Anthropogenic disturbance and environmental factors drive the diversity and distribution of earthworms in São Miguel Island (Azores, Portugal)

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Anthropogenic disturbance and environmental factors drive the diversity and distribution of earthworms in São Miguel Island (Azores, Portugal) J.A. Talaveraa, , L. Cunhab,c, J.R. Arévalod, I.P. Talaverae, P. Killeb, M. Novob,f ⁎

a

Department of Animal Biology (Zoology), University of La Laguna, Tenerife, Spain School of Biosciences, Cardiff University, UK c School of Applied Sciences, University of South Wales, Pontypridd, UK d Department of Botany, Ecology and Vegetal Physiology, University of La Laguna, Spain e Consejería de Educación, Gobierno de Canarias, CEP García Escámez, Tenerife, Spain f Department of Biodiversity, Ecology and Evolution, Complutense University, Madrid, Spain b

ARTICLE INFO

ABSTRACT

Keywords: Earthworm diversity Azores colonization Land use Soil parameters Altitude effects

We present an evaluation of earthworm fauna in São Miguel Island (Azores, Portugal) revealing that it is rich in species in relation to its size and nature. Four families (Acanthodrilidae, Lumbricidae, Megascolecidae and Rhinodrilidae), 15 genera and 27 species were inventoried. About 74% were Palearctic species and 26% were Intertropical, mainly invasive earthworms originating from South-East Asia, of which Amynthas corticis Kingberg, 1867 was most dominant. The first comprehensive checklist of São Miguel earthworms is detailed, and the outdated nomenclature is improved, unifying synonymous taxa such as Lumbricus azoricus Eisen, 1869 and Allolobophoridella eiseni Levinsen, 1884. Seven new earthworm species records are given, highlighting Lumbricus friendi Cognetti, 1904 and Amynthas diffringens Baird, 1869 as cited for the first time in Macaronesia, and therefore expanding their known geographic range to the northern border of this region. Moreover, richness and composition of species were evaluated in relation to environmental and anthropogenic characteristics, including soil properties, altitude, land use intensity or distance to urban nuclei. Our results demonstrated that soil pH affected the establishment of species and that organic matter is positively associated with abundance of some non-native lumbricids (e.g. the anecic Octodrilus complanatus Dugés, 1828) and negatively related to richness and abundance of exotic species such as Amynthas corticis, Amynthas gracilis Kingberg, 1867 and Pontoscolex corethrurus Müller, 1857. Results suggested that land use intensity, represented as five categories ranging from undisturbed sites with native vegetation to sites under intensive agriculture exploitation, is a good predictor of species composition. Higher values of diversity and density of Intertropical species were found in more intensively exploited locations. Moreover, the Palearctic lumbricids, although present in all the disturbance categories tested, were the most diverse group at higher altitudes. The species Dendrodrilus rubidus tenuis Eisen, 1864 and Lumbricus rubellus Hoffmeister, 1843, with narrow distribution range, showed a trend towards natural, non-intensive (NI) and low intensity (LI) systems. Our results indicate that anthropogenic disturbance and altitude are the main drivers of earthworm diversity on the island of São Miguel, making these animals good indicators for land use intensity. Therefore, earthworm surveys may help design conservation programs in protected areas.

1. Introduction

geological time of earthworms' colonization has been subject of debate (Rull et al., 2017). The presence of these annelids in previously uninhabited ecosystems within insular or continental territories provides important clues to the factors affecting their colonization dynamics and present-day distributions. The knowledge on how earthworm presence relates and shapes the aboveground has identified new concerns regarding environmental resilience and implications for terrestrial

The Azorean archipelago is located in the Northern Middle Atlantic Ocean, situated at the triple junction between the African-Eurasian and North-American plates (França et al., 2003). It comprises nine main volcanic islands, of which São Miguel is the largest. This island emerged before the end of the Cenozoic, and its evolution as well as the

⁎ Corresponding author at: Department of Animal Biology, Soil Science and Geology, University of La Laguna, Sciences Faculty (Biology), CP38206 La Laguna, Canary Islands, Spain. E-mail address: [email protected] (J.A. Talavera).

https://doi.org/10.1016/j.apsoil.2019.06.004 Received 21 December 2018; Received in revised form 7 June 2019; Accepted 10 June 2019 0929-1393/ © 2019 Elsevier B.V. All rights reserved.

Please cite this article as: J.A. Talavera, et al., Applied Soil Ecology, https://doi.org/10.1016/j.apsoil.2019.06.004

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ecosystems (Bardgett and van der Putten, 2014). Besides, with the resurgence of interest in earthworms, a particular focus on the relationship between diversity and ecosystem services is becoming a crucial part of ecosystem quality evaluation in an environmental assessment (Lee, 1985; Blakemore, 1999; Bartz et al., 2013; Pascual et al., 2015). The scarcity of predators and high abundance of potential niches within Macaronesian islands, including São Miguel, allow these annelids to become successful invaders (Talavera, 2011). The conversion of native forest to tropical crops has largely contributed to the settlement of nonnative earthworms, altering the diversity footprint and changing soil properties (Talavera, 1992). Several studies have documented such effects, especially in areas that were previously disturbed (Hendrix et al., 2006; Szlávecz and Csuzdi, 2007; Feijoo et al., 2011). Despite the importance of earthworms in insular ecosystems, the richness and abundance of lumbricids have been rarely explored in the Azores, the work by Talavera (1993) the most recent contribution. Moreover, there is no data on the effects of environmental variables on earthworm communities in São Miguel Island. Available bibliographic records (Rosa, 1893; Gates, 1972a, 1972b, 1978, 1982; Michaelsen, 1900, 1910) are far from being accurate and present scarce data, typical of brief expeditions. Two primary sources are those provided by Michaelsen (1891) and Sciacchitano (1964) that reported the presence of a few lumbricids but without describing their ecological and biogeographical traits. These authors also reported the existence of two exotic megascolecids: Pheretima indica (Kinberg, 1867) and Pheretima barbadensis (Beddard, 1892), both Asian species that were transferred to the genus Amynthas by Sims and Easton (1972). These megascolecids are widely distributed throughout the tropical and subtropical regions of the world, and are likely to increase their spread throughout the Macaronesian islands. Recently, Novo et al. (2015) showed the great adaptive potential of Amynthas corticis Kingberg, 1867 to different environmental scenarios in Azores, and Cunha et al. (2011, 2014) reported the presence of Amynthas gracilis Kinberg, 1867 and Pontoscolex corethrurus Müller, 1857 in Furnas geothermal field within São Miguel. The latter is considered to be a pantropical colonizer that tolerates high soil temperatures, generally showing high plasticity (Lavelle et al., 1987). The current research is the result of our own initiative to explore earthworm fauna of some North Atlantic Ocean Islands, particularly those that make up the westernmost boundary of the Palearctic ecoregion (Hendrix et al., 2008), of special interest for regional biodiversity. We intend to provide the first comprehensive checklist of São Miguel earthworms. In this work, we update the list of taxa by adding new records, eliminate erroneous species records, and update the valid names. Moreover, the richness and composition of species in relation to some environmental characteristics and human impact are statistically analyzed. We test the hypothesis that human environmental impact on soil is determining the composition and richness of different groups of species (classified by functional groups and original source), and that altitude is one of the most robust variables to determine species richness. Our results will help better understand the ecology and some of the drivers of earthworm communities at the insular scale and evaluate the idea that these animals may eventually be used as indicators of human disturbance.

