The Life and Death of Jamoytius kerwoodi White; A Silurian Jawless Nektonic Herbivore?

Round 1

Reviewer 1 Report (Previous Reviewer 1)

All my comments have been feedback

Author Response

Does not seem to be anyting I need to comment on from this reviewer

Reviewer 2 Report (Previous Reviewer 3)

Please see the attached file

Comments for author File: Comments.pdf

English is good though some punctuation needs fixing. 

Author Response

My comments are in bold below the notes. I would like to acknowldge the this ourstandingly helpful and constructive review in my acknowldgements, but though the reviewer ticked the 'would like to sign box', their name was not on the review. I have left a blankt to fill it in in the paper, please add.

Review of Brookfield manuscript for Fossils, The life and death of Jamoytius.

Review of the revised version, Dec. 31, 2023:

This version is improved, and I appreciate how the author followed most of my suggestions.  I especially appreciate how he read and cited much more of the Jamoytius literature, and the additional geology made the manuscript even more interesting (e.g., in Fig. 8). I detected some difficulty in integrating all the new Jamoytius information into a consistent story, so below I suggest ways to correct this.  Also, I still think the comparisons with nonparasitic lampreys are too misleading and confusing, because such lampreys do not even feed in this “adult” stage of their lifecycle. They also, unlike Jamoytius, live in streams far from any ocean. I ask again that they be entirely removed from the text, although the brook lamprey illustration in Figure 4B could still remain. One more point is that there are still too many small mistakes in spelling, labeling, commas, etc., so I hope the next draft can be fully polished.

Here are my line-by-line suggestions.  Some point out contradictions and errors, but others are my own interpretations, mostly of Jamoytius feeding, which need not be followed if the author disagrees with them.

Line 8: expand “detritus” to “detritus-feeding.” OK

Line 11: probably should add filter feeder as a third possibility, because you say that in the following line 13, as “microphagous filterers.”

 I have changed to detritivores or herbivoes as I no longer consider filet feeding a possibility

Line 24: remove “the” from “of the even.” OK

Line 28: Miyashita, not Miyashiro.  OK

Line 30: Reeves, not Reves. OK

Line 35: with, not wuht. OK

Figure 2A is cut off at the bottom; unminerlized is misspelled, and “basal support of dorsal fin” should go above “not interpreted” rather than below it. OK changed

Lines 45-61.  This paragraph has problems.  The sentence in lines 53-55 about Paleozoic lampreys lacking toothed discs is wrong because both Priscomyzon and Pipiscius had them (see the Miyashita et al., 2021 paper). This fact invalidates the body-size comparisons in lines 45-50 because the Paleozoic lampreys were both parasitic and small (about 5 cm), meaning that large does not mean parasitic, as was claimed. Also, line 55 says the Paleozoic lampreys were not parasitic but grazers, yet line 52 contradicts that by saying they were parasitic. I suggest avoiding these problems limiting this to Jamoytius’s possible relatives, a theme you continue through the next two paragraphs.  Here is my suggested revision:

I have rewritten this paragraph to account for this comment , not exactly following the recommendted changes, because I have changed my views on Paleozoic lampreys which from observations on their teeth (weak) may have been grazers or scavengers.

Jamoytius bears some resemblance to living lampreys (Fig. 4), with its elongated eel-like body, unjointed branchial basket, and (nearly) unarmored body.  Thus, it has been compared to adult lampreys that are parasitic (Ritchie, 1968??). It is difficult to pin down a true phylogenetic link to lampreys, however, because the fossil record for early lampreys is scanty.  Only four undoubted parasitic lamprey species have been recorded, Priscomyzon from the Devonian (360Ma) and three from the Carboniferous (306Ma) (Miyashita et al., 2021). Furthermore, the post-Paleozoic fossil record of lampreys is equally bad. Based on both . . . [as written] . . . carnivorous lampreys evolved from noncarnivorous early Paleozoic forms (pre-lampreys) and then radiated from the late Cretaceous (~100Ma) and especially from Miocene times (~25Ma) onwards [again, no need to bring up the nonparasitic brook lampreys]. 

