Loyola research in ecology and evolution, et al. 2014). using terrestrial vertebrates as a model, ENM/SDM are widely used to infer with emphasis on mammals and birds. the ecological requirements of species and Since then, Dr. Cerqueira and his to predict their geographic distributions. students developed a research program Such models have been applied to a on vertebrates, involving various broad set of conservation, ecological and fields of ecology and evolution. He evolutionary questions (Zimmermann et has published more than 150 papers, al. 2010), including discovery of new book chapters and books on mammal of known species, discovery and vertebrate ecology, ecology of previously unknown species, spatial of animal adaptations, population conservation prioritization, assessment ecology, ecology, landscape of potential geographic ranges of ecology, ecological biogeography, and , mapping risk of conservation . Dr. Cerqueira disease transmission, forecasting the has mentored dozen of B.Sc., 37 M.Sc., effects of climate change on species 18 Ph.D. students, and 06 postdoctoral distributions and on phylogenetic scholars. His mentorship has produced a diversity, and identifying historical body of independent Brazilian scientists, refugia for (Franklin 2010, especially in the arena of mammalogy. 2013, Peterson et al. 2011). ENM/SDM In 2012, Dr. Cerqueira was elected as can be also particularly useful to support Honorary Member of the American

Oecol. Aust., 19(1): 16-31, 2015 Lorini & Vale 19

Society of Mammalogists, the Society’s production on ENM/SDM followed the highest honor, awarded to few nominees 1990’s progress in computer, statistical in recognition to their distinguished and geoinformation sciences, as well as service to mammalogy, including the theoretical advances in predictive research, teaching, student training, ecology (Guisan and Thuiller 2005, and outreach. Dr. Cerqueira’s work Alexandre et al. 2013). Indeed, the two on diet and water balance biology and review papers that summarized ENM/ on are discussed SDM’s methodology and framework somewhere else (Gentile and Kajin this – Guisan and Zimmermann (2000) and volume, Vieira et al. this volume). Here Guisan and Thuiller (2005) – are ranked we discuss the work of Dr. Cerqueira first and fourth most cited papers in the and his collaborators on biogeography, field, with 2,474 and 1,575 citations, including important contributions respectively (Web of Science, consulted to Brazilian and South American 3 August 2014). biogeography and the understanding From 2005 on, a mean year increase of biogeographical patterns in the rate on percentage of publication Neotropics, and to the development reached 1.56-fold (Figure 1). A peak of ecological niche and distribution on global production output can be modeling. identified when the mean year increase on percentage of publication surpass RESULTS AND DISCUSSION 1.5-fold, which occurred five times from 2005 to 2012. After 2009, more than a Publication trends in Species hundred articles were published yearly Distribution Modeling (Figure 1). After combining and filtering the This second increasing in global articles retrieved from WoS, Scopus production on ENM/SDM seems and SciELO, we found 994 articles to reflect the continued advances in on Ecologic Niche Modeling/Species computer, statistical, geoinformatics and Distribution Modeling (hereafter referred ecoinformatics technology, which eased to as ENM/SDM) and 85 on Ecologic the handling of large amounts of data and Niche Modeling/Species Distribution made the data accessible. Occurrence Modeling in Brazil (hereafter referred data from museum collections, surveys to as ENM/SDM in Brazil) published and monitoring programs, for example, between 1945 and 2012. were digitalized and became freely The global production in the ENM/ available via Internet portals (e.g. SDM field showed a growing trend in Global Biodiversity Information Facility publication from 1990s on, although - GBIF, www.gbif.org; VertNet, www. before 2005 the mean year increase vertnet.org; Ocean Biogeographic rate on percentage of publication did Information System - OBIS, www. not surpass 1.47-fold, and less than ten iobis.org; speciesLink, splink.cria.org. articles were published yearly (Figure br). Environmental data such as climate 1). This first increase in academic (e.g. WorldClim, www.worldclim.