The average temperature (17–18 °C) and the atmospheric humidity of ~80% (Fernandes, 2004) are also significant characteristics of this island. Further details can be found in AEMET-IMP (2012). The above values show seasonal changes and vary with altitude and orientation; for example, the precipitations increase at higher elevations and are greater in the northern flank when compared to the southern flank. Three main volcanic craters with permanent lakes are present in São Miguel: Sete Cidades, Fogo and Furnas. Well established populations of the earthworm P. corethrurus were found in Furnas soils (Cunha et al., 2014), where several active volcanic spots, including fumarole fields, are present (Viveiros et al., 2009). Vascular flora is altitudinally structured, and the proportion of introduced species by settlers is very high (Silva and Smith, 2004). The current forested area occupies only 25% of São Miguel total surface and it is constituted by scarce “laurisilva” and dominant trees introduced from Australia and Japan, such as Pittosporum undulatum Ventenat, 1802, Eucalyptus globulus Labill, 1800, and Cryptomeria japonica Don, 1839 as indicated by Rull et al. (2017). Regarding altitude, three significant zones were considered for the present study. A) Lowlands, including a total of 14 sites located below 250 m. They generally show the highest anthropogenic influence, and according to Fernandes (2004) this area presents scarce rainfall (< 1000 to 1400 mm) and high temperature (average 17 °C) that decreases with elevation. B) Mid or intermediate belt (250–500 m above sea level), including 10 sites, where the mean temperature fluctuates from 14 to 17 °C and the rainfall from 1400 to 1800 mm (Fernandes, 2004). It is a small homogenous zone where the traditional polycultures, as well as large meadows with sparse trees, are abundant. Most of the rural nuclei are located here. C) High lands (mountain belt), with 11 sites widely spread below 500 m. Dense fog is frequent in this zone, which presents the lowest mean temperatures (< 14 °C) and the highest annual rainfall, reaching 4800 mm/annual at the highest peaks. Further climatic data can be found at IPMA (www.ipma.pt/ pt/oclima/normais.clima/1981-2010/020/) (Instituto Português do Mar e Atmosfera). 2.2. Semi-quantitative scale of land use intensity Land use intensity was estimated using a scale with the following five categories (Arévalo et al., 2005; Cameron et al., 2007; Feijoo et al., 2011; Talavera, 2011). (1) Non-intensive (NI): Sites with native vegetation, dominant arboreal cover and lush ferns and presence of endemic grasses. The 8.1% of sampled sites were included within this category (sites 4, 35 and 36). (2) Low intensity (LI): Sites with mature stands. The dominant tree species were coniferous, heather and deciduous tree cover. This category includes forest paths, and sites covered by ferns. The 16.21% of sampled sites were included here (sites 2, 3, 17, 21, 22 and 30). (3) Moderate intensity (MI): Mainly grassland and pastures, with herbaceous species such as Amaranthus, Mentha, and Oxalis, the conifer Cryptomeria and scattered shrubs as well as presence of grazing livestock. The sites within this category represented the 21.65% of sampled sites (sites 1, 8, 20, 28, 31, 32, 33 and 34). (4) High intensity (HI): Spaces adjacent to agricultural holdings. This category also included arable fields surrounding urban nuclei and edge of unpaved roads with dominant ruderal species (weedy in disturbed substrates). The 27.02% of samples sites were included within this category (sites 5, 7, 11, 13, 14, 16, 24, 25, 27 and 29). (5) Very high intensity (VHI): Sites under intensive agriculture exploitation with predominance of exotic crops plantation, e.g. pineapple, fruit orchards, and banana trees. Crop management practices within these sites include the addition of organic fertilizers and pesticides. The 27.02% of samples sites were included within this category (sites: 6, 9, 10, 12, 15, 18, 19, 23, 26 and 37). These sites and those indicated above are detailed in Supplementary Appendix A.

2. Materials and methods 2.1. Study area and altitudinal zones São Miguel is the largest island of the Azorean archipelago and the most densely populated, with maximum elevation of 1103 m above sea level (a.s.l.), an area of 757 km2 and around 125,000 inhabitants. It is located at approximately 860 km from European mainland and 1800 km from North America (Fig. 1A). It presents a temperate climate (subtropical) with low annual thermal variation and an average rainfall of 1700 mm (Rull et al., 2017), which presents asymmetries along the different altitudinal levels.

