Review Reports - Current Knowledge of Helminths of Wild Birds in Ecuador

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

The manuscript reviews the available information on parasitic helminths infecting wild birds in Ecuador. It provides a literature review of a period of almost 60 years, but it reports only 17 peer-review and no peer-review scientific papers/dissertations (most of them without passing a peer-review process), revealing a poor helminthological baseline in Ecuadorian science. In this sense, the manuscript provides valuable information. In general, the manuscript is well-organized and the methodology is appropriate. Although I have some minor comments on the manuscript (see below), I’m not sure of the “validity” of the results of this review since half of references provided for helminths are bachelor/PhD theses (9/18 in my counting; see below) and, hence, they did not pass any peer-review process. In this sense, if the review is accepted, authors should explicitly discuss that half of studies found are not peer-reviewed papers, which may avoid future erroneous citations generalizing the results. Readers should be aware of this limitation when reading and citing this review.

Specific comments

Simple Summary, Abstract and Ln 31: Acantocephala is no longer considered a single phylum. Genetic markers (18S) place monophyletic Acantocephala together with Rotifera in a group called Syndermata. I suggest to show Acantocephala as “Syndermata: Acantocephala” thorough the manuscript.

Ln 9: parasitic helminths.

Ln 13 and 23: Remove “bibliographical reference” as it is assumed that any systematic review provide references.

Ln 30: Not all helminths are parasitic species (most of Nematoda species are free-living organisms). Re-write as “Helminths are metazoan (i.e., multicellular), most of them parasites, classified in three phyla”.

Ln 33: the range 100,000 to 350,000 species of helminths is an estimation, of which 80-90% are still unknown and thus not described. Re-write the sentence indicating that the data showed is an estimation.

Ln 34: Indicate that 16% of helminth diversity is estimated to be bird-specific.

Ln 35: remove “in the”.

Ln 36: “Helminths show different life cycles”.

Ln 40: “individual and population levels”.

Ln 45: “play a key role on ecosystem functioning”.

Ln 48: “in individuals with other infections (e.g., bacteria, viruses)”.

Ln 52: “Earth”.

Ln 55: Maybe express the distance in km instead of miles.

Ln 56: “high endemic fauna”.

Ln 61: Ectoparasites are not pathogens, separate from the list of pathogens.

Ln 70: “A systematic search following… was conducted”.

Ln 71: Why not update the online search? August 2020 is outdated and maybe some papers have been published from 2020 to nowadays. Indeed, you stated in line 87 that 3 studies (2021-2022) have been recently published. Better to update the systematic search and included those 3 papers (and maybe some more) within the “database search” paragraph.

Ln 92: remove “(wild bird species investigated)” as it was stated previously. Maybe simply write “host wild bird species”.

Ln 93: “geographical location of the study”.

Ln 107: “selected information”.

Ln 113: Authors state that 3 phyla were found, but only 2 were actually found (i.e., Trematoda and Nematoda, as any Acantocephala was found).

Ln 115: “genus level”.

Table: In the family Cyclocoelidae, the species Cyclocoelum obscurum is duplicated in two different rows, why not pool them? Idem for family Leucochloridiidae, species Urotocus fusiformis. Also, check scientific names because some have erroneous accent marks.

Results: Maybe I missed something, but the the data displayed in the main text do not coincide with the data provided in the Table (see below the table I constructed based on your data). I counted 18 references (not 17), 35 helminth taxa (not 36) and 64 bird taxa (not 66), including 1 at family level (not 3), 3 at genus level (not 2) and 60 at species level (not 61). Also, the types of documents (papers, PhD dissertations, etc.) in the text do not coincide with those in the Table. Please, re-analyse the data to correctly show the results.