Lines 63 and 64. Not Loganiella but Loganellia. OK

Lines 67-70. Sentence is so long and tortured.  Here is my suggested replacement:

Jamoytius is often classified as the sister taxon of the Upper Devonian fish, Euphanerops longaevus (Fig. 3C; Reeves et al., 2023), even though many of the structures in the available fossils remain unexplained (Janvier and Arsenault, 2007).   OK. But Reeves et al 2003 is on Lasanius, not Jamoytius

Line 78: lifestyles not life styles. OK

Line 84: ranging in size from 14: remove “in size.” OK

Line 89: add reference to Figure 2 as follows: “. . . encircles the very small mouth (seen as 0.5 to 0.7 mm in diameter in Fig. 2).”  Doing so will prepare us for later when you mention the holes in Dictyocaris, which are about the same size. OK

Line 90:  Ritchie mistakenly homologized the oral ring of Jamoytius, with the pre-oral annular ring that supports the sucker of lampreys (see Fig. 11 in Mallatt 2023).  Therefore his conclusion that Jamoytius had a parasitizing sucker was dead wrong, and you don’t need to refute it with the no-teeth argument.  And can remove, “which together suggested that it was an ancestral parasitic lamprey (Ritchie, etc.).” OK

Lines 91-94: this statement would also rule out any “teeth” on the tip of a tongue but later you suggest a lamprey-like tongue that would have used such lingual teeth to procure food. I don’t think you want to do that. You already allowed the possibility of an unpreserved tongue in the Jamoytius fossils, so you can also allow for unpreserved teeth of keratin on its tip.  You spoke of algae-scraping grazing back in line 55, which implies you do support this idea of tongue-teeth.

To avoid the problems, I would rewrite lines 89-94 of the paragraph to read:

. . . encircles the very small mouth (seen as 0.5 to 0.7 mm in diameter in Fig. 2).[Delete a lot from here and proceed from Line 94, as . . .] The controversy about whether this mouth was anterior terminal or subterminal ventral seems to be resolved . . .[to end of line 98, as written]

Lines 99-104:  I suggest that this whole paragraph be shortened to:

The anterior, oropharyngeal region of Jamoytius has room ventrally for a piston-like “tongue” comparable to that of living lampreys (Mallatt, 2023). The tip of this lamprey tongue has toothed plates that grasp and cut food. OK, but I do not think Jamoytius had any teeth – if keratin they would be preserved – have made note on this – keratin is the third most commonly part of vertebrates to be preserved, after bones and teeth.

That is, I would transfer the consideration of the feeding mechanism on soft vegetation from here in lines 101-104 to the first paragraph of the Discussion (see below). OK

Lines 111-123: as I said above, these ideas that Jamoytius was like nonparasitic lampreys, and that the latter evolved into the parasitic lampreys, seem highly likely. How could a lamprey species with a nonfeeding adult and a regressed intestine evolve into one with a feeding adult?  The consensus among lamprey biologists is that parasitics only evolve into nonparasitics, not vice-versa, so parasitism came first in lamprey history.  See Docker, 2009. A review of the evolution of nonparasitism . . . The parasitic suckers of fossil Priscomyzon and Pipiscius also speak of parasitism-first.  I would replace this whole paragraph with this simpler version:

The consensus only applies to post-Mesozoic forms – pre-Mesozoic lampreys do not have the feeding structures of those. All pre-Jurassic lampreys are assigned non-parasitic predatory (I would say scavenger) modes of life.

Its relatively small mouth and lack of jaws and a sucker indicate that Jamoytius did not feed on large prey or parasitize fish.  Its streamlined body shape suggests it was a good swimmer. The comparable agnathans have terminal anterior mouths that do not appear to be protrusible (Fig. 5). Such mouths are often found among omnivorous midwater-feeding fish, which eat anything available by grabbing bits of food as they move (Oleh, 2018). Given Jamoytius’ simple, round mouth opening, nektonic suspension feeding cannot be ruled out, but I prefer to focus on the possibility of a lamprey-like tongue to procure food. More on this in the Discussion.