2.3. Experimental design and earthworm sources In order to obtain a significant database, we used sampling protocols at different spatial scales, covering the ecological areas of interest 2

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N

A

0

50 100

200 Kilometers

N

B

0

5

10

20 Kilometers

Intertropical Species Palearctic Species

0

5

10

20 Kilometers

Fig. 1. Maps of the studied area. A: Geographic positioning of Azores archipelago (global positioning with Azores highlighted in red; local island positioning with São Miguel island highlighted by a yellow circle); B: sample sites within São Miguel Island (Azores); C: Distribution and proportion of Palearctic/Intertropical species in each of the 37 sampling sites. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) 3

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(lowland and mountain sites). Thirty-seven sampling sites were chosen, representing a significant part of the total surface area of São Miguel. A map showing the distribution of the 37 collecting sites in São Miguel is presented in Fig. 1B. Those sites were distributed along an altitudinal gradient from 45 to 960 m a.s.l. and their general characteristics are given in Supplementary Appendix A. For the faunistic component of this manuscript, we integrated records from an unpublished dataset originated in an expedition from 1989 and financed by the National Geographic Society of the U.S.A. For the newly sampled sites, GPS coordinates were registered and at least three standardized 50 cm × 50 cm × 30 cm depth micro-plots were randomly selected. The plots were separated by intervals > 3 m, in order to avoid any neighboring effects and reduce self-correlation effects. According to other authors (Ivask et al., 2007; Szlávecz and Csuzdi, 2007; Feijoo et al., 2011) these square dimensions favor an accurate estimate of the abundance and species richness. A sampling depth of 30 cm has been shown to be effective in volcanic soils of Macaronesian islands that are usually shallow (Talavera, 2007, 2011). To maximize the location of specimens across different niches we searched under rocks and mosses, in leaf litter and compost, under fallen tree rotten trunks, etc. All specimens were hand collected and stored in absolute ethanol. Species identification was performed following Blakemore (2012) and Sims and Easton (1972) for Intertropical species, and Reynolds and Misirhoglu (2018) and Talavera (1990) in the case of Palearctic earthworms. The validated names adopted here are based on Blakemore (2008), Sims and Easton (1972) and Mrsic (1991). We have grouped São Miguel species into (Fig. 1C). a) Palearctic group represented by lumbricids plus Microscolex dubius Fletcher, 1887; which includes taxa originated in the Western Palearctic ecoregion and widely disseminated therein. We consider that São Miguel and other Macaronesian islands are part of this ecoregion (Talavera, 1996, 2007). b) Intertropical group, constituted by megascolecids and the rhinodrilid P. corethrurus, assumed to have originated from Indo-Malaya ecoregion and Guiana plateau respectively. We consider them exotic taxa common in tropical areas between Tropic of Cancer and Tropic of Capricorn parallels. Ecological categories are those proposed by Bouché (1977) and Lee (1985). The taxa cited by other authors but not found by us, Dendrobaena hortensis Michaelsen, 1890, Dendrodrilus rubidus rubidus Savigny, 1826, Dendrodrilus subrubicundus Eisen, 1874 and Eisenia fetida Savigny, 1826, were excluded from statistical analyses. In addition, composite soil samples were taken from the excavated soil (sample estimate = 1 kg) in order to calculate soil abiotic parameters. Methods for determination of soil pH, moisture percentage and organic matter content are described in Novo et al. (2015).

Levene tests respectively) required for ANOVA. Post-hoc comparisons (Tukey test, p < 0.05) were used when significant differences were found. Similar analyses were performed to study the effect of altitudinal zones defined in the study area on soil physical-chemical variables. In this case, a Kruskal-Wallis test for independent samples was implemented because the assumptions of normality and homoscedasticity were not fulfilled. The effect on altitudinal zones and land use intensity on richness and abundance of earthworm species was analyzed through ANOVA and Tukey test as described above. Earthworm species were considered altogether or were classified in groups according to their ecological category (epigeic, endogeic, anecic) or their geographical origin (Palearctic/Intertropical). In order to find direct relationships, we correlated richness, abundance and evenness index of the sites, the different ecological categories, and geographical origin of species with land use intensity, pH, moisture, organic matter, altitude and urban distance (Pearson correlations). Basic statistics (Legendre and Legendre, 1998) were applied using SPSS v. 22 (2013) statistical package. Finally, Sørensen index (Soerensen, 1957) was calculated in order to analyse the similarity of earthworm species composition in São Miguel (SM) when compared to different Palearctic islands, specifically: Gomera (GO); La Palma (PA); Hierro (HI); Madeira (MA); Cape Verde (CV); São Tomé (ST); Saint Helena (SH); Cyprus (CH); Crete (CR); Sicily (SI); Sardinia (SA); Corsica (CO). Mean distance among groups was used for dendrogram conglomeration and representations were based on standardized distance (0–25). Articles including relevant information on the faunistic composition of those islands were reviewed and are referenced in the discussion (see Section 4.1). 3. Results 3.1. Earthworm biodiversity, new records and distributional patterns Twenty-three species and subspecies of earthworms were identified from the 1291 individuals collected in this study. Those, together with species not found by us but cited in previous studies such as D. r. rubidus, D. r. subrubicundus, D. hortensis and E. fetida, constitute a total of 27 nominal taxa within the current known São Miguel earthworm fauna (Table 1), twenty of which are Palearctic in origin and seven are Intertropical, the latter represent the most recent faunistic component. One family (Acanthodrilidae) and eleven new species records are presented for São Miguel and are highlighted with an asterisk in Table 1. These results reveal that the faunal inventory was not saturated, and it is probable that around 25% of the species remain undiscovered. Our results show co-existence of Palearctic and Intertropical species in 80% of the sites, the most spectacular case being the presence of A. corticis (epigeic) and Aporrectodea caliginosa Savigny, 1826 (endogeic) in almost 60% of the ecological niches explored. The mentioned species were found in widely scattered localities from the coast to the mountain belt. In contrast, the scarce presence of Amynthas diffringens Baird, 1869 and Lumbricus friendi Cognetti, 1904 reveals these are infrequent species in São Miguel Island. Richness and abundance of earthworms were heterogeneous within and between sampling sites and significantly unequal at level of the four families found. In terms of diversity, the Acanthodrilidae, represented by the euryhaline M. dubius, showed a distribution restricted to mountain belt, with mature stand trees, which extends between 576 (Lombadas) and 690 m a.s.l. (Achada). The family Rhinodrilidae is represented by the species P. corethrurus, which has been able to adapt to elevated temperatures of soils in the degassing fields at Furnas (180–210 m a.s.l.). It also appears distributed in the lowlands of São Miguel southern edge, preferably in pineapple greenhouse cultivations. Six of the peregrine species found belong to the exotic Megascolecidae. We discovered that A. diffringens, Metaphire californica Kinberg 1867 and Pithemera bicincta Perrier, 1875 are only spread through the lowlands (< 220 m), under high environmental stress, such as agroecosystems within or near urban nuclei. However, A. gracilis and A. corticis

