A Hypothesis on Suspension Feeding in Early Chelicerates (Offacolidae)

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

See attached

Comments for author File: Comments.pdf

Author Response

Point-by-point responses to the Referees’ comments and suggestions.

 

We present the referees' comments in normal typeface and our responses in green bold.

 

Reviewer #1 (Remarks to the Author):

 

We thank Reviewer #1 for the positive evaluation of our work.

 

Reviewer #2 (Remarks to the Author):

 

First, there is a well-established literature on filter feeding by crustaceans that is highly relevant. I suggest looking at them in date order:

Rubenstein, D. I. and M. A. R. Koehl (1977). "The Mechanisms of Filter Feeding: Some Theoretical Considerations." The American Naturalist 111(981): 981-994.

Koehl, M. A. R. (1983). "The Morphology and Performance of Suspension-Feeding Appendages." Journal of Theoretical Biology 105(1): 1-11.

Cheer, A. Y. L. and M. A. R. Koehl (1987). "Paddles and rakes: Fluid flow through bristled appendages of small organisms." Journal of Theoretical Biology 129(1): 17-39.

Hamann, L. and A. Blanke (2022). "Suspension feeders: Diversity, principles of particle separation and biomimetic potential." Journal of the Royal Society Interface 19(186).

Borza, P., et al. (2024). "Niche differentiation among facultative filter feeders: Insights from invasive Ponto-Caspian mysids." Current Zoology 70(4): 513-521.

We have read the suggested papers and included all the relevant information we have found in them.

In particular: Line 61 “Suspension feeders can be broadly divided into passive types, which rely on ambient flow to capture particles—such as barnacles, crinoids, sponges, and corals—and active types, which generate their own feeding currents, typically including most suspension feeding arthropods [27]. This feeding strategy has been extensively studied, with fluid dynamics playing a crucial role in understanding its mechanisms. In this context, Ru-benstein and Koehl [28] presented a theoretical framework based on Reynolds number and appendage motion, offering insights into particle capture beyond the simple con-cept of mesh or comb size and the pure anatomical comparisons. ”

Second, they need to broaden their comparisons. The shrimp Atya gabonensis is much larger than the offacolids. I will also point out how dense the filtration fan of the shrimp is. I would expand the study to look at some of the animals discussed in the papers above (copepods, cladocerans). One possible analog are mole crabs, whose body form resembles that of Offacolus. https://seaunseen.com/mole-crabs/ and are filter feeders.

Mantelatto, F. L., J. M. Paixão, R. Robles, J. N. Teles, and F. C. Balbino. 2023. Evidence using morphology, molecules, and biogeography clarifies the taxonomic status of mole crabs of the genus Emerita Scopoli, 1777 (Anomura, Hippidae) and reveals a new species from the western Atlantic. ZooKeys 1161:169-202.

We have broadened our comparison, added 2 new species and are utilizing the compelling literature suggested. In particular, we have appreciated the suggestion of doing a comparison with mole crabs, the overall body shape of which we found to be a nice case of convergent evolution with Offacolus and a strong argument towards our hypothesis.in particular Line 262 “The suspension feeding mechanisms in the copepods Subeucalanus pileatus have been extensively studied and represent another insightful comparison. Subeucalanus pileatus, like other copepods, directs the water flow with food particles toward itself by moving four pairs of small limbs. When food gets close, it uses another pair of short limbs, the second maxillae, which have long bristles covered with tiny barbs, to catch the food. These limbs open up to let water in, then close tightly, pushing water out only through the small gaps between the bristles. This traps the food particles inside a sort of “bas-ket” made by the bristles [85]. Whether or not an active creation of water flow during feeding was present in offacolids is beyond pure anatomical comparison and will re-quire adequate study. However, what seems clear is that this strategy would require a pelagic lifestyle, which does not fit well with the anatomy of Offacolidae, which appear more suited for bottom-dwelling and a substrate-based suspension feeding activity. This is the case, for example, with the elongated telson, which could have acted as an anchorage. Indeed, the most compelling comparison is between Offacolus and the mole crabs. Emerita sp. (Fig. 2 G and H), as an example, shows an enlarged cephalic carapace as in Offacolus, with a series of appendages with setae protruding from the frontal part and being exposed in a passive way toward the sea currents [86], while the rest of the body is reduced, with the capability of enrolling on itself. The anatomies of Offacolus and the genus Emerita may represent a case of convergent evolution, reflecting ana-tomical adaptations that arose in order to exploit bottom, environmentally cur-rent-based suspension feeding mechanisms. This comparison suggests that Offacolus was the more specialized suspension feeder of the family, in accordance with its more developed exopods and reduced post-cephalic body. Last mention is to the fact that mole crabs are intertidal organisms [86], however, we will not assume such a behavior into Offacolus since it is not in accordance with its paleoenvironment.”

