An Acad Bras Cienc (2021) 93(3): e20201282 DOI 10.1590/0001-3765202120201282 Anais da Academia Brasileira de Ciências | Annals of the Brazilian Academy of Sciences Printed ISSN 0001-3765 I Online ISSN 1678-2690 www.scielo.br/aabc | www.fb.com/aabcjournal
ECOSYSTEMS
Distribution and environmental determinants Running title: DETERMINANTS of darkling beetles assemblages OF TENEBRIONIDAE IN PENÍNSULA VALDÉS (Coleoptera: Tenebrionidae) in Península Valdés (Argentinean Patagonia)
Academy Section: ECOSYSTEMS GERMÁN H. CHELI, RODOLFO CARRARA, LUCAS BANDIERI & GUSTAVO E. FLORES e20201282 Abstract: Arid lands provide several products and services to humankind, but human activities affect this environment, increasing the extinction risk of the native species. Thus, to successfully conserve the biodiversity of these ecosystems, it is necessary to
93 identify which environmental factors infl uence the spatial distribution of the organisms (3) that offer these benefi ts. Darkling beetles play a relevant role on the functioning of 93(3) deserts. Although these insects are among the most abundant and diverse in these environments, there is no agreement on the relative importance that different DOI environmental factors have as determinants of their spatial distribution. In this work, 10.1590/0001-3765202120201282 we assessed the role of climate, vegetation, and soil variables as factors that determine distribution patterns of darkling beetles within the Natural Protected Area Península Valdés (Northeastern Patagonia). Five groups of environmental units were identifi ed, each one with an exclusive tenebrionid species assemblage and different species diversity. The most infl uential environmental variables were temperature, precipitations, and soil texture. Results suggest that the magnitude of several ecosystem processes may vary among the groups of environmental units. We recommend prioritizing the conservation of the fi ve groups of environmental units and incorporating the darkling beetles-environment relationship in future conservation strategies for arid Patagonia. Key words: habitat and climate variables, arid Patagonia, spatial patterns, tenebrionids.
INTRODUCTION Baldi et al. 2017). Preventing the loss of biological diversity is critical for an effective management Arid and semi-arid lands are spatially and conservation strategy of those ecosystems heterogeneous habitats that support high (Northrup et al. 2013). Consequently, it is strongly biodiversity with multiple biological interactions important to increase the understanding of (Whitford 2002, Ayal 2007, Baldi et al. 2017). It the actual factors that promote and maintain is recognized that this biodiversity provides biodiversity and ecosystem processes in arid several products and services to humankind, environments (Mazía et al. 2006, Martínez et al. from economic gains (e.g. sheep wool) to 2018). atmospheric and climatic regulation (Whitford It is known that environmental conditions 2002). However, some human activities such act as ecological filters of regional species as overgrazing and habitat fragmentation are pools, determining species composition at a degrading those habitats leading to biodiversity given time and place (Lichti & Murphy 2010). declines (Whitford 2002, Laity 2008, Ward 2009, In arid ecosystems the distribution of most
An Acad Bras Cienc (2021) 93(3) GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS species is affected by a combination of ambient an important role in the cycle of important soil temperature and rainfalls because these nutrients (Matthews et al. 2010). These insects abiotic factors influence animal ecophysiology can behave either as generalist herbivores (Cloudsley-Thompson 2001, Ward 2009, (Flores & Debandi 2004, Cheli et al. 2009, Bisigato Schowalter 2016). However, the high spatial et al. 2015) or as consumers of the senescent variation in geological substrates and soil vegetation (Ayal 2007, Pizarro-Araya 2010, Cheli types in deserts may also play a key role as 2009) or dead animals (Aballay et al. 2016, Cheli spatial filters, especially for organisms whose 2009). On the other hand, darkling beetles are life cycle is partly developed in the soil (Ward important prey items for numerous vertebrates, 2009). Although related to previous factors, transferring energy from low to higher trophic vegetation may also be essential to desert levels (Ayal & Merkl 1994, Flores, 1998, Formoso animals because, besides offering shelter and et al. 2012). Despite the extensive researches that buffering microclimatic variation, it harbors exist on the ecology of darkling beetles, there greater concentrations of water, soil nutrients, is no agreement on the relative importance of and food (litter or potential prey) (Mazía et the different environmental factors determining al. 2006, Ward 2009, Schowalter 2016). In this their spatial distribution (Krasnov & Shenbrot context, to successfully maintain the products 1996). Some studies have documented that and services provided by the biodiversity of arid the distribution of darkling beetles mainly environments, it is necessary to identify which respond to variations in soil texture (Sheldon & environmental factors determine the presence of Rogers 1984, Crawford 1988, Ayal & Merkl 1994, the living organisms that perform these benefits Matthews et al. 2010). Other works claim that and develop sustainable management strategies vegetation cover and complexity are the main including relations between biodiversity and determinants of the darkling beetles diversity environmental factors (Whitford 2002, Mazía (Cepeda-Pizarro 1989, Parmenter et al. 1989a, et al. 2006, Northrup et al. 2013, Martínez et al. Mazía et al. 2006, Liu et al. 2012). In contrast, 2018). other authors consider that climatic factors Insects represent the majority of species in like temperature and precipitation/humidity desert communities and are an integral part of may have the greatest influence on the spatial their structure and dynamics (Schowalter 2016). distribution of darkling beetles (Parmenter et Darkling beetles (Coleoptera: Tenebrionidae) are al. 1989b, Flores 1998, Cloudsley-Thompson 2001, among the most abundant and diverse biomass Carrara et al. 2011a, Rosas et al. 2019). contributing invertebrates in deserts (Cloudsley- The Natural Protected Area Península Thompson 2001, Cepeda-Pizarro et al. 2005, Cheli Valdés (PV from now onwards) is situated at et al. 2010, Matthews et al. 2010, Baldi et al. 2017). the northeastern portion of Patagonia (42º05’– They comprise about 20,000 species around the 42º53’S; 63º35’–65º04’W) in the Atlantic coast of world (Matthews et al. 2010) and have a relevant Chubut, Argentina. This area, a UNESCO Natural role in the functioning of desert ecosystems World Heritage Site and Biosphere Reserve (Ayal 2007, Pizarro-Araya 2010, Bartholomew and one of the biggest arid protected areas of & El Moghrabi 2018). A number of studies in Argentina, has environmental singularities in deserts around the world have stressed the climate (Coronato et al. 2017), geomorphology importance of darkling beetles as detritivores (Bouza et al. 2017a, b), and soils (Rostagno 1981, in xeric ecosystems, suggesting that they play Bouza et al. 2017a, b) that determine several
An Acad Bras Cienc (2021) 93(3) e20201282 2 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS environmental units within the peninsula (Bertiller et al. 2017) which host a rich biodiversity (Baldi et al. 2017). Knowledge of terrestrial arthropods in PV has been considerably increased during the last decade (e.g. Cheli 2009, Cheli et al. 2010, 2013, Carrara et al. 2011b, Flores et al. 2011, Cheli & Martínez 2017, Baldi et al. 2017, Martínez et al. 2018). Previous studies of darkling beetles diversity in PV have focused on community composition and darkling beetles distribution patterns (Cheli et al. 2013, Flores et al. 2011, Carrara et al. 2011b), but relations among darkling beetles with climate, soil, and vegetation remain almost unknown. The purpose of this study was to analyze the spatial variations of tenebrionid assemblages in PV and to identify the main environmental factors that determine it. For this reason, the following questions will be addressed: Do species composition of tenebrionid assemblages and Figure 1. Location of the study area: the Natural Protected Area Peninsula Valdés, Patagonia, Chubut, diversity vary among environmental units in Argentina. PV? If so, which are the environmental variables that mainly determine this variation? Which is 2017a, b); as the result of this variability it was the relative contribution of soil, vegetation, and possible to recognize 16 environmental units climate variables to the variation of tenebrionid within (Bertiller et al. 2017) (Table I). species assemblages within PV? Data
METHODS Darkling beetle data
Study area Darkling beetle records inside PV were compiled The study was conducted in the Natural Protected from 86 sampling points of previous works in Area Península Valdés (PV), a wide plateau of the study area (Cheli et al. 2010, 2013, Flores et low altitude ranging between 35 m below sea al. 2011, Carrara et al. 2011b, Martínez et al. 2018), level because of a series of central salt flats and plus a trip collecting to PV carried out in January 2 80 m a.s.l. that covers approximately 4000 km 2010 that comprised 48 sites in the 16 terrestrial (Figure 1). Its climate is arid, characterized by environmental units within PV, i.e. three sites per hot, dry summers and relatively cold winters, environmental unit. Thus, a total of 134 sampling with a mean annual temperature of 12ºC, and points (86 + 48 points) have been included. In winds prevailing from the west (Coronato et al. each site, a 20-minutes visual inspection was 2017). Geomorphology, climate, and soil features conducted in an approximately 0.5 ha by three show great variability inside the peninsula observers who scrutinized the ground, shrubs, (Rostagno 1981, Coronato et al. 2017, Bouza et al.