2.4. Statistics Ordination techniques help explain community variation (Gauch, 1982) and have been used here to evaluate trends in earthworm species composition along different environmental gradients. As a technique for direct gradient analysis, we used Canonical Correspondence Analysis (CCA; Hill and Gauch, 1980) in CANOCO version 4.5 (Ter Braak and Šmilauer, 1998) in order to examine how species composition changed across the different plots according to the measured environmental characteristics. The biotic matrix was composed from a set of 23 species and their corresponding abundance in terms of number of individuals appearing in each of the sampled sites (each site was a true replicate). For the CCA, a forward selection procedure was used to choose the variables explaining a significant portion of the variability (Monte Carlo permutation test, 499 interactions) and only these significant variables were included in the analysis. The anthropogenic effect of land use intensity on the physical-chemical variables pH, moisture, organic matter and altitude was tested through a unidirectional ANOVA. Five different levels of land use intensity were considered: 1 to 5 (NI, LI, MI, HI, VHI). Untransformed data fulfilled normality and homoscedasticity (Shapiro-Wilk and 4

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Table 1 List of earthworm taxa (belonging to the families Acanthodrilidae, Lumbricidae, Rhinodrilidae, Megascolecidae) found so far in São Miguel Island (Azores, Portugal). The table includes information on ecozones (EZ); ecological category (EC), Palearctic/Intertropical species (P/I); number of occurrences in the 37 sampled localities (OS); previous cites by other authors (PC); land use intensity of the places where species where found (LUI). Pr = Palearctic region; Or = Oriental region; Nr = Neotropical region; En = Endogeic; An = Anecic; Ep = Epigeic; a = Cunha 2014; b = Cunha 2011; c = Michaelsen 1891; d = Mich. 1910a; e = Mich. 1922; f = Sciacchitano 1964; g = Talavera 1993; ⁎New records for São Miguel. Lumbricus azoricus was described in 1869 by Gustav Eisen with endemism rank, but we believe it to be a misidentification. The morphological characteristics observed in the photograph of holotype (size, absence of tubercula pubertatis and clitellum in segments 24–32), together with the lack of observations within our study, leads to its invalidation and, consequently, it is designated as a junior synonym of Allolobophoridella eiseni. Families/species in São Miguel

EZ

EC

P/I

OS

Acanthodrilidae(⁎) ⁎ Microscolex dubius (Fletcher, 1887)

Pr

En

P

2

Lumbricidae Allolobophora chlorotica (Savigny, 1826) Allolobophoridella eiseni (Levinsen, 1884) Aporrectodea caliginosa (Savigny, 1826) Aporrectodea trapezoides (Dugés, 1828) *Aporrectodea rosea (Savigny, 1826) Dendrobaena hortensis (Michaelsen, 1890) Dendrodrilus r. rubidus (Savigny, 1826) *Dendrodrilus r. tenuis (Eisen, 1874) Dendrodrilus subrubicundus (Eisen, 1874) Eisenia fetida (Savigny, 1826) *Eisenia andrei (Bouché, 1972) Eiseniella tetraedra (Savigny, 1826) *Lumbricus friendi Cognetti, 1904 *Lumbricus rubellus Hoffmeister, 1843 Lumbricus terrestris (Linnaeus, 1758) Octodrilus complanatus (Dugés, 1828) *Octolasion cyaneum (Savigny, 1826) Octolasion lacteum lacteum (Öerley, 1881) *Octolasion lacteum gracile Öerley, 1885

Pr Pr Pr Pr Pr Pr Pr Pr Pr Pr Pr Pr Pr Pr Pr Pr Pr Pr Pr

En Ep En An En Ep Ep Ep Ep Ep Ep Ep An Ep An An En En En

P P P P P P P P P P P P P P P P P P P

2 5 23 3 6 – – 2 – – 5 2 1 2 10 3 17 10 2

Megascolecidae Amynthas corticis (Kinberg, 1867) *Amynthas diffringens (Baird, 1869) Amynthas gracilis (Kinberg, 1867) Amynthas morrisi (Beddard, 1892) *Metaphire californica (Kinberg, 1867) *Pithemera bicincta (Perrier, 1875)

Or Or Or Or Or Nr

Ep Ep Ep Ep Ep En

I I I I I I

29 1 13 2 5 3

c, f b f

NI, LI, MI, HI, VHI HI MI, HI, VHI VHI HI, VHI HI, VHI

Rhinodrilidae Pontoscolex corethrurus (Müller, 1857)

Nr

En

I

3

a

VHI

appear along a wider and varied altitudinal gradient in terms of habitat type, usually in pasture, grassland, mature stands, and managed systems. Of all of them, A. corticis is revealed as the most vigorous and abundant non-native megascolecid; a total of 316 specimens were quantified, corresponding to 78% of the sites sampled, these include the meadows of Espigao das Oveiras (804 m) and the endemic vegetation of Planalto dos Graminhais (961 m). Within lumbricids (see Appendix B, Supplementary data) Ap. caliginosa is the most common, appearing at 62% of the sites. Octolasion cyaneum Savigny, 1826 (46%) and Lumbricus terrestris Linnaeus, 1758 (27%), are following in terms of abundance, both distributed mainly in areas of LI and MI land use. Ap. caliginosa accounts for 28% of the collected specimens, dispersed in most of the studied biotopes, while O. cyaneum constituted 11%, and was often found in arable meadows that are losing their natural vegetation, and in sites with a predominance of intensive agriculture (e.g. Nogueira and Faja do Baixo). Two lumbricids, L. friendi and Dendrodrilus rubidus tenuis Eisen, 1864 are infrequent in São Miguel. L. friendi is associated with clayey soil (altitude, 134 m), where it constitutes an incipient population. Instead, D. r. tenuis has its refuge at the highest altitudes (794–961 m), mainly in undisturbed forest and meadow with endemic vegetation. Sørensen index revealed variability of the insular earthworm fauna within the Palearctic ecozone (Appendix C). The highest dissimilarity of species composition found was between São Miguel and Cape Verde São Tomé, while São Miguel, Madeira and Canary Islands (Gomera, La Palma, Hierro) showed a considerable similarity pattern. When Intertropical species were analyzed separately, the results revealed that