Oecol. Aust., 19(1): 16-31, 2015 20 Publication Trends in SDM and the Contribution of Rui Cerqueira org; CliMond, www.climond.org), times (Web of Science, consulted 3 and land cover/use (e.g. GlobCover, August 2014). due.esrin.esa.int/globcover; CORINE Such results are in agreement with Land Cover, www.eea.europa.eu; CCI Lobo et al. (2010), indicating that - Land Cover, maps.elie.ucl.ac.be/CCI/ ENM/SDM is a field of research that viewer/index.php) also become freely become a hot topic in the ecological, available online. The most illustrative biogeographical or conservation example of the importance of compiling literature in the last two decades. Besides and breaking barriers to access of the massive increase in publications on detailed global geographic databases is ENM/SDM, two book-length syntheses WorldClim’s data, which is repeatedly are now available (Franklin 2010, and massively used in ENM/SDM Peterson et al. 2011). In addittion, the studies. WorldClim is a global climatic extensive citation of the top five papers database freely available on the web, indicates considerable popularity of described by Hijmans et al. (2005) in a the ENM/SDM techniques, as already paper cited 3,276 times (Web of Science, highlighted by Peterson and Soberón consulted 3 August 2014). In parallel, (2012a). The explosion of interest on software packages and platforms for the topic in recent decades has resulted ENM/SDM also become available from a convergence of the growing (e.g. MAXENT, www.cs.princeton. need for information on the spatial edu/~schapire/maxent; openModeller, distribution of biodiversity and new and openmodeller.sourceforge.net; ModEco, improved techniques and data suitable gis.ucmerced.edu; BIOMOD, cran.r- for addressing this need – remote project.org/web/packages/biomod2; sensing, global positioning system Dismo, cran.r-project.org/web/ technology, geographic information packages/dismo). In fact, the second systems, and statistical learning most cited paper in ENM/SDM, methods (Franklin 2010). Indeed, the Phillips et al. (2006), is the article that combination of Geoinformatics and introduced the use of the maximum Ecoinformatics is a promising field that entropy method for modeling species has great potential to optimize decision geographic distributions, implemented support for biodiversity conservation via MAXENT, a free software with a and management (Lorini et al. 2011). friendly graphical user interface. The Such synergy has contributed to ENM/ MAXENT package is one of the most SDM becoming one of the emergent popular tools for ENM/SDM, with over methods in (Skidmore 1,000 published applications since 2006 et al. 2011, Lorini et al. 2011), and part (Merow et al. 2013). Among the top of the basic “toolkit” of macroecologists five papers in ENM/SDM, Guisan and and biogeographers (Peterson and Zimmermann (2000) has been cited Soberón 2012a). 2,474 times, Phillips et al. (2006) 2,314 In regard to ENM/SDM in Brazil, times, Elith et al. (2006) 2,129 times, although the production has also and Guisan and Thuiller (2005) 1,575 increased in the last decade, until 2005

Oecol. Aust., 19(1): 16-31, 2015 Lorini & Vale 21 the mean year increase rate on percentage hand, there were a total of 241 authors of publication did not surpass 1.1-fold. contributing 85 articles related to ENM/ From 2006, however, publications SDM in Brazil. Most authors (79.2%, showed a growing trend. The mean n=191) contributed with one paper and year increase rate on percentage of 17% (n=41) with two to four papers. publication in this period reaching The authors that contributed with five about 1.66-fold, and three peaks on to ten papers (3.3%, n=8) are among the production output can be identified. top nine authors (A. T. Peterson, M. F. However, only after 2009 the number Siqueira, J. C. Nabout, P. De Marco Jr, of articles published yearly surpassed J. A. Diniz-Filho, R. Scachetti-Pereira, ten (Figure 1). R. Gurgel-Gonçalves, C. L. Terrible, In terms of authorship, thousands and R. Cerqueira). Only one author of worldwide authors have contributed contributed with more than ten articles papers to ENM/SDM. Each one of the (A. T. Peterson), and only one published top ten authors in the field contributed on ENM/SDM in Brazil before 2002 with more than 15 papers: A. T. Peterson (R. Cerqueira) (Figure 1). Therefore, (106), A. Guisan (40), W. Thuiller (33), Cerqueira figures among the top ten D. Rodder (31), N. E. Zimmerman (24), authors in Brazil, being the only one E. Martinez-Meyer (24), J. M. Lobo to publish on the topic before 2002. (22), M. Araújo (21), C. H. Graham These results highlight the pioneer (20), and J. Elith (18). On the other contribution of Rui Cerqueira to the

Figure 1. Publications on Ecologic Niche Modeling/Species Distribution Modeling from 1985 to 2012. The graph shows publications worldwide (gray), and from Brazil (black), and the years in which Dr. Rui Cerqueira has contributed publications (*).

