Biodiversity Data Journal :
Research Article
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Corresponding author: Paulo A. V. Borges (paulo.av.borges@uac.pt)
Academic editor: Luís Silva
Received: 04 Jan 2022 | Accepted: 20 Apr 2022 | Published: 10 May 2022
© 2022 Noelline Tsafack, Rosalina Gabriel, Rui Elias, Mário Boieiro, Maria Teresa Ferreira, Paulo Borges
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:
Tsafack N, Gabriel R, Elias RB, Boieiro M, Ferreira MT, Borges PAV (2022) Arthropods and other biota associated with the Azorean trees and shrubs: Laurus azorica (Seub) Franco (Magnoliophyta, Magnoliopsida, Laurales, Lauraceae). Biodiversity Data Journal 10: e80088. https://doi.org/10.3897/BDJ.10.e80088
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This study explores the composition and structure of species communities associated with the native Azorean tree species Laurus azorica (Seub) Franco (Magnoliophyta, Magnoliopsida, Laurales, Lauraceae). Communities were sampled in six Islands covering the occidental (Flores), central (Faial, Pico, Terceira) and eastern (São Miguel, Santa Maria) groups of Azores Archipelago during the BALA project, using standardised sampling protocols for surveying canopy arthropod fauna. In addition, the study characterises the distribution of species regarding their colonisation status and feeding modes and, finally, compares communities of different Islands.
Ninety-four arthropod species totalling 10,313 specimens were collected on L. azorica. The Arthropod community was dominated by Hemiptera species, most of them being herbivores. Endemic and native species showed a very high abundance representing about 94% of the total species abundance. However, despite introduced species being represented by few individuals (6% of the total abundance), their diversity was remarkable (28 species and no significant difference with diversity found in endemic and native species communities). Analysis of rarity patterns revealed a stable community of endemic species (alpha gambin SAD model approaching a log-normal shape), intermediate stable community of native species (alpha SAD gambin model approaching a poisson log-normal) and a less stable community of introduced species (alpha SAD gambin model approaching a log-series shape). A dissimilarity analysis revealed high similarity between communities of Terceira and Pico and high dissimilarity between Flores and Faial communities. We observed a clear individualisation of the different islands when considering endemic species, whereas we observed high overlap when considering native and introduced species groups. Canopy community distribution confirms the results obtained in a previous study which suggest the stability of native and endemic arthropods species communities over introduced species community in native forests fragments.
Arthropod species were richer than bryophytes, lichens and vascular plants species. We found that L. azorica serve as the substrate for very few vascular plants species (four epiphytes species), which were present in all Islands, except Elaphoglossum semicylindricum, which does not occur in Santa Maria. L. azorica shelters a significant number of bryophytes and lichens species. Thirty-two lichens and 92 bryophyte species, including 57 liverworts and 35 mosses, are referred to this phorophyte. Five bryophyte species, all Azorean endemics, are considered Endangered by IUCN Criteria. L. azorica harbours a poor community of epiphyte vascular plant species and all of them were ferns, but the community of bryophytes and lichens are not negligible although very low compared to the community found on other previously studied Azorean trees, the Azorean cedar Juniperus brevifolia.
The present study shows that most islands present particular species distribution patterns without geographical correlation and that conservation programmes should be adapted to each Island. The study, therefore, calls for a specialisation of conservation programmes for each of the Islands.
Laurus azorica, Azores, islands, native forest, arthropods, vascular plants, bryophytes, liverworts, mosses, lichen, endemic, native and introduced species
Forest canopy represents the space between the soil and the atmosphere.
The difficulties in reaching forest canopy for sampling have long restricted the number of studies investigating biodiversity in this habitat (
Several studies showed the exceptional richness of arthropod communities in Azorean native forests (
It is in that context that we decided to fill the gap in Azores. We planned to investigate arthropod and plant communities associated with six main endemic tree species. We organised our investigation in a series of six studies. A first publication explored species communities associated with the Azorean cedar Juniperus brevifolia (Hochst. ex Seub.) Antoine (
The present study focuses on the Azorean endemic tree species Laurus azorica (Seub) Franco. The study characterises the distribution of species regarding their colonisation status and feeding modes and finally compares communities of six Azorean Islands covering the western (Flores), central (Faial, Pico, Terceira) and eastern (São Miguel, Santa Maria) groups. These studies are intended to be the baseline for future evaluations of the impacts of common biodiversity erosion drivers (e.g. habitat loss and degradation, invasive species, climatic changes) on the diversity or organisms associate with the canopy of Azorean endemic trees and shrubs.
L. azorica (Magnoliophyta, Magnoliopsida, Laurales, Lauraceae), the Azorean laurel, is a dioecious evergreen tree that grows up to 15 m height. The leaves (up to 15 cm long and 8 cm wide) are alternate, simple, entire, elliptic, oblong or obovate, acute and aromatic. Young twigs and leaves are brown-tomentose, becoming glabrous. Flowers are yellowish-green; perianth 4-lobed, segments ca. 4 mm. The fruits are fleshy, ellipsoid, up to 2 cm, black (when ripe) (Fig.
