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Article
Peer-Review Record

Diverse Host Spectrum and the Parasitic Process in the Pantropical Hemiparasite Cassytha filiformis L. (Lauraceae) in China

Diversity 2023, 15(4), 492; https://doi.org/10.3390/d15040492
by Zhi-Fang Liu 1,2,3,4,*, Xiu-Qin Ci 4,5, Shi-Fang Zhang 4,6, Xiao-Yan Zhang 4,6, Xue Zhang 7, Li-Na Dong 8, John G. Conran 9 and Jie Li 4,5,*
Reviewer 2: Anonymous
Reviewer 3:
Diversity 2023, 15(4), 492; https://doi.org/10.3390/d15040492
Submission received: 2 February 2023 / Revised: 20 March 2023 / Accepted: 24 March 2023 / Published: 27 March 2023
(This article belongs to the Special Issue Ecology, Evolution and Diversity of Plants)

Round 1

Reviewer 1 Report (Previous Reviewer 2)

This revised manuscript is much improved. Greater detail in methods and editing of additional content has increased the readability and value of the study. There are still some points of ambiguity that need to be addressed and grammar or wording choices to be corrected. Some (but not all) of the language issues have been noted in the pdf with, in some cases, suggested re-wording. It is imperative that the authors carefully evaluate the comments for accuracy.

 

Comments for author File: Comments.pdf

Author Response

Reviewer#1

This revised manuscript is much improved. Greater detail in methods and editing of additional content has increased the readability and value of the study. There are still some points of ambiguity that need to be addressed and grammar or wording choices to be corrected. Some (but not all) of the language issues have been noted in the pdf with, in some cases, suggested re-wording. It is imperative that the authors carefully evaluate the comments for accuracy. 

RESPONSE: Thank you very much for your appreciation of our article. Now we have revised the manuscript according to your notes and comments in the pdf and we have checked our grammar and wording choices with the English native speaker (One of our co-authors John G. Conran). Details can be seen as below.

  1. Parasitic plants have a diverse group of 292 genera approximately 4750 species (1% 33 of all flowering plants) with parasitism evolving at least 12 times [1,2].

RESPONSE: Thanks. We have revised this sentence as “Parasitic plants are a diverse group of 292 genera, approximately 4750 species (1% 33 of all flowering plants) with parasitism evolving at least 12 times.” Page 1, lines 37-38.

  1. This is now much clearer.

RESPONSE: Thanks.

  1. …seeds collected site, as here is the only place that has ripe fruit, when we do sample collections.

RESPONSE: Now we modified the sentence as “…, , but the Guangzhou locality (Zhongkai University of Agriculture and Engineering) was the only one with ripe fruit, despite repeated site visits.” Page 3, lines 112-114.

  1. Much more informative.

RESPONSE: We appreciate your suggestions. Giving more information can illustrate the figure much clear. wehave added the collection longitude, latitude and altitude in the notes, details as “Figure 1. Representative inflorescence and fruits of Cassytha filiformis. a, inflorescences collected in Guangzhou (Guangdong, longitude: E113°17′, latitude: N23°0′, altitude: 10 meter). b, inflorescences collected in Xishuangbanna (Yunnan, longitude: E100°45′, latitude: N22°28′, altitude: 1129 meter). c. inflorescence and unripe fruits collected in Lingshui (Hainan, longitude: E109°54′, latitude: N18°34′, altitude: 76 meter). d. ripe fruit collected in Guangzhou (Guangdong, longitude: E113°17′, latitude: N23°0′, altitude: 10 meter). Scale bars = 5 mm.” Pages 3-4, lines 127-132.

  1. The treated seeds were then grown to the soils which collected in Guangzhou…

 

RESPONSE: Now we revised the sentence as “The treated seeds were then grown in the soils that were collected in Guangzhou…” Page 4, lines 139-140.

 

  1. Because you make a point of noting parasitism of woody vs. nonwoody hosts below, it would be helpful here to indicate which of these hosts are woody.

 

RESPONSE: We appreciate the reviewer for providing this insight. We have added the types of the hosts. Details as Host seeds (Bidens pilosa L. (Asteraceae) herb, Chromolaena odorata (L.) R.M.King & H.Rob. (Asteraceae), herb, Cleome rutidosperma DC. (Cleomaceae), herb, Dimocarpus longan Lour. (Sapindaceae), tree, Mikania micrantha Kunth (Asteraceae), liana, and Scoparia dulcis L. (Plantaginaceae), herb)…” Page 4, lines 143-147.

