Biological Integrity of Azorean Native Forests Is Better Measured in Cold Season

Round 1

Reviewer 1 Report

Authors use arthropod data to assess the seasonal variation of a biological integrity index (IBI) in 12 forest fragments in Azorean islands with different levels of preservation/disturbance. Authors show that IBI decreases with disturbance. They also found significant differences between seasons in preserved not in disturbed forests. IBI values were higher during the “cold semester” (winter and spring) that the warm semester (Summer & Autumn) because the abundance (number of individuals) of exotic species was higher in Summer. Please find some comments for authors to consider:

1.     The title should specify that the study is focused on arthropods and find it

2.     Abstract Line 17. SLAM traps? please spell out

3.     Study area. Lines 84-108. Authors should describe the nature of the disturbances of the forest plots they studied. Are the disturbances natural, man-made?

4.     Line 120. Please provide a table with the georeferences of each of the 12 sites chosen for this study.

5.     The section “study areas” is a nearly exact copy of an extract of a paper recently published in Ecological Indicators (Tsafack et al 2023). Please avoid cut and paste whole paragraphs from previously published papers.

6.     Lines 110-113. Have these data sets been already previously published or used in other studies (ie Tsafack 2023)? Or is this novel data? Please clarify.

7.     Data Accessibility Lines 269-271. I fully understand that authors are still using the data in an ongoing project (LIFE-Beetles) so they choose to make the data available upon request but this is not entirely satisfactory. For instance, it would have been useful to have the distribution data of those 90 K individuals belonging to 351 morphospecies deposited for instance in GBIF to make the data accessible not only to the scientific community bit also to conservation managers and decision makers. I would therefore advise authors to deposit their biodiversity data in this online public platform which would make their data easier to access and more visible as the project LIFE-Beetles progresses.

8.     Conclusion Line 243, “cold seasons (winter and autumn) » but in the text you define cold season as Winter & Spring. Please correct

Author Response

Dear Reviewer,

Thank you for allowing us to review our manuscript entitled: “The impact of exotic arthropod species in Azorean pristine forest is better measured in summer than in cold seasons.” submitted to Diversity. Please, find attached a revised version of our manuscript.

We have incorporated all your corrections and suggestions.

In the following, we explain how we dealt with each comment.

Authors use arthropod data to assess the seasonal variation of a biological integrity index (IBI) in 12 forest fragments in Azorean islands with different levels of preservation/disturbance. Authors show that IBI decreases with disturbance. They also found significant differences between seasons in preserved not in disturbed forests. IBI values were higher during the “cold semester” (winter and spring) that the warm semester (Summer & Autumn) because the abundance (number of individuals) of exotic species was higher in Summer. Please find some comments for authors to consider:

1. The title should specify that the study is focused on arthropods and find it

Authors: Thank you, the title was completed as suggested.

2. Abstract Line 17. SLAM traps? please spell out

Authors: We defined the acronym. SLAM traps: Sea-Land-Air-Malaise traps.

3. Study area. Lines 84-108. Authors should describe the nature of the disturbances of the forest plots they studied. Are the disturbances natural, man-made?

Authors: We added the origin of disturbance in the text please see lines 168-170.

4. Line 120. Please provide a table with the georeferences of each of the 12 sites chosen for this study.

Authors: We added Table 1 presenting the location of each sites.

5. The section “study areas” is a nearly exact copy of an extract of a paper recently published in Ecological Indicators (Tsafack et al 2023). Please avoid cut and paste whole paragraphs from previously published papers.

Authors: The current paper is a companion paper of our previous work Tsafack et al, 2023 published in Ecological Indicators. The methodology is similar even if the questions are different. This is why the method section seems copied.

However, we added details and rephrased the text in a different way such that our current manuscript does not resemble a simple extract. Thank you for your suggestion.

6. Lines 110-113. Have these data sets been already previously published or used in other studies (ie Tsafack 2023)? Or is this novel data? Please clarify.