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Table I. Environmental units of Peninsula Valdes where tenebrionid assemblages were studied, detailing the number of sampling sites in each. The dominant plant formation in each one is described on the right column. * The numbering of the environmental units in this table is the original number assigned to these units by Bertiller et al. (2017). The authors preferred not to vary this numbering so that interested readers can more easily find these units in the reference. Environmental units located outside the peninsula or on its isthmus (see Bertiller et al. 2017) were not considered in this study.
Number of Environmental Main Vegetation Formation sampling Unit* points
1 Perennial grass steppe of Sporobolus rigens and Nassella tenuis 5
Perennial grass steppe of Piptochaetium napostaense, Nassella tenuis and 2 7 Plantago patagonica Perennial grass steppe of Nassella tenuis, Nassella longiglumis with shrubs of 3 3 Chuquiraga avellanedae Shrub-perennial grass steppe of Chuquiraga erinacea subsp. erinacea and 4 7 Nassella tenuis 5 Shrub-perennial grass steppe of Chuquiraga avellanedae and Nassella tenuis 18 7 Shrub steppe of Condalia microphylla and Lycium spp 3 Shrub steppe of Chuquiraga avellanedae and Chuquiraga erinacea subsp. 8 4 erinacea 9 Shrub steppe of Chuquiraga avellanedae and Condalia microphylla 19
10 Shrub steppe of Schinus johnstonii and Lycium chilense 3
11 Shrub steppe of Chuquiraga avellanedae and Mulinum spinosum 12
12 Shrub steppe of Senecio filaginoides and Mulinum spinosum 10 Shrub steppe of Chuquiraga erinacea subsp. hystrix and Chuquiraga 13 10 avellanedae Shrub steppe of Cyclolepis genistoides, Chuquiraga avellanedae and Atriplex 15 6 lampa Shrub steppe of Chuquiraga erinacea subsp. Hystrix, Cyclolepis genistoides and 16 6 Chuquiraga avellanedae whit perennial grasses Mosaic: Perennial grass steppe of Sporobolus rigens and Nassella tenuis (1) and 20 9 Dwarf shrub steppe de Hyalis argentea (6) Mosaic: Perennial grass steppe of Piptochaetium napostaense, Nassella tenuis and Plantago patagonica (2) 21 12 Shrub-perennial grass steppe of Chuquiraga avellanedae and Nassella tenuis (5) rocks, or any other object on the ground that in each environmental unit were performed on could offer shelter for darkling beetles. All sites located at least 10 km from each other. individuals (live or dead) observed during were In order to avoid possible bias, analyses were collected (more details about the collecting performed only with those darkling beetle process can be found in Cheli et al. 2016a). To species with clearly epigeal habits. Individuals increase sampling representativeness, surveys were identified to species level based on
An Acad Bras Cienc (2021) 93(3) e20201282 4 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS reviews and keys by Kulzer (1955, 1963), Flores Environmental variables (1999, 2004), Flores et al. (2011) and comparisons with material deposited in the IADIZA collection. Habitat variables were compiled from three We followed the classification proposed by sources: a) specific bibliography: Rostagno Matthews et al. (2010) and Kamiński et al. (2021) 1981, Bertiller et al. 2017, Bouza et al. 2017a, b; to assign species and genera into subfamilies b) unpublished environmental information and tribes. Following the recent taxonomic kindly offered by Drs. M. Rostagno and P. Bouza changes suggested by Silvestro & Flores (2016), (IPEEC, CCT CENPAT CONICET, pers. com.); and Nyctelia nodosa (Germar, 1823) mentioned in c) satellite images of Moderate Resolution previous works (Cheli et al. 2010, 2013, Carrara Imaging Spectroradiometer (MODIS). Compiled et al. 2011b) was treated here as Nyctelia habitat information was classified into three picipes (Billberg, 1815). After a recent study of classes: 1- Climatic variables: Precipitation; some Kulzer & Kaszab`s type specimens at the Diurnal mean Temperature; Nocturnal mean Hungarian Natural History Museum in Budapest, temperature. 2- Soil variables: Dominant type Hungary, we present an improved list of darkling soil; Geomorphological system (Uplands and beetles species from Peninsula Valdés (Table II). plains, Great endorheic basins and Coastal Here we refer to Hylithus kovaksi Kaszab and zone); Geomorphological Subsystem (Terrace Psectrascelis hirtus Kulzer instead of Hylithus Levels, Aeolian fields, Piedemont Pediments tentyroides (Lacordaire) and Psectrascelis and Bajadas, Coastal Piedemont Pediments, sulcicollis (Waterhouse) listed in our previous Pleistocene beach ridges, Holocene beach work (Carrara et al. 2011b). The tenebrionid ridges); Number of soil horizons; Depth of “A” specimens collected were deposited in the soil horizon (topsoil); Dominant topographic Entomological Collections of IPEEC and IADIZA. Slope; pH; Texture of the most superficial Each tenebrionid record was assigned to an 20 cm of the soil profile (% gravel, % sand, % environmental unit (Bertiller et al. 2017) from clay and % silt); Soil organic carbon content. georeferenced maps and satellite images of 3- Vegetation variables: Normalized Difference PV using QGIS software (QGIS Development Vegetation Index (NDVI); Enhanced Vegetation Team 2018). Because tenebrionid records in PV Index (EVI); Actual Evapotranspiration and did not came from a long-term standardized Potential Evapotranspiration; Functional type sampling, we decided to use incidence data of steppe (perennial grass steppe, dwarf shrub (species presence/absence). With the complied steppe, shrub steppe, perennial grass-shrub records of darkling beetles species, from both steppe); Number of vegetation strata (grassy, previous works (Cheli et al. 2010, 2013, Flores Dwarf-shrubs, low shrubby (<50 cm), tall et al. 2011, Carrara et al. 2011b, Martínez et al. shrubby (>50 cm) strata); Total vegetation cover 2018) and the collecting campaign, a matrix of (%); Vegetation maximums height (cm); Plant species incidence by environmental unit was Species Richness (Table III). constructed (Table II) to perform all statistical analyses.