Twig of Laurus azorica (Seub.) Franco showing the leaves, unripe fruits (green) and ripe fruits (black). On the left are the details of the female and male flowers. Scientific illustration by Fernando Correia (www.efecorreia-artstudio.com). With permission of Azorina – S.A.
Endemic to the Azores, this species is common in submontane laurel forests and Juniperus-Ilex montane forests. Scattered or locally common in Picconia-Morella lowland forests, Juniperus montane woodlands and Pittosporum exotic forests (
Before Portuguese occupation and the process of forest cut for wood consumption and agriculture development, L. azorica was probably one of the most common tree species in the Azores. In fact, submontane laurel forests could have occupied more than 40% of the islands' surface and this species is also very frequent in montane forests that were the dominant vegetation between 600 and 900 m altitude in Faial, Pico, São Jorge, Terceira and São Miguel (
Data related to arthropods were obtained within the scope of the BALA project (Biodiversity of Arthropods in the Laurisilva of the Azores) that started in 1999 (
Arthropods were sampled using a beating tray. We used a modified beating tray, which consisted of an inverted cloth funnel pyramid of 1 m wide and 60 cm deep. A plastic bag was placed at the tip where arthropods, leaves and small branches were collected (
Two kinds of data were assessed for this inventory: literature records (Suppl. material
More details on lichen and plants species sampling can be found in our previous work (
We described and compared the structure and the composition of species communities of L. azorica in different islands. The present analysis design follows the analysis plan of our previous study on taxa associated with Juniperus brevifolia (see
Therefore, for species composition, we compared Islands for their species richness, abundance, functional groups and feeding modes and, for species community structure, we investigated patterns of rarity with species abundance distribution models and with species community similarity analyses.
For all analysis, we used the complete dataset including juveniles and adult specimens identified at the species and morphospecies level (Suppl. material
Species composition
Each species was assigned to a functional group (predator, herbivore, saprophyte and fungivore) and a feeding mode (external digestion and sucking, chewing and cutting, piercing and sucking, siphoning, not feeding) (see
We compared the different islands for their species abundances and richness. Islands were also compared for species abundance and richness within the different trophic functional groups using the Kruskal-Wallis test and a pairwise Dunn test.
Species community structure
We explored rarity patterns of communities using Preston octaves and alpha-gambin values.
We used unimodal gambin models to fit the species abundance distribution at the Archipelago level and in each Island separately. We compared gambin models shapes and the value of the parameter α change between Island communities.
We used Non-metric Multidimensional Scaling (NMDS) to examine the similarity between the different island communities with the Bray-Curtis dissimilarity metric. Bootstrapping approaches were used to analyse the significance of NMDS ordination. First, a Permutational Multivariate Analysis of Variance was performed using the function Adonis to test if species communities were different between Islands. Second, an Analysis of Similarities (ANOSIM) was performed using the function Anosim to examine if the difference was significant. The higher Anosim R-value, the higher the dissimilarity between Islands.
In order to identify species that contributed the most to the dissimilarity observed between Islands, pairwise comparisons were performed using the function Simper with 999 permutations with the Bray-Curtis distance. This analysis also allows us to assess the significance of species contributions.
All analyses were run using the R programme (
Vegetation data were analysed using a descriptive approach because datasets were not large enough to allow comparison between Islands (see Suppl. materials
Species composition
We collected a total of 10,313 specimens, corresponding to 94 species and morphospecies, 50 families, 13 orders and three classes (Table
Summary of arthropod taxa associated with L. azorica. Colonising status, classes and orders with number of families, species and specimens are indicated.
Colonising status Class, Order |
Families |
Species |
Specimens |
Endemic species |
|||
Arachnida |
|||
Araneae |
7 |
11 |
1783 |
Insecta |
|||
Coleoptera |
2 |
2 |
44 |
Hemiptera |
4 |
9 |
1639 |
Lepidoptera |
3 |
6 |
915 |
Microcoryphia |
1 |
1 |
29 |
Neuroptera |
1 |
1 |
106 |
Psocoptera |
2 |
4 |
58 |
Trichoptera |
1 |
1 |
3 |
Native species |
|||
Arachnida |
|||
Araneae |
6 |
7 |
902 |
Opiliones |
1 |
1 |
12 |
Insecta |
|||
Blattaria |
1 |
1 |
379 |
Coleoptera |
2 |
2 |
35 |
Hemiptera |
7 |
10 |
3316 |
Lepidoptera |
2 |
3 |
88 |
Microcoryphia |
1 |
1 |
15 |
Psocoptera |
3 |
5 |
362 |
Thysanoptera |
1 |
1 |
1 |
Introduced species |
|||
Arachnida |
|||
Araneae |
8 |
11 |
402 |
Pseudoscorpiones |
1 |
1 |
2 |
Diplopoda |
|||
Julida |
1 |
1 |
38 |
Insecta |
|||
Coleoptera |
2 |
2 |
5 |
Hemiptera |
3 |
3 |
3 |
Lepidoptera |
1 |
4 |
87 |
Psocoptera |
2 |
2 |
79 |
Thysanoptera |
2 |
4 |
10 |
Species richness
Considering species richness of the different islands and in the Archipelago as a whole, we found that endemic, native and introduced species were evenly distributed and no difference was observed amongst the three groups regarding their number of species (Fig.
