Canadian Journal of Zoology
Macroecological approach for scorpions (Arachnida, Scorpiones): beta-diversity in Brazilian montane forests
Journal: Canadian Journal of Zoology
Manuscript ID cjz-2019-0008.R2
Manuscript Type: Article
Date Submitted by the 09-Apr-2019 Author:
Complete List of Authors: Foerster, Stênio; Universidade Federal de Pernambuco, Programa de Pós-Graduação em Genética, Departamento de Genética DeSouza, Adriano; Universidade Federal da Paraíba, Lira, André; Universidade Federal de Pernambuco, Programa de Pós- GraduaçãoDraft em Biologia Animal, Departamento de Zoologia. Rua Professor Moraes Rego, S/N, Cidade Universitária, Cep 50670-420.
Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?:
Macroecology, Caatinga, Brejos de altitude, Scorpions, BIOGEOGRAPHY Keyword: < Discipline, ECOLOGY < Discipline, Scorpiones
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Macroecological approach for scorpions (Arachnida, Scorpiones): beta-diversity in
Brazilian montane forests
S.I.A. Foerster1*, A.M. DeSouza2, A.F.A Lira3
1Programa de Pós-Graduação em Genética, Departamento de Genética, Universidade
Federal de Pernambuco, Avenida da Engenharia, s/n, Cidade Universitária, CEP 50740-
580, Recife, Brazil. [email protected]
2Programa de Pós-Graduação em Ciências Biológicas, Departamento de Sistemática e Ecologia, Universidade Federal da DraftParaíba, Cidade Universitária, João Pessoa, Paraíba, CEP 58051-900, Brazil. [email protected]
3Programa de Pós-Graduação em Biologia Animal, Departamento de Zoologia,
Universidade Federal de Pernambuco, Rua Prof. Moraes Rego s/n, Cidade Universitária,
Recife, Brazil, CEP 50670-420. [email protected]
*Author for correspondence: [email protected]
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Macroecological approach for scorpions (Arachnida, Scorpiones): beta-diversity in
Brazilian montane forests
S.I.A. Foerster, A.M. DeSouza, A.F.A Lira
Abstract
The montane forests of northeastern Brazil are patches of rainforests, surrounded by xeric vegetation, originated during the expansion of rainforests in the Pleistocene epoch. Their historical processes make these areas ideal for biogeographical investigations of organisms, particularly in groups with low dispersion and habitat specificity, such as scorpions. We perform a macroecological investigation of the community assembly process of scorpions, disentangling the pattern of β-diversity to test the hypothesis that the similarity in the composition of scorpionDraft fauna in areas of montane forests and coastal rainforests is greater when these localities are geographically close. We also investigated if larger patches of montane forests exhibit a positive species-area relationship. Our results state that species replacement accounts for 71% of the total scorpion β-diversity in montane forest remnants. Additionally, scorpion assemblages were influenced by the spatial arrangement, with a higher similarity between the fauna of montane forests and coastal forests when these areas were geographically close. We did not find a species- area relationship in montane forest patches. The expressive contribution of species replacement to the overall β-diversity may reflect both the high environmental heterogeneity and the historical and independent colonization events that took place in these areas.
Keywords: Macroecology, Biogeography, Scorpiones, Ecology, Caatinga, Brejos de altitude, Scorpions.
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Introduction
Biogeographers and ecologists studying the origin and the variation of species
composition at a regional scale are able to progressively record the historical and
evolutive processes that generate regional diversity patterns; however, much more can be
done through providing empirical support for the development of effective conservation
strategies, such as the geographical delimitation of natural reserves. The diversity of a
given taxon on a regional scale can be expressed as a function of evolutionary factors
such as the timing and level of differentiation between lineages, as well as ecological
aspects, including events of expansion and contraction of suitable habitats (Graham and
Fine 2008). Similarly, this same perspective can be applied to explain the mechanisms of community assembly (Graham and FineDraft 2008; Cavender-Bares et al. 2009). The variation in species composition between sites within a region of interest is defined as β-diversity
(Whittaker 1960, 1972) and its origins have been discussed based on three main
hypotheses: I. biotic interactions, assuming that species composition is uniform
throughout large areas, emphasizing the role of the hierarchy of dominance among
competing species in the structuring of communities (Legendre et al. 2005; Tuomisto and
Ruokolainen 2006; Kunstler et al. 2012; Segre et al. 2014), especially in closely related
species (Weiher et al. 2011); II. random autocorrelated fluctuations, assuming that species
are equivalent in demographic and competitive aspects; however, they present random
differences in their spatial dispersion capabilities that justify the variation in species
composition among sites (Hubbell 2001; Tuomisto et al. 2003; Legendre et al. 2005;
Tuomisto and Ruokolainen 2006; Chase et al. 2010; Carvalho et al. 2011; Myers et al.
2013; Gianuca et al. 2017), in this case, low dispersal rates are commonly related to
increases in β-diversity (Soininen et al. 2007; Myers et al. 2013; Hawkins et al. 2015);
and finally, III. environmental conditions, wherein species composition is modulated by
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environmental characteristics (Legendre et al. 2005; Veech and Crist 2007; López-
González et al. 2015; Alahuhta et al. 2017). According to the last hypothesis, the landscape is a mosaic that possesses its own set of environmental characteristics
(Legendre et al. 2005), and increased levels of β-diversity are expected to occur in landscapes with high environmental heterogeneity (Heino et al. 2015; López-González et al. 2015; Liu et al. 2018).
The first step in understanding the β-diversity relies on its quantification and several methods are available to do so (Wilson and Shmida 1984; Koleff et al. 2003;
Legendre and De Cáceres 2013; Legendre 2014); some of them based on partitioning β- diversity into its two components: species replacement and richness difference (Harrison et al. 1992; Williams 1996; LennonDraft et al. 2001; Baselga 2010, 2012; Baselga and Orme 2012; Legendre 2014). According to Legendre (2014), the replacement component is a result of species turnover (gain or loss) over an ecological gradient that is sufficiently long, while the richness difference represents quantitative changes in species richness among sites. Elucidating these components is a key factor that can guide the establishment of natural reserves (Baselga 2010). For example, a high contribution of richness difference indicates the priority of areas with high levels of α-diversity, while the dominance of species replacement implies that species composition is not uniform among sites, extending the conservation priority to several sites within a landscape (Legendre et al. 2005; Baselga 2010; Gianuca et al. 2017).
Fragmented landscapes with high environmental heterogeneity tend to harbor a great variability in species composition when compared to contiguous homogeneous regions (Freestone and Inouye 2006; Veech and Crist 2007; Astorga et al. 2014; Socolar et al. 2016). In addition, special attention is given to patterns of β-diversity in topographically heterogeneous landscapes, which might be involved with dispersal
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limitation of species (Finn et al. 2006; Astorga et al. 2014; Gonzáles-Reyes et al. 2017).
The montane forest remnants (MFRs) of northeastern Brazil are good examples of
heterogeneous environments with an altitudinal contrast. These areas are pockets of
rainforests located at altitudes above 600 m (Veloso et al. 1991), surrounded by a matrix
of xeric vegetation known as Caatinga (Andrade-Lima 1982), which is classified as a
Seasonally Tropical Dry Forest (Pennington et al. 2000; Santos et al. 2012). The origin
of MFRs goes back to the Pleistocene when the Atlantic rainforest penetrated the Caatinga
domain during its expansion and persisting only in environments with a suitable
microclimate after retraction (Andrade-Lima 1982). While the Caatinga domain receives
less than 900 mm of precipitation per year, the orographic rainfall that reaches the MFRs
results in up to 1800 mm of precipitation per year (Andrade et al. 2018). Aside from its
topographical profile, the biotic componentDraft that results in the high heterogeneity of MFRs
is its complex vegetation physiognomy, compounded by typical elements of the Atlantic
forests of southeastern Brazil, and species related to the Amazon rainforest (Prance 1982;
Rizzini 1997; Ferraz et al. 1998; Rodal and Nascimento 2002; Bandeira et al. 2003;
Tabarelli and Santos 2004; Santos et al. 2007). At the same time, endemic species of
several groups occur in MFRs; however, from an evolutive perspective, their biota is still
underestimated (Santos et al. 2007). Arthropods, for example, are an extremely
representative group in tropical forests, reaching around 75 % of total biomass, and
playing a key role in many ecosystem services in these environments (Wilson and Kinne
1990; Laurance et al. 2002). Nevertheless, only a few studies on arthropods of MFRs are
available today (e.g. Lourenço 1988; Bandeira and Vasconcellos 2004; Locatelli et al.