Oecol. Aust., 19(1): 16-31, 2015 22 Publication Trends in SDM and the Contribution of Rui Cerqueira fields of species distribution modeling In what is arguably one of his team and biogeography in Brazil, that will be best scientific contributions, Gabriel presented and discussed in the following Marroig and Cerqueira uses the Amazon sections. Lagoon Hypothesis, restricted until then to geology, to explain diversification in Rui Cerqueira’s contributions to the Neotropics (Marroig and Cerqueira biogeographical studies 1997). The hypothesis combines the Cerqueira has made few, but Refuge and Riverine Barrier Hypotheses quite important contributions to the with evidences indicating the existence understanding of biogeographical of an extensive lagoon in the Amazon patterns in the Neotropics. He has basin, millions of years ago. This lagoon also been the fearful professor of was likely formed several times, in the biogeography course of Federal marine regressions and transgressions University of Rio de Janeiro bachelor cycles, when sea level increased up to 180 program in Ecology for decades. m above current level. The hypothesis Cerqueira (1982) discusses the helps to explain several biogeographical biogeography of South American patterns in South America, particularly mammals during the Quaternary, in mammals, birds and fishes. The providing a review of vegetational and Amazon Lagoon Hypothesis is climatic changes (glaciations cycles) illustrated using the example of Spider during that period, and a detailed analysis Monkeys (Ateles spp.), which display of present-day mammal distribution a of differentiated populations patterns. He presents and discusses bordering the Amazon River, forming a three main distribution patterns of South ring species. According to the authors, American mammals, using rodents, several bird and some primate groups marsupials, primates and edentates show biogeographical patterns similar examples: (i) those that fit the disjunct to Ateles. distribution of open , forests or Another important contribution mountains, (ii) those that may be related of Dr. Cerqueira to the biogeography to forest refugia, and (iii) those that seem of Neotropical fauna concerns to the not to correlate directly to historical origins and biogeographical affinities causes. Cerqueira (1982) emphasizes of restinga mammals. As discussed in how Pleistocene Refugia (Prance 1982), this volume by Vieira and collaborators, although a major advance in Neotropical water deprivation experiments with biogeography at the time, should not be rodents typical of restinga, revealed a used to explain every observed pattern relation between occupancy and of speciation. The study also defends diet choice on a local scale. Cerqueira, that the two distinct mammal faunas however, has thought of restinga at of the Quaternary cannot be easily much broader temporal and spatial correlated with major climatic events, scales. Restinga is an found because there were several such events along beaches of the Brazilian Atlantic during the Quaternary. Forest, with herbaceous and arbustive-

Oecol. Aust., 19(1): 16-31, 2015 Lorini & Vale 23 arboreal vegetation occurring on sandy (Lorini et al. 2010, Pessôa et al. 2010, coastal plains formed by marine deposits Tavares et al. 2010, 2011). in the late Quaternary (Ab’Saber 1977, According to Cerqueira (1995), Scarano 2002, Rocha et al. 2007). determining the area occupied by Cerqueira’s work on mammals of the a given species at a given time, i.e. Maricá restinga of Rio de Janeiro, the species’ geographic distribution, developed during the 90’s (e.g. forms the basis of Biogeography. Cerqueira 1984, Cerqueira et al. 1990, In the following section we present Gentile and Cerqueira 1995, Gentile et the advances on species’ distribution al. 1995, Gentile et al. 1997, Freitas et modeling in Brazil brought about by Dr. al. 1997, Santori et al. 1997) provided Rui Cerqueira’s work. Cerqueira with important insights into Rui Cerqueira’s contributions to restinga’s biogeography. In a review Species Distribution Modelling studies of the subject, he discusses restinga’s low endemicity and the prevalence Cerqueira has worked on species of a particular subset of species from distribution modeling since the nearby biomes, in light of Pleistocene beginning of his career and for a long glacial cycles, particularly sea level time was the only biologist working