Total of number morphospecies and abundances for endemic (END), native non-endemic (NAT) and non-native introduced (INT) arthropods species associated with L. azorica in the six Islands (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira). Differences were assessed using a Chi-square test. Chi-square test estimates and significance are indicated.
Number of specimens |
Number of species |
|||||||||||
Total |
END |
NAT |
INT |
χ2 |
p |
Total |
END |
NAT |
INT |
χ2 |
p |
|
FAI |
577 |
112 |
456 |
9 |
569.8 |
<0.0001 |
25 |
9 |
11 |
5 |
2.24 |
0.33 |
FLO |
313 |
181 |
111 |
21 |
123.3 |
<0.0001 |
29 |
14 |
11 |
4 |
5.45 |
0.07 |
PIC |
954 |
432 |
454 |
68 |
295.6 |
<0.0001 |
50 |
22 |
17 |
11 |
3.64 |
0.16 |
SMG |
1202 |
705 |
463 |
34 |
576.4 |
<0.0001 |
52 |
21 |
19 |
12 |
2.58 |
0.28 |
SMR |
855 |
202 |
544 |
109 |
368.3 |
<0.0001 |
38 |
15 |
13 |
10 |
1 |
0.61 |
TER |
6412 |
2945 |
3082 |
385 |
2159.4 |
<0.0001 |
71 |
24 |
25 |
22 |
0.20 |
0.91 |
Total |
10313 |
4577 |
5110 |
626 |
3490.8 |
<0.0001 |
94 |
35 |
31 |
28 |
0.79 |
0.67 |
Proportion of overall arthropods species associated with L. azorica separately for the three colonising statuses: endemic (End), native (Nat) and introduced (Int) at Archipelago (AZO) and at the different Island level (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira).
At Island level, we found that over 94 species observed at the Archipelago level and 71 species were collected in Terceira (Table
Species collected belong to thirteen orders. We found that most species were spiders (Araneae) at the Archipelago level and in almost every Island. This finding was true for the overall species as well as for the three colonising groups. Lepidoptera and Hemiptera were the second most rich groups (Fig.
Proportion of arthropods species associated with L. azorica per order for all species (A) and for the three colonising status separately endemic (B), native (C) and introduced (D) species at Archipelago (AZO) and Island level (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira).
Abundance
Considering the Archipelago as a whole, most specimens were from native species (about 50%), endemic species accounted for 44% of collected individuals, whereas introduced species account for only 6% of the collected individuals (Fig.
Specimens proportion of arthropods associated with L. azorica separately for the three colonising statuses: endemic (End), native (Nat) and introduced (Int) at Archipelago (AZO) and at the different Island level (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira).
The six most abundant species have 50% of the total abundance: the native Trioza laurisilvae Hodkinson, 1990 (Hemiptera) (n = 2675); the endemic spider Gibbaranea occidentalis Wunderlich, 1989 (Araneae) (n = 662); the endemic moth Argyresthia atlanticella Rebel, 1940 (Lepidoptera) (n = 510); the native spider Lathys dentichelis (Simon, 1883) (Araneae) (n = 498), the endemic spider Savigniorrhipis acoreensis Wunderlich, 1992 (Araneae) (n = 34) and the endemic tree hopper Cixius azoterceirae Remane & Asche, 1979 (Hemiptera) (n = 426) (see details in Suppl. material
Faial Island shows the highest number of specimens and Flores the lowest (Suppl. material
Considering the Archipelago as a whole (Fig.
Abundance proportion of arthropods associated with L. azorica per order for all species (A) and for the three colonising statuses separately endemic (B), native (C) and introduced (D) species at Archipelago (AZO) and Island level (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira).
At Island level, Hemiptera and Araneae account for more than 75% of species abundances in all species, endemic or native species groups. A different pattern was observed within introduced species; spiders, lepidopterans and booklice were the most abundant groups (Fig.
Functional groups and feeding modes
Herbivores and predators represent about 80% of total species abundance and richness at the Archipelago level, as well as at the Island level. Herbivores were represented by 41 species (6159 specimens) and predators by 37 species (3225 specimens) (Fig.
Abundance (A) and number of species (B) proportions of arthropods associated with L. azorica per different functional groups (S - saprophyte, P - predator; H - herbivore; F – fungivore) at Archipelago level (AZO) and Island level (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira).
A comparison between Islands showed that abundance of herbivores per unit sample was higher in FAI and the difference was significant between FAI and FLO (Suppl. material
Crossing functional and colonising groups, we found that most herbivores were endemics and native species, while most predators were introduced species. The distribution pattern was observed both for abundance and species richness (Suppl. materials
Species fall into four different feeding modes: external digestion and sucking; chewing and cutting; piercing and sucking; and siphoning. Very few species, 5% of the total species abundance (six species and 570 individuals), were siphoning species amongst them, five species were endemic species and one introduced species. Most individuals exhibited piercing and sucking feeding mode representing about 50% of the overall species abundance (5075 individuals). However, the chewing and cutting group was the most diverse group represented by 35 species (37% and 1581 individuals) (Fig.