2004; Silva et al. 2007).
Among litter-dwelling arthropods, scorpions are sensitive to environmental
disturbances in tropical forests, responding especially to the negative effects of habitat
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fragmentation (Lira et al. 2015, 2016, 2017). Scorpions are primarily sedentary animals
(Benton 1992; Peretti et al. 1999; Yamaguti and Pinto-da-Rocha 2006; Nime et al. 2016), with low dispersal rates (Polis 1985; Nime et al. 2016; Lira et al. 2018), and some degree of habitat specialization has been attributed to this taxon (Polis 1990; Prendini 2001;
Bryson Jr et al. 2013; Monod et al. 2013; Ojanguren-Affilastro et al. 2016). In addition, environmental factors, such as temperature, precipitation, edaphic properties (hardness, texture, soil and litter cover), and vegetation physiognomy have been found to be essential for structuring scorpion assemblages at the local scale (Foord et al. 2015). Thus, if we consider the MFRs of northeastern Brazil as “moisture islands” distributed across a matrix of xeric vegetation (Caatinga Dry Forest), an asymmetric contribution of the species replacement and richness difference on the overall β-diversity of scorpion assemblages in areas of MFRs could be expected.Draft In addition, if the MFRs act as refugia for scorpions in the semiarid region of Brazil, there must be a species-area relationship (Connor and
McCoy 1979, 2001) in these landscapes. Considering that low-dispersal organisms, such as scorpions, are highly informative tools to analyze biogeographical patterns at different scales of time and space (Bryson Jr et al. 2016), we investigated the scorpion assemblages of MFRs, quantifying the contribution of species replacement and richness difference to the overall β-diversity of these arachnids. We also tested the hypotheses that the similarity in the composition of the fauna of scorpions in areas of MFRs and coastal Atlantic forests is greater when these areas are geographically close to one another, and larger remnants of montane forests support a greater number of species, that is, a positive species-area relationship.
Materials and methods
Occurrence data and field work
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Data on the occurrence of scorpions were obtained from inventories conducted at
seven montane forest locations in the state of Pernambuco (Figure 1), located in the
municipalities of Águas Belas (09°5'3.24"S, 37°3'4.32"W), Bonito (Reserva Municipal
Mata do Mucury 08°30'57.72"S, 35°42'54.67"W), Brejo da Madre de Deus (Reserva
Particular do Patrimônio Natural Mata do Bitury: 08°14'16.33"S, 36°24'30.27"W),
Caruaru (Parque Natural Municipal João Vasconcelos Sobrinho: 08°22'50.03''S,
36°02'18.41''W), Inajá (Reserva Biológica da Serra Negra: 08°39'10.47"S,
38°1'39.72"W), Taquaritinga do Norte (07°54'58.29"S, 36°02'01.02"W), and Triunfo
(Mata da Furna dos Holandeses: 07°50'18.49"S, 38°4'39.74"W). Fieldwork was
conducted between April and July 2016, by two collectors equipped with tweezers and
ultraviolet light lanterns. In each MFR, random walks were performed in three nights
(07:00 pm – 01:00 am). SpecimensDraft were placed in containers containing 70% alcohol,
and were then sent to the laboratory for identification. Species identification was
performed according to Lourenço (1982, 2002), and Esposito et al. (2017). Voucher
specimens were deposited in the arachnid collections at the Universidade Federal de
Pernambuco, and Universidade Federal da Paraíba. We also included additional
information on scorpion fauna of the Araripe National Forest, a MFR situated on the
Araripe Plateau, in the state of Ceará (07°20'42"S, 39°25'6"W), and of the coastal Atlantic
forest (CAF) areas in northeastern Brazil (Table S1). As a criterion for the inclusion of
literature data in our analyzes, studies that comprise similar field procedures (collections
at night with ultraviolet light) and sample effort (hours/area) were prioritized. In this way,
to access the scorpion fauna of the Araripe National Forest, data from Azevedo et al.
(2016) were included, while for the CAF, data from Lira and Albuquerque (2014), Lira
et al. (2017), and Lira et al. (2019) were considered. The species Troglorhopalurus lacrau
(Lourenço & Pinto-da-Rocha, 1997) (= Rhopalurus brejo Lourenço, 2014) was removed
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from the dataset of Araripe Plateau, because it is a troglophile species (Esposito et al.
2017), and its microhabitat requirements does not necessarily reflect the environmental conditions provided by a MFR. For comparison purposes, data on the scorpion fauna of
Caatinga Dry Forests were also included (Araújo et al. 2010; Carmo et al. 2013).
Although the sampling procedures applied in these studies does not meet the criterion mentioned above, they are the unique inventories conducted in Caatinga areas near to the
MFRs.
Data analysis
We used a binary matrix of scorpion species per sample site (only areas of MFRs), as the input for the ‘adespatial’ packageDraft (Dray et al. 2018) in R software version 3.5.1 (R
Core Team 2018) to measure and partition β-diversity into its two components
(replacement and richness difference), based on Podani-family decomposition of
Sørensen dissimilarity coefficient (Legendre 2014). To evaluate the effect of the spatial arrangement on scorpion assemblages among all sample sites, we performed principal coordinates of neighbourhood matrix (PCNM) (Borcard and Legendre 2002; Borcard et al. 2004; Legendre and Borcard 2006), using as the input, a matrix containing the geographical distances between the sample sites obtained from their respective geographical coordinates. We applied a detrended correspondence analysis (DCA) (Hill and Gauch 1980; Gauch 1982) to measure the heterogeneity of our dataset (species × sites matrix), following the recommendations of Lepš and Šmilauer (2003), and Legendre and
Legendre (2012). Subsequently, the spatial eigenfunctions from the PCNM were used as explanatory variables in a canonical correspondence analysis (CCA), to measure the effect of spatial configuration on the scorpion assemblages of the sample sites. A permutation test for CCA (ANOVA-like) was used to test the significance of the CCA
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2 results under 9999 permutations, and the adjusted coefficient of determination (r adj) was
applied to quantify the contribution of the spatial data on the variable response
2 (community composition); r adj was also obtained using 9999 permutations. The
similarity between scorpion assemblages was measured using cluster analysis based on
the Bray-Curtis index, which is performed using the unweighted pair-group method with
arithmetic mean (UPGMA) agglomeration method, and by non-metric multidimensional
scaling (NMDS). Finally, the species-area relationship (SAR) was performed using the
power function, which is a non-linear model suitable to describe any type of SAR
2 (Dengler 2009). All analysis (PCNM, DCA, CCA, ANOVA-like, r adj, UPGMA, NMDS,
and SAR) were performed in the R software using the ‘vegan’ package (Oksanen et al.
2018). Draft The area of the MFRs was obtained by means of overlaying altimetric images in
SRTM format, and Landsat-8 bands downloaded from the Earth Explorer platform
(https://earthexplorer.usgs.gov/). The Landsat-8 bands were collected by the Operational
Land Imager Sensor, and correspond to the bands 8, 4, 3, and 2 (Barsi et al. 2014). These
bands were combined in ArcGIS version 10.2 (ESRI 2013) to produce images in RGB
color scheme with a final resolution of 15 m (Fig. S1 and S2). ArcGIS software was also
used to overlay the Landsat-8 and SRTM images, as well as to delimit the MFRs based
on altitude and vegetation cover, and subsequently, to calculate the area (Km2) of that
delimitations. Maps were also created with ArcGIS software, using images in SRTM
format and shapefiles from World Wide Fund for Nature - WWF (Olson et al. 2001),
representing the vegetation cover of the CAF (code NT0151), and the ecotonal zone
between CAF and the Caatinga Dry Forests (code NT0152).