An Acad Bras Cienc (2021) 93(3) e20201282 5 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS X X X X X X X X X X X X 0 0 0 0 0 0 0 0 0 0 0 0 0 21 X X X X X X X X X X X 0 0 0 0 0 0 0 0 0 0 0 0 0 0 20 X X X X X X X X X 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 16 X X X X X X X X X X X X X X 0 0 0 0 0 0 0 0 0 0 0 15 X X X X X X X X X X X X X X 0 0 0 0 0 0 0 0 0 0 0 13 X X X X X X X X X X 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 12 X X X X X X X X X X X X X X 0 0 0 0 0 0 0 0 0 0 0 11 X X X 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 10 X X X X X X X X 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 9 X X X X X X 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 8 Envionmental unit Envionmental 7 X X X X 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 X X X X X X X X X X 5 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 X X X X X X X X X X 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 4 X X X X 3 X X 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 X X X X X X X X X 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 X X X X X X X X X X X X 0 0 0 0 0 0 0 0 0 0 0 0 0 Prao_sp Epip_cris Prao_spe Psec_hirt Sala_laco Blap_pun Hyli_kova Caly_peni Caly_pata Prao_sgra Prao_arge Acronym* Nycte_circ Pata_colla Nycte_pici Ecno_bruc Pata_quad Mitra_aran Plat_kusch Emma_hirt Lepty_tube Pime_spha Nycte_dors Lepty_nord Nycte_darw Emma_cren Species Nyctelia picipes Nyctelia Nyctelia darwini Nyctelia Nyctelia dorsata Nyctelia Hylithus kovaksi Salax lacordairei Salax Psectrascelis hirtus Psectrascelis Plathestes kuscheli Plathestes Ecnomoderes bruchi Ecnomoderes Emmallodera hirtipes Emmallodera Nyctelia circumundata Nyctelia Blapstinus punctulatus Blapstinus Patagonogenius collaris Patagonogenius Epipedonota cristallisata Epipedonota Pimelosomus sphaericus Pimelosomus Mitragenius araneiformis Mitragenius Leptynoderes tuberculata Leptynoderes Praocis (Hemipraocis) sp.1 (Hemipraocis) Praocis Leptynoderes nordenskioldi Leptynoderes Patagonogenius quadricollis Patagonogenius Calymmophorus peninsularis Calymmophorus Calymmophorus patagonicus Calymmophorus Praocis (Orthogonoderes) argentina (Orthogonoderes) Praocis Praocis (Hemipraocis) sellata peninsularis sellata (Hemipraocis) Praocis Emmallodera crenaticostata crenaticostata crenaticostata Emmallodera Praocis (Hemipraocis) sellata granulipennis sellata (Hemipraocis) Praocis Tribe Edrotini Praocini Praocini Praocini Praocini Praocini Praocini Praocini Opatrini Stenosini Nycteliini Nycteliini Nycteliini Nycteliini Nycteliini Nycteliini Nycteliini Nycteliini Nycteliini Scotobiini Scotobiini Scotobiini Scotobiini Trilobocarini Physogasterini Blaptinae Subfamily Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Pimeliinae Tenebrioninae Tenebrioninae Tenebrioninae Tenebrioninae Tenebrionid species (and their supraspecific taxonomic classification) recorded for the environmental units within Peninsula Valdes. The Valdes. Peninsula units within environmental for the recorded classification) taxonomic species (and their supraspecific II. Tenebrionid Table units: 0 = species absent; X = 2. Environmental used in Figure I. * Species acronym that in Table as units is the same numbering of the environmental present.
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GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS PH
7.72 7.43 7.72
7.98 8.154 7.643 7.845 7.845 7.845 7.845 7.845 8.057 8.057 8.083 8.083 8.083 Soil Organic Carbon Organic Soil
0.71 0.74 0.74 0.32 0.74 0.22 0.65 0.32 0.723 0.723 0.702 0.702 0.702 0.831 0.702 0.702 Clay (%) Clay 1 1 12
7.7 45.1 11.8 11.8 11.8
11.8 11.8 13.3 13.3 16.04 16.04 16.04 22.66 Silt (%) Silt
6.6 6.6 22.1 18.2 15.8
15.8 15.8 15.8 15.8 28.2 12.41 12.41 12.41 13.18 13.18 20.56 Sand (%) Sand
72.4 72.4 72.4 72.4 72.4 92.4 70.2 26.7 92.4 69.8 71.51 71.51 71.51 73.48 73.48 56.78 Gravels (%) Gravels 5 5
73 10
6.17 3.37 3.37 2.53 2.53 9.67 2.53 14.17 14.17 14.17 14.17 14.17 Num. Soil horizons Soil Num.
1 1 1 2 2 2
2 2 2 1.7 1.7 1.7 1.7 1.7 2.7 2.3 Depth soil horizon A (cm) A horizon Depth soil 1
17 10 20 20 8.5 8.5 8.5
13.33 13.33 13.33 13.33 13.33 10.67 10.33 10.67 Veg. Species Richness Species Veg.
9 9 8 6 11 11 11 11 12 12 12 13 19 16 10 20 Veg. height (cm) height Veg.
75 75 55 95 50 80 90 20 20 30 80 30 90 80 80 115 Veg. cover (%) cover Veg.
75 70 55 70 55 50 50 50 65 65 60 85 50 80 40 60 Dominant Slope Dominant
1 1 1 1 1 1 1 1 3 3 3 3 2 2 2 2 Geomoph. subsystem Geomoph.
1 1 1 1 1 2 3 3 4 4 2 4 5 6 4 4 Geomorph. system Geomorph.
1 1 1 1 1 1 1 2 2 3 3 3 3 3 3 3 Soil type Soil
1 1 7 3 7 5 2 4 4 2 2 6 3 4 4 4 Veg. strata Veg.
1 2 3 2 3 3 2 3 2 2 2 2 2 3 3 2 Steppe functional type functional Steppe
1 1 1 2 5 5 5 5 5 5 5 5 5 3 4 4 Temp .Night (K°) .Night Temp
284.8
284.57 285.07 285.48 285.152 284.175 283.911 284.129 285.963 284.376 284.633 284.435 284.769 284.833 284.582 284.823 Temp. Day (K°) Day Temp.