Nº helminth taxa	Nº bird taxa	Nº Refs
Nematoda	Penelope obscura	30 – PhD dissertation
Dispharynx sp.	Penelope purpurascens	31 – Paper
Contracaecum sp.	Phoebastria irrorata	32 – Paper
Ascaridia sp.	Spheniscus mendiculus	20 – Paper
Ascaridia columbae	Coccyzus melacoryphus	33 – Bachelor dissertation
Ascaridia galli	Crotophaga ani	29 – Bachelor dissertation
Heterakis gallinarum	Setophaga petechia aureola	43 – Bachelor dissertation
Heterakis sp.	Bubulcus ibis	37 – Bachelor dissertation
Capillaria sp.	Phalacrocorax harrisi	38 – Bachelor dissertation
Onchocercidae gen. sp.	Mustelirallus erythrops	34 – Paper
Strongyloidea gen. sp.	Nyctanassa violacea pauper	35 – Bachelor dissertation
Strongyloides sp.	Pelecanus occidentalis urinator	36 – Bachelor dissertation
Trichuris sp.	Phoebastria irrorata	44 – Paper
Cestoda	Anhima cornuta	45 – Paper
Hymenolepis nana	Camarhynchus pallidus	41 – Paper
Tetrabothrius sp.	Chlauna torquata	40 – PhD dissertation
Gen. nov. Cestoda gen. sp.	Columba livia	46 – Paper
Trematoda	Megascops albogularis	42 – Paper
Brachylaimidae gen. sp.	Patagioenas fasciata
Cyclocoelum obscurum	Pavo cristatus
Cyclocoelum tringae	Phalcoboenus carunculatus
Selfcoelum brasilianum	Sarcoramphus papa
Bothrigaster variolaris	Vultur gryphus
Lubens lubens	Amazona amazonica
Zonorchis meyeri	Amazona autumnalis
Zonorchis delectans	Psittacara erythrogenys
Brachylecithum rarum	Anatidae
Heterophyidae gen. sp.	Anser spp.
Neodiplostomum sp.	Fulica ardesiaca
Neodiplostomum ellipticum	Phalacrocorax brasilianus
Echinostomatidae gen. sp.	Ara macao
Tanaisia bragai	Cygnus spp.
Tanaisia fedtschenkoi	Amazona farinosa
Urotocus fusiformis	Ara severus
Leucochloridium sp.	Formicarius analis
Prosthogonimus cuneatus	Formicarius colma
Renicola sp.	Calidris melanotos
Cardiocephaloides sp.	Tringa solitaria
	Rostrhamus sociabilis
	Gymnopithys leucaspis
	Willisornis poecilinotus
	Phlegopsis erythroptera
	Pygiptila stellaris
	Thamnomanes ardesiacus
	Laterallus sp.
	Laterallus spilonota
	Cymbilaimus lineatus
	Epinecrophylla ornata
	Hypocnemis cantator
	Myrmelastes hyperythrus
	Myrmoborus myotherinus
	Myrmotherula axillaris
	Isleria hauxwelli
	Myrmotherula schisticolor
	Phlegopsis nigromaculata
	Myrmelastes leucostigma
	Thamnomanes caesius
	Chamaeza nobilis
	Hafferia fortis
	Frederickena undiliger
	Hylophylax naevius
	Myrmothera campanisona
	Sclateria naevia
	Sula nebouxii

Figure: Please, add the scale.

Ln 170: Now 19 records? They were 17 at the beginning… And I counted 18.

Ln 172: “parasitic helminths”. Also, update the number of taxa (helminths and birds) thorough the discussion (see above my comment on results).

Ln 175-178: I suggest authors to go more in deep on this point, i.e., take into account that most studies are not peer-reviewed papers and, thus, conclusions and future citations should consider this limitation.

Ln 182: “molecular tools”.

Ln 185: Added to Díaz et al. (2022), maybe cite also Binkiene et al. (2021) (Parasites & Vectors, 14: 137. Doi: 10.1186/s13071-021-04614-8), which call for more genetic studies on parasitic avian nematodes.

Ln 189: “only 3 out of 18 studies were performed in the Amazon region”.

Ln 191: “distributed through high diversity Ecuadorian areas, such as…”.

Ln 201: infecting, not affecting since you do not check for the effects of helminths.

References: check the references because there are some mistakes. Also, add bachelor or PhD thesis when citing the respective dissertations.

Comments on the Quality of English Language

Author Response

Dr. Jukka Jokimäki

Editor-in-Chief

Birds

Dear Dr. Jokimäki

We wish to submit a revised version of an article entitled “Current Knowledge of Helminths of Wild Birds in Ecuador” for consideration by the Journal of Birds.

Sincerest thanks for your response on the manuscript. We appreciate the valuable and useful contribution made by the reviewers, which definitely helped to improve the manuscript.