Results
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The scorpion γ-diversity of MFRs comprises 12 species, while only six species are reported for the CAF. Six scorpion species that occur in MFRs are not shared with
CAF: Ananteris franckei Lourenço, 1982, Bothriurus rochai Mello-Leitão, 1932,
Hadrurochactas araripe Lourenço, 2010, Jaguajir agamemnon (C.L. Koch, 1839),
Jaguajir rochae (Borelli, 1910), and Tityus martinpaechi Lourenço, 2001. On the other hand, each scorpion species from CAF is present in at least one MFR (Table 1).
β-diversity analysis revealed a high contribution of the species replacement component (71%), in contrast to that of richness difference (29%), resulting in an overall
β-diversity of 0.3076. The dataset representing the scorpion assemblages of the sample sites are markedly heterogeneous (length of the first axis on DCA = 4.1075), and the scorpion species composition is influencedDraft by the spatial arrangement of the sample sites (CCA: F = 2.6331; P < 0.01). In addition, the spatial configuration of the sample sites
2 explained 51% (r adj = 0.5128) of the variation in scorpion species compositions in these localities. Cluster analysis from the scorpion assemblage, using UPGMA, resulted in two groups: the western group, comprising Araripe and Triunfo, and the central-eastern group, comprising all remaining MFRs including the CAF (Figure 2). These clusters were corroborated by non-metric multidimensional scaling (Figure 3), that resulted in a weak stress (0.0594). Finally, the steepness of the species-area relationship, inferred by the power function, did not show statistical significance (z = 0.0827; P = 0.4167).
Discussion
This study describes the pattern of scorpion β-diversity in montane forest remnants of northeastern Brazil, emphasizing the contribution of the species replacement and the richness difference components to the overall β-diversity, as well as its
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relationship with the spatial arrangement of the study sites. The high species replacement
between MFRs (71%) implies that the composition of scorpion species in these areas may
be distributed across an ecological gradient, indicating that these environments can act as
a refugia for scorpion β-diversity. The theory that the MFRs of northeastern Brazil
represent a refugium for several taxa has been discussed extensively by Andrade-Lima
(1982) and Vanzolini (1981). Subsequent studies also demonstrated the importance of
MFRs for the maintenance of vertebrates (Mares et al. 1985; Araújo and da Silva 2017;
Rocha et al. 2018), and invertebrates (Paluch et al. 2011; Monteiro et al. 2016) in the
semiarid region of Brazil. For scorpions, our results support the notion that the MFRs of
northeastern Brazil represent a microrefugium (sensu Rull 2009) as these environments
are small areas that provide suitable conditions for the persistence of some scorpion
species outside their main distributionDraft area, which is the case in the following species:
Ananteris mauryi Lourenço, 1982, Tityus brazilae Lourenço & Eickstedt, 1984 and Tityus
pusillus Pocock, 1893. These three species are associated with moist habitats under the
rainforest domain (Lourenço 1982, 1988, 2010; Bertani et al. 2008; Porto et al. 2013; Lira
et al. 2018), being rare or absent in inventories carried out in areas of Caatinga Dry Forest,
where J. rochae, Bothriurus asper Pocock, 1893 and B. rochai are the most abundant
species (Araújo et al. 2010; Carmo et al. 2013). In addition to the faunistic differences
regarding scorpion communities of the Caatinga Dry Forest and MFRs, the pattern of
scorpion β-diversity observed in our study, with an expressive contribution of the species
replacement, can be interpreted as a result of distinct colonization events and community
assembly mechanisms that occurred in the MFRs. In theory, the community assembly of
the scorpion assemblages in MFRs can be correlated with the expansion of the Amazon
and Atlantic rainforests during the climatic fluctuations of the Quaternary period (see
Sobral-Souza et al. 2015), which has been recognized as a key factor in the formation of
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the current vegetation cover in the MFRs (Tabarelli and Santos 2004; Wang et al. 2004;
Montade et al. 2014; Rohde et al. 2014).
Between the specific taxa that occur in the western MFRs (Table 1), the genus
Hadrurochactas Pocock, 1893 corresponds to a typical element of the Amazonian rainforest (Lourenço 2010, 2016). The presence of this genus on the Araripe plateau and
Maranguape region (other MFRs not included in our analysis) provides further evidence for the contribution of the Amazon rainforest to the scorpion community assemblage of these two MFRs, already suggested by Lourenço (1988, 2010). It must be taken into account, however, that the occurrence of the genus Hadrurochactas Pocock, 1893 in the
Maranguape region and Araripe Plateau is limited to the type localities of Hadrurochactas brejo (Lourenço, 1988)Draft and H. araripe. In addition, the single record of H. araripe was made in 1963, while for H. brejo, the date of collection is unknown
(Lourenço, 1988). Thus, new expeditions are needed (and encouraged) to provide a better resolution on the geographical distribution of chactid scorpions outside the Guyana-
Amazon region, that represents its main distribution range (Lourenço, 2010). On the other hand, our results indicate the contribution of the coastal Atlantic forest to the scorpion community assembly of the MFRs that comprise the central-eastern group (Figure 2).
Within the central-eastern group, the MFRs of Bonito, and Taquaritinga do Norte are situated in an ecotonal zone between the Caatinga Dry Forest and CAF (Figure 1) known as ‘Agreste’ (Ferreira et al. 2018). This ecotone is defined as a subdivision of the Caatinga
Dry Forest, and its vegetation cover is broadly composed by typical Caatinga elements, with high abundance of Cactaceae and Bromeliaceae (Andrade-Lima 1960). Despite this, these three MFRs are well-defined, containing a combination of topographic, climatic and vegetation profile that differs from the surrounding vegetation (Tabarelli and Santos
2004). The MFRs of central-eastern group harbor some scorpion species typically
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associated with the coastal Atlantic forest, such as A. mauryi, T. pusillus, and T. brazilae
(Lira and Albuquerque 2014; Lira et al. 2018), both absent in the MFRs of the western
group (Table 1, Figure 2). The pattern of scorpion species distribution among MFRs of
the central-eastern group and CAF, is very similar to those reported by Rodal and Sales
(2008) for plant communities of MFRs situated in the eastern slope of the Borborema
Plateau (a geomorphological formation that includes Bonito and Taquaritinga do Norte).
Interestingly, the hypothesis of the historical contribution of the Amazon and the coastal
Atlantic forests to the scorpion community assembly of the western and central-eastern
MFRs, respectively, is in accordance with the distribution models of Neotropical
rainforests proposed by Sobral-Souza et al. (2015). According to these models, during the
last glacial maximum, the range of the Amazon forest extended close to the region of the
western MFRs (Araripe Plateau), Draft while the coastal Atlantic forests expanded to the
regions comprising the central-eastern MFRs. In fact, there is botanical evidence
supporting the theory that the vegetation of MFRs is a result of floristic disjunction of
both the Amazon and coastal Atlantic forests (Costa et al. 2003). Therefore, the variation
in the rainforest ranges due to climatic fluctuations during the Quaternary period has been
considered an important factor in shaping the current patterns of diversity and distribution
of several taxa in the Neotropics (Haffer 1969; Cabanne et al. 2008; Carnaval and Moritz
2008; Turchetto-Zolet et al. 2013). In this way, the historical cycles of expansion and
contraction of the Neotropical rainforest during the Quaternary period may have favored
the migration of scorpion species from the Amazon and coastal Atlantic forests to the
western and central-eastern MFRs, respectively.
The matrix of xeric vegetation that separates the MFRs is represented by the
Caatinga, which is a vast and well-defined area of Seasonally Dry Tropical Forest (SDTF)
that occurs mainly in northeastern Brazil (Pennington et al. 2000; Santos et al. 2012).