307.39
303.78 307.721 309.142 308.411 307.267 307.367 307.672 307.619 308.071 309.767 305.397 305.226 308.637 306.399 306.093 Pot. Evapotranspiration Pot.
257.2 272.12 257.61 267.77
263.411 261.813 261.242 256.192 263.922 257.644 265.933 260.681 273.806 260.978 265.556 249.806 Actual Evapotranspiration Actual 8.9
8.17 9.37 7.753 9.461
8.061 8.748 9.093 8.404 12.711 12.167 12.622 11.408 12.878 10.075 14.306 Precipitation (mm) Precipitation
9.912
25.48 9.245 9.959 19.118 11.775 11.461 15.212 12.873 15.799 19.632 28.476 13.803 14.209 14.209 10.849 EVI 9557500 12316200 12255900 11470000 12210000
12610000 10988400 10454000
12112857.14 13932571.43 11119083.33 12088777.78 10956222.22 12430555.56 9653333.333 8984666.667 NDVI 17857200
21174800 16762400 21356000 19835600 20474000 19902000 20429000
20935777.78 18661333.33 19876666.67 18835333.33 14370666.67 16399833.33 22585428.57 24952305.56 Environmental unit * unit Environmental 1 7 5 2 3 9 4 8 11 15 12 13 21 16 10 20 Habitat variables recorded for the environmental units within Peninsula Valdes. * The numbering of the environmental units is the same as that as units is the same * The numbering of the environmental Valdes. units within Peninsula the environmental for recorded variables III. Habitat Table fast with (4-10%), // 3: inclined runoff with moderate (2-4%), slope gently // 2: runoff with slow (2-2%), slope 1: flat Dominant Slope: I. References: in table 3: Torripsamment // (Sin BT) Xerollic (O) + Calciorthids Xeric 2:Torripsamment // horizon) clay (BT Xerollic 1: Natrargids (Soil Taxonomy): Soil Type runoff. sand 6: Loose soils) // Aquollic (saline Tipic + Salorthids 5: Torripsamment // horizon) Tipic (saline 4: Torripsamment // Xerollic + Natrargids Xeric grass Perennial type: 1: Functional Steppe Xerollic. + Natrargids without fine material (gravels) Patagonicos 7: Rodados // Xeric + Torripsamment blanket 1: System: Geomorphological 5 Shrub steppe. // steppes grass 4 Shrub-perennial // steppes grass-shrub 3 Perennial // steppe 2 Dwarf-shrub // steppe 2: // Levels 1: Terrace Subsystem: Geomorphological zone. C: coastal 3: System // basins endhoreic B: great 2: System // A: and plains uplands System ridges. beach // 6: Holocene ridges beach Pleistocene // 5: Pediments Piedemont Coastal // 4: Pediments and Bajadas // 3: Piedemont Aeolian fields
An Acad Bras Cienc (2021) 93(3) e20201282 7 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS
Statistical data analysis with correlations higher than r = 0.7 were We applied non-metric multidimensional scaling previously excluded from analyses. To assess (NMDS) to visualize the variation in composition the relative importance of soil, vegetation, and of the darkling beetle community among climatic variables on changes in the structure environmental units within PV. The purpose of the darkling beetle community, a variation of this technique is to perform an ordination partitioning analysis (VARPART) was performed of the samples in function of their species via RDA (Borcard et al. 2011, Legendre & Legendre similarity (Clarke & Warwick 2001, Legendre 2012). Significance of global RDA analysis, & Legendre 2012). We performed the analysis individual axes, and for each testable fraction of based on a matrix of biological similarity, using the variation partitioning were evaluated using the Sørensen index as a measure of distance unrestricted Monte Carlo permutation tests with on the taxa incidences (Legendre & Legendre 499 permutations (Borcard et al. 2011, Legendre 2012). Differences among the groups evidenced & Legendre 2012). by the NMDS ordination were tested using a Following Chao et al. (2014) and Hsieh et one-way analysis of similarity (ANOSIM) (Clarke al. (2016), darkling beetle diversity was studied & Warwick 2001, Legendre & Legendre 2012). This using integrated sample-size and coverage- test allows comparing assemblages as function based rarefaction/extrapolation sampling of factors based on distance measurements. curves with Hill numbers based on incidence ANOSIM significance was determined using 999 data (qΔ). Hill numbers for incidence data are random permutations of group membership. based on the relative species incidence in the To identify tenebrionid species that sites that constitute the studied assemblages characterize variation in beetles’ assemblages (Chao et al. 2014). To incorporate the full effect among environmental units, a Principal of relative species incidences on diversity Components Analysis (PCA) was performed estimation, curves were plotted for the Hill (Borcard et al. 2011, Legendre & Legendre 2012). numbers q = 0, q =1 and q = 2. The parameter q It is known that PCA can be affected by double- determines the sensitivity of qΔ to the relative zero cases (Ruokolainen & Blanchet 2014); to species incidences. When q = 0, the incidence of avoid this inconvenience, data were transformed individual species is not considered, so that 0Δ using Hellinger distance (Borcard et al. 2011, indicates simply species richness. If q = 1, species Legendre & Legendre 2012, Ruokolainen & are weighted in proportion to their incidence Blanchet 2014). We evaluated how many PCA (more weight on “typical” species) and it is axes were significant using the broken-stick homologous to the exponential of the Shannon distribution. PCA axes with larger percentages of index (Shannon diversity). When q = 2, the explained variance than the broken-stick model estimated number of effective species is similar were considered significant (Borcard et al. 2011, to the inverse of the Simpson index (Simpson Legendre & Legendre 2012). diversity) giving more weight to species widely In order to relate habitat variables present in the community (dominant species) with the structure of the darkling beetle (Chao et al. 2014). A diversity profile (a plot of qΔ community, a Redundancy Analysis (RDA) was vs. q from q = 0 to =3) was also performed (Chao performed. Environmental variables used in et al. 2014, Hsieh et al. 2016). The slope of the RDA analyses were previously standardized. diversity profile curve reflects the unevenness To avoid multicollinearity, those variables of species relative incidences. The more uneven
An Acad Bras Cienc (2021) 93(3) e20201282 8 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS the distribution of relative species incidences, Praocis (Orthogonoderes) argentina Kulzer (in the more steeply the curve declines (Chao et shrub steppes of Chuquiraga avellanedae and al. 2014, Hsieh et al. 2016). The relationship Mulinum spinosum) and Praocis (Hemipraocis) between sample coverage and sample size was sp.1 (in shrub steppes of Chuquiraga erinacea studied using a sample completeness curve subsp. hystrix and Chuquiraga avellanedae). for both smaller rarefied samples and larger Twenty-four percent of species were present in extrapolated samples (Chao et al. 2014, Hsieh 26-50% of the environmental units, and an equal et al. 2016). All curves were plotted with their percentage in 51-75%. Only two species (8%) were 95% confidence intervals. If their intervals do widely distributed among environmental units not overlap, the curves are statistically different (between 76-100%): Emmallodera hirtipes Kulzer (Chao et al. 2014, Hsieh et al. 2016). and Epipedonota cristallisata (Lacordaire), both We performed NMDS, ANOSIM, PCA, RDA of which were present in all environmental and VARPART analyses using metaMDS, anosim, units, except for the shrub steppe of Schinus rda and varpart functions of the vegan package johnstonii and Lycium chilense (Table II). (Oksanen 2019) for R (R Core Team 2018). We evaluated how many PCA axes were significant Variation in the tenebrionid species with the evplot function for R (Borcard et al. assemblages 2011). Diversity analyses were performed using The NMDS evidenced that the specific the iNEXT package for R (Hsieh et al. 2016). composition of the darkling beetle community varies among different environmental units within PV, consequently five tenebrionid species RESULTS assemblages can be identified (Figure 2). The first
Taxonomic Composition The 134 sampling points compiled into the 16 environmental units within PV, contained 378 records of tenebrionid beetles. As a result, the presence of 25 species of tenebrionid beetles belonging to three subfamilies and eight tribes was found inside PV (Table II). Forty-four percent of the species (11 species) were registered in up to 25% of the environmental units. Five species (20% of the species) were recorded exclusively in one environmental unit: Calymmophorus peninsularis Flores & Cheli (in shrub steppes of Figure 2. NMDS diagram showing the ordination Cyclolepis genistoides, Chuquiraga avellanedae of the environmental units within PV according to and Atriplex lampa), Nyctelia darwini Waterhouse their tenebrionid species composition. Polygons (in shrub-herbaceous steppes of Chuquiraga represent each of the three main tenebrionid avellanedae and Nassella tenuis), Pimelosomus species assemblages identified by ANOSIM (Group 1 = triangles; Group 2 = squares; Group 3 = circles) sphaericus Burmeister (in shrub steppes of while assemblages present in only one environmental Chuquiraga avellanedae, Cyclolepis genistoides unit are represented by a hexagon (Group 4) and a and Chuquiraga erinacea subsp. hystrix), diamond (Group 5).
