Research Article |
Corresponding author: Stylianos M. Simaiakis ( ssimaiakis@yahoo.com ) Academic editor: Ivan H. Tuf
© 2015 Gabriella Papastefanou, Eleni Panayiotou, Moissis Mylonas, Stylianos M. Simaiakis.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Papastefanou G, Panayiotou E, Mylonas M, Simaiakis SM (2015) Centipede assemblages along an urbanization gradient in the city of Heraklion, Crete (Greece). In: Tuf IH, Tajovský K (Eds) Proceedings of the 16th International Congress of Myriapodology, Olomouc, Czech Republic. ZooKeys 510: 163-179. https://doi.org/10.3897/zookeys.510.8414
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Global urbanization is a major force that causes alteration and loss of natural habitats. Urban ecosystems are strongly affected by humans and there is a gradient of decreasing human influence from city centers to natural habitats. To study ecological changes along this continuum, researchers introduced the urban-rural gradient approach. The responses of centipedes to an urbanization gradient (urban-suburban-rural areas) were studied using pitfall traps in and near the city of Heraklion, in the island of Crete, Greece, from November 2010 to November 2011. Our results do not support the intermediate disturbance hypothesis, in which suburban areas located in the transitional zone between urban and rural habitats failed to indicate significant increase in terms of species richness and diversity.
Abundance, activity density, Eupolybothrus litoralis , Lithobius nigripalpis , pitfall traps, Scolopendra cretica , Scutigera coleoptrata , spatial distribution, species diversity, temporal distribution
With respect to global threats, some scientists believe that our planet is facing a new biodiversity crisis, frequently called as the sixth mass extinction, which is a human-caused phenomenon (
A city represents an ideal terrestrial ecosystem to investigate fauna composition. It retains specific microclimatic and hydrological parameters and is sensitive to human activities and climate change (
Nowadays thousands of species are characterized as nationally extinct, threatened, or near threatened in broad habitats, particularly in urban areas, as a result of the significant declining areas of natural patches. These habitats represent an important patchily distributed environment for thousands of species (
The effect of urbanization on biodiversity has focused primarily on vertebrates (e.g.,
Because of the relatively high diversity and the quite high availability of species occurrence records, centipedes provide a suitable taxonomic group for studying ecological aspects. However, only few studies have focused on the impact of urbanization on centipede species assemblages. In this study we performed several comprehensive analyses to investigate the responses of centipede species in the city of Heraklion, on Crete. In particular:
we quantify species richness, abundance and diversity along an urban-rural gradient,
we study centipede species structure emphasizing on the spatial and temporal distribution along the three urbanization zones, and,
we explore patterns of distribution of the identified generalist species.
The city of Heraklion (35°20'0"N; 25°8'0"E) is the largest city of Crete and the fourth largest in Greece located in the centre of the northern coast of the island. It covers an area of approximately 24 km2 with an estimated population of 173,450 (according to the General Population Census 2011) at a density of 7,227 residents per square kilometer. Heraklion is mainly flat with several prominent hills, characterized by numerous floral species, mainly introduced, such as Hirschefeldia incana and Conyza albida (common species along the roadsides), Petromarula pinnata (endemic plant of Crete), Ailanthus altissima (dominant plant at the archaeological site of Knossos), Hyoscyamus aureus (common in the Venetian city walls) (for further habitat description see also
We selected three sampling areas along an urbanization gradient, as proposed by the Globenet protocol (
Map of the study area and sampling sites in and near Heraklion city. U urban sites (U1 athletic centre, roads, parking area, buildings and gardening activities U2 roads, parking area, dense buildings and gardening activities U3 Heraklion port, roads, numerous buildings and gardening activities) S suburban sites (S1 hotels, roads, sandy substrate S2 hotels, electricity power factory, roads S3 industrial area, roads, numerous buildings) R rural sites (R1–R3 roads and little grazing).
Centipedes were collected with pitfall traps along the aforementioned urban–rural gradient in accordance to the GLOBENET program protocol for capturing soil arthropods (
Centipede species richness for each site was estimated using two nonparametric richness estimators, in particular Chao1 and Bootstrap (see
In terms of richness the number of species and genera was counted at each site. We also calculated the diversity of centipedes using: (i) the Shannon diversity index H’ (for further details see
We calculated activity density in terms of number of individuals per 100 trap-days at each habitat along the gradient. The temporal distribution of centipede assemblages was analysed in terms of the average number of species per sampling period, i.e., one month, called ᾱ diversity, and the proportion of cumulative α diversity, known as a measure of temporal turnover (
where S is the total number of species captured in a site (
where Sj is the number of species captured in sampling period j, Sk the number of species captured in consecutive sampling period k (k=j+1) and Vjk the common species captured in periods j and k. After these calculations, temporal beta diversity (βt) was measured as the average for each site assemblage.