We have modified the paper in response to the extensive and insightful reviewers’ comments. We have re-written and add some sections in the results and discussion to fully address the reviewers’ comments. Please find revised text highlighted in red color.

Please find in the next section the point-by-point responses to reviewers’ comment.

We look forward to hearing from you regarding our submission. We would be glad to respond to any further questions and comments that you may have.

Thank you for your consideration.

Reviewer #1:

Specific comments

Simple Summary, Abstract and Ln 31: Acantocephala is no longer considered a single phylum. Genetic markers (18S) place monophyletic Acantocephala together with Rotifera in a group called Syndermata. I suggest to show Acantocephala as “Syndermata: Acantocephala” thorough the manuscript.

We agree with the reviewer´s comment. Changes has been made as indicated.

Ln 9: parasitic helminths. Ln 13 and 23: Remove “bibliographical reference” as it is assumed that any systematic review provide references. Ln 30: Not all helminths are parasitic species (most of Nematoda species are free-living organisms). Re-write as “Helminths are metazoan (i.e., multicellular), most of them parasites, classified in three phyla”. Ln 33: the range 100,000 to 350,000 species of helminths is an estimation, of which 80-90% are still unknown and thus not described. Re-write the sentence indicating that the data showed is an estimation. Ln 34: Indicate that 16% of helminth diversity is estimated to be bird-specific.

We agree with the reviewer and have revised sections accordingly.

Ln 35: remove “in the”. Ln 36: “Helminths show different life cycles”. Ln 40: “individual and population levels”. Ln 45: “play a key role on ecosystem functioning”. Ln 48: “in individuals with other infections (e.g., bacteria, viruses)”. Ln 52: “Earth”. Ln 55: Maybe express the distance in km instead of miles. Ln 56: “high endemic fauna”. Ln 61: Ectoparasites are not pathogens, separate from the list of pathogens. Ln 70: “A systematic search following… was conducted”.

Grammatical errors were modified as indicated.

Ln 71: Why not update the online search? August 2020 is outdated and maybe some papers have been published from 2020 to nowadays. Indeed, you stated in line 87 that 3 studies (2021-2022) have been recently published. Better to update the systematic search and included those 3 papers (and maybe some more) within the “database search” paragraph.

We agree with the reviewer and have revised sections accordingly

Ln 92: remove “(wild bird species investigated)” as it was stated previously. Maybe simply write “host wild bird species”. Ln 93: “geographical location of the study”. Ln 107: “selected information”. Ln 113: Authors state that 3 phyla were found, but only 2 were actually found (i.e., Trematoda and Nematoda, as any Acantocephala was found). Ln 115: “genus level”.

Grammatical errors were modified as indicated.

Table: In the family Cyclocoelidae, the species Cyclocoelum obscurumis duplicated in two different rows, why not pool them? Idem for family Leucochloridiidae, species Urotocus fusiformis.

We agree with the reviewer and have revised sections accordingly

Also, check scientific names because some have erroneous accent marks.

Grammatical errors were modified as indicated.

Results: Maybe I missed something, but the the data displayed in the main text do not coincide with the data provided in the Table (see below the table I constructed based on your data). I counted 18 references (not 17), 35 helminth taxa (not 36) and 64 bird taxa (not 66), including 1 at family level (not 3), 3 at genus level (not 2) and 60 at species level (not 61). Also, the types of documents (papers, PhD dissertations, etc.) in the text do not coincide with those in the Table. Please, re-analyse the data to correctly show the results.

We agree with the reviewer and have revised sections accordingly.

Figure: Please, add the scale.

Changes have been made accordingly

Ln 170: Now 19 records? They were 17 at the beginning… And I counted 18. Ln 172: “parasitic helminths”. Also, update the number of taxa (helminths and birds) thorough the discussion (see above my comment on results).

We appreciate the reviewer’s comment, and we have revised sections accordingly.

Ln 175-178: I suggest authors to go more in deep on this point, i.e., take into account that most studies are not peer-reviewed papers and, thus, conclusions and future citations should consider this limitation.

We appreciate the reviewer’s comment, and we have developed and rewritten the discussion section.