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According to our spatial analysis, the similarity in the composition of scorpion species of
MFRs and CAF is greater when these areas are geographically close to one another
(Figure 3). Further, the fact that that the geographical configuration explains 51% of the scorpion species composition on the MFRs indicates that the Caatinga vegetation surrounding the MFRs is an effective barrier to the migration of these arachnids. This is true especially for scorpions that require moist environments, such as A. mauryi, T. brazilae, T. pusillus and Chactidae species (genus Hadrurochactas) because the climatic and edaphic conditions present in the xeric Caatinga are not conducive for the presence of these species. Finally, the unexpected pattern of species-area relationship (SAR) reported in our study requires further investigation, including data from other MFRs to predict if the scorpion richness is correlated to the remnant area. For the time being, the absence of SAR and the high speciesDraft replacement between the MFRs, clearly indicate that conservation strategies should not be targeted exclusively to large areas or areas with high α-diversity, as some small patches of MFRs also act as microrefugia, harboring species that could not persist in the matrix of xeric vegetation that surrounds these moist islands.
Using scorpion bionomics and evaluating the patterns of β-diversity of these arachnids, we provide the first macroecological approach testing hypotheses regarding the community assembly of this species in eight montane forest remnants of northeastern
Brazil. Furthermore, we provide empirical support that could be useful for the delimitation of priority areas for conservation purposes. The expressive contribution of species replacement to the overall scorpion β-diversity is a reflection of high environmental heterogeneity, as well as the historical and independent colonization events that took place in the MFRs. The Caatinga vegetation that surrounds the MFRs is an effective ecological barrier for the flow of rainforest scorpions, allowing several
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degrees of faunistic differentiation between the MFRs. A recent study demonstrates that
the MFRs are one of the most transformed ecoregions of northeastern Brazil (Silva and
Barbosa 2017). Thus, independent of the area of the remnant forest or the levels of α-
diversity, conservation strategies should address all MFRs, because these areas are
equally important in providing a suitable habitat not only for scorpions but to any taxa
that require mesic conditions similar to those of rainforests, and markedly different from
those of the Caatinga Dry Forest.
References
Alahuhta, J., Kosten, S., Akasaka, M., Auderset, D., Azzella, M.M., Bolpagni, R., Bove,
C.P., Chambers, P.A., Chappuis, Draft E., Clayton, J., Winton, M., Ecke, F., Gacia, E.,
Gecheva, G., Grillas, P., Hauxwell, J., Hellsten, S., Hjort, J., Hoyer, M.V., Ilg, C., Kolada,
A., Kuoppala, M., Lauridsen, T., Li, E.H., Lukács, B.A., Mjelde, M., Mikulyuk, A.,
Mormul, R.P., Nishihiro, J., Oertli, B., Rhazi, L., Rhazi, M., Sass, L., Schranz, C.,
Søndergaard, M., Yamanouchi, T., Yu, Q., Wang, H., Willby, N., Zhang, X.K., and
Heino, J. 2017. Global variation in the beta diversity of lake macrophytes is driven by
environmental heterogeneity rather than latitude. J. Biogeogr. 44: 1758–1769.
doi:10.1111/jbi.12978
Andrade-Lima, D. 1960. Estudos fitogeográficos de Pernambuco. Arquivos do Instituto
de Pesquisas Agronômicas, Recife.
Andrade-Lima, D. 1982. Present-day refuges in northeastern Brazil. In Biological
Diversification in the Tropics. Edited by G.T. Prance. Columbia University Press, New
York. pp. 245–251.
15 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 16 of 37
Andrade, E.M., Aquino, D.N., Chaves, L.C.G., and Lopes, F.B. 2017. Water as Capital and Its Uses in the Caatinga. In Caatinga: The Largest Tropical Dry Forest Region in
South America. Edited by J.M.C. da Silva, I.R. Leal, and M. Tabarelli. Springer,
Switzerland. pp. 281–302.
Araújo, H.F.P., and da Silva, J.M.C. 2017. The Avifauna of the Caatinga: Biogeography,
Ecology, and Conservation. In Caatinga: The Largest Tropical Dry Forest Region in
South America. Edited by J.M.C. da Silva, I.R. Leal, and M. Tabarelli. Springer,
Switzerland. pp. 181–210.
Araújo, C.S., Candido, D.M., de Araújo, H.F., Dias, S.C., and Vasconcellos, A. 2010.
Seasonal variations in scorpion activities (Arachnida: Scorpiones) in an area of Caatinga vegetation in northeastern Brazil.Draft Zoologia, 27(3): 372–376. doi: 10.1590/S1984- 46702010000300008
Astorga, A., Death, R., Death, F., Paavola, R., Chakraborty, M., and Muotka, T. 2014.
Habitat heterogeneity drives the geographical distribution of beta diversity: the case of
New Zealand stream invertebrates. Ecol. Evol. 4(13): 2693–2702. doi:
10.1002/ece3.1124
Azevedo, R., Moura, E.D.S., Lopes, A.S., Carvalho, L.S., Dias, S.C., and Brescovit, A.D.
2016. Arachnids from Araripe Plateau, Ceará, Brazil. Check List, 12(4): 1–9. doi:
10.15560/12.4.1920
Bandeira, A.G., and Vasconcellos, A. 2004. Efeitos de perturbações antrópicas sobre as populações de cupins (Isoptera) do Brejo dos Cavalos, Pernambuco. In Brejos de altitude em Pernambuco e Paraíba: História natural, ecologia e conservação. Edited by K.C. Pôrto,
J.J.P. Cabral, and M. Tabarelli. Ministério do Meio Ambiente, Brasília. pp. 145–152.
16 https://mc06.manuscriptcentral.com/cjz-pubs Page 17 of 37 Canadian Journal of Zoology
Bandeira, A.G., Vasconcellos, A., Silva, M.P., and Constantino, R. 2003. Effects of
habitat disturbance on the termite fauna in a highland humid forest in the Caatinga
domain, Brazil. Sociobiology, 42(1): 117–128.
Barsi, J., Lee, K., Kvaran, G., Markham, B., and Pedelty, J. 2014. The spectral response
of the Landsat-8 operational land imager. Remote Sens. 6(10): 10232–10251. doi:
10.3390/rs61010232.
Baselga, A. 2010. Partitioning the turnover and nestedness components of beta
diversity. Global Ecol. Biogeogr. 19(1): 134–143. doi: 10.1111/j.1466-
8238.2009.00490.x
Baselga, A. 2012. The relationship between species replacement, dissimilarity derived
from nestedness, and nestedness.Draft Global Ecol. Biogeogr. 21(12): 1223–1232. doi:
10.1111/j.1466-8238.2011.00756.x
Baselga, A, and Orme, C.D.L. 2012. betapart: an R package for the study of beta
diversity. Methods Ecol. Evol. 3(5): 808–812. doi: 10.1111/j.2041-210X.2012.00224.x
Benton, T.G. 1992. The ecology of the scorpion Euscorpius flavicaudis in England. J.
Zool. (Lond.) 226(3): 351–368. doi: 10.1111/j.1469-7998.1992.tb07484.x
Bertani, R., Nagahama, R.H, and Ortega, D.R.M. 2008. Novos registros de Tityus
brazilae Lourenço and Eickstedt, 1984 (Scorpiones, Buthidae) para o Brasil, e
observações sobre o habitat da espécie. Boletín de la Sociedad Entomológica
Aragonesa, 43: 513–515.
Borcard, D., and Legendre, P. 2002. All-scale spatial analysis of ecological data by means
of principal coordinates of neighbour matrices. Ecol. Model. 153(1-2): 51–68. doi:
10.1016/S0304-3800(01)00501-4
17 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 18 of 37
Borcard, D., Legendre, P., Avois-Jacquet, C., and Tuomisto, H. 2004. Dissecting the spatial structure of ecological data at multiple scales. Ecology, 85(7): 1826–1832. doi:
10.1890/03-3111
Bryson Jr, R.W., Riddle, B.R., Graham, M.R., Smith, B.T., and Prendini, L. 2013. As old as the hills: montane scorpions in southwestern North America reveal ancient associations between biotic diversification and landscape history. PLoS One, 8(1): doi:
10.1371/journal.pone.0052822
Bryson Jr, R.W., Savary, W.E., Zellmer, A.J., Bury, R.B., and McCormack, J.E. 2016.