An Acad Bras Cienc (2021) 93(3) e20201282 9 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS was present in a group of environmental units distinguished group 2 (clumped on the right of conformed by units 1, 4, 20, 21 (G1); the second in this axis), from the other environmental units units 11, 12, 13, 15, and 16 (G2); units 2, 3, 5, 8 and (located on the left of the ordination diagram). 9 conform the third (G3); species assemblage G4 This group of environmental units (G2) had a was only found in environmental unit 7 (shrub tenebrionid assemblage mainly characterized steppes of C. microphilla and Lycium sp.), and by the presence of Emmallodera crenaticostata G5 in unit 10 (shrub steppes of S. johnstonii crenaticostata Blanchard, Psectrascelis hirtus, and Lycium chilense). Figure 2 shows a distant Patagonogenius collaris (Kulzer), Praocis location of environmental units 7 and 10 with (Hemipraocis) sp. 1, and to a lesser extent Salax respect to the rest of the members of the other lacordairei Guérin-Méneville, Calymmophorus groups (G1, G2 and G3), evidencing that both peninsularis, Calymmophorus patagonicus units have extremely dissimilar tenebrionid Bruch, Patagonogenius quadricollis (Fairmaire), compositions. Analysis of similarities confirmed Pimelosomus sphaericus, and Plathestes that the composition of darkling beetles species kuscheli Kulzer (Figure 3a). The second PCA varied significantly among the five tenebrionid axis, accounting for 19.9% of the darkling species assemblages (ANOSIM: R = 0.76; p = 0.001; beetle variability, mainly distinguished G3 999 permutations, Table IV). and G5 (in their negative portion) from G1 The first two PCA axes explained together (located in the positive sector of this axis). G3 almost 50% of the variation in the tenebrionid was mainly characterized by the presence of species composition, evidencing the same Nyctelia picipes, Mitragenius araneiformis Curtis ordination of environmental units as NMDS and to a lesser extent Plathestes kuscheli. G1 did (Figure 3a). The broken-stick distribution typically Leptynoderes nordenskioldi Kulzer, model showed that only these two axes explain Leptynoderes tuberculata Curtis, Nyctelia a significant proportion of the variation in the circumundata Lesne, Nyctelia dorsata Fairmaire, darkling beetle species composition among Ecnomoderes bruchi Gebien occurred, and to a environmental units within PV (Figure 3b). The lesser extent Hylithus kovaksi and Blapstinus first axis, explaining 29.3% of the variability in punctulatus Solier (Figure 3a). The composition darkling beetle species composition, essentially of tenebrionid assemblage in the environmental
Table IV. Differences in similarity among tenebrionid species assemblages present in the five groups of environmental units analyzed with ANOSIM. Note: * Groups 4 and 5 were excluded from pairwise test because performing multiple comparisons ANOSIM requires the groups to be composed by more than one element in size (Legendre & Legendre 1998, Clarke & Warwick 2001).
Pairwise Tests* Groups of environmental units Global Test Groups R Statistic P
G1 (11, 12, 13, 15,16) 1 vs 3 0.812 0.008
G2 (1, 4, 20, 21) Global R = 0.756 1 vs 2 0.734 0.016 G3 (2, 3, 5, 8, 9) ( p = 0.001)
G4 (7) 3 vs 2 0.541 0.008
G5 (10)
An Acad Bras Cienc (2021) 93(3) e20201282 10 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS unit 10 (G5) was similar to that of G3 but with composition within PV was constituted by: pH, singular absence of Emmallodera hirtipes and Diurnal mean Temperature, Number of soil Epipedonota cristallisata (both species were horizons, Actual Evapotranspiration, % clay, present in all environmental units, except for this Precipitation, Nocturnal mean temperature, environmental unit). In addition, the tenebrionid Soil organic carbon content, and NDVI. These species assemblage in environmental unit 7 (G4) variables explained 77.2% of the variation in the was similar to that in G2 but whit the notable tenebrionid species composition and showed a absence of B. punctulatus. significant relationship for the overall test on all constrained axes (Pseudo F = 2.2626; p = 0.001; Habitat characteristics responsible for the with 999 permutations). The ordination space variation in the composition of tenebrionid defined by the first two RDA axes (Figure 4) species assemblage explained 45.7% of the total variation in darkling RDA analyses evidenced that the combination beetle species composition and evidenced of environmental variables that explained the same ordination of environment units and the greatest variability in tenebrionid species
Figure 3. A. Ordination of the environmental units as a function to their tenebrionid species composition in PV on the plain defined by the first two axes of PCA. The tenebrionid species assemblages are represented by different symbols (Group 1 = triangles; Group 2 = squares; Group 3 = circles; Group 4 = hexagon; Group 5 = diamond). Species acronyms as in Table II. B. Significance of PCA axes applying the broken-stick distribution. PCA axes with larger percentages of variance than the broken-stick variances were considered significant.