PC

LUI NI, LI

c c, f, g d c, f e c, f c c, f c, f f f f

LI, HI NI, LI, MI, NI, LI, MI, HI, VHI LI, MI, HI, – – NI, LI – – MI, HI LI, HI HI LI NI, LI, MI, HI, VHI LI, MI, HI, NI, LI, MI, LI, HI

HI, VHI HI, VHI VHI

HI, VHI VHI HI

São Miguel, together with La Palma, Gomera and Madeira, show a slight faunal affinity with Saint Helena. However, Mediterranean Islands were clearly differentiated (see Appendix C b). 3.2. Effects of altitude, land use intensity and edaphic variables on earthworm species Predictors previously selected by Monte Carlo test in the CCA were altitude, pH and organic matter content (p < 0.01; Fig. 2). Axis I revealed the expected spatial differentiation between the Palearctic and Intertropical species. This context suggests a clear trend of the lumbricids D. r. tenuis, Lumbricus rubellus Hoffmeister, 1843 and Octolasion lacteum Öerley, 1881 to occupy sites with abundant organic matter. It also shows that the megascolecid Pi. bicincta and the rhinodrilid P. corethrurus were associated to soils with lower organic matter content, coinciding with intense human influence (categories HI; VHI) and the low lands. Two species groups have clustered along axis II, where pH is the most robust predictor. The first was composed of the epigeics M. californica, Amynthas morrisi Beddard, 1892 and the infrequent A. diffringens; these species were found in soils with higher pH (6.5–7) indicating a trend towards less acidic soils. Higher pH values also influenced the spatial ordination of the second group that was composed of the endogeic O. cyaneum and the anecics Octodrilus complanatus Dugés, 1828 and L. friendi. In fact, the latter two appear in arable grasslands with nearly neutral soils (pH: 6.82–7.00). In contrast, trends of Octolasion lacteum gracile Öerley, 1885, M. dubius and epigeic species D. rubidus tenuis and L. rubellus revealed an acid-tolerance behavior, as 5

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Results showed that the abundance of endogeic species is significantly higher at sites presenting low land-use intensity (Table 3: F4.32 = 4.13, p < 0.01). No differences were found for the epigeics and anecics. Moreover, richness and abundance of Intertropical species, mainly megascolecids, were higher in the most intensely managed systems (HI-VHI, Table 3). Up to four species within the same site were found, for example in Courela (VHI; A. corticis, A. gracilis, M. californica and Pi. bicincta), whereas Belem Faja de Baixo (VHI) provided the largest number of A. corticis (25 individuals). Correlations among the selected variables and species richness and abundance have been revealed (Table 4). Abundance and richness of Intertropical earthworms showed negative relationships with organic matter content and distance to urban nuclei (DUN). Moreover, their abundance showed a negative relationship with moisture, and their richness showed a positive relation with pH and a negative relation with altitude (Table 4). Our data also demonstrated positive relationships between abundance of Palearctic earthworms and organic matter, altitude and distance to urban nuclei (Table 4). These results are in agreement with the CCA (Fig. 2), showing that the abundance/richness of the earthworms found within the study area do not depend on a single environmental variable, but on the combination of several variables and their interactions. Regarding ecological categories, we found that the abundance of epigeic species is positively associated with pH, indicating that lower abundances are recorded in more acidic soils. A negative relationship was found however with soil moisture. Abundance of anecic species was positively correlated to organic matter and altitude, while abundance of endogeics was positively correlated to DUN (Table 4).

1.0

Selected enviromental variables, sites and species coordinates

Altitude

Drt

Lru

Ola

CCA - Axis II

Pco

Mdu Olg

Ete Aca

Lte

Aro

Aei

Aco Agr Ean

Pbi Atr

Ach

Org_mat

Mca Amo Ocy Adi

Oco

-1.0

Lfr pH

-1.0

CCA - Axis I

1.0

Fig. 2. Projections of axes I, II in CCA analysis (using the selected environmental variables by the Monte Carlo test). Distribution of earthworm species (see triangles). Sites in polygons are enclosed indicating different soil intensity use (class 1: thick line; class 2: thick dotted line; class 3: slashed line; class 4: dotted line; class 5: solid line). The constrained eigenvalues are Axis I: 0.48 and Axis II: 0.35 and the total inertia is 82.4%. Intertropical species are highlighted in bold whereas Palearctic species are shown in regular font. See complete names of species in Appendix B.

4. Discussion 4.1. Earthworm richness, affinities and taxonomic notes Only four out of the 11 families of known earthworms (Jamieson, 1988; Omodeo, 2000) have been found in São Miguel. We have confirmed that Lumbricidae is the most diverse, while scarcity of acanthodrilids contrasts with its richness and abundance in Canaries and Madeira (Talavera, 1996, 2007). Earthworm species composition found in this study is similar to that prevailing in other nearby North Atlantic islands, such as Madeira (Talavera, 1996, 2011). However, it differs substantially from species richness in nearby continental territories. For example, six families and 43 species are known in western Iberian Peninsula (Trigo et al., 1990), while eight families and more than 60 earthworm species have been recorded in northwest Africa (Michaelsen, 1900; Somon, 1995; Baha and Berra, 2001; Omodeo et al., 2003; Csuzdi and Tondoh, 2007; Csuzdi et al., 2009, 2015). We have updated the inventory of known earthworm species in São Miguel, raising the number to 27 taxa, 16 of which were previously cited by other authors (Michaelsen, 1891, 1910; Sciacchitano, 1964; Talavera, 1993; Cunha et al., 2011, 2014,) and 11 of which are new records (Table 1). We have also verified that earthworm fauna in São Miguel is constituted by non-native earthworms coming from temperate climates, where they are widely distributed. Their origins are Palearctic and Intertropical, as it is the case for earthworms in Canaries and Madeira (Talavera, 1996, 2007, 2011), but not in Cape Verde, although less explored (Cognetti de Martiis, 1908). Regarding São Tomé (Csuzdi, 2005) only A. corticis, A. morrisi, and P. corethurus records match those in São Miguel and global species composition between both islands is differentiated as shown by the Sørensen index analyses. Six endemic species are found in São Tomé, but none in São Miguel, which may be due to their different geological age (15 and 4 million years respectively, Rull et al., 2017). Most of the species known on Saint Helena island in the southern Atlantic area (Gates, 1977) are present in São Miguel. Greater differences in the earthworm fauna from both islands would be expected considering their geographical distance, and two reasons for their similarity could be hypothesized: a) European settlers