Abundance (A) and number of species (B) proportions of arthropods associated with L. azorica per different feeding modes at Archipelago (AZO) and Island level (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira). S - saprophyte, P - predator; H - herbivore; F – fungivore and Ex - external digestion and sucking; Ch - chewing and cutting; Pi - piercing and sucking; Si - Siphoning.
Crossing analysis between feeding mode and colonising groups revealed a pattern similar to the functional group. Most endemic and native species were herbivores with piercing and sucking feeding mode and most introduced species were predators with external digestion and sucking (Suppl. materials
Species community structure
In this study, we considered rare species as those represented by seven individuals or less (see
Distribution of rare species. Sample coverage (SC) and the first seven frequency counts (f1 ... f7) for all endemic, native and introduced species in the six Islands (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira). The first seven frequencies indicate the numbers of species represented by only 1, 2, 3, ... 7 individuals (singletons, doubletons, tripletons etc.) and Propf1f7 indicates the proportion of the sum of the first seven frequencies (i.e. proportion of rare species) to the total number of species (see the total number of species in Table
SC |
f1 |
f2 |
f3 |
f4 |
f5 |
f6 |
f7 |
Propf1f7 |
|
All species in the archipelago |
|||||||||
Total_total |
1 |
12 |
6 |
10 |
5 |
4 |
1 |
4 |
45 |
Total_Endemic |
1 |
1 |
1 |
3 |
0 |
1 |
0 |
0 |
17 |
Total_Native |
1 |
3 |
2 |
3 |
2 |
1 |
0 |
3 |
45 |
Total_Introduced |
0.99 |
8 |
3 |
4 |
3 |
2 |
1 |
1 |
79 |
All species in Islands |
|||||||||
Total_FAI |
0.98 |
11 |
5 |
0 |
1 |
1 |
0 |
2 |
80 |
Total_FLO |
0.98 |
7 |
7 |
2 |
2 |
0 |
0 |
0 |
62 |
Total_PIC |
0.98 |
17 |
3 |
5 |
2 |
1 |
1 |
0 |
58 |
Total_SMG |
0.99 |
11 |
9 |
4 |
3 |
2 |
1 |
1 |
60 |
Total_SMR |
0.99 |
6 |
5 |
5 |
4 |
1 |
0 |
0 |
55 |
Total_TER |
1 |
12 |
5 |
4 |
5 |
2 |
4 |
1 |
46 |
Endemic species in Islands |
|||||||||
Endemic_FAI |
0.96 |
4 |
1 |
0 |
1 |
0 |
0 |
0 |
67 |
Endemic_FLO |
0.97 |
5 |
2 |
0 |
1 |
0 |
0 |
0 |
57 |
Endemic_PIC |
0.99 |
6 |
2 |
3 |
1 |
0 |
0 |
0 |
55 |
Endemic_SMG |
1 |
1 |
6 |
0 |
2 |
0 |
1 |
0 |
48 |
Endemic_SMR |
1 |
1 |
2 |
1 |
2 |
1 |
0 |
0 |
47 |
Endemic_TER |
1 |
0 |
1 |
1 |
1 |
2 |
0 |
0 |
21 |
Native species in Islands |
|||||||||
Native_FAI |
0.99 |
3 |
4 |
0 |
0 |
0 |
0 |
1 |
73 |
Native_FLO |
0.99 |
1 |
4 |
2 |
0 |
0 |
0 |
0 |
64 |
Native_PIC |
0.99 |
6 |
0 |
0 |
1 |
1 |
1 |
0 |
53 |
Native_SMG |
0.99 |
4 |
1 |
3 |
0 |
1 |
0 |
1 |
53 |
Native_SMR |
1 |
1 |
3 |
2 |
1 |
0 |
0 |
0 |
54 |
Native_TER |
1 |
3 |
1 |
1 |
2 |
0 |
4 |
1 |
48 |
Introduced species in Islands |
|||||||||
Introduced_FAI |
0.59 |
4 |
0 |
0 |
0 |
1 |
0 |
0 |
100 |
Introduced_FLO |
0.96 |
1 |
1 |
0 |
1 |
0 |
0 |
0 |
75 |
Introduced_PIC |
0.93 |
5 |
1 |
2 |
0 |
0 |
0 |
0 |
73 |
Introduced_SMG |
0.83 |
6 |
2 |
1 |
1 |
1 |
0 |
0 |
92 |
Introduced_SMR |
0.96 |
4 |
0 |
2 |
1 |
0 |
0 |
0 |
70 |
Introduced_TER |
0.98 |
9 |
3 |
2 |
2 |
0 |
0 |
0 |
73 |
Overall, 13% of species were represented by only one individual (singleton). At the Archipelago level, about 29% of introduced species and 10% of native species were represented by only one individual, whereas only 3% of endemic species were singletons. The proportions of singletons species were variable between the different Islands and the higher proportions were found within introduced species ranging from 25% in FLO Island to 80% in FAI Island (Suppl. material
Species abundance distribution patterns
Preston’s abundances frequency distribution, also called octaves (
The overall assemblage at the Archipelago level, showed a poisson log-normal distribution shape (PLN) (A) with abundances distributed into 12 octaves and 45% of species falling in the first three octaves 0, 1, 2 and, therefore, considered rare species (
Species abundance distribution histograms for arthropods species communities associated with L. azorica collected in the Azores Archipelago with predicted values of the gambin models (black dots) for all species (A), endemic (B), native (C) and introduced (D) species. Graphs (B), (C) and (D) are scaled equally for the Y axis.