on changes, starting thousands of years the subject in Brazil, as demonstrated ago (Cerqueira 2000). To Cerqueira, in the section about Publication Trends what makes restinga unique are the in ENM/SDM (Figure 1). Cerqueira’s combination of origins and the particular first contribution was 30 years ago, on a ensemble of species capable of surviving study of the distribution of the opossums in that xeric environment. With marine of the genus Didephis (Cerqueira 1985), transgression, sea level increased developed during his doctorate at the up to 8 m above current level (Late University of London, in England. In Pleistocene transgression, ca. 123,000 this pioneer work, Cerqueira investigates years BP, Suguio 2001), flooding many the ecological factors that determine the portions of restingas, which would be occurrence of species of the genus in reduced and fragmented into islets. South America. He associates climatic, During subsequent marine regression altitudinal and vegetation information to these areas would reconnect, although species’ occurrence records. A qualitative within a generalized semi-arid climatic analysis reveals that the different condition. These climatic events created forms show no preference for terrain, interesting /colonization vegetation or morphoclimatic domain dynamics, which Cerqueira discusses in (sensu Ab’Saber 1977). The plotting of terms of the speciation of a few endemic sites in a latitude x altitude space also reptiles and the only bird endemic shows that “highland and lowland” of restinga, Formicivora litoralis. also does not explain the distribution These publications of Cerqueira were of the different species, contrary to was fundamental to the recent discussions what known at the time (Hershkovitz and reviews about restinga’s 1969). Cerqueira shows, however, that

Oecol. Aust., 19(1): 16-31, 2015 24 Publication Trends in SDM and the Contribution of Rui Cerqueira different forms occur in distinct climatic and analysis of variance to establish conditions by carrying a discriminant which climatic variables are related function analysis on site’s climatic data. to species occurrence, using antwren He also discusses the implications of birds of the genus Formicivora as last glacial maxima on the distribution an example. Cerqueira extracts the and isolation of different forms of the maximum and minimum climatic values genus Didelphis. More interestingly, from the sample of occurrence records, the study goes beyond a description establishing the range of values where of environmental versus distribution the species is found. He also maps relationship, mapping species’ potential the vegetation types where the species distribution by superposing vegetation is known to occur from those same and climatic data, in what Cerqueira occurrence records. Cerqueira then maps calls “a testable hypothetical map”. species’ potential distribution as the area This work served as the basis for a where the range of climatic values and publication that was, for a long time, the vegetation boundaries coincide. main reference for species distribution At that time, Cerqueira developed a modeling in Brazil (Cerqueira 1995). digital climatic database and analytical Back then the methods used to determine package (called LabVertCli), which species’ distribution (mostly drawing would interpolate data from Brazilian a line surrounding species’ outermost meteorological stations, providing occurrence records), did not take climatic data for any location within into account ecological requirements Brazil, in a precursor of today’s (Udvardy 1969). The study argues extensively used WorldClim dataset that mapping species’ distribution (see section about Publication Trends based on environmental factors is more in SDM). The method to map species’ biologically meaningful and proposes a potential distribution and the LabVertCli method for doing it. Cerqueira presents dataset was applied in a number of the “potential distribution” of a species subsequent studies, mostly with primates. as the area where it finds its “niche” A study on marmosets and tamarins in and “habitat” (sensu Whittaker et al. Rio de Janeiro State (Cerqueira et al. 1973). In order to circumscribe such 1998) shows that climate, vegetation distribution, we must first establish and topography can determine the which environmental variables are distribution of the Buffy-tufted-ear related to