An Acad Bras Cienc (2021) 93(3) e20201282 11 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS darkling beetle assemblages than the first two temperature, number of soil horizons, and axes of PCA (Figure 3a). actual evapotranspiration (Figure 4). At the same The environmental relationship assessed by time, the second RDA axis explained 17.7% of the first RDA axis explained 28% of the variation the variation in the composition of tenebrionid in the tenebrionid species composition (Pseudo assemblages (Pseudo F = 4.6689; p = 0.027; 999 F = 7.3806; p = 0.001; 999 permutations) showing permutations) and evidenced that tenebrionid that the tenebrionid assemblage present species assemblages in G3 and G5 were positively in group G2 was positively correlated with correlated to clay percentage in soil and real nocturnal mean temperature and precipitation, evapotranspiration; while those in G1 were and negatively with soil pH, diurnal mean related with greater NDVI and soil organic carbon
Figure 4. Ordination of the tenebrionid species (continuous lines), habitat variables (dotted lines) and environmental units (triangles, squares, and circles) on the plain defined by the first two axes of RDA. The tenebrionid species assemblages are represented by different symbols (Group 1 = triangles; Group 2 = squares; Group 3 = circles; Group 4 = hexagon; Group 5 = diamond). Numbers designate species: 1. Praocis (Hemipraocis) sellata granulipennis // 2. Nyctelia dorsata // 3. Nyctelia circumundata // 4. Leptynoderes tuberculata // 5. Salax lacordairei // 6. Praocis (Hemipraocis) sellata peninsularis // 7. Patagonogenius quadricollis // 8. Patagonogenius collaris // 9. Psectrascelis hirtus // 10. Calymmophorus patagonicus // 11. Emmallodera crenaticostata crenaticostata // 12. Plathestes kuscheli // 13. Mitragenius araneiformis // 14. Nyctelia picipes // 15. Blapstinus punctulatus // 16. Hylithus kovaksi // 17. Ecnomoderes bruchi // 18. Leptynoderes nordenskioldi // 19. Epipedonota cristallisata // 20. Emmallodera hirtipes. Variables acroyms: SOC: Soil organic carbon content // NT: Nocturnal mean temperature // DT: Diurnal mean Temperature // Precip: Precipitation // R.Evap: Real Evapotranspiration // NumHor: Number of soil horizons // NDVI: Normalized Difference Vegetation Index // Clay: % of clay in soil texture // PH: soil pH.
An Acad Bras Cienc (2021) 93(3) e20201282 12 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS content (Figure 4). Finally, tenebrionid species The sample-size-based curves of the G1, G2 assemblage in G4 responded to intermediate and G3 showed that 95% confidence bands of environmental characteristics between G1 and darkling beetle richness (q = 0) widely overlap G3. among the three assemblages, indicating that The Variation Partitioning Analysis showed species richness is nearly similar for all (Figure that climate and soil features were the greatest 8a). The estimate of the effective number of determinants of the tenebrionid variability species in the assemblages considering their within PV, explaining 15% and 14% respectively; incidences (q = 1), showed that almost all 95% while vegetation explained only 1% (Figure 5). confidence intervals of G2 do no overlap (except The covariation (interaction) between climate for very small sizes) with those of G1 and G3 (Figure and soil variables added 9% to the explained 8b). Consequently, diversity of this assemblage variability in the darkling beetle species is significantly greater than the other two. At the composition, while the triple-interaction same time, when q = 2, in G3 it is lower than G1 climate-soil-vegetation added only 6 % more and G2 (Figure 8c). From the comparison among (Figure 5). coverage-based curves, the number of effective species estimated for q = 0, 1, and 2 show Tenebrionid species diversity variation among similar ordering of diversities as in the sample- environmental units of PV size-based curve (Figure 8d, 8e, 8f). However, The sample coverage for the recorded darkling these coverage-based curves clearly show that beetle fauna of PV was 0.97 (CV: 0.707), indicating G2 presented greater darkling beetle species that sampling was complete, and therefore, the diversity than the other two assemblages, since tenebrionid inventory is reliable. Figure 6 shows their 95% confidence bands never overlapped that 95% confidence intervals of the empirical when q = 1 and almost never when q = 2 (Figure and theoretical diversity curves overlapped 8e, 8f). Briefly, from both sample-size-based entirely in the profile. Consequently, a reliable and coverage-based sampling curves, darkling darkling beetle species diversity is estimated for beetle species richness (q = 0) did not differ the sampled community. At the same time, the among groups of environmental units, while the slope of the estimated diversity profile reflected estimated number of effective species for q = a moderate unevenness of darkling beetle 1, and 2 decreased from G2 > G1 > G3 (Figure 8). species incidences in PV (Figure 6). It was not possible to statistically compare the The sample coverage for assemblages in G1, tenebrionid species diversity of assemblages G2 and G3 were respectively 93.33%, 92.35%, and present in G4 and G5 with the remaining groups 86.49 (Figure 7). Additionally, this curve showed of environmental units because analyses require that 95% confidence bands for the three groups groups of environmental units to be composed widely overlapped among them, indicating that by more than one element in size (Chao et al. sampling completeness is nearly similar for 2014, Hsieh et al. 2016). However, table II showed the three darkling beetle assemblages (Figure that the number of registered tenebrionid 7). For G1 the effective number of species in species in both environmental units was lower the assemblage for q = 0, q = 1 and q = 2 were than in the other units (4 and 3 respectively). respectively 16, 14.3 and 13.4; for G2: 23, 19.3 and 17; while for G3: 14, 11.3 and 10 (solid triangles, circles and squares in Figure 8).
An Acad Bras Cienc (2021) 93(3) e20201282 13 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS
Figure 5. Variation partitioning of RDA for the relationship among habitat variables and composition of tenebrionid species assemblages in PV. Three sets of explanatory variables were included: climate, soil and vegetation variables. The percentages corresponded to the variability in tenebrionid assemblage composition explained by each set of explanatory variables and their interactions.
Figure 6. Tenebrionid diversity profiles curves plotting Hill numbers qΔ (∞) as a function of order q, 0 ≤ q ≤ 3. The slope of the diversity profile curves reflects the unevenness of species relative incidences. When the more uneven the distribution of relative species incidences is, the more steeply the curve declines (Chao et al. 2014, Hsieh et al. 2016). The continuous line represents the theoretical diversity profile, while the dotted line is the empirical diversity profile. Both curves were plotted with their 95% confidence intervals.
Figure 7. Sample completeness curve. The three main tenebrionid species assemblages identified by ANOSIM are represented by different symbols (Group 1 = triangles; Group 2 = squares; Group 3 = circles). It was not possible to include sample completeness curves for G4 and G5 groups because statistical analyses require groups of environmental units to be composed by more than one element in size (Chao et al. 2014, Hsieh et al. 2016). All curves were plotted with their 95% confidence intervals. Continuous lines represent the interpolated and dotted lines the extrapolated portions of the curve.
An Acad Bras Cienc (2021) 93(3) e20201282 14 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS
Figure 8. Sample-size and coverage-based rarefaction/extrapolation sampling curves with Hill numbers based on incidence data (q = 0, 1, 2) among the three main tenebrionid species assemblages identified by ANOSIM (Group 1 = triangles; Group 2 = squares; Group 3 = circles). It was not possible to include sample-size and coverage-based rarefaction/extrapolation sampling curves for G4 and G5 groups because statistical analyses require groups of environmental units to be composed by more than one element in size (Chao et al. 2014, Hsieh et al. 2016). All curves were plotted with their 95% confidence intervals. Continuous lines represent the interpolated and dotted lines the extrapolated portions of the curve. Upper: Sample-size-based rarefaction/extrapolation sampling curves. Bottom: Coverage-based rarefaction/extrapolation sampling curves.