Considering the three colonising groups, native species assemblage also showed the PLN shape Fig.
Analysis of gambin α-values are consistent with the shapes of the different models. Considering the Archipelago level, endemic species group showed the highest α-value (7.55) followed by native (2.32) and introduced (1.15) species. The same pattern was observed in the different Islands, except in FLO, where the introduced species group has the highest α-value (7.08), followed by native (3.52) and endemic (2.33) species (Fig.
Alpha values and confidence intervals of species abundance distribution models for arthropods, collected on L. azorica in the Azores Archipelago. Values are given for all species, endemic, native and introduced species in the six Islands (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira).
α-value |
CI95_low |
CI95_high |
|
All species in the Archipelago |
|||
Total_total |
2.12 |
1.546 |
2.851 |
Total_Endemic |
7.55 |
4.444 |
12.455 |
Total_Native |
2.32 |
1.335 |
3.837 |
Total_Introduced |
1.15 |
0.582 |
2.097 |
All species in Islands |
|||
Total_FAI |
0.69 |
0.303 |
1.386 |
Total_FLO |
2.80 |
1.333 |
5.581 |
Total_PIC |
1.48 |
0.857 |
2.436 |
Total_SMG |
1.69 |
1.066 |
2.594 |
Total_SMR |
2.21 |
1.296 |
3.608 |
Total_TER |
2.19 |
1.497 |
3.136 |
Endemic species in Islands |
|||
Endemic_FAI |
1.40 |
0.264 |
5.437 |
Endemic_FLO |
2.33 |
0.665 |
6.932 |
Endemic_PIC |
2.19 |
0.934 |
4.734 |
Endemic_SMG |
3.00 |
1.526 |
5.597 |
Endemic_SMR |
9.90 |
3.791 |
24.923 |
Endemic_TER |
11.84 |
5.973 |
22.764 |
Native species in Islands |
|||
Native_FAI |
1.041 |
0.330 |
2.658 |
Native_FLO |
3.515 |
1.139 |
9.954 |
Native_PIC |
1.991 |
0.735 |
4.696 |
Native_SMG |
2.438 |
1.062 |
5.133 |
Native_SMR |
2.657 |
1.043 |
6.102 |
Native_TER |
2.779 |
1.471 |
4.947 |
Introduced species in Islands |
|||
Introduced_FAI |
0.41 |
0.006 |
3.264 |
Introduced_FLO |
7.08 |
0.672 |
53.975 |
Introduced_PIC |
1.29 |
0.285 |
4.590 |
Introduced_SMG |
1.51 |
0.358 |
5.265 |
Introduced_SMR |
1.40 |
0.3186 |
4.787 |
Introduced_TER |
0.87 |
0.3583 |
1.846 |
Alpha values of Gambin models for species distributions for arthropods species communities associated with L. azorica at Archipelago (AZO) and Island level (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira) for all species (TOT), endemic (END), native (NAT) and introduced (INT) species. Lines represent 95% confidence intervals.
Species community similarity
We found high similarity between communities of Terceira (TER) and Pico (PIC) in one hand and, on the other hand, high dissimilarity between FLO and FAI (lowest (PIC-TER) and highest (FLO-FAI) Bray-Curtis index values) (Table
Dissimilarity analysis between Islands for arthropod species communities, associated with L. azorica using: all species(A), endemic (B), natives (C) and introduced (D) species. Values of Bray-Curtis dissimilarity index (lower half diagonal), number of shared species between the Islands (upper half diagonal) and number of species present in the Island (main diagonal in bold) are given. FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira.