Authors: Yes, the datasets have been published. Most of our data are published in Biodiversity Data Journal and are publicly available in our website GIMS Global Island Monitoring Scheme and in Azorean Biodiversity Portal which is linked to gbif.org. We now cited these works in line 164.

7. Data Accessibility Lines 269-271. I fully understand that authors are still using the data in an ongoing project (LIFE-Beetles) so they choose to make the data available upon request but this is not entirely satisfactory. For instance, it would have been useful to have the distribution data of those 90 K individuals belonging to 351 morphospecies deposited for instance in GBIF to make the data accessible not only to the scientific community bit also to conservation managers and decision makers. I would therefore advise authors to deposit their biodiversity data in this online public platform which would make their data easier to access and more visible as the project LIFE-Beetles progresses.

Authors: Thank you for spotting this mistake. Indeed, all the data is available in Data Papers and now clarified in line 164. We changed the text accordingly.

8. Conclusion Line 243, “cold seasons (winter and autumn) » but in the text you define cold season as Winter & Spring. Please correct

Authors: Thank you, we corrected.

We hope that you are satisfied with this revision and that the manuscript is now in a suitable form for publication.

All the best,

Noelline Tsafack

(on behalf of all coauthors)

Author Response File: Author Response.pdf

Reviewer 2 Report

The authors investigated seasonal patterns in preserved and disturbed native forests in the Azores measured as biological integrity. Moreover, the authors compared the effects using several insect groups - endemic/native/introduced species and a functional sub-group formed by saproxylic species only, and similarly also the same (?) divisions for the insect individuals.

The authors collected a large amount of samples (but did not provide more details about the taxonomic categories). They show that the preserved forests show a significant seasonal pattern with the highest integrity values in spring and winter seasons, whereas the disturbed forests show a large variation of the indexes and thus the seasonal pattern is not significant, despite the similar trends. Exotic non-native species prevailed in all seasons except winter, thus likely causing the distortions.

In general, I see the paper as very interesting and with important findings. However, the authors are rather secretive regarding the details, and the text is condensed and thus complicated with some shortenings. 

I would like to read a piece of information about the taxonomic group investigated, if the authors used only beetles or some other insect order, or if it was from different orders, they should clearly state that they identified the samples as morphospecies already in Methods and not in the Results. Also, it seems that the authors used also something like "%sInt", despite the lack of this category in Methods, on the other hand, the "%sSap" and "%nSap" categories were apparently not used in the Results.

Finally, I would welcome also an additional analysis, which would mix the effects of preserved and disturbed sites and the native/endemic/invasive species across the seasons. Such a result would show what causes the seasonal distortions in the disturbed sites.

I hope that the authors will easily prepare a new version and I would be happy to see the paper published.

Author Response

Dear Reviewer,

Thank you for allowing us to review our manuscript entitled: “The impact of exotic arthropod species in Azorean pristine forest is better measured in summer than in cold seasons.” submitted to Diversity. Please, find attached a revised version of our manuscript.

We have incorporated all your corrections and suggestions.

In the following, we explain how we dealt with each comment.

The authors investigated seasonal patterns in preserved and disturbed native forests in the Azores measured as biological integrity. Moreover, the authors compared the effects using several insect groups - endemic/native/introduced species and a functional sub-group formed by saproxylic species only, and similarly also the same (?) divisions for the insect individuals.

Authors: The different arthropod groups are the ones that composed the multimetric biological integrity. They are now presented in Table 2. They were selected among 16 other groups to form the index.

The authors collected a large amount of samples (but did not provide more details about the taxonomic categories).

Authors: Thank you, we expanded the section describing the dataset and added the taxonomic categories present in the dataset. Please see Lines 180-184.

They show that the preserved forests show a significant seasonal pattern with the highest integrity values in spring and winter seasons, whereas the disturbed forests show a large variation of the indexes and thus the seasonal pattern is not significant, despite the similar trends. Exotic non-native species prevailed in all seasons except winter, thus likely causing the distortions.

In general, I see the paper as very interesting and with important findings.