the species and map their Marmoset (Callithrix aurita) and the geographic distribution. The overlap of Golden-Lion-Tamarin (Leontopithecus the mapped variables should equate to rosalia), but not that of the White-tufted- species’ potential distribution. Cerqueira ear Marmoset (C. jacchus), which has then provides a detailed protocol for great invasive potential because of its gathering, treating and analyzing ability to survive in disturbed habitats. occurrence and environmental data. He Contradicting common knowledge at proposes a combination of descriptive the time, the authors conclude that the statistics, multiple discriminant analysis Golden-Lion-Tamarin is not an inhabitant

Oecol. Aust., 19(1): 16-31, 2015 Lorini & Vale 25 of Atlantic forest (sensu lato), and that Cerqueira’s most recent studies show this species' macrohabitat is characterised that he is keeping with the development by a mosaic of lowland swamp and of the field, using new datasets and broad-leaved forest. They also conclude analytical approaches. Teixeira et al. that the White-tufted-ear Marmoset (2014) proposes a method to gather displaces the Buffy-tufted-ear Marmoset needed information to determine the as a consequence of habitat degradation conservation status of rare, small- rather than by direct . This ranged, forest species classified as “Data study was an early warning about the Deficient” by the International Union for potential risk that aloctone invasive Nature Conservation (IUCN). Cerqueira marmosets (C. jacchus and C. penicilatta) and his colleagues combine maximum can represent to authoctone threatened entropy distribution modeling (Phillips species like Buffy-tufted-ear Marmoset and Dudík 2008) with connectivity (C. aurita). In a study focusing on analysis to indicate new sites for the capuchin monkeys (Cebus nigritus and search of a newly described nectar C. robustus), Cerqueira and his crew call bat (Lonchophylla peracchii), and the attention to the issue of distribution discusses its likely IUCN conservation limits in taxa exhibiting parapatric status. Finally, Cerqueira’s most recent distribution patterns (Vilanova et al. publication (Vale et al. this volume) maps 2005). Cerqueira and his colleagues show the distribution of Neotropical wild cats that vegetation is the main determinant under climate change scenarios using of these species’ distribution, while rivers the ensemble of various distribution and interspecific interactions are key in modeling algorithms (Araújo and defining their distribution boundaries. New 2007) and the most up-to-date The next study about primates, focusing climatic change forecasts (IPCC 2013). on Buffy-headed marmoset (Callithrix They predict important contraction of flaviceps), innovates by using a non-linear climatically suitable areas for virtually method (logistic regression) to model all Neotropical cats, with particularly climatic distribution, in combination worrisome predictions for the Guiña with (Olson et al. 2001) (Leopardus guigna) and the Andean as environmental predictor variable Cat (L. jacobitus). Both are already (Grelle and Cerqueira 2006). This article threatened under IUCN, and the later is also discusses the role of interspecific of special concern given that highland interactions in parapatric taxa. Finally, species are particularly susceptible to a a study with six antbirds of the genus warming climate. Drymophila assesses the role of climate Dr. Rui Cerqueira’s contribution and vegetation on species’ distribution, to the understanding of ecological showing that discriminant analysis was biogeography and distribution modeling not satisfactory for sympatric species, in Brazil is undeniable. His vision when compared with similar analysis of distribution is aligned to what is carried out on parapatric species (Rajão recently called “distribution ecology”, et al. 2010). an approach that understand distribution