DISCUSSION suggested that tenebrionids are distributed in discrete units within the peninsula. At the This work evidenced that darkling beetles same time, our findings about environmental make a discretionary use of habitat types factors that determine distribution patterns based on the environmental factors present of darkling beetles in PV are in agreement in PV. Variations in assemblage composition with those evidenced by other epigeal beetle patterns among environmental units were communities both in northwestern (Mazía mainly determined by the variation in climatic et al. 2006, Werenkraut & Ruggiero 2012) and and edaphic features, and to a lesser extent southern Patagonia (Rosas et al. 2019). Sheldon by vegetation characteristics. These findings & Rogers (1984), in a study at a similar scale confirmed those of Carrara et al. (2011b), who
An Acad Bras Cienc (2021) 93(3) e20201282 15 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS carried out in Arizona, USA, found that the piedemont pediments, and G5 in Holocene majority of darkling beetle species occurred in beach ridges, respectively. It should be noted all or most of the environmental units. However, that in both assemblages the smaller number most of the tenebrionid species inhabiting of tenebrionid species were recorded. It is also the peninsula showed narrow distributions. remarkable the low incidence of species in the This fact evidences their relatively constricted tenebrionid assemblage present on the north- environmental preferences, which is especially eastern tip of the peninsula (G5) where small evident in the five species that were found only mixed patches of Schinus polygamus and Lycium in one environmental unit. In the present study chilense are the only vegetation. Considering the few tenebrionid species were widely distributed previous discussion on the variables that most among environmental units, which suggest that affect the distribution of these beetles in the darkling beetles from Península Valdés may peninsula, it may be caused by the convergence have narrow tolerance limits to environmental of some particular features that determine a very variations than those in the American northern unfavorable environment for the establishment hemisphere. of the majority of tenebrionid species inhabiting The present work allows clustering PV. This environment, the youngest within PV, environmental units within the peninsula is constituted entirely by beach ridges recently into five groups, each one with an exclusive originated during the Holocene from successive darkling beetles species assemblage. The first coastal marine deposits. Consequently, their group of environmental units is represented poorly developed soils are still large gravelly by established sandy aeolian fields, where areas of bare soil without any vegetation nor perennial grass steppes are the dominant litter cover, and extremes temperatures (Bouza vegetation and photosynthetic activity and soil et al. 2017a, Bertiller et al. 2017). organic carbon content are the greatest of the Considering the ecological relevance that peninsula (Rostagno 1981, Bouza et al. 2017a, darkling beetles have in arid ecosystems and b). The second group of environmental units is taking into account the restricted distribution composed by piedmont pediments of the coastal observed for seven species inside PV (C. zones and piedmont pediments and “bajadas” peninsularis, N. darwini, P. sphaericus, P. of great endorheic basins (salt flats), where (Orthogonoderes) argentina, P. (Hemipraocis) more abundant rains and more elevated night sp.1, S. lacordairei and C. patagonicus), temperatures than the remaining environment to maximize the chances of an effective units of the peninsula are present (Rostagno preservation of the biodiversity and ecological 1981, Bouza et al. 2017a, b). The third group is processes in the region, we strongly recommend constituted by the alluvial plains (terraces) of to prioritize the conservation efforts on at least the peninsula, where daytime temperatures some of the environmental units inside each of are higher, rains are lower, soils profiles are the groups identified in this study. Since many more complex (due to the presence of hardy of the environmental units within PV are similar horizons that hinder root development), and to other areas in the northeastern Patagonia consequently Chuquiraga avellanedae is the (Beeskow et al. 1997), the same environmental dominant shrub (Rostagno et al. 1981). The fourth factors determining the structure and diversity of and fifth tenebrionid species assemblages are darkling beetles species in PV may be expected only present in environmental units G4 in coastal
An Acad Bras Cienc (2021) 93(3) e20201282 16 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS for the rest of the region; however, more studies very important for darkling beetle community would be necessary to corroborate this thought. patterns within PV. These findings agree with In agreement with other authors, daytime other authors who pointed out that edaphic temperatures and rainfall were among the variables are important determinants of the most important environmental variables that structure of darkling beetle communities (e.g. explained the distribution of darkling beetles Sheldon & Roger 1984, Ayal & Merkl 1994, in PV (de los Santos et al. 2002, Werenkraut & Krasnov & Shenbrot 1996, de los Santos et al. Ruggiero 2012, Liu et al. 2012, Bartholomew & 2002, Perner et al. 2005, Werenkraut & Ruggiero El Moghrabi 2018, Rosas et al. 2019). Since both 2012, Rosas et al. 2019). Generally, it is assumed temperatures and rainfall also determine much that soil variables have mainly indirect effects of the spatial variation in the structure of beetle on insects through their influence on the communities in the northwest (Werenkraut & composition of the plant community (Perner et Ruggiero 2012) and the southernmost extreme al. 2005, Werenkraut & Ruggiero 2012); however, of Patagonia (Rosas et al. 2019), it is expected the variation partitioning procedures performed that these variables will be very important for in this study showed that there is no shared these insects in all arid Patagonia. According effect between soil and vegetation variables on to Parmenter et al. (1989b), we found that the explanation of spatial distribution patterns temperature was more influential on darkling of darkling beetles in PV. In addition, most of beetles distribution than precipitation. This is the tenebrionid species present in PV belong to also supported by our field observations on PV the subfamily Pimeliinae (Flores 1998, Matthews about several tenebrionid species performing et al. 2010) and to the Tenebrioninae tribe behaviors related to thermoregulation, e.g. Scotobiini (Kulzer 1955, Matthews et al. 2010) burrowing in the substrate, “shuttling” between (Table II), which have hypogeal larvae (Flores open areas exposed to sunshine and shade 1998, Matthews et al. 2010, Silvestro & Michat places, and “stilting”-elevating the body as high 2016, Cheli G.H. pers.Obs.). Consequently, we as possible above the hot substrate- (Cloudsley- argue that soil variables mostly have a direct Thompson 2001, Cheli & Martínez 2017). However, influence on the spatial distribution patterns of in accordance with the results obtained by other darkling beetles within PV. This is additionally authors (e.g. Marino 1986, Crawford 1988, de los supported by the fact that in our study the higher Santos et al. 2002), precipitation was also very incidence and diversity of tenebrionid species important to explain variation in darkling beetles were present in the group of environmental distribution patterns inside PV. It is known that units with the most soft-packed soils. These conserving corporal water is crucial for the soils have low adhesion between their particles survival of these insects in arid ecosystems due to their medium size (Rostagno 1981, Bouza (Flores 1998, Cloudsley-Thompson 2001, de los et al. 2017b). Consequently, may be easier for Santos et al. 2002), and the fact that more than darkling beetles to dig in softer soil in their 90% of the darkling beetles species recorded in search for shelter, oviposition suitable places, PV have characteristics compatible with high or and food supply (Crawford 1988, Krasnov & very high adaptations to retain water (Carrara et Shenbrot 1996, de los Santos et al. 2002, Carrara al. 2011b) is in agreement with those ideas. et al. 2011b, Flores et al. 2011). In contrast, At the same time, soil pH, the number soils with high percentage of clay and several of soil horizons, and soil texture were also horizons (in general related to the presence