Authors: Thank you

However, the authors are rather secretive regarding the details, and the text is condensed and thus complicated with some shortenings.

Authors: We have expanded the text and added details. Particularly, we added details on the study areas and on the datasets. We also added two more tables one to summarize information on sites description and location (Table 1) and one to show the quantitative values for each metric included in IBI-SLAM and their scores (Table 2).

I would like to read a piece of information about the taxonomic group investigated, if the authors used only beetles or some other insect order, or if it was from different orders, they should clearly state that they identified the samples as morphospecies already in Methods and not in the Results.

Authors: We added the different taxonomic groups collected in the samples (see lines 177-181) and also the information that species were sorted at morphospecies level to be later identify at species level by the senior coauthor (P.A.V.B.) see lines 180-184.

Also, it seems that the authors used also something like "%sInt", despite the lack of this category in Methods, on the other hand, the "%sSap" and "%nSap" categories were apparently not used in the Results.

Authors: We added Table 2 that summarizes the values and scores of metrics that were used in the IBI. The final IBI value is the sum of each of the seven metrics, therefore, they were all used in the results.

Finally, I would welcome also an additional analysis, which would mix the effects of preserved and disturbed sites and the native/endemic/invasive species across the seasons. Such a result would show what causes the seasonal distortions in the disturbed sites.

Authors: Table 4 and 5 present how IBI varies across seasons and semesters no matter their biogeographic status. We found that IBI seasonal distortions in the disturbed sites were due to different distribution dynamics of exotic introduced species between summer and winter seasons, and between warm and cold semesters.

I hope that the authors will easily prepare a new version and I would be happy to see the paper published.

Authors: We appreciate your comments that highly guided to improve our manuscript.

We hope that you are satisfied with this revision and that the manuscript is now in a suitable form for publication.

All the best,

Noelline Tsafack

(on behalf of all coauthors)

Author Response File: Author Response.pdf

Reviewer 3 Report

Comments on the MS  

The impact of exotic species in Azorean pristine forest is best measured in summer than in cold seasons.

By Noelline Tsafack^1,2*, Sébastien Lhoumeau¹, Alejandra Ros-Prieto¹, Loic Navarro¹, Timea Kocsis¹, Sónia Manso², Telma Figueiredo², Maria Teresa Ferreira², Paulo A. V. Borges^1,3

The aim of the authors is to optimize a biointegrety index (IBI) based on arthropods caught with SLAM traps, to determine in which season the index performs best, and to take into account the colonisation status of the analysed species. The arthropods for the study were collected from a large database built up over more than 30 years.

The MS would be much more readable if it did not refer to publications to understand even basic terms, but explained them in detail.

The information given in the MS is difficult or impossible to understand for someone who is not familiar with the subject. Even the most important terms and definitions are not explained or are described in later chapters, especially the IBI index or the SLAM methods. The applicability, meaning and behaviour of the index in different contexts are not explained. I do not understand why the index only considers saproxylic species and no other guilds.

What is the overall aim of the analyses? How can the analyses be evaluated if the rationale for the selection of the taxa is not explained? Are there focal groups? What kind of traps were included and were all data on arthropod ocurrance combined? Why were taxa selected from three islands, from which years and what types of habitat were compared? How do you cope with all this heterogeneity? Can these data be analysed using univariate statistics?

The ecological situation in the Azores is poorly described; how many natural areas remain, are there any areas at all that have not been heavily influenced by man? Are these areas mainly mountainous? Are they isolated or connected? Are the results applicable to other systems?

Little is learned about the ecological impact of invasive species, except that there are seasonal differences, which the authors suggest significantly alters the IBI index. Other effects of invasive species on the ecosystem are discussed in very general terms.

What are invasive species communities?

I am sorry that I cannot be more positive, but I hope that my comments will at least be helpful for future work.

Author Response

Dear Reviewer,

Thank you for allowing us to review our manuscript entitled: “The impact of exotic arthropod species in Azorean pristine forest is better measured in summer than in cold seasons.” submitted to Diversity. Please, find attached a revised version of our manuscript.