suggested by the pH range (4.74–5.73). The variables pH, moisture and organic matter were evaluated in relation to the three altitudinal zones (low, mid, high, Fig. 3), and for each anthropogenic level (Fig. 4) using ANOVA. Significant differences were found for soil pH. Tukey post-hoc test showed that the pH tends to be higher at low and middle altitudinal zones (Fig. 3A: F2.34 = 2.28, p < 0.01), as well as in the intensities of land use VHI and HI (Fig. 4A: F4.32 = 4.62, p < 0.01). No significant differences were observed for the moisture in relation with altitude and land use (Fig. 3B: F2.34 = 0.17, ns; Fig. 4B: F4.32 = 1.35, ns), probably because the average moisture value of the sites grouped by zones presented a discrete homogeneity (values exhibited a difference of only 0.4% among them). In contrast, our results suggest that organic matter proportions were higher at the least intervened sites (Fig. 4C: F4.32 = 3.98, p < 0.01), and that the intensity of anthropogenic use tends to decrease with altitude (Fig. 4D: F4.32 = 14.25, p < 0.01). Our results show that richness of Intertropical earthworms is significantly driven by altitude (F2.34 = 6.73, p < 0.01) and the highest number of species is found at the low and warm lands of São Miguel (Table 2). Those sites are characterized by strong agricultural diversification where fertilizers rich in salts of carbonates and phosphates are often used. In contrast, abundance of Palearctic species was significantly higher above 500 m a.s.l. (Table 2: F2.34 = 6.26, p < 0.01), and in LI land use sites (Table 3: F4.32 = 4.54, p < 0.01). Those are located in the mountain belt where there is abundant organic matter (decomposed vegetal remains), favoring the presence of L. terrestris and O. lacteum. Altitude had a significant effect on endogeics abundance, which was greater at higher altitudes (Table 2: F2.34 = 5.29, p < 0.01). There were no clear differences in terms of the abundance and richness of the anecic and epigeic species in relation to altitude; however, we argue that epigeics tend to be more abundant and diverse below 400 m (e.g. Amynthas). 6

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a) 8

a

7

ab

6

b

pH

5 4 3 2 1 0 Low lands

Mid lands

High lands

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b) 8 7

Moisture (%)

6 5 4 3 2 1 0 Low lands

Mid lands

High lands

Altudinal category

c)

30

Organic ma!er (%)

25 20 15 10 5 0 Low lands

Mid lands

High lands

Altudinal category Fig. 3. Mean values of pH, moisture and organic matter (standard deviation represented in error bars) for each altitudinal category: Low (low land), 0–250; Mid (intermediate zone), 250–500; High (mountain), > 500 m). Identical letter above the bars indicated non-significant differences.

from the Portuguese Algarve area were established in both islands, bringing lumbricids; b) both islands were important stopovers of historical transcontinental routes, where earthworms may have travelled. Regarding geologically older Mediterranean islands (Sicily, Corsica, Sardinia, Cyprus and Crete), certain coincidences are found with São Miguel concerning the lumbricids, specially the presence of circumMediterranean species (Omodeo, 1964, 1984; Omodeo and Rota, 1987; Martinucci and Omodeo, 1988; Pavlíček and Csuzdi, 2016; Szederjesi,

2017). However, classification analyses based on Sørensen index mainly showed dissimilarities with those islands, where no Intertropical species have been registered, suggesting that they have never been in contact with the emitting sources. No similarities where found between earthworm fauna in São Miguel and other Pacific islands, such as Quelpart (Blakemore, 2013), New Hebrides (Lee, 1981), New Caledonia (Michaelsen, 1913), the Solomon Islands (Lee, 1969), and Papua New Guinea (Easton, 1984), which are characterized by a great diversity of 7

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a) 8

ab

7

ab

a

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LI

6

b

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VHI

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VHI

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Moisture (%)

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MI Land use intensity

c)

35

a Organic ma!er (%)

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ab 20

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15 10 5 0 NI

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200 0 NI

LI

MI

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Land use intensity (caption on next page) 8

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Fig. 4. Mean values of pH, moisture, organic matter and altitude (standard deviation represented in error bars) for each anthropogenic intensive use levels. Identical letter above the bars indicated non-significant differences.

earthworm diversity usually decreases when altitude increases from 1250 to 2250 (Decaëns, 2010; Salomé et al., 2011). However, in São Miguel this occurs between 800 and 1100 m. Soil variables, such as pH, moisture and organic matter have been described as good predictors for earthworm communities (Lee, 1985; Edwards and Bohlen, 1996). Here, we show that abundance and richness of Intertropical species were negatively correlated to organic matter content. On the other hand, Palearctic species were more abundant in rich in organic matter soils found at higher altitudes, where endogeic Ap. caliginosa and O. lacteum dominated. Our results coincide with those obtained in similar islands (Bouché, 1973; Talavera, 1996, 2007), or even distant continental ecosystems (Bouché, 1972; Salomé et al., 2011). This pattern may suggest competition as a possible mechanism influencing species distribution in relation to organic matter content. Regarding pH, most of the species have been found in soils with pH values between 4.65 and 7. Similar pH ranges were found for invasive lumbricids in Canada (Addison, 2009) and for American peregrine species (Edwards and Bohlen, 1996). It is known that soil acidification reduces earthworm diversity (Edwards and Bohlen, 1996), which we found to be the case of Amynthas. According to Muys and Granval (1997), epigeic species are good soil pH indicators. In this regard, Amynthas showed a trend towards a neutral soil pH, whereas D. rubidus tenuis and L. rubellus behaved as the most acid-tolerant species, as also shown by Tiunov et al. (2006). Endogeic species Ap. caliginosa, O. cyaneum and P. corethrurus showed preferences for pH values between 5 and 6, similar to what Lavelle et al. (1994) reported in tropical ecosystems. The most relevant result for moisture was a negative relationship with the abundance of Intertropical species, as indicated by Snyder et al. (2011) and Russell et al. (2016). Only Ap. caliginosa was found in extreme moisture conditions, as shown by other studies (Ivask et al., 2007; Salomé et al., 2011).