Among others, we performed one-way ANOVA tests for differences in richness, abundance, activity density, and diversity (Shannon H’, temporal diversity, βt and proportion of cumulative α represented by average α, α %) along the urbanization gradient.
We also performed a non-metric multi-dimensional scaling (NMDS) ordination plot based on Bray-Curtis dissimilarities of square-root transformed centipede abundance data, to find out whether there are structural differences in centipede assemblages along the urban–rural gradient. Structural differences may concern species composition and species activity density. NMDS analysis was performed in PAST 2.16 (
Overall, 993 individuals (36.3 individuals per site / 100 trap-days) were collected and identified, belonging to 18 centipede species (8.0 ± 1.7 per site) and 11 genera (5.9 ± 0.9 per site) (Table S1 in Suppl. material
The total and average abundance were maximal in suburban sites, minimal in urban sites, and intermediate in the rural sites (Fig.
Summary results of centipede species diversity for each site (R: rural, S: Suburban, U: urban). Richness is shown in terms of captured genera (G), species (S), total number of individuals in samples (Sa). Species diversity is estimated based on Shannon-Wiener (H’) and Evenness (J’) diversity indices. Sampling effort is shown in terms of expected number of species (Se) based on Chao 1 and Bootstrap estimators (mean ± SD) and completeness of samplings (Sc). Temporal diversity is shown in terms of activity density (A), average species richness (ᾱ), proportion of cumulative α represented by average α diversity (α%), and temporal beta diversity (βt).
Site | G | S | Sa | H’ | J’ | Se Chao 1 (mean ± SD) | Se Bootstrap (mean ± SD) | Sc | A | ᾱ | α% | βt |
---|---|---|---|---|---|---|---|---|---|---|---|---|
U1 | 4 | 4 | 37 | 0.72 | 0.51 | 4.12 ± 0.72 | 4.48 ± 0.29 | 0.93 | 12.14 | 1.17 | 29.17 | 62.96 |
U2 | 6 | 9 | 74 | 1.61 | 0.56 | 9.77 ± 2.16 | 9.98 ± 0.05 | 0.91 | 25.68 | 2.25 | 25.00 | 60.15 |
U3 | 7 | 8 | 83 | 1.55 | 0.59 | 8.54 ± 1.38 | 8.85 ± 0.28 | 0.92 | 25.66 | 2.67 | 33.33 | 57.27 |
S1 | 6 | 9 | 132 | 1.51 | 0.50 | 10.00 ± 2.26 | 9.85 ± 0.02 | 0.91 | 43.93 | 3.25 | 36.11 | 49.85 |
S2 | 5 | 8 | 162 | 0.75 | 0.27 | 9.00 ± 2.25 | 9.05 ± 0.03 | 1.00 | 53.30 | 2.33 | 29.17 | 60.30 |
S3 | 6 | 7 | 205 | 1.17 | 0.46 | 7.35 ± 1.22 | 7.68 ± 0.09 | 0.93 | 66.35 | 3.00 | 42.86 | 45.61 |
R1 | 6 | 9 | 98 | 1.62 | 0.56 | 12.00 ± 4.48 | 10.07 ± 0.33 | 0.82 | 31.58 | 3.00 | 33.33 | 71.04 |
R2 | 7 | 9 | 106 | 1.31 | 0.41 | 12.51 ± 4.74 | 10.56 ± 0.27 | 0.79 | 33.95 | 2.42 | 26.85 | 74.39 |
R3 | 6 | 9 | 96 | 1.68 | 0.60 | 9.37 ± 2.09 | 9.51 ± 0.27 | 0.95 | 33.69 | 3.17 | 35.18 | 42.88 |
The activity density (individuals/100 trap-days) of centipede assemblages ranged from ca 12.1 to 25.7 in urban habitats (mean value of 21.2 ± 7.8), from ca 43.9 to 66.3 in suburban habitats (mean value of 54.5 ± 11.3), and from ca 31.6 to 34.0 in rural sites (mean value of 33.1 ± 1.3) (see Table
The difference in species richness along the urbanization gradient was not statistically significant (Table
One-way ANOVA results showing statistical differences of species richness, abundance, activity density (A density), and diversity (Shannon H’, temporal diversity, βt and proportion of cumulative α represented by average α, α%), along the urbanization gradient in Heraklion. Degrees of freedom (DF), sum of squares (SS), mean square (MS), F values (F). The last column shows the significant differences between the gradient levels (p < 0.05) based on the Tukey test. R: rural, S: suburban, U: urban.