Oecol. Aust., 19(1): 16-31, 2015 26 Publication Trends in SDM and the Contribution of Rui Cerqueira as referring to differences between within a scientific field (Verbeek et al. places either in individual residence 2002, Tian et al. 2008). We provide times, population abundances, species a quantitative characterization of occurrences, or probabilities of use, scientific activity related to “Species depending on ecological scales and levels Distribution Modeling” and “Species of organization (Cassini 2013). This Distribution Modeling in Brazil”, by broad view of the species’ distribution performing a scientometric analysis issue can be appreciated in Cerqueira’s of data retrieved from three scientific contribution to diet, water balance publication databases: (i) Web of and populations studies, discussed in Science (WoS) from Thompson this volume (Vieira et al. this volume, Institute for Scientific Information - Gentile and Kajin this volume). Dr. ISI (http://isiwebofknowledge.com), Rui Cerqueira has formed a crew of (ii) Scopus from Elsevier (http://www. researchers on ecological biogeography hub.sciverse.com), and (iii) Scientific and distribution modeling, as can be Electronic Library Online (SciELO) attested by his diverse co-authorship, from FAPESP/ CNPq/BIREME/OPAS/ which is carrying on his legacy on this OMS consortium (http://www.scielo. exciting and rapidly expanding scientific org). The WoS is the most detailed field. and accurate scientific database of peer-reviewed articles published in ACKNOWLEDGEMENTS English, besides being the most used for scientometric analysis (Verbeek et We are thankful to Rui Cerqueira for introducing al. 2002, Falagas et al. 2008, Gavel us to ENM/SDM back in the day. We thank the and Iselid 2008). On the other hand, the financial support of MCTI/CNPq/FAPs PELD (Grant No. 34/2012), PROBIO II/MCTI/MMA/GEF, CNPq Scopus database covers a larger number PPBio/Rede BioM.A. (Grant No. 477524/2012-2), of journals that publish articles in Brazilian Research Network on Global Climate Change languages other than English (Falagas - Rede CLIMA/MCTI, Rede CLIMA/MCTI (MMV - Grant No. 01.0405.01), FAPERJ APQ1 (Grant No. et al. 2008, Gavel and Iselid 2008). The E-=26/111.577/2014), and CNPq Universal (Grant SciELO database, although much less No. 444704/2014). comprehensive, covers South American journals that are not indexed by WoS MATERIAL AND METHODS or Scopus. We search databases for articles published from 1945 through Scientometric and bibliometric 2012, using “species distribution analysis quantify and assess trends and model*”, “ecologic* niche model*” characteristics in scientific production in or “potential distribution model*” and a particular science area. These analyses “Brazil*” as the keywords to search can be a useful tool for evaluating the parts of titles, abstracts, or keywords. results of scientific activity, providing We combined articles retrieved from a synoptic overview of the research the three databases and, after filtering area, contributing, therefore, to the to remove replications and articles not understanding of the state of the art related to ENM/SDM, we analyzed the

Oecol. Aust., 19(1): 16-31, 2015 Lorini & Vale 27 retained articles in terms of publication biogeographical range. 219 p. Springer, New year and authorship. York, USA. In addition, we also used the Lattes Cerqueira, R. 1982. South American landscapes and their mammals. Pages 539-539 in platform to search for Rui Cerqueira’s M. Mares and H. Genoways, editors. Mammalian publications on Biogeography (not Biology in South America. University of ENM/SDM). The Lattes Platform is Pittsburgh, Pittsburgh, USA. an information system maintained by Cerqueira, R. 1984. Comunidades animais. the National Council for Scientific and Pages 275-284 in L. D. Lacerda, D. S. D. Araújo, R. Cerqueira, and B. Turcq, editors. Restinga: Technological Development (CNPq) origem, estrutura e processos. CEUFF, Niterói, that manages science and technology Brazil. information about individual researchers Cerqueira, R. 1985. The distribution of and institutions working in Brazil Didelphis in South America (Polyprotodontia, (Mena-Chalco and Cesar-Junior 2009). Didelphidae). Journal of Biogeography 12:135- 145. The Lattes Platform is a valuable tool Cerqueira, R. 1995. Determinação de to obtain information on individual distribuições potenciais de espécies. Pages researchers, as all researchers and 141-161 in P. Perez, J. L. Valentin, and F. A. S. institutions are required by the CNPq to Fernandez, editors. Tópicos em Tratamento de maintain their records up to date. Dados Biológicos. PPGE/UFRJ, Rio de Janeiro, Brazil. Cerqueira, R. 2000. Biogeografia das REFERENCES restingas. Pages 65-75 in F. A. Esteves and L. D. Lacerda, editors. Ecologia de Restingas e Lagoas Ab’Saber, A. N. 1977. Os domínios Costeiras. NUPEM/UFRJ, Macaé, Brazil. morfoclimáticos na América do Sul: primeira Cerqueira, R., F. A. S. Fernadez, and M. F. aproximação. Morfologia 52:1-23. Q. S. Nunes. 