Line 141: remove one of the commas after 2016. OK

Line 144: after mudstones, add “belonging to the Priesthill Group.” OK

Line 147: period goes after 1998) not after facies OK

Line 152: add period after 1998). OK

Line 155: . . . the phyllocarid Ceratiocaris. Most modern phyllocarids . . . OK

Line 166: contrasts, not contrast. OK

Figure 8B and line 183:  the legend tells of organic-rich silt cap and varve layers, but I cannot see them. Please add labels to the figure to show them. OK added to figure

Line 199: the, not he. OK

Line 220: lists, not list. OK

Line 224: instead of “which error” say “an error that” OK

Line 230: delete “yet” and add “dubiously” before “attributed.” OK

Line 234: Ainiktozoon not Anitkozoon. OK

Table 1, lines 239-263: the entries in the middle column do not align, nor do those in the left column. OK changed

Lines 269-270:  this phyllocarid is not a shrimp so the shrimp diets in Albertoni + Walker do not apply.  It is hard to find what phyllocarids eat on Google.  One source I found said they eat shrimps, fish, carcasses, and meat. OK added  a note on living phyllocarids

Lines 288-296: the point was not getting across that Dictyocaris was originally thought to be an arthropod.  So I suggest this change on line 291: OK

. . . of Jamoytius. Dictyocaris specimens were originally thought to be large arthropod carapaces (Stormer, 1935), and Ritchie (1963) proposed the holes were parasitic injuries from Jamoytius mouths. However, Dictyocaris is never found even partially articulated [as written, to Line 295] . . . seems too many to be from parasitism on an arthropod, considering the size of Jamoytius (14-18 cm). Dictyocaris thus is likely a plant (Ritchie, 1963), meaning the holes could be from plant matter on which Jamoytius fed.

Line 301: “because” is always clearer than “as.” OK

Line 302: add a word: found in eurypterids in higher fish beds . . OK .  

Line 304: add some words: (Figs. 10A, 11). For example, Erettopterus from the same bed, with its small pincers and compound eyes, was . . . OK

Line 309-310: Ainiktozoon and Loganellia are misspelled. OK

Figure 11: Loganellia is misspelled. OK

Line 315: attached, not attaches. OK

Line 316: add comma after patches. OK

Line 328: I suggest starting the Discussion with this new topic sentence: OK

Here are further considerations on Jamoytius’ feeding and locomotion.

Line 334: Mallatt, not Mallat.

Line 336: Here is a good place to propose the feeding mechanism more fully:

. . . particulate feeding or grazing on plants (Oleh, 2018). And again, the mouth-sized holes in the possible plant Dictycaris suggest a shredding herbivory with a blade-toothed, piston tongue.  Or, if no such teeth existed, then Jamoytius might have used the tongue to generate oral suction to remove the pieces from the soft plant. OK

Line 340: in fact, like the related euphaneropids, OK

Line 350: the Jamoytius-associated organisms. OK

Line 351: despite the latter’s possibly autapomorphic, elongated branchial basket, could be close to the stem lampreys. OK

Line 352-353: again remove this comparison to nonparasitic lampreys (which implies these lampreys are herbivorous). The sentence is easily removed, without interrupting your argument. OK

Line 353: simpler to say “Lampreys” than Petromyzontids here.  OK

Line 359: probably brackish and deeper-water basin OK

Line 360: surface-feeding detritivore or herbivore.  OK

Line 361: again, delete this sentence about nonparasitic lampreys, for the additional reason that such lampreys live far upstream at great distances from any ocean whereas Jamoytius lived close to the sea. Very different paleoenvironments!  OK

Lines 451 and 455: Mallatt not Mallat. OK

Reviewer 3 Report (New Reviewer)

Although three cladograms are presented in Figure 3, most of the author's comparisons are to lampreys, only one possible resolution. The interpretation of a sister group relationship between Jamoytius and anaspids is incorrect, this is not what Figure 3B shows. 'Jamoytius and and its likely euphaneropid sisters...could be plausible stem lampreys' is also an incorrect interpretation of the cladogram shown in Figure 3C. This is used for the basis of the rest of the paragraph (and the last sentence of the Conclusions section), which is pure speculation.