(A) | FAI | FLO | PIC | SMG | SMR | TER |
FAI | 25 | 14 | 19 | 21 | 23 | 13 |
FLO | 0.84 | 29 | 25 | 22 | 17 | 24 |
PIC | 0.8 | 0.67 | 50 | 40 | 29 | 41 |
SMG | 0.87 | 0.78 | 0.66 | 52 | 26 | 46 |
SMR | 0.78 | 0.7 | 0.65 | 0.74 | 38 | 33 |
TER | 0.78 | 0.62 | 0.5 | 0.61 | 0.54 | 71 |
(B) | FAI | FLO | PIC | SMG | SMR | TER |
FAI | 9 | 5 | 8 | 8 | 5 | 8 |
FLO | 0.77 | 14 | 11 | 10 | 8 | 10 |
PIC | 0.78 | 0.71 | 22 | 18 | 13 | 18 |
SMG | 0.91 | 0.85 | 0.75 | 21 | 12 | 17 |
SMR | 0.76 | 0.73 | 0.64 | 0.79 | 15 | 13 |
TER | 0.77 | 0.69 | 0.57 | 0.7 | 0.56 | 24 |
(C) | FAI | FLO | PIC | SMG | SMR | TER |
FAI | 11 | 7 | 8 | 9 | 6 | 11 |
FLO | 0.86 | 11 | 9 | 8 | 7 | 10 |
PIC | 0.77 | 0.59 | 17 | 14 | 10 | 15 |
SMG | 0.81 | 0.64 | 0.52 | 19 | 10 | 17 |
SMR | 0.77 | 0.62 | 0.63 | 0.66 | 13 | 11 |
TER | 0.76 | 0.5 | 0.43 | 0.48 | 0.47 | 25 |
(D) | FAI | FLO | PIC | SMG | SMR | TER |
FAI | 5 | 2 | 3 | 4 | 2 | 5 |
FLO | 0.96 | 4 | 4 | 4 | 2 | 4 |
PIC | 0.75 | 0.84 | 11 | 8 | 6 | 8 |
SMG | 0.88 | 0.91 | 0.72 | 12 | 4 | 8 |
SMR | 0.83 | 0.88 | 0.76 | 0.86 | 10 | 9 |
TER | 0.79 | 0.88 | 0.6 | 0.66 | 0.79 | 22 |
Non-metric Dimensional Scaling (NMDS) with Bray-Curtis dissimilarities for arthropod species communities, associated with L. azorica collected in the six Islands (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira) using: all species (A), endemic (B), native (C) and introduced (D) species with stress values, respectively 0.182, 0.194, 0.138 and 0.175.
NMDS ordination also revealed that the different Islands were closer or more distant depending on whether we considered all species or species separated in different colonising statuses (Fig.
Considering all species: NMDS ordination (Fig.
Within endemic species, NMDS ordination (Fig.
ANOSIM sustained the structure observed in the different groups. Dissimilarities between the different Islands were all significant (P < 0.001) and R2 values indicated the highest dissimilarity within endemic species (R2 = 0.80), intermediate dissimilarity when considering all species (R2 = 0.66) or native species (R2 = 0.42) and very low dissimilarity within introduced species (R2 = 0.36).
Vascular plants
There are only four vascular plants, epiphytes of L. azorica and they are all ferns: Hymenophyllum tunbrigense (L.) Sm.; Vandenboschia speciosa (Willd.) G.Kunkel; Elaphoglossum semicylindricum (T.E.Bowdich) Benl; Polypodium macaronesicum subsp. azoricum (Vasc.) Rumsey, Carine & Robba (see Suppl. material
Bryophytes
We found that L. azorica was the substrate for both liverworts and mosses. Liverworts were represented by 57 species (three orders Jungermanniales, Metzgeriales and Porellales, comprising 18 families) (Suppl. material
The 35 moss species belong to five orders (Bryales, Dicranales, Hookeriales, Hypnales and Orthotrichales). Most of species belong to order Hypnales (19 species; 54%), whereas Dicranales accounts for about a quarter of the species (nine species; 26%) (Suppl. material
Lichens
The lichen community was composed of 32 species sorted into four classes (Arthoniomycetes, Dothideomycetes, Eurotiomycetes and Lecanoromycetes) and 13 identified orders (Arthoniales, Caliciales, Lecanorales, Monoblastiales, Ostropales, Peltigerales, Pertusariales, Pleosporales, Pyrenulales, Strigulales, Teloschistales, Trypetheliales, Verrucariales) (Suppl. material
A crucial point in a conservation programme is to accrue fine knowledge of species communities living in a particular system. In most ecosystems, the task is difficult, but thanks to their limited size and isolation, the probability to meet this fine grain knowledge in islands is high.
In the present study, carried out in Azores Islands, we explored arthropods and plant canopy species communities. We focused on species communities living on the endemic tree species L. azorica. We investigated the structure and composition of invertebrates and plants species community in six Azorean Islands covering the western (Flores), central (Faial, Pico, Terceira) and eastern (São Miguel, Santa Maria) Islands groups.
Communities species composition
Colonising status
Arthropods species communities on L. azorica were dominated by native and endemic species. The ten most abundant species are all endemic or native (Suppl. material
These results support those of a recent study in Azorean native forest, but whose samples were obtained with SLAM traps. Considering four dominant orders (Araneae, Coleoptera, Lepidoptera and Psocoptera), very few specimens of introduced species (6%) were collected, whereas the number of species was not different for endemic or native species groups (
Taxonomic composition
Amongst the thirteen orders collected in this study, Hemiptera was the most abundant group and Araneae was the most diverse group. Together, Hemiptera and Araneae assemble more than 75% of abundances and more than 50% of number of species collected. However, within introduced species, Araneae was both the most abundant and the most diverse group. The ten most abundant species are mostly composed by Araneae and Hemiptera along with a moth and a cockroach (Suppl. material
Our results support previous findings (
Functional and feeding groups
Our results revealed the dominance of herbivores and predators species representing up to 80% of both number of species and number of specimens. The proportion of functional groups is consistent with the taxonomic composition that we previously developed. In fact, most of Hemiptera species being herbivores and all spider species being predators, the proportion of functional groups observed was then foreseeable. This is similar to functional groups observed on J. brevifolia (
We found that this general pattern (dominance of herbivores tailed by predators and few saprophytes) was a common pattern observed in the different Islands. Moreover, the distribution of functional groups within the colonising groups was similar with some exceptions for the introduced taxa. The two fungivores species belong to the introduced taxa. We observed a dominance of saprophytes specimens in Flores (FLO) (> 50% of abundance).