We have incorporated all your corrections and suggestions.

In the following, we explain how we dealt with each comment.

The impact of exotic species in Azorean pristine forest is best measured in summer than in cold seasons.

By Noelline Tsafack1,2*, Sébastien Lhoumeau1, Alejandra Ros-Prieto1, Loic Navarro1, Timea Kocsis1, Sónia Manso2, Telma Figueiredo2, Maria Teresa Ferreira2, Paulo A. V. Borges1,3

The aim of the authors is to optimize a biointegrety index (IBI) based on arthropods caught with SLAM traps, to determine in which season the index performs best, and to take into account the colonisation status of the analysed species. The arthropods for the study were collected from a large database built up over more than 30 years.

The MS would be much more readable if it did not refer to publications to understand even basic terms, but explained them in detail.

The information given in the MS is difficult or impossible to understand for someone who is not familiar with the subject. Even the most important terms and definitions are not explained or are described in later chapters, especially the IBI index or the SLAM methods. The applicability, meaning and behaviour of the index in different contexts are not explained. I do not understand why the index only considers saproxylic species and no other guilds. What is the overall aim of the analyses? How can the analyses be evaluated if the rationale for the selection of the taxa is not explained? Are there focal groups?

Authors: Sorry that we have not detailed these points before. In the current version, we added details on the study areas and particularly on the datasets.

Particularly, we presented the different orders collected [lines 180-184: These datasets include the total abundance of the following target groups: Diplopoda (Chordeumatida, Julida), Chilopoda (Geophilomorpha, Lithobiomorpha, Scolopendromorpha), Arachnida (Araneae, Opiliones, Pseudoscorpiones) and Insecta (Archaeognatha, Blattaria, Coleoptera, Hemiptera, Microcoryphia, Neuroptera, Psocodea, Thysanoptera, Trichoptera, Hymenoptera- Formicidae)].

We also explained how IBI were built. From a first selection between 32 parameters we selected 16 candidates parameters. From that 16 parameters we selected the final 7 parameters that are now used to calculate the IBI. We also added Table 2 that summarize the 7 parameters.

Saproxylic guild was the most important guild at differentiating preserved forest sites from disturbed forest sites; and was selected among others: fungivores, predators, herbivorous and generalist species which at the end were not selected because they were less important to differentiate preserved from disturbed forest sites.

What kind of traps were included and were all data on arthropod ocurrance combined?

Authors: Only SLAM traps (Sea-Land-Air-Malaise traps) were used in this study and data were combined to represent seasons and semesters.

Why were taxa selected from three islands, from which years and what types of habitat were compared?

Authors: We selected these three islands to have data collected at the same period with the same type of traps (SLAM) and also to have a balance number of preserved and disturbed forest sites.

How do you cope with all this heterogeneity?

Authors: Since we simplify disturbance factor into a binary representation (preserved vs. disturbed), heterogeneity was not a problem.

Can these data be analysed using univariate statistics?

Authors: We conducted Wilcoxon and Kruskal-Wallis tests which are non-parametric univariate statistical analysis.

The ecological situation in the Azores is poorly described; how many natural areas remain, are there any areas at all that have not been heavily influenced by man?

Are these areas mainly mountainous? Are they isolated or connected? Are the results applicable to other systems?

Authors: We expanded the description of the study area (see 2.1. Study areas). Among the nine islands Terceira is the one with the higher proportion of native forest with largest connected area. Native forest fragments are mostly at high altitude. The results of this study can serve as inspiration for other system but a precaution should be taken to adapt the IBI to the given system for which standardized endemic, native non-endemic and introduced exotic species richness and abundance should be obtained (see now in Lines 396-399).

Little is learned about the ecological impact of invasive species, except that there are seasonal differences, which the authors suggest significantly alters the IBI index. Other effects of invasive species on the ecosystem are discussed in very general terms. What are invasive species communities?

Authors: Introduced exotic arthropods in Azores are now a large fraction of the known list of species (references 8 and 23 in the manuscript). We now add some text on the topic in the Discussion.