Third, I don’t think that the environment occupied can be used to test the hypothesis. Except for highly muddy environments, suspension feeders can be found in nearly all marine habitats.

The reviewer is right to point out that suspension feeders are widespread in marine environments, and we agree that the mere presence of such feeders in a given environment isn’t, on its own, definitive proof for a specific hypothesis. However, in scientific reasoning, not all evidence needs to be absolute to be valuable.

There are varying degrees of support for a hypothesis. Some insights strongly support a claim, while others provide only moderate or indirect support. It’s a mistake to assume that only absolute correlations, like "if A, then always B", are useful. Conditional or probabilistic statements, such as "if A, then probably B" or "if A, then possibly B," can also contribute meaningfully, especially when considered alongside other lines of evidence.

So, while it’s true that most systems can sustain suspension feeding, not all do, nor at all times in history, and certainly not with the same intensity or ecological dynamics. For these reasons, we consider the environmental context one of several factors that moderately support our hypothesis.

Fourth. The only test they propose that might give useful results is using functional morphology. I would greatly expand this, starting with the papers above.

We removed this last method as a possible one to test our hypothesis. And expanded on the fluidodynamic background of the second using the literature suggested by the reviewer.

Finally, even if the gnathobases of these animals could not crush shells, as does modern Limulus, could they have been eating soft bodied animals, such as various small worms? BTS, see:

Bicknell, R. D. C., J. A. Ledogar, S. Wroe, B. C. Gutzler, W. H. Watson, and J. R. Paterson. 2018. Computational biomechanical analyses demonstrate similar shell-

crushing abilities in modern and ancient arthropods. Proceedings of the Royal Society B: Biological Sciences 285(1889).

Exactly for this reason, we cited the optimal foraging theory (see comment below). The chelicerae of Offacolidae are extremely small and delicate, and could not handle and take apart anything of a substantial size. They appear mostly to be useful for collecting trapped particles from the other appendages. The gnathobases on the other hand are extremely reduced in the group (probably of non-masticatory use). This anatomical asset do not let imagine the animals to be active predators.

Some small points:

1. The appendages of Dibasterium look quite different than that of Offacolus. They are chelate. The body forms are also quite different. This has relevance and should be discussed.

The endopods are chelate, the exopods are not, and this is true in the whole family. They all possesses setae.

2. Line 108. See no reason to cite Popper.

Amended.

3. Line 183. I do not see the relevance of optimal foraging theory in this context!

See above.

Reviewer 2 Report

Comments and Suggestions for Authors

This is a fascinating hypothesis regarding filter feeding in Chelicerata, a mode of feeding not hitherto recognized in this arthropod group. I have certainly wondered about the strange arrangement of legs in Offacolus and Dibasterium. Two really nice aspects of this study stand out: 1) that the authors look not only at functional morphology but also at the sedimentary (i.e. palaeoecological) environment and the climatic zones inhabited by the Offacolidae, and 2) the authors offer a number of methods by which the hypothesis can be tested. Therefore, this is not simply arm-waving, but a serious proposal, backed up by evidence, and with an outline of future possibilities.

Author Response

Point-by-point responses to the Referees’ comments and suggestions.

 

We present the referees' comments in normal typeface and our responses in green bold.

 

Reviewer #1 (Remarks to the Author):

 

We thank Reviewer #1 for the positive evaluation of our work.