Regarding species feeding mode, species communities found on L. azorica were mostly piercing and sucking species corresponding to species of the order Hemiptera and, therefore, representing about 50% of the overall species abundance (5075 individuals). Distribution patterns of species according to their feeding mode was closely related to their functional groups. Most endemic and native species were herbivores with piercing and sucking feeding mode, whereas most introduced species were predators with external digestion and sucking (
Community species structure
Investigations on rarity and similarity patterns show that community structure at the Archipelago level contrast most of Islands communities’ structures. Some Islands, like Terceira (TER) and Santa Maria (SMR), showed high similarity with the study at the Archipelago level. However, for the other Islands, similarities with Archipelago level seem to depend on the colonising status of the species.
Rarity patterns
At the Archipelago level as well as for all Islands, a gambin model log-series (LS) shape fitted introduced species distribution, indicating that most of the introduced species were rare. LS-shape models are characteristic of simple species communities with dominance of rare species and very few represented by high number of individuals (
On the other side, gambin models fitting endemic and native species distributions fitted log-normal (LN) and poisson log-normal (PLN) shapes. LN distributions are generally considered describing stable communities (
The present study suggests that introduced species communities are not yet well established on the L. azorica canopy which seems to be a stable refuge for indigenous (endemic and native) species communities.
Similarity patterns
Patterns of similarity between different Islands mainly rely on the colonising status, whether species were endemic, native or introduced species. Considering all species, no clear pattern emerged, communities of the six Islands overlapped, showing high similarities in species assemblages.
Contrary to communities collected on Juniperus brevifolia (
All species of vascular plants collected on L. azorica (four species) were epiphytes species and none was hemiparasites, contrasting the hemiparasite found on J. brevifolia (Arceuthobium azoricum Wiens & Hawksw) (
L. azorica shelters a diverse community of lichen and bryophytes, but we found that species diversity was lower than on Juniperus brevifolia community. This might be explained by the crinkled structure of J. brevifolia which offers diverse micro-habitats in all parts of the tree (
It is worth stressing that L. azorica supports a rich epiphyllous community, a feature which is characteristic of the Macaronesian mature forests, but very rare in other temperate habitats. More than 20 species have been found growing on L. azorica' leaves, adding a whole new layer of life to the Azorean forests.
About a fifth of the bryophytes, found associated with L. azorica, are IUCN conservation concern' species: seven mosses (three species, endangered; four species, vulnerable) and 12 liverworts (seven species endangered; five species vulnerable). Amongst the identified threats to the conservation of native ecosystems and species, both the habitat (
Our study identifies the contribution of the endemic tree L. azorica in supporting arthropods and plant species communities in native forest fragments. Although L. azorica seems to support poor communities compared to J. brevifolia, we found that profiles of species distribution provide clear insights on overall species distribution in native forest. Canopy community distribution confirms the results obtained in a previous study which suggest the stability of native and endemic species communities over introduced species community in native forests fragments (
At the Azorean scale, the study warns again generalisations, suggesting that most Islands present a particular species distribution pattern without geographical correlation and that conservation programmes should be adapted to each Island.
The authors of this manuscript would like to thank Sociedade de Gestão Ambiental e Conservação da Natureza – Azorina S.A. for the permission to use the scientific illustration of L. Azorica (Fig. 1). We are grateful to all researchers who collaborated in the field and laboratory during the BALA project, funded by Direcção Regional dos Recursos Florestais (Project 17.01-080203): Álvaro Vitorino, Anabela Arraiol, Ana Rodrigues, Artur Serrano, Carlos Aguiar, Catarina Melo, Francisco Dinis, Genage André, Emanuel Barcelos, Fernando Pereira, Hugo Mas, Isabel Amorim, João Amaral, Joaquín Hortal, Lara Dinis, Paula Gonçalves, Sandra Jarroca, Sérvio Ribeiro and Luís Vieira. The Forest Services provided local support in each Island. Acknowledgments are due to all the taxonomists who assisted in the identification of the morphotypes: Andrew Polaszek, António Bivar de Sousa, Artur Serrano, Arturo Baz, Fernando Ilharco, Henrik Enghoff, Jordi Ribes, José Quartau, Jörg Wunderlich, Ole Karsholt, Richard Strassen, Volker Manhert and Virgílio Vieira.
NT and MTF are currently funded by the project from Direcção Regional do Ambiente—LIFE IP AZORES NATURA (LIFE17 IPE/PT/000010) (2019). PAVB, RE and RG are funded by the project AZORESBIOPORTAL–PORBIOTA (ACORES-01-0145-FEDER-000072) (2019).
Ethical review and approval were waived for this study since it did not involve vertebrates.