Ln 182: “molecular tools”. Ln 185: Added to Díaz et al. (2022), maybe cite also Binkiene et al. (2021) (Parasites & Vectors, 14: 137. Doi: 10.1186/s13071-021-04614-8), which call for more genetic studies on parasitic avian nematodes.

We agree with the reviewer and have revised sections accordingly.

Ln 189: “only 3 out of 18 studies were performed in the Amazon region”. Ln 191: “distributed through high diversity Ecuadorian areas, such as…”. Ln 201: infecting, not affecting since you do not check for the effects of helminths.

Grammatical errors were modified as indicated.

References: check the references because there are some mistakes. Also, add bachelor or PhD thesis when citing the respective dissertations.

We agree with the reviewer and have revised sections accordingly.

Author Response File: Author Response.pdf

Reviewer 2 Report

Comments and Suggestions for Authors

The manuscript is a well-written overview of helminths in birds from Ecuador. The authors followed all the rules in literature search and preparing the manuscript. The review is carried out in accordance with all the rules of similar review articles. The authors have collected all the available English and Spanish-language literature on this theme. Of course, there are quite a few sources for analysis (17 in total).

However, I believe that the paper needs to be improved in order to be published. My comments and suggestions are as follows:

1. Why was the literature search limited to only two databases? Why the authors did not look for information in the most well-known databases Web of Science and Scopus?

2. The map still needs to be redone. The Galapagos Islands should be located where they should be - to the left of the mainland. The map should also have a scale. And it is better to place the names of provinces on the map.

3. The authors provide information about helminths found in birds of Ecuador in the form of a table, but the Discussion does not contain an analysis of this data.

What are the most common parasite species (families, classes) in birds of Ecuador? Are host-specific parasites identified or are the identified parasite species broadly specific? Common geographical distribution of detected helminths. Do helminths found in birds have veterinary or medical significance as potential pathogens? Etc.

4. Table 1 needs to be redone. The first and second columns should be combine to “Helminth species”, where family name of helminths and phylum name will appear above the species name:

Cestoda

Hymenolepididae

Hymenolepis nana (Weinland, 1858)

Column title “Site in Host” better fix it to “Localization” or “Site of infection”.

In column “Host species” only the Latin names of birds should be left. In scientific articles, try not to use common animal names, please use only Latin.

Please check Table 1. Especially with regards to the Latin names of helminths. For example, correct name of the parasites – Hymenolepis nana (Siebold, 1852), Cyclocoelum tringae (Stossich, 1902). Check all Latin names.

Cyclocoelum obscurum is mentioned twice. Perhaps you should combine data.

Also check use of italics; typos (Tringa solitaria (Wilson, 1813) (Wilson, 18132)) .

According to the rules of International Code of Zoological Nomenclature (ICZN), only one author is given after the Latin name. For example, Cyclocoelum obscurum (Leidy, 1887).

5. Information from lines 114-116 should be included to the Abstract. “Thirty-six helminth taxa” looks wrong.

6. So how many sources did you find on the topic - 17 (line 106) or 19 (line 171)?

And some small remarks:

In key words – “Animals” are unnecessary. This keyword need be deleted.

Please provide references in the text and in Table 1 in regular font, not superscript.

Subsections in Materials and Methods should be numbered as in Results. And write words in capital letters (2.1. Database Search)

Line 185 – Please, make reference according to MDPI journal rules.

Authors contribution. Please, use only name initials here.

In my opinion, the manuscript can be published, but some corrections are needed.

Author Response

January 22^st, 2024

Dr. Jukka Jokimäki

Editor-in-Chief

Birds

Dear Dr. Jokimäki

We wish to submit a revised version of an article entitled “Current Knowledge of Helminths of Wild Birds in Ecuador” for consideration by the Journal of Birds.

Sincerest thanks for your response on the manuscript. We appreciate the valuable and useful contribution made by the reviewers, which definitely helped to improve the manuscript.

Please find in the next section the point-by-point responses to reviewers’ comment.

We look forward to hearing from you regarding our submission. We would be glad to respond to any further questions and comments that you may have.

Thank you for your consideration.

Reviewer #2:

Why was the literature search limited to only two databases? Why the authors did not look for information in the most well-known databases Web of Science and Scopus?

We agree with the reviwer´s comment. Web of Science and Scopus Databases have been included in the systematic search.