Comments for author File: Comments.pdf

Author Response

I have made changes to the cladogram text in the revised paper and changed cladogram 3B so it is now a sister taxon to the anaspids (as well as euphanerops) – I  also changed text later on. Taxonomic relationships do not really have much bearing on an organisms mode of life due to analogy and homology.   Dolphins and ichthyosaurs have similar adaptative morphologies  pointing to a similar modes of life – but they are not related.

Author Response File: Author Response.pdf

Round 2

Reviewer 3 Report (New Reviewer)

The author has done a good job of pulling back from phylogenetic arguments and focusing on palaeoenvironments and anatomical comparisons. Some parts still seem speculative to me (a piston-like jaw is present because there is room for it in Jamoytius), but I suggest minor revision. Please see the attached.

Comments for author File: Comments.pdf

No

Author Response

All reviewer3's 2nd round comments are on an annotated PDF which I emailed back to Ms Li together with an unannoatedt text. I cannot do a point-by-point reply as there is no reviewer text. But I provide again the annotatedt PDF file with my replies

Author Response File: Author Response.pdf

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

This is an interesting paper to discuss the lifestyle and paleoenvironment of the enigmatic c. The author thought the Jamoytius is more comparable  to lamprey than ostracodermi in the lifestyle and paleoenvironment. The result is consist with recent phylogenetic results. However, the introduction omit a little recent progress on the phylogenetic and swimming speed’s analysis for the early vertebrates.  The paper can accepted after minor revision.

44-45  Jamoytius lived an active lifestyle only based on morphological analysis here, but two recent papers about the Evolutionary analysis of swimming speed in early vertebrates can be considered, which indicates that the anaspids is the fastest swimmer among the stem-ganthostomes.

56-58 The most recent progress on the position of Jamoytius on cladograms is sister to Euphanerops nested in Anaspids, and the Anaspid as a whole to be the stem-Cyclostomi.

Miyashita et al, 2019, PNAS

Author Response

The author thought the Jamoytius is more comparable  to lamprey than ostracodermi in the lifestyle and paleoenvironment. The result is consist with recent phylogenetic results. However, the introduction omit a little recent progress on the phylogenetic and swimming speed’s analysis for the early vertebrates.  The paper can accepted after minor revision.

I have added quite a bit more on recent progress in the taxonomy – though this is not what the paper is about; also more on the swimming speed.

44-45  Jamoytius lived an active lifestyle only based on morphological analysis here, but two recent papers about the Evolutionary analysis of swimming speed in early vertebrates can be considered, which indicates that the anaspids is the fastest swimmer among the stem-ganthostomes.

I have now added swimming speed discussion.

56-58 The most recent progress on the position of Jamoytius on cladograms is sister to Euphanerops nested in Anaspids, and the Anaspid as a whole to be the stem-Cyclostomi. Miyashita et al, 2019, PNAS

I have added some more recent papers on the phylogenetic position of Jamoytius, though this is not what the paper is about, but left the cladograms unchanged as they summarize the main phylogenetic alternative positions well.

Author Response File: Author Response.pdf

Reviewer 2 Report

Comments for author File: Comments.pdf

Author Response

“The article includes scant details on the phylogenetic placement of Jamoytius and is missing citations to several extremely relevant recent studies: namely Reeves et al 2023; Reeves & Sansom 2023; Chevrinais et al 2018; Keating & Donoghue 2016; Miyashita et al 2021, 2019. It then proceeds to interpret Jamoytius as a stem-lamprey, largely ignoring alternate hypotheses of affinity.”

This paper is NOT about its affinity but its ecology, as the title states, but I should have updated and considered the relevant more recent taxonomic studies as the first reviewer also noted – now done

“Several arthropod taxa are not included in the taxon list.” I used the taxon list of Lovelock (1998) which did not included very rare members of the Jamoytius community and those which are incorrectly recorded as from the Jamoytius bed, but I now include some of those recorded on Ritchie’s (1963). Some cited as such, do not come from the Jamoytius laminated siltstone beds.