An Acad Bras Cienc (2021) 93(3) e20201282 17 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS of argillic horizons) are very hard-packed (see habitat to which they are specific, they provide Rostagno 1981 and Bouza et al. 2017b) and thus no information on the direction of monitoring difficult to dig for several tenebrionid species ecological changes, because they are restricted (Doyen & Tschinkel 1974, Crawford 1988, Krasnov to a single ecological state (Mc Geoch et al. 2002). & Shenbrot 1996). This is in agreement with the Therefore, in order to maximize the information lower incidence and diversity of tenebrionid on habitat quality extracted from bioindicator species observed in those environmental units assemblages and to improve the efficiency of in PV with hard-packed soils. bioindication systems, those authors suggest Several authors argue that vegetation, to study those species having different degrees especially shrub cover, is the main determinant of preference for different ecological states, of habitat selection for darkling beetles at local i.e. with intermediate habitat specificity (called scales (see Parmenter et al. 1989a, Mazía et al. detector species) jointly with characteristic 2006, Liu et al. 2012). However, the present study, species. These species can indicate the direction carried out on a regional scale, did not show of environmental change by their prevalence that percentage of plant cover, plant species as the habitat changed from their less towards richness nor vegetation structure mainly their more preferred habitat state. Following determine distribution patterns of tenebrionid this framework, to estimate the direction of beetles within PV. Recently Martínez et al. (2018), possible environmental changes in PV, we working locally in steppes of southern PV, found strongly recommend to incorporate in futures that variables related to vegetation influenced monitoring of tenebrionid assemblages those more than soil on the abundance and diversity species distributed in several environmental of epigeal arthropods. At the same time, Mazía units (e.g. P. kuscheli and B. punctulatus) jointly et al. (2006), also at local scale, showed a strong with characteristic species in futures monitoring influence of shrub patches on darkling beetles of tenebrionid assemblages. habitat use in a steppe of northwest Patagonia. Finally, the introduction of domestic Inconsistencies among our findings with those livestock in the arid Patagonia produced of the above mentioned studies in Patagonia changes in vegetation and soil that altered may be due to the fact that both species fundamental ecosystem processes, increasing distribution patterns and ecological processes desertification and biodiversity loss (Beeskow et are scale-dependent. Thus, the processes to al. 1997, Bisigato et al. 2005, 2009, Chartier et al. which tenebrionid species distribution patterns 2011, Rossi & Ares 2012). Moreover, despite being respond may be different according to the scale a nature reserve, PV is not the exception (Cheli of analyses (Colombini et al. 2005). More research et al. 2016b, Baldi et al. 2017, Cheli & Martínez comparing arthropod distribution patterns at 2017). Consequently, it is to be expected that different scales in the region will help to clarify anthropogenic disturbances, as grazing, would these considerations. interact with environmental factors determining The present study identified species the composition of tenebrionid assemblages in with high habitat specificity and fidelity (i.e., the area. In this context, taking into account the characteristic species, like C. peninsularis, L. ecological relevance of tenebrionid beetles in PV nordenskioldi, P. hirtus, N. picipes). Although (Cheli et al. 2009, Carrara et al. 2011b, Flores et al. changes in the abundance of characteristic 2011, Baldi et al. 2017, Cheli & Martínez 2017), we species are useful for monitoring within the recommend incorporating these darkling beetle
An Acad Bras Cienc (2021) 93(3) e20201282 18 | 22 GERMÁN H. CHELI et al. DETERMINANTS OF TENEBRIONIDAE IN PENÍNSULA VALDÉS assemblages into future conservation strategies Conservation. In: Bouza P & Bilmes A (Eds), Late Cenozoic for arid Patagonia, including characteristic of Península Valdés, Patagonia, Argentina. Springer Earth System Sciences. Springer, Cham., p. 263-303. and detector species, their relationship with environmental factors and anthropogenic BARTHOLOMEW A & EL MOGHRABI J. 2018. Seasonal preference of darkling beetles (Tenebrionidae) for shrub disturbances. vegetation due to high temperatures, not predation or food availability. J Arid Environ 156: 34-40. DOI: 10.1016/j. Acknowledgments jaridenv.2018.04.008.
We warmest thanks to Drs. Mario Rostagno, Pablo Bouza, BEESKOW AM, DEL VALLE HF & ROSTAGNO CM. 1997. Los and MSc Ana Maria Beeskow who kindly shared with us sistemas fisiográficos de la región árida y semiárida many unpublished Península Valdés environmental data, de la Provincia de Chubut. Delegación Regional SECYT, and whose helpful comments have greatly improved Puerto Madryn, Chubut, 144 p. early drafts of the present manuscript. We thank to Alejandra Bueno for her language assistance and two BERTILLER MB, BEESKOW AM, BLANCO PD, IDASZKIN YL, PAZOS anonymous reviewers for their valuable comments GE & HARDTKE L. 2017. Vegetation of Península Valdés: that greatly improved this manuscript. We deeply Priority Sites for Conservation. In: Bouza P & Bilmes thank IPEEC (CCT CENPAT-CONICET) and Fundación Vida A (Eds), Late Cenozoic of Península Valdés, Patagonia, Silvestre Argentina for providing facilities and logistic Argentina. Springer Earth System Sciences. Springer, support; Association of owners of Península Valdés Cham., p. 131-159. (PROPENVAL); Administrator of the protected area, and BISIGATO AJ, BERTILLER MB, ARES JO & PAZOS GE. 2005. Effect Fundación Vida Silvestre Argentina who allowed access of grazing on plant patterns in arid ecosystems of to the study area. We are grateful to Secretaría de Patagonian Monte. Ecography 28: 561-572. Turismo y Áreas Naturales Protegidas and Secretaría de BISIGATO AJ, SAÍN CL, CAMPANELLA MV & CHELI GH. 2015. Fauna of the Chubut province for providing collecting Leaf traits, water stress, and insect herbivory: Is food permissions. Field work was supported by Agencia selection a hierarchical process? Arthropod-Plant Inte Nacional de Promoción Científica y Tecnológica (PICT 9: 477-485. 2012-2660), CONICET (PIP 112-200801-00162; PIP 112- 201101-00987; PUE-IPEEC-CONICET Nº 22920160100044) BISIGATO AJ, VILLAGRA PE, ARES JO & ROSSI BE. 2009. Vegetation and the International Barcode of Life Project (iBOL). Trip heterogeneity in Monte Desert ecosystems: A multi-scale to Budapest Museum of GEF in 2018 to study Kulzer and approach linking patterns and processes. J Arid Environ Kaszab’s type specimens was supported by CONICET, 73: 182-191. Argentina and by a grant awarded by The Ernst Mayr BORCARD D, GILLET F & LEGENDRE P. 2011. Numerical ecology Grants Committee (Harvard University). with R. Springer: New York, New York, NY, p. 319.
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