 

Reviewer #2 (Remarks to the Author):

 

First, there is a well-established literature on filter feeding by crustaceans that is highly relevant. I suggest looking at them in date order:

Rubenstein, D. I. and M. A. R. Koehl (1977). "The Mechanisms of Filter Feeding: Some Theoretical Considerations." The American Naturalist 111(981): 981-994.

Koehl, M. A. R. (1983). "The Morphology and Performance of Suspension-Feeding Appendages." Journal of Theoretical Biology 105(1): 1-11.

Cheer, A. Y. L. and M. A. R. Koehl (1987). "Paddles and rakes: Fluid flow through bristled appendages of small organisms." Journal of Theoretical Biology 129(1): 17-39.

Hamann, L. and A. Blanke (2022). "Suspension feeders: Diversity, principles of particle separation and biomimetic potential." Journal of the Royal Society Interface 19(186).

Borza, P., et al. (2024). "Niche differentiation among facultative filter feeders: Insights from invasive Ponto-Caspian mysids." Current Zoology 70(4): 513-521.

We have read the suggested papers and included all the relevant information we have found in them.

In particular: Line 61 “Suspension feeders can be broadly divided into passive types, which rely on ambient flow to capture particles—such as barnacles, crinoids, sponges, and corals—and active types, which generate their own feeding currents, typically including most suspension feeding arthropods [27]. This feeding strategy has been extensively studied, with fluid dynamics playing a crucial role in understanding its mechanisms. In this context, Ru-benstein and Koehl [28] presented a theoretical framework based on Reynolds number and appendage motion, offering insights into particle capture beyond the simple con-cept of mesh or comb size and the pure anatomical comparisons. ”

Second, they need to broaden their comparisons. The shrimp Atya gabonensis is much larger than the offacolids. I will also point out how dense the filtration fan of the shrimp is. I would expand the study to look at some of the animals discussed in the papers above (copepods, cladocerans). One possible analog are mole crabs, whose body form resembles that of Offacolus. https://seaunseen.com/mole-crabs/ and are filter feeders.

Mantelatto, F. L., J. M. Paixão, R. Robles, J. N. Teles, and F. C. Balbino. 2023. Evidence using morphology, molecules, and biogeography clarifies the taxonomic status of mole crabs of the genus Emerita Scopoli, 1777 (Anomura, Hippidae) and reveals a new species from the western Atlantic. ZooKeys 1161:169-202.

We have broadened our comparison, added 2 new species and are utilizing the compelling literature suggested. In particular, we have appreciated the suggestion of doing a comparison with mole crabs, the overall body shape of which we found to be a nice case of convergent evolution with Offacolus and a strong argument towards our hypothesis.in particular Line 262 “The suspension feeding mechanisms in the copepods Subeucalanus pileatus have been extensively studied and represent another insightful comparison. Subeucalanus pileatus, like other copepods, directs the water flow with food particles toward itself by moving four pairs of small limbs. When food gets close, it uses another pair of short limbs, the second maxillae, which have long bristles covered with tiny barbs, to catch the food. These limbs open up to let water in, then close tightly, pushing water out only through the small gaps between the bristles. This traps the food particles inside a sort of “bas-ket” made by the bristles [85]. Whether or not an active creation of water flow during feeding was present in offacolids is beyond pure anatomical comparison and will re-quire adequate study. However, what seems clear is that this strategy would require a pelagic lifestyle, which does not fit well with the anatomy of Offacolidae, which appear more suited for bottom-dwelling and a substrate-based suspension feeding activity. This is the case, for example, with the elongated telson, which could have acted as an anchorage. Indeed, the most compelling comparison is between Offacolus and the mole crabs. Emerita sp. (Fig. 2 G and H), as an example, shows an enlarged cephalic carapace as in Offacolus, with a series of appendages with setae protruding from the frontal part and being exposed in a passive way toward the sea currents [86], while the rest of the body is reduced, with the capability of enrolling on itself. The anatomies of Offacolus and the genus Emerita may represent a case of convergent evolution, reflecting ana-tomical adaptations that arose in order to exploit bottom, environmentally cur-rent-based suspension feeding mechanisms. This comparison suggests that Offacolus was the more specialized suspension feeder of the family, in accordance with its more developed exopods and reduced post-cephalic body. Last mention is to the fact that mole crabs are intertidal organisms [86], however, we will not assume such a behavior into Offacolus since it is not in accordance with its paleoenvironment.”