 

  1. The new section from lines 140 to 150 is still confusing. Is this a fair re-statement through line 144?: ... were also collected from the sites of C. filiformis seed collection, Guangzhou (...). These six species were confirmed as hosts of C. filiformis based on field observation of haustoria. We filled pots (18 cm diameter, 16 cm height) with soil collected from these field sites and sowed a minimum of five seeds of a single species per pot. There were 3 pots per host species for a total of 18 pots. 

RESPONSE: We appreciated your suggestions and have revised this part, details as … were also collected from the sites of C. filiformis seed collection, Guangzhou (Zhongkai University of Agriculture and Engineering, Guangdong). These six species were confirmed as hosts of C. filiformis, based on field observation of haustoria. We filled pots (18 cm diameter, 16 cm height) with soil collected from these field sites and sowed a minimum of five seeds of a single species per pot, with three replicate pots per host species for a total of 18 pots. Hosts were observed at the same time each day (10 a.m.) in each pot once germination had commenced.” Pages 4-5, lines 147-153.

 

  1. "Trafficking" does not seem to be the best term here. Perhaps "interplay" or "interaction" would be more precise.

RESPONSE: Thanks for your suggestions and we have changed the word “trafficking” to “interaction”. Page 5, line 154.

 

  1. It is not clear when the C. filiformis was introduced? As seeds? Seedlings? Is the following a fair restatement of 145 to 150?: to investigate the process of host acquisition we introduced a single C. filiformis (seed? seedling?) to each of the 18 pots of single-host species (hosts were seeds or seedlings? If seedlings, how old?) and grew them under controlled conditions in a PHCbi CO2 incubator (18 h light, 6 h dark) at 24-27 C (for how long? What observations were made?).

 

RESPONSE: We appreciated your suggestions and have revised this part, details as… five seeds of C. filiformistogether to form host–laurel dodder parasitization system. This system was cultivated under controlled conditions in PHCbi CO2 Incubator (18 h light, 6 h dark) at 24–27 °C. From germination to growth conditions, C. filiformis as well as hosts were observed at the same time each day (10 a.m.) in each pot.” Page 5, lines 157-161.

 

  1. using two methods of classifying species: (1) life history (woody or herbaceous), and (2) ...

 

RESPONSE: Thanks for your suggestions and we have changed them. Page 5, line 164.

 

  1. We recorded the

 

RESPONSE: Thanks for your suggestions and we have changed. Page 5, line 165.

 

  1. dodder as well as the hosts the percent germination exceeded 80%.

 

RESPONSE: We appreciated your suggestion and have revised this part, details as “For the laurel dodder as well as the hosts the percent germination exceeded 80%.” Page 5, line 181.

 

  1. Lines 175-177 are not clear. Did it take 8 weeks for parasitism to occur following germination (of the host or of the parasite?) or did the C. filiformis vine require 8 weeks following first contact to form haustoria? Line 176 sounds like the same C. filiformis vine that is attacking M. micrantha is also connecting to C. rutidosperma.

 

RESPONSE: Here means “eight weeks for parasitism to occur following germination of the host liana species M. micrantha (Fig. 3d). And then the same C. filiformis vine that is attacking M. micrantha (Asteraceae) is also connecting to herb species C. rutidosperma (Cleomaceae) a month later (Fig. 3e–h)”. I hope it is clear now. Page 5, lines 187-190.

 

  1. If the suggested revision above is correct, there were three replicates for each host species. Can you be more quantitative? Average (+sd) days to germination of parasite, of host, and average days to first haustorium for each species?

 

RESPONSE: We appreciate the reviewer for providing this insight. We have added the contents, details as “The average time to germination of C. filiformis was 21 days (± 18–24 SD) and for the host species: M. micrantha (3 ± 3–4), B. pilosa (5 ± 4–6), C. odorata (5 ± 4–6), C. rutidosperma (7 ± 6–8), S. dulcis (8 ± 7–9), and D. longan (21 ± 20–22).” Page 5, lines 181-184.

 

  1. Table S1 (third tab) is very useful. It looks like some of the counts in the first column are not correct.

 

RESPONSE: Thanks for your suggestions and we have changed.

 

  1. host species

 

RESPONSE: Changed. Page 6, lines 217-218.

 

  1. The word "generalist" should apply to the parasite rather than the host. I think you mean C. filiformis is a generalist hemiparasite that is associated with many host species that are relatively common.

