One of my classes assigns write-ups on invertebrate peer-reviewed literature, so I figured that I might as well cannibalize and extend my original report to post it here. I also gave a short talk on Remipedia that a "lucky" few were subjected to - let's hope this is a more coherent format.
I have an inexplicable intellectual attraction to relictual organisms, making remipedes fascinating to me despite my relative unfamiliarity with Crustacea. I should point out that the popular conception of a "crustacean" is essentially synonymous with Decapoda (shrimp, lobsters, crabs, etc.) and excludes all of the other various clades of mandible-bearing arthropods with two pairs of antennae, two maxillae pairs and division into tagma (e.g. cephalothorax, pereon, pleon). Remipedes are the exception to the latter trait and simply possess a head with a long, homonomously segmented trunk somewhat reminiscent of myriapods (especially chilopods = centipedes), onychophorans and some polychaete annelids. It was long assumed that arthropods evolved from a long-bodied annelid-like ancestor so early remipede morphological workers (i.e. those in the 80's and 90's!) assumed that remipedes lay at the base of the crustacean phylogenetic tree; one worker even used remipedes to root the crustacean phylogenetic tree and placed them in a more basal position than Burgess Shale arthropods (Odaraia, Canadaspis) (Schram and Koenemann 2004). As we'll see later, the only modern consensus about remipede relations is that they aren't at the base of the "crustacean" family tree...
The unpigmented, eyeless, marine cave-dwelling members of class Remipedia were first discovered off the Bahamas in 1979* and were described by Yeager (1981). Remipedes were later found in other Caribbean locales such as the Yucatan peninsula, the Turks and Caicos, Cuba, and the Canary islands - incredibly they've also been found in roughly antipodal Western Australia as well (Yager and Humphreys 1996). Yager (1981) suggested that a remipede had in fact been described before: the enigmatic Carboniferous Tesnusocaris (described in 1955) which also possessed homonomous segments with paddle-like appendages. Emerson and Schram (1990) re-described Tesnusocaris with both a pair of uniramous ventrolateral appendages used for swimming and a midventral pair used for sculling; the authors hypothesized that this two appendage pair state is a "missing link" between uniramous and biramous appendages. Koenemann et al. (2007a) found some aspects of the authors' reconstruction questionable** (the two limb pairs per segment?) but still used their description of Tesnusocaris as an outgroup for their phylogeny of modern remipedes (Nectiopoda) - despite potential weirdness Tesnusocaris still did have distinctively remipedian head appendages. The Mazon Creek assemblage of Illinois (home of Pohlsepia and Tullimonstrum) yielded the remipede Cryptocaris which also has the three pairs of prehensile cephalic appendages (maxillule, maxilla and maxilliped), but was not complete enough for analysis by Koenemann et al. (2007a). So, it looks like Remipedia has an even worse ghost lineage syndrome than octopuses.
* Another class of possibly primitive crustaceans, Cephalocarida, was discovered off Long Island Sound in 1953. Granted, remipedes are ~1.5-4.5 cm in length and cephalocarids are 4 mm, but discovering new classes still sounds like a major surprise.
** They cite a later paper from the same authors in 1991 from the Proceedings of the San Diego Society of Natural History. I'm assuming that it's a more thorough version of their Science article.
Not much is known about the reproduction, life history and behavior of remipedes; what is known is fascinating, if somewhat contradictory. Being blind, remipedes have a gigantic olfactory apparatus and use their second pair of antennae to drive currents past the "fields of aesthetascs" on their first antennae pair; their ability to detect low odor concentrations has been confirmed by observations of their quick attraction to dead fish (Fanenbruck et al. 2004). Remipedes have been observed to be slow swimmers but they are not strict scavengers, they have raptorial mouthparts including a fang-like first maxillae and have been observed engaging in predatory behavior (Kohlhage and Yager 1994, Fanenbruck et al. 2004). The maxillule fangs connect to glands which are presumably involved in injecting prey; while empirical evidence of injection doesn't exist, the probable mechanics of injection have been worked out (van der Ham and Felgenhauer 2007). The potentially injected substance is apparently an oxygen-carrying respiratory pigment (!) - another substance capable of turning the hemocyanin-like compound into a harmful phenoloxidase has yet to be discovered (van der Ham and Felgenhauer 2007). In case you're diving in obscure marine caves, don't worry about remipede bites as they apparently have no adverse affect on people (Koenemann et al. 2007b). While the aforementioned evidence seemingly suggests that remipedes are sluggish marine centipede analogues - lab observations of Speleonectes indicate that they spend almost all of their time (>99%) filter feeding (Koenemann et al. 2007b). Koenemann's website has a video summary (warning, 50 megabytes) of 2-3 months of observed behavior, including some of the rare instances of predation (3!). From the video, it can be noted that the thoracic appendages are always moving (even at rest) and remipedes are capable of a fast "snake-like" strikes and coiling (Koenemann et al. 2007b). Even though these remipedes aren't very big animals (~4 cm), I would hesitate in calling them sluggish (note that some parts of the video are at 5x). It seems likely that remipedes spend most of their time filter feeding in the wild as well and engage in facultative predation/scavenging whenever something comes their way - the lack of these behaviors in the lab could be artifacts due to the environment and/or the (relatively) high abundance of potential prey.