Genomic data reveal ancient microendemism in forest scorpions across the California
Floristic Province. Mol. Ecol. 25(15): 3731–3751. doi: 10.1111/mec.13707
Cabanne, G.S., d’Horta, F.M., Sari,Draft E.H., Santos, F.R., and Miyaki, C.Y. 2008. Nuclear and mitochondrial phylogeography of the Atlantic forest endemic Xiphorhynchus fuscus
(Aves: Dendrocolaptidae): biogeography and systematics implications. Mol. Phylogenet.
Evol. 49(3): 760–773. doi: 10.1016/j.ympev.2008.09.013
Carmo, R.F.R., Amorim, H.P., and Vasconcelos, S.D. 2013. Scorpion diversity in two types of seasonally dry tropical forest in the semi-arid region of Northeastern Brazil. Biota
Neotrop. 13(2): 340–344. doi: 10.1590/S1676-06032013000200037
Carnaval, A.C., and Moritz, C. 2008. Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest. J. Biogeogr. 35(7): 1187–1201. doi:
10.1111/j.1365-2699.2007.01870.x
Carvalho, J.C., Cardoso, P., Crespo, L.C., Henriques, S., Carvalho, R., and Gomes, P.
2011. Determinants of beta diversity of spiders in coastal dunes along a gradient of mediterraneity. Divers. Distrib. 17(2): 225–234. doi: 10.1111/j.1472-4642.2010.00731.x
18 https://mc06.manuscriptcentral.com/cjz-pubs Page 19 of 37 Canadian Journal of Zoology
Cavender‐Bares, J., Kozak, K.H., Fine, P.V., and Kembel, S.W. 2009. The merging of
community ecology and phylogenetic biology. Ecol. Lett. 12(7): 693–715. doi:
10.1111/j.1461-0248.2009.01314.x
Chase, J.M. 2010. Stochastic community assembly causes higher biodiversity in more
productive environments. Science, 328(5984): 1388–1391. doi:
10.1126/science.1187820
Connor, E.F., and McCoy, E.D. 1979. The statistics and biology of the species-area
relationship. Am. Nat. 113(6): 791–833. doi: 10.1086/283438
Connor, E.F., and McCoy, E. D. 2001. Species-area relationships. In Encyclopedia of
Biodiversity. Edited by S. Levin. Academic Press, Cambridge. pp. 397–411.
Costa, L.P. 2003. The historical bridgeDraft between the Amazon and the Atlantic Forest of
Brazil: a study of molecular phylogeography with small mammals. J. Biogeogr. 30(1):
71–86. doi: 10.1046/j.1365-2699.2003.00792.x
Dengler, J. 2009. Which function describes the species–area relationship best? A review
and empirical evaluation. J. Biogeogr. 36(4): 728–744. doi: 10.1111/j.1365-
2699.2008.02038.x
Dray, S., Bauman, D., Blanchet, G., Borcard, D., Clappe, S., Guenard, G., Jombart, T.,
Larocque, G., Legendre, P., Madi N., and Wagner, H.H. 2018. adespatial: Multivariate
Multiscale Spatial Analysis. R package version 0.3-2. Available from https://CRAN.R-
project.org/package=adespatial [accessed 28 November 2018].
ESRI 2013. ArcGIS Desktop: Relase 10. Version 10.22. Available from
https://www.esri.com/en-us/home [accessed 30 November 2018].
19 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 20 of 37
Esposito, L.A., Yamaguti, H.Y., Souza, C.A., Pinto-Da-Rocha, R., and Prendini, L. 2017.
Systematic Revision of the Neotropical Club-Tailed Scorpions, Physoctonus,
Rhopalurus, and Troglorhopalurus, Revalidation of Heteroctenus, and Descriptions of
Two New Genera and Three New Species (Buthidae: Rhopalurusinae). Bull. Am. Mus.
Nat. Hist. (415): 1–136. doi: 10.1206/0003-0090-415.1.1
Ferraz, E.M.N., Rodal, M.J.N., Sampaio, E.V., and Pereira, R.D.C.A. 1998. Composição florística em trechos de vegetação de caatinga e brejo de altitude na região do Vale do
Pajeú, Pernambuco. Rev. bras. Bot. 21(1): 7–15. doi: 10.1590/S0100-
84041998000100002
Ferreira, L.M.R., Esteves, L.S., de Souza, E.P., and Santos, C.A.C. 2018. Impact of the Urbanization Process in the AvailabilityDraft of Ecosystem Services in a Tropical Ecotone Area. Ecosystems, 1–17. doi: 10.1007/s10021-018-0270-0
Finn, D.S., Theobald, D.M., Black, W.C., and Poff, N.L. 2006. Spatial population genetic structure and limited dispersal in a Rocky Mountain alpine stream insect. Mol.
Ecol. 15(12): 3553–3566. doi: 10.1111/j.1365-294X.2006.03034.x
Foord, S.H., Gelebe, V., and Prendini, L. 2015. Effects of aspect and altitude on scorpion diversity along an environmental gradient in the Soutpansberg, South Africa. J. Arid
Environ. 113: 114–120. doi: 10.1016/j.jaridenv.2014.10.006
Freestone, A.L., and Inouye, B.D. 2006. Dispersal limitation and environmental heterogeneity shape scale‐dependent diversity patterns in plant communities. Ecology, 87(10): 2425–2432. doi: 10.1890/0012-
9658(2006)87[2425:DLAEHS]2.0.CO;2
Gauch, H.G.Jr. 1982. Multivariate Analysis in Community Ecology. Cambridge
University Press, Cambridge.
20 https://mc06.manuscriptcentral.com/cjz-pubs Page 21 of 37 Canadian Journal of Zoology
Gianuca, A.T., Declerck, S.A., Lemmens, P., and de Meester, L. 2017. Effects of dispersal
and environmental heterogeneity on the replacement and nestedness components of
β‐diversity. Ecology, 98(2): 525–533. doi: 10.1002/ecy.1666
González-Reyes, A.X., Corronca, J.A., and Rodriguez-Artigas, S.M. 2017. Changes of
arthropod diversity across an altitudinal ecoregional zonation in Northwestern
Argentina. PeerJ, 5: e4117. doi: 10.7717/peerj.4117
Graham, C.H., and Fine, P.V. 2008. Phylogenetic beta diversity: linking ecological and
evolutionary processes across space in time. Ecol. Lett. 11(12): 1265–1277. doi:
10.1111/j.1461-0248.2008.01256.x
Haffer, J. 1969. Speciation in Amazonian forest birds. Science, 165(3889): 131–137.
Harrison, S., Ross, S.J., and Lawton,Draft J.H. 1992. Beta diversity on geographic gradients in
Britain. J. Anim. Ecol. 61(1): 151–158. doi: 10.2307/5518
Hawkins, C.P., Mykrä, H., Oksanen, J., and Vander Laan, J.J. 2015. Environmental
disturbance can increase beta diversity of stream macroinvertebrate assemblages. Global
Ecol. Biogeogr. 24(4): 483–494. doi: 10.1111/geb.12254
Heino, J., Melo, A.S., and Bini, L.M. 2015. Reconceptualising the beta
diversity‐environmental heterogeneity relationship in running water systems. Freshw.
Biol. 60(2): 223–235. doi: 10.1111/fwb.12502
Hill, M.O., and Gauch, H.G. 1980. Detrended correspondence analysis: an improved
ordination technique. In Classification and Ordination. Edited by E. van der Maarel.
Springer, Dordrecht. pp. 47–58.
Hubbell, S.P. 2001. The unified neutral theory of biodiversity and biogeography.
Princeton University Press, New Jersey.