I have made notes on these; for example the synziphosurine Cyamocephalus loganensis is represented by only one specimen from Lesmahagow (Anderson, 1999) and attributed to the Jamoytius bed solely on its matrix by Currie (1927). ?Hardiopterus lanarkensis and the other Lesmahagow arthropods not on my list, which were noted by Dunlop et al. (2002), Currie (1927) Woodward (1868), Hunter (1968), Waterston (1979) and the single specimen of the Chasmataspid Loganamaraspis dunlopi, described by Tetlie and Braddy (2004 for 2003) come from stratigraphically higher horizons (the Kip Burn Formation) or are museum specimens located only as from Lesmahagow with no detailed locality data and with siltstone matrices which occur throughout the Lesmahagow strata in higher fish beds, and cannot therefore be assigned to, or considered as part of, the Jamoytius bed. The Logan reservoir now covers a lot of the exposures recorded by Peach and Horne (1899) between the Jamoytius bed and the Ceratiocaris beds at Shanks Castle. So the simple label Logan river is meaningless for locations purposes.

I take great exception to the comment: “the manuscript includes grid references and site photos from Lesmahagow. I believe that it is both unnecessary and unethical to include this information.”

While the older works of Ritchie (1963, 1968), Rolfe (1992) and Dineley and Metcalfe (1999) gave grid references before the illegal collecting and SSSI site designation, both the Scottish Geological Trust, and the Geological Conservation Review, still show both grid references and detailed location maps of Birk Knowes on their websites and the appendix to the Scottish Natural Heritage Research Report No. 1014 (2018) also gives grid references: I suppose these are unethical organizations. For many years the entire Birk Knowes site has been surrounded by an over three metre high fence with access only by a padlocked gate and with a resident warden in nearby Lesmahagow. It is now very difficult to vandalize. While fossil collecting has stopped (there is really enough fossil material now available for study in museums, etc.), in summer 2022, I got official permission to access the site to collect small samples for hitherto neglected sedimentological, geochemical and dating studies. It is pretty standard practice to give accurate locations and views of studied sites in research publications.

This reviewer also states that; “this study does not present any new information that is relevant for interpreting the affinity of Jamoytius.” Correct, this paper is NOT about its affinity but its ecology, as the title states (the is what “life and death” means), though this may or may not have some relevance to it affinity, the problems of which, I have now updated in the revised manuscript. While the anatomy of an organism (and this is difficult for Jamoytius) is important in determining its mode of life, its affinity is irrelevant to this, due to problems of analogy and homology.

This reviewer said he signed the review which I appreciate – but the name was not on the review comments I got. I never give anonymous reviews – if cannot identify yourself with a comment you should not be making it.

Major comments

Some figures are low resolution with pixelation artefacts (Fig1A, E; Fig 2C; Fig 3A, B; Fig 4A; Fig 6A; Fig 7; Fig 8).

O.K. now sorted

Pg.1 . Reference (Loon 2018) is missing from the reference list.

Not now necessary - omitted

Pg. 3. The faunal list is incomplete. I am by no means an expert on the Lesmahagow fauna, but a cursory search shows that a chasmataspid has been described from the Patrick Burn formation (Tetlie & Brady 2003). Reviewing Dunlop et al 2020 (https://wsc.nmbe.ch/resources/fossils/Fossils19.0.pdf) suggests there are more missing arthropods. I believe that ?Hardieopterus lanarkensis should be included at the very least. I am left wondering if there are any other taxa missing.

These and other forms recorded from the Jamoytius bed are not from it. – I have made notes on these in paper. Dunlop et al 2020 is a large compilation and naturally accepted the locality designations without critical evaluation. None of the omitted arthropods can be definitely assigned to the Jamoytius bed.

Pg. 2. “The non-carnivorous species, such as Lethenteron appendix, the American brook lamprey, evolved from carnivorous ancestors”. There is no citation supporting this statement. In fact, ancestral state estimation from the most recent phylogenetic study of lampreys (Brownstein & Near 2023) weakly supports the opposite - that parasitic lampreys evolved from non-parasitic ancestors.