megascolecids and rhinodrilids but scarcity of lumbricids. They are clearly influenced by the Australasian ecozone, and no commercial or agricultural exchanges have occurred between them and Macaronesia. Molecular studies have been recently carried out on some species complexes (Pérez-Losada et al., 2009; Martinsson and Erséus, 2017; Taheri et al., 2018b). However, it is not the purpose of this paper to delve into the recurrent theme of genetic verification of cryptic species but to evaluate the faunistic component of São Miguel island at a greater scale and to find environmental preferences and indicators among higher level groups, taking into account ecological categories and geographical origin of the earthworms. The endogeic Ap. caliginosa and the anecic Aporrectodea trapezoides Dugés, 1828 are part of Ap. caliginosa species complex, their identification is supported by rigorous and currently valid morphological and ecological characters; see details in Pérez-Losada et al. (2009). Seven cryptic species within morphospecies L. rubellus have been discussed (Martinsson and Erséus, 2017). Nevertheless, the specimens found in São Miguel (only six) show similar ecological characteristics and a clear constancy in taxonomic characters that support our identification (Gates, 1978; Zicsi, 1981; Mrsic, 1991). The genetic diversity of P. corethurus in São Miguel has been assessed in Cunha et al. (2014), and its morphology has been discussed recently (Taheri et al., 2018a). Ecological preferences of different genetic lineages of Amynthas in São Miguel have been previously assessed by Novo et al. (2015). 4.2. Earthworm species relationships with environmental variables The abundance of Palearctic earthworms was positively related to altitude. On the other hand, Intertropical species abundance and richness were negatively correlated with altitude. This pattern is similar to that found in other North Atlantic islands (Sciacchitano, 1964; Gates, 1977; Talavera, 1996, 2007; Csuzdi, 2005), suggesting that Intertropical earthworms are more sensitive to the altitudinal gradient, which generally implies colder temperatures at the higher levels. Altitude also showed a positive effect on endogeic earthworms, favoring their abundance at the highest locations (> 500 m). Similar patterns have been observed in Madeira (Talavera, 2011) and central-western islands of Canaries (Talavera, pers. obs.). The absence of the anecic O. complanatus at the highest altitudes differs from results obtained in similar islands (Talavera, 2007; Szederjesi, 2017), suggesting that its introduction has been relatively recent and it did not have the time to spread to the highest lands. A number of cases have documented that

4.3. Land use intensity and distance to urban nuclei Previous studies have suggested a link between soil management and earthworm diversity and abundance (Enckell and Rundgren, 1988; Domínguez et al., 2009; Feijoo et al., 2011). We show the same for the first time within an insular scenario in the northern Atlantic. An increase of Intertropical species in sites subjected to a strong human intervention (MI, HI, VHI) has been verified, especially for the epigeics A. corticis and A. gracilis. Addison (2009) and Masin et al. (2011) found

Table 2 Mean values and standard deviation (mean ± SD) for the richness and abundance of earthworm species at different altitudinal category (Low = 0–250, Mid = 250–500, High > 500 m). Species were analyzed as a total or as groups based on ecological category (epigeic/endogeic/anecic) or distribution (Palearctic/ Intertropical). Superscripts indicate significant differences (p < 0.05 in Tukey test). The last columns indicate the F value of the ANOVA (in subscripts the degrees of freedom) and the probability associated to the F (P). (⁎)Evenness index of Smith and Wilson. Ecological properties

Low (low land)

Mid

High (mountain)

F2,34

P

N (number of species) Total richness Total abundance Total Evar(⁎) Richness epigeics Abundance epigeics Richness endogeics Abundance endogeics Richness anecics Abundance anecics Richness palearctics Abundance palearctics Richness intertropicals Abundance intertropicals

11 4.18 ± 1.94 44.45 ± 23.19 0.56 ± 0.19 1.81 ± 1.17 14.88 ± 13.3 1.63 ± 0.81 15.5 ± 12.76ab 0.56 ± 0.81 2.94 ± 5.58 2.25 ± 1.61 14.63 ± 15.30a 1.75 ± 1a 18.69 ± 13.38

20 4.05 ± 2.01 32.3 ± 17.71 0.64 ± 0.22 2.1 ± 0.74 16 ± 3.68 1.8 ± 0.92 9.8 ± 7.82a 0.3 ± 0.48 2.1 ± 3.67 2 ± 0.82 12.8 ± 8.50a 1.9 ± 0.56a 15.1 ± 3.54

6 4.17 ± 0.75 27.67 ± 6.62 0.66 ± 0.17 1.55 ± 1.04 12.36 ± 10.53 2.18 ± 1.17 30.18 ± 21.07b 0.45 ± 0.52 1.91 ± 2.51 3.36 ± 1.8 34 ± 20.68b 0.82 ± 0.40b 10.45 ± 9.04

0.02 2.13 0.61 0.74 0.32 1.01 5.29 0.15 0.12 2.13 6.26 6.73 2.07

n.s. n.s. n.s. n.s. n.s. n.s. p < 0.01 n.s. n.s. n.s. p < 0.01 p < 0.01 n.s.

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Table 3 Mean values and standard deviation (mean ± SD) for the richness and abundance of earthworm species at different intensity land use levels (1 = non intensive (NI), 2 = low (LI), 3 = moderate (MI), 4 = high HI), 5 = very high (VHI). Species were analyzed as a total or as groups based on ecological category (epigeic/endogeic/ anecic) or distribution (Palearctic/Intertropical). Superscripts indicate significant differences (p < 0.05 in Tukey test). The last columns indicate the F value of the ANOVA (in subscripts the degrees of freedom) and the probability associated to the F (P). (⁎)Evenness index of Smith and Wilson. Ecological properties

1 (NI)

2 (LI)

3 (MI)

4 (HI)

5 (VHI)

N (number of species)

3

6

8

10

10

Total richness Total abundance Total Evar(⁎) Richness epigeics Abundance epigeics Richness endogeics Abundance endogeics Richness anecics Abundance anecics Richness palearctics Abundance palearctics Richness intertropicals Abundance intertropicals