The map still needs to be redone. The Galapagos Islands should be located where they should be - to the left of the mainland.The map should also have a scale. And it is better to place the names of provinces on the map.

Changes have been made accordingly

The authors provide information about helminths found in birds of Ecuador in the form of a table, but the Discussion does not contain an analysis of this data. What are the most common parasite species (families, classes) in birds of Ecuador? Are host-specific parasites identified or are the identified parasite species broadly specific? Common geographical distribution of detected helminths. Do helminths found in birds have veterinary or medical significance as potential pathogens? Etc.

Table 1 needs to be redone. The first and second columns should be combine to “Helminth species”, where family name of helminths and phylum namewill appear above the species name:

Cestoda

Hymenolepididae

Hymenolepis nana (Weinland, 1858)

Column title “Site in Host” better fix it to “Localization” or “Site of infection”.

In column “Host species” only the Latin names of birds should be left. In scientific articles, try not to use common animal names, please use only Latin.

We appreciate reviewer’s comment. To follow the editor´s suggestion, common names have been kept in table, but the order of information has been updated.

Please check Table 1. Especially with regards to the Latin names of helminths. For example, correct name of the parasites –Hymenolepis nana (Siebold, 1852), Cyclocoelum tringae (Stossich, 1902). Check all Latin names.

We appreciate the reviewer[s comment. Latin names of helminths and their authoritative references were in accordance the the Global Biodiversity Information Facility (https://www.gbif.org/). In this sense, it appears as Cyclocoelum tringae (Brandes, 1892). Nevertheless, parasites names were re-check according to the GBIF web page.

Cyclocoelum obscurumis mentioned twice. Perhaps you should combine data. Also check use of italics; typos (Tringa solitaria (Wilson, 1813) (Wilson, 18132)) .

Changes have been made accordingly

According to the rules of International Code of Zoological Nomenclature (ICZN), only one author is given after the Latin name. For example, Cyclocoelum obscurum(Leidy, 1887).

Changes have been made accordingly

Information from lines 114-116 should be included to the Abstract.“Thirty-six helminth taxa” looks wrong. So how many sources did you find on the topic - 17 (line 106) or 19 (line 171)?

We appreciate the reviewer’s comment, and we have revised sections accordingly.

And some small remarks: In key words – “Animals” are unnecessary. This keyword need be deleted.. Please provide references in the text and in Table 1 in regular font, not superscript. Subsections in Materials and Methods should be numbered as in Results. And write words in capital letters (1. Database Search) Line 185 – Please, make reference according to MDPI journal rules. Authors contribution. Please, use only name initials here. In my opinion, the manuscript can be published, but some corrections are needed.

We appreciate the reviewer’s comment, and we have revised sections accordingly.

Author Response File: Author Response.pdf

Round 2

Reviewer 1 Report

Comments and Suggestions for Authors

The manuscript has improved considerably after the revisions of the Editor and Reviewers, especially concerning the PRISMA methodology and exposition of results. Some minor changes, together with those pointed out by the second reviewer, need to be addressed before the acceptance:

- Ln 35: Remove the second "still".

- Ln 36: helminth species instead of helminth diversity

- Ln 80: Remove i.e.

- Ln 104: include a space before [32]

- Ln 114: write as Fig. 1

- Ln 115: Reviewed literature was published and was carried out

- Ln 134: at family level

- Ln 140: from which 9 are endemic in Ecuador.

- Ln 152: sample sizes ranging from 1 to 68...

- Ln 153: remove oscillated

- Ln 154: add ranging

- Ln 156: latin name S. mendiculus

- Ln 158: also add ranging

- Ln 206: Change to: "This highlights the need for more research on helminths parasitizing wild birds in Ecuador".

- Ln 208: a peer-review process

- Ln 209: put in number (40)

- Ln 226: remove both

- Ln 229: insert a space before [10]. Also, better to define "Host immunosupression".

- Ln 231: with stressful and overcrowding conditions

- Ln 237: add a comma after conditions

- Ln 260: add a comma after sense

Author Response

Dr. Jukka Jokimäki

Editor-in-Chief

Birds

Dear Dr. Jokimäki

We wish to submit a revised version of an article entitled “Current Knowledge of Helminths of Wild Birds in Ecuador” for consideration by the Journal of Birds.