21 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 22 of 37
Koleff, P., Gaston, K.J., and Lennon, J.J. 2003. Measuring beta diversity for presence– absence data. J. Anim. Ecol. 72(3): 367–382. doi: 10.1046/j.1365-2656.2003.00710.x
Kunstler, G., Lavergne, S., Courbaud, B., Thuiller, W., Vieilledent, G., Zimmermann,
N.E., Kattge, J., and Coomes, D.A. 2012. Competitive interactions between forest trees are driven by species' trait hierarchy, not phylogenetic or functional similarity: implications for forest community assembly. Ecol. Lett. 15(8): 831–840. doi:
10.1111/j.1461-0248.2012.01803.x
Laurance, W.F., Lovejoy, T.E., Vasconcelos, H.L., Bruna, E.M., Didham, R.K., Stouffer,
P.C., Gascon, C., Bierregaard, R.O., Laurance, S.G., and Sampaio, E. 2002. Ecosystem decay of Amazonian forest fragments: a 22‐year investigation. Conserv. Biol. 16(3): 605– 618. doi: 10.1046/j.1523-1739.2002.01025.xDraft
Legendre, P. 2014. Interpreting the replacement and richness difference components of beta diversity. Global Ecol. Biogeogr. 23(11): 1324–1334. doi: 10.1111/geb.12207
Legendre, P., and Borcard, D. 2006. Quelles sont les échelles spatiales importantes dans un écosystème? In Analyse Statistique de Données Spatiales. Edited by J.J. Droesbeke,
M. Lejeune, and G. Saporta. Éditions TECHNIP, Paris. pp. 425–442.
Legendre, P., and De Cáceres, M. 2013. Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecol. Lett. 16(8): 951–963. doi:
10.1111/ele.12141
Legendre, P., and Legendre, L. 2012. Numerical Ecology. Elsevier, Amsterdam.
Legendre, P., Borcard, D., and Peres-Neto, P.R. 2005. Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecol. Monogr. 75(4):
435–450. doi: 10.1890/05-0549
22 https://mc06.manuscriptcentral.com/cjz-pubs Page 23 of 37 Canadian Journal of Zoology
Lennon, J.J., Koleff, P., Greenwood, J.J.D., and Gaston, K.J. 2001. The geographical
structure of British bird distributions: diversity, spatial turnover and scale. J Anim.
Ecol. 70(6): 966–979. doi: 10.1046/j.0021-8790.2001.00563.x
Lepš, J., and Šmilauer, P. 2003. Multivariate Analysis of Ecological Data Using
CANOCO. Cambridge University Press, Cambridge.
Lira, A.F.A., and Albuquerque, C.M.R. 2014. Diversity of scorpions (Chelicerata:
Arachnida) in the Atlantic Forest in Pernambuco, northeastern Brazil. Check List, 10(6):
1331–1335. doi: 10.15560/10.6.1331
Lira, A.F.A., Rego, F.N.A.A., and Albuquerque, C.M.R. 2015. How important are
environmental factors for the population structure of co-occurring scorpion species in a
tropical forest? Can. J. Zool. 93(1): Draft15–19. doi: 10.1139/cjz-2014-0238
Lira, A.F.A., de Araújo, V.L.N., DeSouza, A.M., Rego, F.N.A.A., and Albuquerque,
C.M.R. 2016. The effect of habitat fragmentation on the scorpion assemblage of a
Brazilian Atlantic Forest. J. Insect Conserv. 20(3): 457–466. doi: 10.1007/s10841-016-
9878-6.
Lira, A.F.A., Damasceno, E.M., Silva-Filho, A.A.C., and Albuquerque, C.M.R. 2017.
Linking scorpion (Arachnida: Scorpiones) assemblage with fragment restoration in the
Brazilian Atlantic Forest. Stud. Neotrop. Fauna Environ. 53(2): 107– 112. doi:
10.1080/01650521.2017.1413823.
Lira, A.F.A., DeSouza, A.M., and Albuquerque, C.M.R. 2018. Environmental variation
and seasonal changes as determinants of the spatial distribution of scorpions (Arachnida:
Scorpiones) in Neotropical forests. Can. J. Zool. 96(9): 963–972. doi: 10.1139/cjz-2017-
0251.
Lira, A.F.A., Salomão, R.P., and Albuquerque, C.M.R. 2019. Pattern of scorpion
23 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 24 of 37
diversity across a bioclimatic dry-wet gradient in Neotropical forests. Acta Oecol.
96(2019): 10-17. doi: 10.1016/j.actao.2019.02.004
Liu, J., Vellend, M., Wang, Z., and Yu, M. 2018. High beta diversity among small islands is due to environmental heterogeneity rather than ecological drift. J. Biogeogr. 45(10):
2252–2261. doi: 10.1111/jbi.13404
Locatelli, E., Machado, I.C., and Medeiros, P. 2004. Riqueza de abelhas e a flora apícola em um fragmento da mata serrana (Brejo de Altitude) em Pernambuco, Nordeste do
Brasil. In Brejos de altitude em Pernambuco e Paraíba: História natural, ecologia e conservação. Edited by K.C. Pôrto, J.J.P. Cabral, and M. Tabarelli. Ministério do Meio
Ambiente, Brasília. pp. 153–177.
López‐González, C., Presley, S.J., DraftLozano, A., Stevens, R.D., and Higgins, C.L. 2015.
Ecological biogeography of Mexican bats: the relative contributions of habitat heterogeneity, beta diversity, and environmental gradients to species richness and composition patterns. Ecography, 38(3): 261–272. doi: 10.1111/ecog.00813
Lourenço, W.R. 1982. Révision du genre Ananteris Thorell, 1891 (Scorpiones, Buthidae) et description de six espèces nouvelles. Bull. Mus. Natl. Hist. Nat. 4(1-2): 119–151.
Lourenço, W.R. 1988. Première evidence de la présence d’une faune scorpionique amazonienne relictuelle dans les ‘brejos’ de la caatinga du nord-est du Brésil. Bull. Soc. sci. Bretagne, 59: 147–154.
Lourenço, W.R. 2002. Scorpions of Brazil. Les editions de l'If, Paris.
Lourenço, W.R. 2010. The disrupted pattern of distribution of the genus Hadrurochactas
Pocock; evidence of past connections between Amazon and the Brazilian Atlantic forest. C. R. Biol. 333(1): 41–47. doi: 10.1016/j.crvi.2009.11.002
24 https://mc06.manuscriptcentral.com/cjz-pubs Page 25 of 37 Canadian Journal of Zoology
Lourenço, W.R. 2016. Scorpions from the Mitaraka Massif in French Guiana: Description
of one new genus and species (Scorpiones: Chactidae). C. R. Biol. 339(3-4): 141–146.
doi: 10.1016/j.crvi.2016.02.003
Mares, M.A., Willig, M.R., and Lacher Jr, T.E. 1985. The Brazilian Caatinga in South
American zoogeography: tropical mammals in a dry region. J. Biogeogr. 12(1): 57–69.
doi: 10.2307/2845029
Monod, L., Harvey, M.S., and Prendini, L. 2013. Stenotopic Hormurus Thorell, 1876
scorpions from the monsoon ecosystems of northern Australia, with a discussion on the
evolution of burrowing behaviour in Hormuridae Laurie, 1896. Rev. Suisse Zool. 120(2):
281–346.
Montade, V., Ledru, M.P., Burte, J.,Draft Martins, E.S.P.R., Verola, C.F., Costa, I.R. D., and
Silva, F.H.M. 2014. Stability of a Neotropical microrefugium during climatic
instability. J. Biogeogr. 41(6): 1215–1226. doi: 10.1111/jbi.12283
Monteiro, L.S., Garcia, A.C.L., Oliveira, G.F., and Rohde, C. 2016. High diversity of
Drosophilidae in high-altitude wet forests in Northeastern Brazil. Neotrop. Entomol.
45(3): 265–273. doi: 10.1007/s13744-016-0364-3
Myers, J.A., Chase, J.M., Jiménez, I., Jørgensen, P.M., Araujo‐Murakami, A.,
Paniagua‐Zambrana, N., and Seidel, R. 2013. Beta‐diversity in temperate and tropical
forests reflects dissimilar mechanisms of community assembly. Ecol. Lett. 16(2): 151–
157. doi: 10.1111/ele.12021
Nekola, J.C., and White, P.S. 1999. The distance decay of similarity in biogeography and
ecology. J. Biogeogr. 26(4): 867–878. doi: 10.1046/j.1365-2699.1999.00305.x
25 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 26 of 37
Nime, M.F., Casanoves, F., and Mattoni, C.I. 2016. Microhabitat use and behavior differ across sex-age classes in the scorpion Brachistosternus ferrugineus (Scorpiones:
Bothriuridae). J. Arachnol. 44(2): 235–244.