I am sorry that I cannot be more positive, but I hope that my comments will at least be helpful for future work.

Authors: Thank you for your helpful comments.

We hope that you are satisfied with this revision and that the manuscript is now in a suitable form for publication.

All the best,

Noelline Tsafack

(on behalf of all coauthors)

Author Response File: Author Response.pdf

Round 2

Reviewer 3 Report

Dear authors,

In my opinion, the MS still lacks important basic information that would make it

Understandable. You find the most important below.

I) The added background information has improved the MS. However, there are still terms introduced that are not explained at all or only later, such as the definition of the IBI index itself, forest types or the term biological integrity. Such terms have to be explained when they are used for the first time.

II) I still do not understand what factors go into calculating the IBI index. Please provide the mathematical formula to make the statements in the MS understandable.

Making biological statements about forest types without having information on the animal communities is difficult to understand and requires detailed justification.

More generally, what insights does the index provide that the data alone cannot, and what is the practical application of the IBI index?

III) The selection of taxa for the calculation of the index is still insufficiently explained. For example, why were these particular islands and these particular taxa selected from the decades-old database and not others? Why was not all available information used?                     

How do communities with high integrity differ in taxa-, species- and functional composition, in diversity and structure differ from those with low integrity? Are communities of endemic species those with highest integrity?  

IV) Species differ in frequency distribution and alpha and beta diversity at different times of the year. The comparison of less diverse winter communities with diverse early summer communities based only on a multifactorial index is incomprehensible to me without detailed explanation and ecological reference.

The different behaviour of the IBI index in differently disturbed systems may suggest a general relationship between index value and disturbance or naturalness, but the ecological reasons for this are not discussed.

Author Response

Dear Reviewer,

Thank you for giving us the possibility of submitting an improved version of our manuscript entitled: “The impact of exotic arthropod species in Azorean pristine forest is better measured in summer than in cold seasons.” submitted to Diversity.

We are grateful to the Referee for these further comments. We did our best to incorporate all her/his corrections and suggestions. In the following, we explain how we dealt with each comment.

Dear authors,

In my opinion, the MS still lacks important basic information that would make it

Understandable. You find the most important below.

1. I) The added background information has improved the MS. However, there are still terms introduced that are not explained at all or only later, such as the definition of the IBI index itself, forest types or the term biological integrity. Such terms have to be explained when they are used for the first time.

 Authors: We expanded the introduction section and we have introduced the main Azores forest types, exotic and native forest (see lines 67-74); The terms biological integrity and IBI index were also explained at the first appearance in the text (Lines 90-95).

1. II) I still do not understand what factors go into calculating the IBI index. Please provide the mathematical formula to make the statements in the MS understandable.

Making biological statements about forest types without having information on the animal communities is difficult to understand and requires detailed justification.

More generally, what insights does the index provide that the data alone cannot, and what is the practical application of the IBI index?

 Authors: Please see lines 222-229 and Table 2 that present the seven parameters (percentages of endemic species (1. %sEnd) and individuals (2. %nEnd); of native species (3. %sNat) and individuals (4. %n Nat); of and saprophylic species (5. %sSap) and individuals (6. %nSap); and introduced individuals (7. %nInt) used to calculate the IBI).

We added the mathematical formula with S the score of each of the seven parameters, for an overall IBI value ranging from 0 to 14.

We have not expanded more on the methodology on the construction of the IBI because it was the main goal of our paper published in Ecological Indicators doi: 10.1016/j.ecolind.2023.110592. And the present paper aimed at exploring the best season to measure IBI in native and exotic forests.