1990. Mamíferos da restinga da Alexandre, B. R., M. L. Lorini, and C. Barra de Maricá. Papéis Avulsos de Zoologia E. V. Grelle. 2013. Modelagem preditiva de São Paulo 37: 141-157. distribuição de espécies ameaçadas de extinção: Cerqueira, R., G. Marroig, and L. Pinder. um panorama das pesquisas. Oecologia Australis 1998. Marmosets and Lion-Tamarins Distribution 17: 483-508. (Callithrichidae, Primates) in Rio de Janeiro Araújo, M. B., and A. Guisan. 2006. Five (or State, South-Eastern Brazil. Mammalia 62:213- so) challenges for species distribution modeling. 226. http://dx.doi.org/10.1515/mamm.1998.62. Journal of Biogeography 33:1677-1688. http:// 2.213 dx.doi.org/10.1111/j.1365-2699.2006.01584.x Colwell, R. K., and T. F. Rangel. 2009. Araújo, M., and M. New. 2007. Ensemble Hutchinson’s duality: the once and future forecasting of species distributions. Trends in Ecology and Evolution 22:42-47. http://dx.doi. niche. Proceedings o f the National Academy org/10.1016/j.tree.2006.09.010 of Sciences of the United States of America Box, E.O. 1981. Macroclimate and plant 106:19651-19658. http://dx.doi.org/10.1073/ forms: an introduction to predictive modelling in pnas.0901650106 . Vegetatio 45:127-139. de Candolle, A.P. 1855. Geographie Buisson, L., W. Thuiller, N. Casajus, S. Botanique Raisonnee: ou, Exposition des faits Lek, and G. Grenouillet. 2010. Uncertainty in principaux et des lois concernant la distribution ensemble forecasting of species distribution. géographique des plantes de l’époque actuelle. Global Change Biology 16:1147-1157. http:// Vols. 1 & 2. 1365p. V. Masson, Paris, France. dx.doi.org/10.1111/j.1365-2486.2009.02000.x Diniz-Filho, J. A. F., L. M. Bini, T. F. Rangel, Cassini, M. H. 2013. Distribution Ecology: R. D. Loyola, C. Hof, D. Nogués-Bravo, and from individual habitat use to species M. B. Araújo. 2009. Partitioning and mapping

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Oecol. Aust., 19(1): 16-31, 2015 30 Publication Trends in SDM and the Contribution of Rui Cerqueira of on Earth. Bioscience 51:933-938. http:// Rocha, C. F. D., H. G. Bergallo, M. Van dx.doi.org/10.1641/0006-3568(2001)051[0933: Sluys, M. A. S. Alves, and C. E. Jamel., 2007. TEOTWA]2.0.CO,2 The remnants of restinga habitats in the Brazilian Pessôa, L. M., W. C. Tavares, and S. Siciliano, Atlantic Forest of Rio de Janeiro state, Brazil: editors. Mamíferos de restingas e manguezais do habitat loss and risk of disappearance. Brazilian Brasil. 2010. 282p. Sociedade Brasileira de Journal of Biology 67:263-273. http://dx.doi. Mastozoologia, Rio de Janeiro, Brazil. org/10.1590/S1519-69842007000200011 Peterson, A. T., J. Soberón, R. G. Pearson, R. Santori, R. T., D. Astua-de-Moraes, C. E.V. P. Anderson, E. Martínez-Meyer, M. Nakamura, Grelle, and R. Cerqueira. 1997. Natural diet at a and M. B. Araújo. 2011. Ecological Niches restinga forest and laboratory food preferences of and Geographic Distributions. 328p. Princeton the opossum Philander frenata in Brazil. Studies University Press, Princeton, USA. in Neotropical Fauna and Environment 32:12-16. Peterson, T. A., and J. Soberón. http://dx.doi.org/10.1076/snfe.32.1.12.13460 2012a. Integrating fundamental concepts of Scarano, F. R. 2002. Structure, function ecology, biogeography, and sampling into and floristic relationships of plant communities effective ecological niche modeling and species in stressful habitats marginal to the Brazilian distribution modeling. Plant Biosystems 146:789- Atlantic rain forest. Annals of Botany 90:517- 796. http://dx.doi.org/10.1080/11263504.2012.7 524., http://dx.doi.org/10.1093/aob/mcf189 40083 Skidmore, A. K., J. Franklin, T. P. Dawson, Peterson, T. A., and J. Soberón. 2012b. Species and P. Pilesjo. 2011. Geospatial tools address distribution modeling and ecological niche emerging issues in spatial ecology: a review and modeling: getting the concepts right. Natureza & commentary on the Special Issue. International Conservação 10:1-6. http://dx.doi.org/10.4322/ Journal of Geographical Information Science natcon.2012.019 25:337-365. http://dx.doi.org/10.1080/1365881 Phillips, S. J., and M. Dudík, 2008. Modeling 6.2011.554296 of species distributions with MAXENT: new Soberón, J. 2007. Grinnellian and eltonian extensions and a comprehensive evaluation. niches and geographic distributions of species. Ecography 31:161-175. http://dx.doi.org/10.1111/ Ecological Letters 10:1115-1123. http://dx.doi. j.0906-7590.2008.5203.x org/10.1111/j.1461-0248.2007.01107.x Phillips, S. J., R. P. Anderson, and R. E. Soberón, J. M. 2010. Niche and area of Shapire. 