Third, I don’t think that the environment occupied can be used to test the hypothesis. Except for highly muddy environments, suspension feeders can be found in nearly all marine habitats.

The reviewer is right to point out that suspension feeders are widespread in marine environments, and we agree that the mere presence of such feeders in a given environment isn’t, on its own, definitive proof for a specific hypothesis. However, in scientific reasoning, not all evidence needs to be absolute to be valuable.

There are varying degrees of support for a hypothesis. Some insights strongly support a claim, while others provide only moderate or indirect support. It’s a mistake to assume that only absolute correlations, like "if A, then always B", are useful. Conditional or probabilistic statements, such as "if A, then probably B" or "if A, then possibly B," can also contribute meaningfully, especially when considered alongside other lines of evidence.

So, while it’s true that most systems can sustain suspension feeding, not all do, nor at all times in history, and certainly not with the same intensity or ecological dynamics. For these reasons, we consider the environmental context one of several factors that moderately support our hypothesis.

Fourth. The only test they propose that might give useful results is using functional morphology. I would greatly expand this, starting with the papers above.

We removed this last method as a possible one to test our hypothesis. And expanded on the fluidodynamic background of the second using the literature suggested by the reviewer.

Finally, even if the gnathobases of these animals could not crush shells, as does modern Limulus, could they have been eating soft bodied animals, such as various small worms? BTS, see:

Bicknell, R. D. C., J. A. Ledogar, S. Wroe, B. C. Gutzler, W. H. Watson, and J. R. Paterson. 2018. Computational biomechanical analyses demonstrate similar shell-

crushing abilities in modern and ancient arthropods. Proceedings of the Royal Society B: Biological Sciences 285(1889).

Exactly for this reason, we cited the optimal foraging theory (see comment below). The chelicerae of Offacolidae are extremely small and delicate, and could not handle and take apart anything of a substantial size. They appear mostly to be useful for collecting trapped particles from the other appendages. The gnathobases on the other hand are extremely reduced in the group (probably of non-masticatory use). This anatomical asset do not let imagine the animals to be active predators.

Some small points:

1. The appendages of Dibasterium look quite different than that of Offacolus. They are chelate. The body forms are also quite different. This has relevance and should be discussed.

The endopods are chelate, the exopods are not, and this is true in the whole family. They all possesses setae.

2. Line 108. See no reason to cite Popper.

Amended.

3. Line 183. I do not see the relevance of optimal foraging theory in this context!

See above.

Round 2

Reviewer 1 Report

Comments and Suggestions for Authors

This is much improved from the original version. I have one remaining objection, which is the retention of the reference to optimal foraging theory (OFT) . I still fail to see how this paper relates to it. How? Simply saying  the appemdages are "ineffective at immobilizing, and penetrating dismembering prey of a reasonable size, as per the optimal foraging theory" is insuffcient and seems like a misunderstanding of what OFT is. Optimal foraging theory has a huge literature which often disagrees with what the theory is, what its relevance is, or even if it can be tested. It is mainly a theory that describes how organisms make behavioral choices during food gathering, not a description of morphology. An old  but useful summary of the assumptions of the theory are given by:  Perry, G., and E. R. Pianka. 1997. Animal foraging: past, present and future. Trends in ecology & evolution 12(9):360-364. 
OFT is not restricted to predation. This paper discusses it in context of filter feeding: Shimeta, J., and P. A. Jumars. 1991. Physical-mechanisms and rates of particle capture by suspension-feeders. Oceanography and Marine Biology 29:191-257.

  

Author Response

We are happy the reviewer find our manuscript improved and we have now removed the statement ", as per the optimal foraging theory [77,78]" on line 191.