 

RESPONSE: Yes, exactly. Now this sentence changed as “This confirms that C. filiformis is a generalist hemiparasite that is associated with many host species that are relatively common…” Pages 7-8, lines 248-249.

 

  1. In this discussion of host ranges are you referring to the differences observed in your study vs. Zhang et al.? Please clarify.

 

RESPONSE: Thanks for your suggestions and we have added the comparison between them, details as “Four angiosperm families had at least 10 hosts species (Table S1): Rubiaceae (12), Lauraceae (11), Phyllanthaceae (11) and Asteraceae (10). These results differ from the study of Zhang et al. [6], where they reported seven families at world level with at least 10 host species: Anacardiaceae, Asteraceae, Euphorbiaceae, Fabaceae, Myrtaceae, Phyllanthaceae, and Rubiaceae.” Page 7, lines 243-247.

 

  1. corresponding

 

RESPONSE: Changed. Page 8, lines 255-256.

 

  1. This needs some re-wording. Perhaps the following: This study investigated the host range of C. filiformis over major areas of its geographic range in China and reported observations of germination and parasitism of selected host species.

 

RESPONSE: Thanks. We have modified the sentence as your suggestion, details see “This study investigated the host range of C. filiformis over major areas of its geographic range in China and reported observations of germination and parasitism of selected host species.” Page 10, lines 325-327.

Author Response File: Author Response.docx

Reviewer 2 Report (Previous Reviewer 3)

Manuscript "Diverse host spectrum and the parasitic process in the pantropical hemiparasite Cassytha filiformis L. (Lauraceae) in China"

by Zhi-Fang Liu, Xiu-Qin Ci, Shi-Fang Zhang, Xiao-Yan Zhang, Xue Zhang, Li-Na Dong, John G. Conran, Jie Li in its present form contains the necessary corrections. Comments have been removed in general.

However, this does not apply to the design and quality of Figure 5.

The drawing needs to be improved to be readable. You should especially pay attention to the signatures in the circle - their resolution does not allow you to understand what is written there, either when enlarged or when using special software. It is unacceptable.

If corrected, the article may be published.

Author Response

Reviewer#2

Manuscript "Diverse host spectrum and the parasitic process in the pantropical hemiparasite Cassytha filiformis L. (Lauraceae) in China"

by Zhi-Fang Liu, Xiu-Qin Ci, Shi-Fang Zhang, Xiao-Yan Zhang, Xue Zhang, Li-Na Dong, John G. Conran, Jie Li in its present form contains the necessary corrections. Comments have been removed in general.

1. However, this does not apply to the design and quality of Figure 5.

The drawing needs to be improved to be readable. You should especially pay attention to the signatures in the circle - their resolution does not allow you to understand what is written there, either when enlarged or when using special software. It is unacceptable.

If corrected, the article may be published.

RESPONSE: Thank you very much for your appreciation of our article. We appreciate your comments. Now we have redone Figure 5 and enlarged the fonts for species names etc. I hope the quality of Figure 5 is clear now.

Author Response File: Author Response.docx

Reviewer 3 Report (New Reviewer)

I consider that:

It would be important to indicate on a map the regions studied (for foreign readers it is difficult to locate the regions).

It is necessary to indicate the voucher number of the specimens.

It could be included, to complete the bibliographic information,

Parra-Tabla, V., Tun-Garrido, J., García-Franco, J., & Martínez, M. (2023). The recent expansion of the invasive hemiparasitic plant Cassytha filiformis and the reciprocal effect with its main hosts.

Author Response

Reviewer #3

I consider that:

  1. It would be important to indicate on a map the regions studied (for foreign readers it is difficult to locate the regions).

RESPONSE: We appreciate the reviewer for providing this insight. We have added the provinces of our collection sites in Fig S1.

  1. It is necessary to indicate the voucher number of the specimens.

RESPONSE: Yes, we have the voucher number of the specimens in Table S1, please check, thanks.

  1. It could be included, to complete the bibliographic information, 

Parra-Tabla, V., Tun-Garrido, J., García-Franco, J., & Martínez, M. (2023). The recent expansion of the invasive hemiparasitic plant Cassytha filiformis and the reciprocal effect with its main hosts.