DF | SS | MS | F | p | Tukey test | |
---|---|---|---|---|---|---|
Species richness | 2 | 12.39 | 6.19 | 2.39 | 0.11 | |
Abundance | 2 | 2664.11 | 1332.06 | 0.91 | 0.41 | |
Shannon H’ | 2 | 2.70 | 1.35 | 0.27 | 0.77 | |
A density | 2 | 47.65 | 23.82 | 4.47 | 0.02 | U < R, S |
βt | 2 | 653.45 | 326.72 | 0.96 | 0.39 | |
α% | 2 | 5.56 | 2.78 | 3.09 | 0.03 | U < R, S |
The structural difference of urban centipede assemblages compared to the other two habitat zones was apparent when we performed NMDS. The two-dimensional (2D) ordination plot explained 90% of the variance in the distance matrix (Axis 1: 72 %, Axis 2: 18 %, stress = 0.12; see Fig.
Scolopendra cretica was the dominant species in rural and suburban sites covering 50.6% and 86.9% of the total captures in these sites respectively. However, in urban sites its capturing coverage lowered to 2.1%, while the dominant species in urban sites was Scutigera coleoptrata (72.7%). S. coleoptrata also covered a large portion of captures in rural areas (21%). Two more species could be considered dominant, namely Lithobius nigripalpis that covers 14.1% and 18.5% of the total captures in urban and suburban sites respectively, and, Eupolybothrus litoralis that covers 25.5% and 19.8% of the total captures in urban and suburban sites respectively. L. nigripalpis was also dominant in rural areas covering 12.8% of the total captures. The percentage of individuals of opportunistic centipede species to the total individuals proved to differ significantly along the urbanization gradient. The abundance of opportunistic species in the suburban sites was 1.75 and 2.7 times higher than their abundance in rural and urban sites respectively (Fig.
Total and average abundance of all four generalist species as well as average abundance of each generalist species along the urban-rural gradient, Eupolybothrus litoralis (♦), Lithobius nigripalpis (▲), Scolopendra cretica (■), Scutigera coleoptrata (●). White columns show total abundance, grey columns show average abundance with bars with standard deviation.
According to several studies, urbanization reduces species richness in many animal groups owing to the impoverished flora, in terms of habitat loss (
Unlike the aforementioned examples, our results failed to indicate negative urbanization effect on centipede species richness and diversity.
Additionally, in terms of species richness and diversity, our results are not statistically significant to support the suburban peak (
As for temporal beta diversity (βt), it showed no difference among the three zones indicating no variance in species richness between sampling periods. The high (βt) values found, in most cases above 50, are attributed to nomadic assemblages or degraded habitats, under fast environmental alterations or intense perturbations (
The structure of centipede assemblages differed substantially along the urban-rural gradient. We also observed great similarity in centipede diversity between rural and suburban sites. The distribution from rural to suburban areas is not impossible since in suburban sites human constructions retain green areas as centipede habitats. Within the city of Heraklion though, species composition is significantly different from both rural and suburban due to great habitat loss and fragmentation. The four generalist species (Eupolybothrus litoralis, Lithobius nigripalpis, Scolopendra cretica, Scutigera coleoptrata) were found in great abundance in all zones. However, highest centipede abundance was found in suburban areas, followed by the rural areas and fewer individuals were caught in the centre of the city, showing that mild human pressure can promote the abundance of these species. Three species, namely Lithobius aeruginosus, L. lapidicola, and Schendyla nemorensis were found exclusively in the city centre, suggesting that human activities such as gardening and landscaping introduce new species in cities through transferred soil. On the other hand, Cryptops trisulcatus and Pachymerium ferrugineum occurred only in suburban sites indicating specific habitat preferences under large stones and sand soil substrate, respectively. Although Scolopendra cretica was the dominant species in rural and suburban habitats, its capturing coverage was extremely low in urban environments showing low tolerance to the intense human activity. In contrast, Scutigera coleoptrata with a capturing coverage of about 73% showed a highly opportunistic character in the city habitats. Finally, only one representative of the species Lithobius pamukkalensis was collected in rural sites, which is so far the most western distribution of this species in Crete.
Different studies consistently highlight alternative animal responses to urbanization. Even same animal groups differed in their reaction to the increasing human activity in different cities. Our study failed to indicate negative urbanization effect on centipede species richness and diversity in the city of Heraklion. It is noteworthy that even though there is a trend of increasing abundance towards the suburban habitats, the difference was not confirmed statistically. Furthermore, our results are not consistent with those that have supported the intermediate disturbance hypothesis. This means that the suburban environment of Heraklion may not be considered as transitional zone between natural and urban habitats.
We thank Aris Nersessian and Nikos Tsirigotakis for their contribution to set pitfall traps in the field and collecting specimens. We are grateful to Manolis Nikolakakis for mapping sampling sites. We also thank two anonymous referees for their critical comments on the manuscript and Marc Rossello for improving the clarity of the manuscript.
Abundance and activity density of centipede species per sampling site.
Data type: occurrence
Explanation note: List of species and individuals captured at each sampling site.