Sincerest thanks for your response on the manuscript. We appreciate the valuable and useful contribution made by the reviewers, which definitely helped to improve the manuscript in this final version.

We have modified the paper in response to the reviewers’ comments. Please find revised text highlighted in red color.

Please find in the next section the point-by-point responses to reviewers’ comment.

We look forward to hearing from you regarding our submission. We would be glad to respond to any further questions and comments that you may have.

Thank you for your consideration.

Reviewer #1:

- Ln 35: Remove the second "still". Ln 36: helminth species instead of helminth diversity. Ln 80: Remove i.e. Ln 104: include a space before [32]. Ln 114: write as Fig. 1. Ln 115: Reviewed literature was published and was carried out. Ln 134: at family level. Ln 140: from which 9 are endemic in Ecuador. Ln 152: sample sizes ranging from 1 to 68... Ln 153: remove oscillated. Ln 154: add ranging. Ln 156: latin name S. mendiculus. Ln 158: also add ranging. Ln 206: Change to: "This highlights the need for more research on helminths parasitizing wild birds in Ecuador". Ln 208: a peer-review process. Ln 209: put in number (40). Ln 226: remove both. Ln 229: insert a space before [10]. Also, better to define "Host immunosupression". Ln 231: with stressful and overcrowding conditions. Ln 237: add a comma after conditions. Ln 260: add a comma after sense.

We agree with the reviewer and have revised sections accordingly.

Author Response File: Author Response.pdf

Reviewer 2 Report

Comments and Suggestions for Authors

The article by Ecuadorian colleagues has become much better. But there were (and still appeared) minor errors:

1. Lines 23,129 – It would be more correct to write it like this: “Nematodes of the genus Ascaridia Dujardin, 1844 …”

2. correct writing: “… the Rock pigeon Columba livia Gmelin, 1789 …” And there is no need to put the Latin name in parenthesis here. The same corrections need to be made in lines 141-147.

3. According the rules of MDPI all words in names of subsections must be capitalized: “2.1. Database Search; 2.2. Study Selection, etc.”

4. A paragraph cannot consist of one sentence (129-131). Therefore, such single sentences must be attached above or below.

5. correct writing: “… Onchocercidae gen. sp. …” (Line 156)

6. In Table 1 – Please, follow the International Code of Zoological Nomenclature: Only one Author!

Selfcoelum brasilianum (Stossich, 1903) without Dronen & Blend

Lubens lubens (Braun, 1901) without Travassos

Zonorchis delectans (Braun, 1901) without Travassos

After correcting these minor errors, the article is ready for publication.

Author Response

Dr. Jukka Jokimäki

Editor-in-Chief

Birds

Dear Dr. Jokimäki

We wish to submit a revised version of an article entitled “Current Knowledge of Helminths of Wild Birds in Ecuador” for consideration by the Journal of Birds.

We have modified the paper in response to the reviewers’ comments. Please find revised text highlighted in red color.

Please find in the next section the point-by-point responses to reviewers’ comment.

We look forward to hearing from you regarding our submission. We would be glad to respond to any further questions and comments that you may have.

Thank you for your consideration.

Reviewer #2:

The article by Ecuadorian colleagues has become much better. But there were (and still appeared) minor errors:

Lines 23,129 – It would be more correct to write it like this: “Nematodes of the genus Ascaridia Dujardin, 1844 …” correct writing: “… the Rock pigeon Columba livia Gmelin, 1789 …” And there is no need to put the Latin name in parenthesis here. The same corrections need to be made in lines 141-147. According the rules of MDPI all words in names of subsections must be capitalized: “2.1. Database Search; 2.2. Study Selection, etc.” A paragraph cannot consist of one sentence (129-131). Therefore, such single sentences must be attached above or below. correct writing: “… Onchocercidae gen. sp. …” (Line 156). In Table 1 – Please, follow the International Code of Zoological Nomenclature: Only one Author! Selfcoelum brasilianum (Stossich, 1903) without Dronen & Blend Lubens lubens (Braun, 1901) without Travassos Zonorchis delectans (Braun, 1901) without Travassos. After correcting these minor errors, the article is ready for publication.

We agree with the reviewer and have revised sections accordingly.