RESPONSE: We appreciated your suggestion. Now we have added this bibliographic information in our study, details see “… and Parra-Tabla et al. [45]” Page 9, line 261. And “That is different from Parra-Tabla et al., who studies the host of C. filiformis distributed in the coastal dunes of Yucatan. They claimed the frequency of parasitized plants by C. filiformis was not dependent on host plant abundance [45]. Pages 9-10, lines 306-309 and the reference in page 15, lines 464-466.

Author Response File: Author Response.docx

This manuscript is a resubmission of an earlier submission. The following is a list of the peer review reports and author responses from that submission.


Round 1

Reviewer 1 Report

 1. The introduction is superficial. You should have reviewed the findings of previous papers dealing with the host range of Cassytha and explain why would be the newly expected results from China interesting. You could have mentioned more about Cuscuta, with whom Cassytha shares a striking phenomenon of convergent evolution of stem parasitism. There are multiple recent studies in Cuscuta using network analysis to describe the host range.

2.1. Plant materials

1. What is exactly the herbarium material that was used to extract the diversity host data? Three general sources are cited for the data, but no details. Looking over these herbarium specimens, most do not have any host present on the sheet or recorded in the labels, so how many herbarium specimens were actually used in this study? You should provide a detailed list of the herbarium specimens used for each host data entry. Sometimes Cassytha is mistaken for Cuscuta and having a clear herbarium voucher list would allow future researchers to verify and perhaps make corrections to the host range presented.

You could add for each host the specimen information:

Location

Collection date

Collector & number

Herbarium

Host family

Host genus

Host species

Honk-Kong

27 Sep 1972

Shiu Ying Hu 12162

GH, PE

Anacardiaceae

Rhus

chinensis

Honk-Kong

27 Sep 1972

Shiu Ying Hu 12162

GH, PE

Lauraceae

Litsea

glutinosa

 How were the hosts identified? Or did you use the identifications of the hosts provided in the herbarium labels? If yes, how were these identities verified? Once you have all this in a spread sheet, you could calculate the frequency of occurrence of particular host families, genera and species within the total host range. See this paper:

Costea, M., ElMiari, H., Farag, R., Fleet, C. and Stefanović, S., 2020. Cuscuta sect. Californicae (Convolvulaceae) revisited:‘cryptic’speciation and host range differentiation. Systematic Botany, 45(3), pp.638-651.

 2.2. Data analysis

Trimming down from a larger tree is not an “analysis”. Even if had been constructed from Genbank data, what is actually the purpose of this tree?

Results

3.2. I don’t know why results of the host from outside China are presented in this section, which should only include the results in the present study.

Your tree looks impressive, but it actually doesn’t show anything that could not have been inferred directly from APG IV.

Discussions

Section 4.1. Orobanchaceae have a completely different biology as root parasites. I suggest trying to compare with Cuscuta which is much more similar.

Section 4.2. “The effects of parasitic plants” doesn’t have anything to do with the results of this article. This part can be entirely deleted.

 

 

Reviewer 2 Report

This study by Zhi-Fang Liu et al. examines the host range and phylogenetic relationship among hosts of the vining hemiparasite Cassytha filiformis.  The approach is primarily qualitative observation although an experiment on germination is noted. Compared to other vining parasites of plants, e.g., species of Cuscuta, less if known of the taxonomic relationships and physiological interplay between C. filiformis and host plants. This manuscript makes use of existing records in addition to the new records described here to broaden our knowledge of a species with important economic and ecological impact.

The main contribution would be the information summarized in Figs. 4 and 5. The taxonomic breadth of hosts and their range of life forms is notable.  It seems likely that the authors could mine more from their data, both from their own field records and the full set including records from other studies.  Will these data be made available to other scholars?

Unfortunately, the manuscript has a number of shortcomings which are detailed below. The goals of the paper are not well written and not entirely achieved.  Overall, more detail is needed for methods in the field and lab. Examination of germination is called an experiment but no hypothesis or predictions are provided and details of the methods are not clear. Thus it is likely the results are overstated.  Below are specific points.

In the fourth sentence of the Introduction, it is not clear which partner could experience stabilizing selection. This idea needs to be developed more if it is central to the paper. Otherwise remove this sentence.

 

Use of the words host and parasite need some clarification. Just to be clear from an ecological perspective, a plant is a parasite if it forms functional haustoria to the detriment of the parasitized plant (host), i.e., the parasite benefits as it reduces the performance of the host. Benefit and harm are not assessed in this study and so the focus is on putative hosts.