Conceptualisation, NT, RG, RBE, and PAVB; data curation, RG, RBE and PAVB; formal analysis, NT; funding acquisition, RG, RBE, MTF and PAVB; investigation, NT, RG, RBE, MB; MTF and PAVB; methodology, NT, RG, RBE and PAVB; project administration, RG, RBE, MB; MTF and PAVB software, NT, supervision, RG, RBE and PAVB; validation, NT, RG, RBE, MB; MTF and PAVB; writing—original draft NT, RG, RBE and PAVB writing—review and editing, NT, RG, RBE, MB; MTF and PAVB. All authors have read and agreed to the published version of the manuscript.
The authors declare no conflict of interest.
List of references used in the survey of mosses, liverworts (bryophytes) and lichens associated with Laurus azorica.
List of vascular plants (Division Pteridophyta) associated with Laurus azorica. All species are present in the studied Islands with the exception of Elaphoglossum semicylindricum, which does not occur on Santa Maria. Colonisation status for each species (Status) distinguishes amongst natives (NAT), Azorean endemics (END) and Macaronesian endemics (MAC). All Pteridophyta species are epiphytes.
List of liverworts (Marchantiophyta) associated with Laurus azorica in the various Azorean Islands. Records coming from literature (L), please check Supplementary Material 1 and/or from the Cryptogamic Collection of the Herbarium of the University of the Azores (AZU) (H).
List of mosses (Bryophyta) associated with Laurus azorica in the various Azorean Islands. Records coming from literature (L), please check Supplementary Material 1 and/or from the Cryptogamic Collection of the Herbarium of the University of the Azores (AZU) (H).
List of lichens (Ascomycota) associated with Laurus azorica in the various Azorean Islands. Records coming from literature (L), please check Supplementary Material 17 and/or from the Cryptogamic Collection of the Herbarium of the University of the Azores (AZU) (H). All lichens are considered native in the Azores.
The classification system follows the general guidelines presented in Borges et al. (2010). The colonising status of each species is as follows: E – endemic; N – native; I – introduced. Islands coded as follows: FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira.
Comparison of standardised species richness values between the different Islands (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira) for all species (A), endemic (B), native (C) and introduced (D) species. Different letters indicate significant differences between Islands, based on Dunn’s multiple comparison test (p < 0.05).
Standardised values of abundance in the different Islands (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira) for all species (Total), endemic (END), native (NAT) and introduced (INT) species.
Comparison of standardised abundance values between the different Islands (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira) for all species (A), endemic (B), native (C) and introduced (D) species. Different letters indicate significant differences between Islands, based on Dunn’s multiple comparison test (p < 0.05).
Comparison of standardised abundance values species according to their different trophic groups: herbivores (A), predator (B), aprophyte (S). Different letters indicate significant differences between Islands, based on Dunn’s multiple comparison test (p < 0.05). FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira. Fungivores are not represented as the group was represented by only two species and seven individuals present in three Islands (SMG, SMR, TER).
Proportion of abundance per different functional groups at Archipelago (AZO) and Island level (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira) for all species (A), endemic (B), native (C) and introduced (D) species. S - saprophyte; P - predator; H - herbivore; F – fungivore.
Proportion of species per different functional groups at Archipelago (AZO) and Island level (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira) for all species (A), endemic (B), native (C) and introduced (D) species. S - saprophyte; P - predator; H - herbivore; F – fungivore.
The classification system follows the general guidelines presented in Borges et al. (2010), with the higher taxa listed in a phylogenetic sequence, from the less derived to more derived groups. The families, genera and species are listed by alphabetical order. The colonisation status of each species is presented in the 5th column of the list as follows: E – endemic; N – native; I – introduced. The functional group is given in the 6th column as follows: P – predator; H – herbivore; S – saprophyte; F – fungivore; Ex – External digestion and sucking; Ch – Chewing and cutting; Pi - Piercing and sucking; Si - Siphoning; No – Not feeding. X indicates species occurrence in the different Islands FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira. Ten species identified only at the morphospecies level are not presented in the table.
Proportion abundance per different feeding modes at Archipelago (AZO) and Island level (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira) for all species (A), endemic (B), native (C) and introduced (D) species. S - saprophyte; P - predator; H - herbivore; F – fungivore and Ex - external digestion and sucking; Ch - chewing and cutting; Pi - piercing and sucking; Si - siphoning.
Proportion of species per different feeding modes at Archipelago (AZO) and Island level (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira) for all species (A), endemic (B), native (C) and introduced (D) species. S - saprophyte; P - predator; H - herbivore; F – fungivore and Ex - external digestion and sucking; Ch - chewing and cutting; Pi - piercing and sucking; Si - siphoning.
Proportions of rare species (the first seven frequencies- Propf1f7), singleton species (represented by one individual Propf1), doubletons species (represented by two individuals-Propf2) and tripletons species (represented by three individual-Propf3). Proportions are calculated for all endemic, native and introduced species at the Archipelago level and in the six Islands (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira).
Species abundance distribution histograms for arthropods collected in six Islands (FAI – Faial; FLO – Flores; PIC – Pico; SMG – São Miguel; SMR – Santa Maria; TER – Terceira) of Azores Archipelago with predicted values of the gambin model (black dots) all species (1st column.total), endemic (2nd column.End), native (3rd column.Nat) and introduced (4th column.Int) species. Graphs of the same column are scaled equally for the Y axis.