Ojanguren-Affilastro, A.A., Mattoni, C.I., Ochoa, J.A., Ramírez, M.J., Ceccarelli, F.S., and Prendini, L. 2016. Phylogeny, species delimitation and convergence in the South
American bothriurid scorpion genus Brachistosternus Pocock 1893: Integrating morphology, nuclear and mitochondrial DNA. Mol. Phylogenet. Evol. 94: 159–170. doi:
10.1016/j.ympev.2015.08.007
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’hara, R. Simpson,
G.L., Solymos, P., Stevens, M.H.H., Szoecs, E., and Wagner, H. 2011. vegan: Community ecology package. R packageDraft version 2.5-3. Available from https://cran.r- project.org/package=vegan [accessed 28 November 2018].
Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N.,
Underwood, E.C., D'Amico, J.A., Itoua, I., Strand, H.E., Morrison, J.C., Loucks, C.J.,
Allnutt, T.F., Ricketts, T.H., Kura, Y., Lamoreux, J.F., Wettengel, W.W., Hedao, P.,
Kassem, K.R. 2001. Terrestrial ecoregions of the world: a new map of life on Earth.
Bioscience, 51(11): 933–938.
Paluch, M., Mielke, O.H.H., Nobre, C.E.B., Casagrande, M.M., Melo, D.H.A., and
Freitas, A.V.L. 2011. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the
Parque Ecológico João Vasconcelos Sobrinho, Caruaru, Pernambuco, Brazil. Biota
Neotrop. 11(4): 229–238. doi: 10.1590/S1676-06032011000400020
Pennington, R.T., Prado, D.E., and Pendry, C.A. 2000. Neotropical seasonally dry forests and Quaternary vegetation changes. J. Biogeogr. 27(2): 261–273. doi: 10.1046/j.1365-
2699.2000.00397.x
26 https://mc06.manuscriptcentral.com/cjz-pubs Page 27 of 37 Canadian Journal of Zoology
Peretti, A.V., Acosta, L.E., and Benton, T.G. 1999. Sexual cannibalism in scorpions: fact
or fiction? Biol. J. Linn. Soc. 68(4): 485–496. doi: 10.1111/j.1095-8312.1999.tb01184.x
Polis, G.A. 1990. Ecology. In The Biology of Scorpions. Edited by G.A. Polis. Stanford
University Press, Stanford. pp. 247–293.
Polis, G.A., McReynolds, C.N., and Ford, R.G. 1985. Home range geometry of the desert
scorpion Paruroctonus mesaensis. Oecologia, 67(2): 273–277. doi:
10.1007/BF00384298
Porto, T.J., Carnaval, A.C., and da Rocha, P.L.B. 2013. Evaluating forest refugial models
using species distribution models, model filling and inclusion: a case study with 14
Brazilian species. Divers. Distrib. 19(3): 330–340. doi: 10.1111/j.1472-
4642.2012.00944.x Draft
Prance, G.T. 1982. Forest refuges: evidences from woody angiosperms. In Biological
Diversification in the Tropics. Edited by G.T. Prance. Columbia University Press, New
York. pp. 137–158.
Prendini, L. 2001. Substratum specialization and speciation in southern African
scorpions: The Effect Hypothesis revisited. In Scorpions 2001. In Memoriam Gary A.
Polis. Edited by V. Fet, and P.A. Selden. British Arachnological Society, UK. pp. 113–
138.
R Core Team. 2018. R: A language and environment for statistical computing. Available
from https://www.R-project.org/ [accessed 28 November 2018].
Rizzini, C.T. 1997. Tratado de Fitogeografia do Brasil: Aspectos ecológicos, sociológicos
e florísticos. Âmbito Cultural Edições, Rio de Janeiro.
27 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 28 of 37
Rocha, P.A., Ruiz-Esparza, J., and Ferrari, S.F. 2018. Differences in the structure of the bat community between a cloud forest refuge and a surrounding semi-arid Caatinga scrubland in the northeastern Brazil. J. Arid Environ. 151: 41–48. doi:
10.1016/j.jaridenv.2017.11.005
Rodal, M.J.N., and Nascimento, L.D. 2002. Levantamento florístico da floresta serrana da reserva biológica de Serra Negra, microrregião de Itaparica, Pernambuco, Brasil. Acta
Bot. bras. 16(4): 481–500. doi: 10.1590/S0102-33062002000400009
Rodal, M.J.N., and Sales, M.F. 2008. Panorama of the Montane Forests of Pernambuco,
Brazil. In The Atlantic Coastal Forest of Northeastern Brazil. Edited by W.W. Thomas.
The New York Botanical Garden, New York. pp. 541–559.
Rohde, C., Silva, D., Oliveira, G.F.,Draft Monteiro, L.S., Montes, M.A., and Garcia, A.C.L.
2014. Richness and abundance of the cardinigroup of Drosophila (Diptera,
Drosophilidae) in the Caatinga and Atlantic Forest biomes in northeastern Brazil. An.
Acad. Bras. Ciênc. 86(4): 1711–1718. doi: 10.1590/0001-3765201420130314
Rull, V. 2009. Microrefugia. J. Biogeogr. 36(3): 481–484. doi: 10.1111/j.1365-
2699.2008.02023.x
Santos, A.M.M., Cavalcanti, D.R., Silva, J.M.C.D., and Tabarelli, M. 2007.
Biogeographical relationships among tropical forests in north‐eastern Brazil. J.
Biogeogr. 34(3): 437–446. doi: 10.1111/j.1365-2699.2006.01604.x
Santos, R.M., Oliveira‐Filho, A.T., Eisenlohr, P.V. Queiroz, L.P., Cardoso, D.B., and
Rodal, M.J. 2012. Identity and relationships of the Arboreal Caatinga among other floristic units of seasonally dry tropical forests (SDTFs) of north‐eastern and Central
Brazil. Ecol. Evol. 2(2): 409–428. doi: 10.1002/ece3.91
28 https://mc06.manuscriptcentral.com/cjz-pubs Page 29 of 37 Canadian Journal of Zoology
Segre, H., Ron, R., De Malach, N., Henkin, Z., Mandel, M., and Kadmon, R. 2014.
Competitive exclusion, beta diversity, and deterministic vs. stochastic drivers of
community assembly. Ecol. Lett. 17(11): 1400–1408. doi: 10.1111/ele.12343
Silva, J.M.C., and Barbosa, L.C.F. 2017. Impact of Human Activities on the Caatinga. In
Caatinga: The Largest Tropical Dry Forest Region in South America. Edited by J.M.C.
da Silva, I.R. Leal, and M. Tabarelli. Springer, Switzerland. pp. 359–368.
Silva, F.A.B., Hernández, M.I.M., Ide, S., and Moura, R.D.C. 2007. Comunidade de
escarabeíneos (Coleoptera, Scarabaeidae) copro-necrófagos da região de Brejo Novo,
Caruaru, Pernambuco, Brasil. Rev. Bras. Entomol. 51(2): 228–233. doi: 10.1590/S0085-
56262007000200014
Sobral-Souza, T., Lima-Ribeiro, M.S.,Draft and Solferini, V.N. 2015. Biogeography of
Neotropical Rainforests: past connections between Amazon and Atlantic Forest detected
by ecological niche modeling. Evol. Ecol. 29(5): 643–655. doi: 10.1007/s10682-015-
9780-9
Socolar, J.B., Gilroy, J.J., Kunin, W.E., and Edwards, D.P. 2016. How should beta-
diversity inform biodiversity conservation?. Trends Ecol. Evol. 31(1): 67–80. doi:
10.1016/j.tree.2015.11.005
Soininen, J., Lennon, J.J., and Hillebrand, H. 2007. A multivariate analysis of beta
diversity across organisms and environments. Ecology, 88(11): 2830–2838. doi:
10.1890/06-1730.1
Tabarelli, M., and Santos, A.M.M. 2004. Uma breve descrição sobre a história natural
dos brejos nordestinos. In Brejos de altitude em Pernambuco e Paraíba: História natural,
ecologia e conservação. Edited by K.C. Pôrto, J.J.P. Cabral, and M. Tabarelli. Ministério
do Meio Ambiente, Brasília. pp. 17–24.