2006. Maximum entropy modeling of distribution modeling: a population ecology species geographic distributions. Ecological perspective. Ecography 33:159-167. http:// Modelling 190:231-259. http://dx.doi. dx.doi.org/ 10.1111/j.1600-0587.2009.06074.x org/10.1016/j.ecolmodel.2005.03.026 Soberón, J. M., and M. Nakamura. 2009. Prance, G. T. 1982. Biological diversification Niches and distributional areas: concepts, in the Tropics. 714p. Columbia University Press, methods, and assumptions. Proceedings o f the New York, USA. National Academy o f Sciences o f the United Prasad, P. V. V., K. J., Boote, L. H., Allen, States of America 106:19644-19650. http:// J. E., Sheehy, and J. M. G. Thomas., 2006. dx.doi.org/10.1073/pnas.0901637106 Species, and cultivar differences in Stockwell, D. R. B., and D. P. Peters. 1999. spikelet fertility and harvest index of rice in The GARP modelling system: Problems and response to high temperature stress. Field solutions to automated spatial prediction. Journal Crops Research 95:398-411. http://dx.doi.org/ of Geographical Information Science 13:143-158. 10.1016/j.fcr.2005.04.008 http://dx.doi.org/10.1080/136588199241391 Rajão, H., R. Cerqueira, and M. L. Suguio, K. 2001. Geologia do Quaternário Lorini. 2010. Determinants of geographical e Mudanças Ambientais: Passado + Presente distribution in Atlantic Forest species of the = Futuro? 366p. Paulo’s Comunicação e Artes genus Drymophila (Aves, Thamnophilidae). Gráficas, São Paulo, Brazil. Zoologia 27:19-29. http://dx.doi.org/10.1590/ Tavares, W. C., and L. M. Pessôa. 2010. S1984-46702010000100004 Variação morfológica em populações de Trinomys

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(Thomas, 1921) de restingas e matas de baixada to climate change. Oecologia Australis this no estado do Rio de Janeiro. Pages 131-153 in volume. L. M. Pessôa, W. C. Tavares and S. Siciliano, Verbeek, A. K., K. Debackere, M. Luwel, and editors. Mamíferos de restingas e manguezais do E. Zimmermmann. 2002. Measuring progress Brasil. Sociedade Brasileira de Mastozoologia & and evolution in science and technology. I: Museu Nacional, Rio de Janeiro, Brazil. the multiple uses of bibliometric indicators. Tavares, W. C., L. M. Pessôa, and P. R. International Journal of Management Reviews Gonçalvez. 2011. New species of Cerradomys 4:179-211. http://dx.doi.org/10.1111/1468- from coastal sandy plains of southeastern 2370.00083 Brazil (Cricetidae: Sigmodontinae). Journal Vieira, M. V., R. Finotti, and R. Santori. of Mammalogy 92:645-658. http://dx.doi. in press. Diet selection and water balance org/10.1644/10-MAMM-096.1 to understand niche partitioning and spatial Teixeira, T. S. M., M. M. Weber, D. Dias, M. distribution of small mammals: a research L. Lorini, C. E. L. Esbérard, R. L. M. Novaes, program of Dr. Rui Cerqueira. Oecologia R. Cerqueira, and M. M. Vale. 2014. Combining Australis this volume. environmental suitability and habitat connectivity Vilanova, R., J. S. Silva Junior, C. E. to map rare or Data Deficient species in the V. Grelle, G. Marroig, and R. Cerqueira. Tropics. Journal for Nature Conservation 22:384- 2005. Limites vegetacionais e climáticos das 390. http://dx.doi.org/10.1016/j.jnc.2014.04.001 distribuições de Cebus nigritus e C. robustus Tian, Y., C. Wen, and S. Hong. 2008. (Cebinae, Platyrrhini). Neotropical Primates Global scientific production on GIS research 13:14-19. http://dx.doi.org/10.1896/1413- by bibliometric analysis from 1997 to 2006. 4705.13.1.14 Journal of Informetrics 2:65-74. http://dx.doi. Whittaker, R. H., S. A. Levin, and R. B. Root. org/10.1016/j.joi.2007.10.001 1973. Niche, habitat and . American Udvardy, M. D. F. 1969. Dynamic Naturalist 107:321-338. Zoogeography: with special reference to land Zimmermann, N. E., T. C. Edwards Jr., C. animals. 445 p.Van Nostrand Reinhold, New H. Graham, P. B. Pearman, and J. C. Svenning. York, USA. 2010. New trends in species distribution Vale, M. M., M. L., Lorini, and R. Cerqueira. modelling. Ecography 33(6): 985-989. http:// in press. Neotropical wild cats susceptibility dx.doi.org/10.1111/j.1600-0587.2010.06953.x

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