2.67 ± 0.58 24.33 ± 14.05a 0.69 ± 0.15 1±1 5 ± 6.24 1.33 ± 0.58 17.67 ± 14.22b 0.33 ± 0.58 1.67 ± 2.89 2.33 ± 0.58ab 21 ± 15.62ab 0.33 ± 0.58a 3.33 ± 5.77a

5 ± 2.1 54.5 ± 26,68b 0.58 ± 0.22 1.83 ± 1.17 13.5 ± 12.5 2.67 ± 1.37 38.5 ± 23.92b 0.5 ± 0.55 2 ± 2.95 4 ± 2.1a 43.17 ± 22.1b 1 ± 0ab 11.33 ± 10.15ab

3.75 ± 1.16 26.38 ± 6.86ab 0.5 ± 0.14 1.75 ± 0.89 15.38 ± 5.95 1.88 ± 0.83 9.75 ± 10.71a 0.13 ± 0.35 1.25 ± 3.54 2.25 ± 0.89ab 12.13 ± 10.38a 1.5 ± 0.53ab 14.25 ± 5.12ab

4.9 ± 1.66 33.8 ± 12.64ab 0.67 ± 0.19 2.4 ± 0.97 16.9 ± 6.08 1.8 ± 0.79 12.7 ± 6.68a 0.7 ± 0.82 4.2 ± 6.56 3.1 ± 1.37ab 18.4 ± 10.55ab 1.8 ± 0.79b 15.4 ± 6.64ab

3.5 ± 2.07 35.2 ± 21.23ab 0.66 ± 0.25 1.5 ± 0.97 14.6 ± 15.56 1.5 ± 0.85 18.9 ± 14.98b 0.5 ± 0.71 1.7 ± 2.87 1.6 ± 1.35b 13.3 ± 17.31a 1.9 ± 1.1b 21.9 ± 14.62b

F4.32

P

1.84 2.64 1.04 1.65 0.75 1.80 4.13 0.91 0.65 3.31 4.54 3.37 2.51

n.s. p < 0.01 n.s. n.s. n.s. n.s. p < 0.01 n.s. n.s. p < 0.01 p < 0.01 p < 0.01 p < 0.01

Table 4 Pearson correlation values among the selected variables and earthworm species richness and abundance, discriminating for their geographical origin and ecological categories (see Materials and methods). The values in bold indicate significant correlation (*p < 0.05; **p < 0.01). LUI = land use intensity (anthropogenic) DUN = distance to urban nuclei. (⁎)Evenness index of Smith and Wilson. Species Total Epigeics Anecics Endogeics Palearctics Intertropicals

LUI Richness Abundance Evar(⁎) Richness Abundance Richness Abundance Richness Abundance Richness Abundance Richness Abundance

−0.011 −0.073 0.124 0.093 0.186 −0.205 −0.212 0.124 0.039 −0.302 −0.354⁎ 0.517⁎⁎ 0.467⁎⁎

Variables pH

Moisture

O.M. %

0.095 0.068 −0.027 0.227 0.361⁎ −0.179 −0.196 0.171 0.174 −0.097 −0.086 0.371⁎ 0.267

−0.058 −0.052 0.328 −0.180 −0.446⁎⁎ −0.005 0.171 0.125 0.155 0.032 0.232 −0.169 −0.474⁎⁎

−0.080 0.256 0.003 −0.031 −0.317 −0.121 0.458⁎⁎ 0.013 0.090 0.137 0.561⁎⁎ −0.390⁎ −0.469⁎⁎

similar results but in continental areas. This suggests that managed systems, although geographically distant, are efficient receptors of vigorous peregrine species. The exotic P. corethurus, with recognized capacity for invading anthropogenic sites (Talavera, 1992; Hendrix et al., 2006; Feijoo et al., 2011) was also found within managed systems of São Miguel (mainly pineapple cultivations but also meadows). Endogeic lumbricids were the most abundant in moderate or less managed soils, as previously shown in other volcanic islands (Talavera, 1996, 2007) and continental scenarios (Masin et al., 2011; Juárez-Ramón and Fragoso, 2014). Epigeic D. r. tenuis, Eiseniella tetraedra Savigny, 1826 and L. rubellus showed tendencies towards the least intervened habitats (LI, NI) with accumulation of organic matter in the surface and linked to mature stands. Overall, our results agree with previous observations, suggesting that earthworms are good indicators of land use intensity (Paoletti, 1999; Huerta et al., 2005). Distance to the nearest urban nuclei (DUN) was revealed as a secondary predictor but still a very interesting one because of its linkage with land use intensity. Arévalo et al. (2005) considered it as an important factor for exotic species richness. Within São Miguel, Intertropical and Palearctic showed opposite trends. The lower the DUN the higher the abundance and richness of Intertropical species (Amynthas and Pontoscolex). However, the greater the DUN the higher the abundance of Palearctic species, agreeing with the studies by Talavera (2007, 2011).

Altitude (m)

DUN (m)

−0.026 0.274⁎ −0.111 −0.089 −0.080 0.127 0.398⁎ −0.118 −0.123 0.226 0.462⁎⁎ −0.458⁎⁎ −0.289

−0,14 0,25 −0,12 −0,16 −0,28 −0,09 −0,11 −0,03 0.488⁎⁎ 0,07 0.497⁎⁎ −0.407⁎ −0.399⁎

5. Conclusions Our study shows that earthworm communities in São Miguel are mainly dependent on altitude, land use intensity and to a lesser extent on soil variables. We report diversity patterns depending on those factors: 1) Dominance of megascolecids at lowland sites with land-use intensities HI and VHI, most of them being epigeic. 2) Greater representation of lumbricids on high land (mountain belt) with lesser human influence, MI and LI. 3) Scarce presence of earthworm species in non-intensive systems (NI). Meanwhile both groups of earthworms coexist in 80% of the sampled sites, they seem to present opposite ecological preferences. Whether these patterns are caused by competition between species would be a subject of further research. Acknowledgements The authors would like to thank Dr. John Morgan for his valuable collaboration on field sampling and design of the research project and the team that helped to collect the specimens. We are also very grateful to the editor and reviewers who greatly helped to improve the manuscript with their comments. MN was supported by a UCM Postdoctoral Fellowship from Complutense University of Madrid and LC by a Marie Curie Fellowship (MSCA-IF-2014-GF-660378). This study was funded by the grant NERC NE/I026022/1.

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Appendix A. Supplementary data

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