Yes, have made this clearer in revision

Fig. 4A. This is cited as ‘courtesy deviantart.com’. My understanding is that art hosted on this website is not under a creative commons licence. There is no artist attributed to this image. Does the author have permission to reproduce this image, or any of the images in this manuscript?

I have omitted fig 4A – the others I have permission from Nobu Tamura for. The lampreys of fig. 4 are from North Carolina Public Resources Commission and are in public domains as is the Devonian lamprey figure.

Reviewer 3 Report

See the downloaded document. 

Comments for author File: Comments.pdf

Author Response

Review of Brookfield manuscript for Fossils, The life and death of Jamoytius, Oct. 7, 2023.

This is an interesting paper with good potential. I appreciate how it uses the sedimentology, paleoecology, and inferred lifestyles of the accompanying animals (Table 1) to deduce the feeding mode and nektonic existence of Jamoytius. Its conclusion that Jamoytius was a surface-feeding herbivore is reasonable to me.

However, I feel the paper could benefit from more rigor and attention to detail. It seems like the Jamoytius literature was read briefly and not really mastered. Most telling is that the cited works stop around 2010, missing the findings since then. I list some of the newer papers below, which should be mastered and cited in the revised manuscript. I would also like to see Jamoytius’s proposed feeding mechanism, presumably based on a lamprey-like tongue, presented in more depth. The paper by Mallatt (2023; pages 309-310, 293, and its Figs. 6 and 12E) is relevant for this because it points out that the oropharyngeal floor of Jamoytius has room for a piston-like tongue, and the apex of this tongue in lampreys has biting and cutting plates---plates that could have been used to shear off pieces of plants. Mallatt (2023: Fig. 12E) also proved that Jamoytius did not have a suctorial apparatus like that formed by lamprey lips.

I have added reference to a lot more of the recent phylogenetic and anatomical research and to the inferred piston-like tongue

More suggestions for increasing the rigor are offered next, where I go through the article by line number:

Line 29 says Jamoytius was the earliest vertebrate with camera eyes, but I think that distinction goes to the Cambrian Haikouichthys instead.

Correct - omitted

Line 32-33 correctly says Mallatt formerly thought Jamoytius could have been an ancestral parasitic lamprey, but a change of mind about the parasitism is reflected in Mallatt (2023, pp. 309-310).

I agree Jamoytius not parasitic

Line 43 talks of Jamoytius having a hypocercal tail and how that tail was used for swimming. But the caudal region of Jamoytius is unknown in the fossils. This section therefore should be stated more carefully, less certainly: “Assuming that Jamoytius, like other anaspid-like fishes, had a hypocercal tail . . .”

Correct - changed

Line 48: Four Paleozoic fossil lampreys are now known, not three, given the demonstration that Pipiscius is a lamprey (Miyashita et al., 2021).

Correct - changed

Line 52 tells of Jamoytius having an uncertain position on phylogenetic trees as of the year 2010. Newer phylogenies are more favorable to the author’s interpretations, putting Jamoytius inside the cyclostome total-group, within a paraphyletic Anaspida and often as the sister group of another, traditional anaspid. See Miyashita et al. (2019, 2021) and Dearden it al. (2023). In summary, Jamoytius is now classified as a true relative of lampreys, and the trees in Figure 2 should be updated.

The trees on the figure are only used as an illustration of the possible phylogenies. The actual taxonomic status and affinity of Jamoytius is irrelevant and difficult due to analogy and homology. I am interpreting its ecology using its anatomy, adaptative morphology and paleoenvironmental information.   

Line 59. This mention of the nonfeeding brook lampreys may be misleading. Can it be deleted? It implies that Jamoytius did not feed, which is not the author’s intention. It is better to focus on Jamoytius’s feeding apparatus, such as proposing it had a lamprey-like tongue that it used for slicing plants but not for suction or parasitizing fish.

O.K. changed

Line 117: Loganiella is a thelodont, not an anaspid as claimed; Figure 4 also incorrectly calls it an anaspid.

Yes – now used more general term agnathan