 

Is goal #1 to determine how many species of plants in China are parasitized by C. filiformis? Or, how many of the known hosts of C. filiformis are parasitized in China? For goal #3, why would a species be considered a host if it does not improve or impact the survival and performance compared to no host? Perhaps the question should be "are some parasitized species qualitatively better hosts?"?

 

The photographs are very good, but please provide a physical description and life history of the species in the text, either when C. filliformis is first introduced or in the Methods. Also in Fig. 1, can the scale for the photos be included or described?

What do the resources in lines 81-84 actually indicate? i.e., do they give precise locations for where C. filiformis had been observed?  Were all the C. filiformis that were encountered evaluated for putative hosts or was there a sampling regimen (e.g., random points along transects)? When flowers and fruits were collected, were the hosts identified, and were all hosts species bearing reproductive C. filiformis similarly sampled?

The first paragraph of the Methods needs to provide more information. How many sites are shown on the map? Does this collection area match the geographical distribution of the hemiparasite?

The work on germination needs more detail. From how many separate sites were seeds collected? Did each pot have one C. filiformis seed or were all 10 in the same pot? If this is an experiment, what constitutes a replicate? The photos of Fig. 3 show host plants and the text indicates “… were germinated simultaneously with C. filiformis.” Does this mean hosts were in the germination pots? If so, how were these hosts included, and were any pots with no host? How big were the pots? Did all seeds eventually germinate or was there a cut-off date? Why were these species selected as hosts? How were these data analyzed? Please include the family name for each host species.

The description for letter c in Figure 3 needs to be revised. Do you mean "dead Cassytha filiformis" and are they shown unsuccessfully parasitizing a viable host? What does the red arrow indicate? It is difficult to make out which vine is the parasite and which is the host in figures e-h.

Where are the results of the germination experiment? What percentage of hemiparasite seeds germinated with each host? How many successfully parasitized each host? Was there a window of opportunity for parasitism to take place before the host was no longer susceptible? Is a host even needed?

Lines 135-136 suggest a growth response of the hemiparasite to plant characteristics as well as the environment but neither of these factors were actually tested. A more conservative statement would be that the hemiparasite was most commonly observed on such plants and in such habitat, if that is indeed the case. These percentages are repeating what is found in Table 1. The table is useful for organizing the information and so the text can focus on the important comparisons.

In line 136 "Attacked" is imprecise. Do you mean "produced well-formed haustoria"?

In line 137-138, the language needs to be more precise. Does the percentage mean 84.49% of all hosts, defined by the presence of haustoria, were woody taxa? Or were 84.49% of woody taxa parasitized?

What is a shrub host ratio? For example, Is 36.9% for China the percent of all hosts that are shrubs? Host range is typically expressed as sums (not percent or ratios). It might be more informative starting with line 139 to express host range as the number of hosts that are trees, shrubs, etc. and determine how many unique hosts there are across all geographic areas.

Fig. 4, Provide more description. What does green indicate? Shouldn’t the last word of the caption be “hosts”?

Fig. 5 caption could be more descriptive.

Line 173-174, where was degree of benefit demonstrated?

Line 176, "host preference" is not an accurate description. Unless host availability is controlled and host selection is then confirmed, there is no way of knowing if the hemiparasite "prefers" a particular host.

Line 178, what is a "large-scale hemiparasite"? Does this mean broad geographic range or broad host range, perhaps?

Remove the work "While" in lines 192, 196, and 233.

Comments for author File: Comments.pdf

Reviewer 3 Report

Manuscript "Diverse host spectrum and the parasitic process in the pantropical hemiparasite Cassytha filiformis L. (Lauraceae) in China" by authors Zhi-Fang Liu, Xiu-Qin Ci, Shi-Fang Zhang, Xiao-Yan Zhang, Xue Zhang, Li- Na Dong, John G. Conran, Jie Li presents an original botanical study of interactions with other species and parasitism of Cassytha filiformis. This study was performed correctly and demonstrates the features of the distribution of this species and the possibility of its further study. This work has both applied and fundamental significance. The text of the manuscript does not contain all the necessary parts, it is required to add the resulting conclusion. The literature review and discussion is correct, although it does not contain some of the old references and the evolutionary aspect.

There are still some shortcomings of the work, for example, there are no rulers in the photographs, which does not allow judging the size, which is important for photographs taken with magnification - this should be corrected (Figure 1, Figure 2 C). Also, the resolution in Figure 5 should be improved, since the inscriptions are not readable.

After correcting these issues, the article can be accepted.

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