Since it premises with Karr et al., 1986 (https://semspub.epa.gov/work/01/554353.pdf) in fresh marine ecosystems, the use of multiple parameters indices to measure ecosystems biological integrity have been praise for its numerous advantages. Zhu et al., 2021 (https://doi.org/10.1016/j.ecolind.2021.107882) pointed the fact that the complexity of ecosystems health cannot be access with a single parameter but with multiple parameters of the system for a more comprehensive understanding of the overall system condition. In our studies, we found that some parameter if considered individually might mislead the comprehension of ecosystems. For instance, abundance of native non-endemic species (nNat) was surprisingly positively related to disturbance contrasting the hypothesis that all native species indicators are well supported in good health status forest (preserved sites). This parameter was included in the calculation of IBI but with decreasing percentages (i.e. a system with more than 47% nNat receives a score of 0; a system with % nNat between 33% and 47% receives a score of 1 and a system of % nNat less than 33% receives a score of 2, please see Table 2). ). However, native non-endemic species richness (%sNat), endemic species richness (%sEnd) and abundance (%nEnd) are positively correlated with habitat quality, which shows that most indicators related with indigenous species are positively related with the good status of the forest.

III) The selection of taxa for the calculation of the index is still insufficiently explained. For example, why were these particular islands and these particular taxa selected from the decades-old database and not others? Why was not all available information used?           

How do communities with high integrity differ in taxa-, species- and functional composition, in diversity and structure differ from those with low integrity? Are communities of endemic species those with highest integrity? 

 Authors: We briefly described the methodology of IBI construction from line 211 to 228. The section was brief on purpose, because it was the main goal of the first paper that we published in Ecological Indicators (doi: 10.1016/j.ecolind.2023.110592) and the present paper aims at investigating which season or semester are the best to measure the biological integrity of native and exotic forests.

For this objective, we selected in our database, islands data with homogenous data features: (i)Data collected at the same period, a ten-year period extending from 2012 to 2022; (ii)data collected one time per season in all years without missing samples around 15th March for Winter sample, 15th June for Spring sample, 15th September for Summer sample and 15th December for Autumn sample; and (iii)data collected with the same passive flight-intercept SLAM trap (Sea, Land and Air Malaise trap; 110 x 110 x 110 cm (MegaView Science Co. Ltd., Taichung City, Taiwan)).

The IBI index indicates the overall system biological integrity. It is the sum of scores attributed according to the proportion of the seven parameters which for some parameter indicate an aspect of functional structure (Example %Sap) of species community supported by the system, and for other parameters the species richness or abundance aspect of the system; it is not possible the infer the exact functional composition of the system since not all functional parameters were included in IBI calculation; So, based on IBI, we can not infer an independent comparison of the following communities structure aspects - taxa-, species- and functional composition, between systems of different biological integrity levels.

1. IV) Species differ in frequency distribution and alpha and beta diversity at different times of the year. The comparison of less diverse winter communities with diverse early summer communities based only on a multifactorial index is incomprehensible to me without detailed explanation and ecological reference.

The different behaviour of the IBI index in differently disturbed systems may suggest a general relationship between index value and disturbance or naturalness, but the ecological reasons for this are not discussed.

 Authors: In our knowledge, this is the first study that attempt to understand how biotic integrity of a system change across time. The result obtained in pristine forests show clearly that exotic arthropods are entering the system mostly in summer and autumn and IBI can act as an indicator for invasiveness in these native forests (see lines 329-339) and (340-351) for a discussion on the thematic

We agree that species dynamics follow seasonal turnover for species physiological reasons. In the present study, we are not investigating species dynamics but the system biological integrity using the multiparametric index IBI. So, it might not be a surprise that the IBI is different between seasons. But what is interesting is the difference observed between the different systems indicating when to measure IBI for each. We suggested a tentative explanation (please see lines 368 to 375) but these hypotheses can only be tested in further studies.

We would like to thank once again the reviewer for her/his detailed and useful comments, which helped us to ameliorate the manuscript. We hope that he/she is satisfied with this revision and that the manuscript is now in a suitable form for publication.

All the best,

Noelline Tsafack

(on behalf of all coauthors).

Author Response File: Author Response.pdf

Round 3

Reviewer 3 Report

The authors have taken the comments into account and integrated them into the MS. The content of the MS has improved considerably. Good luck for further research!

Author Response

Thank you so much!