29 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 30 of 37
Tuomisto, H., and Ruokolainen, K. 2006. Analyzing or explaining beta diversity?
Understanding the targets of different methods of analysis. Ecology, 87(11): 2697–2708. doi: 10.1890/0012-9658(2006)87[2697:AOEBDU]2.0.CO;2
Tuomisto, H., Ruokolainen, K., and Yli-Halla, M. 2003. Dispersal, environment, and floristic variation of western Amazonian forests. Science, 299(5604): 241–244. doi:
10.1126/science.1078037
Turchetto‐Zolet, A.C., Pinheiro, F., Salgueiro, F., and Palma‐Silva, C. 2013.
Phylogeographical patterns shed light on evolutionary process in South America. Mol.
Ecol. 22(5): 1193–1213. doi: 10.1111/mec.12164
Vanzolini, P.E. 1981. A quasi-historical approach to the natural history of the differentiation of reptiles in tropical Draftgeographic isolates. Pap. Avulsos Zool. 34(19): 189–
204.
Veech, J.A., and Crist, T.O. 2007. Habitat and climate heterogeneity maintain beta‐diversity of birds among landscapes within ecoregions. Global Ecol.
Biogeogr. 16(5): 650–656. doi: 10.1111/j.1466-8238.2007.00315.x
Veloso, H.P., Rangel-Filho, A.L.R., and Lima, J.C.A. 1991. Classificação da Vegetação
Brasileira, Adaptada a um Sistema Universal. IBGE, Rio de Janeiro.
Wang, X., Auler, A.S., Edwards, R.L., Cheng, H., Cristalli, P.S., Smart, P.L., Richards,
D.A., and Shen, C.C. 2004. Wet periods in northeastern Brazil over the past 210 kyr linked to distant climate anomalies. Nature, 432(7018): 740–743. doi:
10.1038/nature03067
Weiher, E., Freund, D., Bunton, T., Stefanski, A., Lee, T., and Bentivenga, S. 2011.
Advances, challenges and a developing synthesis of ecological community assembly
30 https://mc06.manuscriptcentral.com/cjz-pubs Page 31 of 37 Canadian Journal of Zoology
theory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366(1576): 2403–2413. doi:
10.1098/rstb.2011.0056
Williams, P.H. 1996. Mapping variations in the strength and breadth of biogeographic
transition zones using species turnover. Proc. R. Soc. Lond. B Biol. Sci. 263(1370): 579–
588. doi: 10.1098/rspb.1996.0087
Wilson, E.O., and Kinne, O. 1990. Success and Dominance in Ecosystems: The case of
the social insects. Ecology Institute, Germany.
Wilson, M.V., and Shmida, A. 1984. Measuring beta diversity with presence-absence
data. J. Ecol. 27(3): 1055–1064. doi: 10.2307/2259551
Whittaker, R.H. 1960. Vegetation of the Siskiyou mountains, Oregon and
California. Ecol. Monogr. 30(3): 279–338.Draft doi: 10.2307/1943563
Whittaker, R.H. 1972. Evolution and measurement of species diversity. Taxon, 21(2/3):
213–251. doi: 10.2307/1218190
Yamaguti, H.Y., and Pinto-da-Rocha, R. 2006. Ecology of Thestylus aurantiurus of the
Parque Estadual da Serra da Cantareira, São Paulo, Brazil (Scorpiones, Bothriuridae). J.
Arachnol. 34(1): 214–220. doi: 10.1636/T04-37.1
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Table 1. Composition of scorpion assemblages of montane forest remnants and coastal
Atlantic forest areas of northeastern Brazil assessed in this study: Águas Belas (AGU),
Bonito (BON), Brejo da Madre de Deus (BRE), Caruaru (CAR), Inajá (INA),
Taquaritinga do Norte (TAQ), Triunfo (TRI), Araripe (ARA), and coastal Atlantic forest
(CAF).
Sampling sites
Species AGU BON BRE CAR INA TAQ TRI ARA CAF
Bothriuridae
Bothriurus asper Pocock, 1893 X X X
Bothriurus rochai Mello-Leitão, 1932 X
Buthidae Ananteris franckei Lourenço, 1982 Draft X X Ananteris mauryi Lourenço, 1982 X X X
Jaguajir rochae (Borelli, 1910) X X
Jaguajir agamemnon (C.L. Koch, 1839) X
Tityus brazilae Lourenço & Eickstedt, X X X
1984
Tityus martinpaechi Lourenço, 2001 X
Tityus neglectus Mello-Leitão, 1932 X X X X X X
Tityus pusillus Pocock, 1983 X X X X X X X
Tityus stigmurus (Thorell, 1876) X X X X X
Chactidae
Hadrurochactas araripe Lourenço, 2010 X
Number of species 3 4 2 3 4 3 4 6 6
Remnant area (Km2) 41.8 2.6 53.5 41.1 9.2 34.8 26.8 301.8 -
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Figure captions
Figure 1. Graphical representation of the relief of the state of Pernambuco and the
southern portion of the state of Ceará in northeastern Brazil, showing the sampling
localities of montane forests: Águas Belas (Agu), Bonito (Bon), Brejo da Madre de Deus
(Bre), Caruaru (Car), Inajá (Ina), Taquaritinga do Norte (Taq), Triunfo (Tri), and Araripe
(Ara). Service Layer Credits: Earth Explorer (USGS), WWF, IBGE.
Figure 2. Cluster analysis based on the UPGMA agglomeration method, showing the
relationship of the scorpion fauna of eight montane forest remnants of northeastern Brazil
and the coastal Atlantic forest. The scale represents the dissimilarity between the scorpion
fauna of the localities assessed using the Bray-Curtis index.
Figure 3. Bidimensional representationDraft of the NMDS performed from the dissimilarity
matrix (Bray-Curtis) of scorpion species composition in the sampling localities: coastal
Atlantic forest (CAF), Águas Belas (AGU), Bonito (BON), Brejo da Madre de Deus
(BRE), Caruaru (CAR), Inajá (INA), Taquaritinga do Norte (TAQ), Triunfo (TRI), and
Araripe (ARA).
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Supplementary material
Table S1. Data on the scorpion fauna of coastal Atlantic forest of northeastern Brazil extracted from literature.
Figure S1. Graphical representation of the montane forest remnants (polygons) of the central-eastern group: Águas Belas (A), Bonito (B), Brejo da Madre de Deus (C), Caruaru (D), Inajá (E), and Taquaritinga do Norte (F). All pictures were constructed using Landsat-8 imagens captured in 2016 by the Operational Land Imager Sensor.
Figure S2. Graphical representation of the montane forest remnants (polygons) of the western group, showing the remnants of Triunfo (A), and Araripe (B). All pictures were constructed using Landsat-8 imagens captured in 2016 by the Operational Land Imager Sensor.
Draft
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Draft
Graphical representation of the relief of the state of Pernambuco and the southern portion of the state of Ceará in northeastern Brazil, showing the sampling localities of montane forests: Águas Belas (Agu), Bonito (Bon), Brejo da Madre de Deus (Bre), Caruaru (Car), Inajá (Ina), Taquaritinga do Norte (Taq), Triunfo (Tri), and Araripe (Ara). Service Layer Credits: Earth Explorer (USGS), WWF, IBGE.
200x192mm (600 x 600 DPI)
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Draft Cluster analysis based on the UPGMA agglomeration method, showing the relationship of the scorpion fauna of eight montane forest remnants of northeastern Brazil and the coastal Atlantic forest. The scale represents the dissimilarity between the scorpion fauna of the localities assessed using the Bray-Curtis index.
109x72mm (300 x 300 DPI)
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Draft
Bidimensional representation of the NMDS performed from the dissimilarity matrix (Bray-Curtis) of scorpion species composition in the sampling localities: coastal Atlantic forest (CAF), Águas Belas (AGU), Bonito (BON), Brejo da Madre de Deus (BRE), Caruaru (CAR), Inajá (INA), Taquaritinga do Norte (TAQ), Triunfo (TRI), and Araripe (ARA).
124x109mm (300 x 300 DPI)
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