So, what are remipedes?
Despite looking like hypothetical ancestral arthropods, remipedes are obviously quite specialized. If we ignore their confusing mosaic of morphological traits for the time being, molecular evidence gives us a wide range of opinions on their placement. Regier et al. (2005) suggested close kinship with cephalocarids and a somewhat more distant relation with branchiopods (both viewed as morphologically "primitive"), oh and all of those groups were in a clade containing hexapods, i.e. insects and kin! The authors note that all of the members probably had ancestors either near-shore or in marginal (read: really weird) marine habitats, possibly the result of competition from other crustaceans, myriapods and chelicerates (Regier 2005). Cook et al. (2005) used mtDNA to place remipedes in a derived clade with Collembola (hexapods!) - mind you in thus study both hexapods and crustaceans were paraphyletic! Since none of the other studies reach any consistent placement, let's look at morphology.
Unexpectedly, remipedes have an order of magnitude more neurons than other taxa like branchiopods and maxillopods and their complex brains resemble those of malacostracans and hexapods (Fanenbruck et al. 2004). Also unexpected are the recently discovered larvae of remipedes, which happen to be non-feeding (lecithotrophic) in a manner similar to malacostracans such as euphausiaceans and dendrobranchiates (Koenemann et al. 2007c). Remipedes larvae share many traits with the lecithotrophic malacostracans but differ in having three pairs of uniramous cephalic limbs, biramous trunk limbs and caudal rami developing on an anal somite rather than a teslon (Koenemann et al. 2007c). The first trait is especially odd since you would expect a maxilliped to resemble a trunk appendage during development, but this somehow is not the case. Convergence can't be ruled out of course, but the coincidence of similar brain morphology and occasionally similar development is interesting (unless the two are somehow connected). Koenemann et al. (2007c) echo a previous study which tenuously concluded that remipedes, cephalocarids and "most of the maxillopodans and malacostracans" form a clade to the exclusion of other crustaceans.
The previous study Koenemann et al. (2007c) are referencing (Schram and Koenemann 2004) used extinct and extant arthropods (including Tesnusocaris) in their analysis. One of the characters united remipedes with Eucrustacea was gonopore placement on the 6th through 8th thoracic segments - I'm not sure how this was coded in for remipedes. Interestingly, even this analysis found insects to lay within the group traditionally known as "crustaceans" - could it be that molecular and morphological camps are finally starting to agree?
This of course isn't everything on remipedes, but it should at least give an idea of the pioneering work being done on this fascinating group. Well, this took far too long to write, I've got obligations to fulfill like crazy...
References:
Cook, Charles E. et al. 2005. Mitochondrial genomes suggest that hexapods and crustaceans are mutually paraphyletic. Proc Biol Sci. 272, 1295–1304
Emerson, Michael J. and Schram, Frederick R. 1990. The Origin of Crustacean Biramous Appendages and the Evolution of Arthropoda. Science 250, 667-669
Fanenbruck, Martin et al. 2004. The brain of the Remipedia (Crustacea) and an alternative hypothesis on their phylogenetic relationships. PNAS 101, 3868-3873.
van der Ham, Joris L. and Felgenhauer, Bruce E. 2007. The functional morphology of the putative injecting apparatus of Speleonectes tanumekes (Remipedia). Journal of Crustacean Biology 27, 1-9
Koenemann, Stefan et al. 2007a. Phylogenetic analysis of Remipedia (Crustacea). Diversity & Evolution 7, 33–51
Koenemann, Stefan et al. 2007b. Behavior of Remipedia in the Laboratory, with supporting Field Observations. 2007. Journal of Crustacean Biology 27, 534-542
Koenemann, Stefan et al. 2007c. Post-embryonic development of remipede crustaceans. Evolution & Development 9, 117-121
Kohlhage, Klaus and Yager, Jill. 1994. An Analysis of Swimming in Remipede Crustaceans. Philosophical Transactions: Biological Sciences 346, 213-221
Regier, Jerome C. et al. 2005. Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proc Biol Sci. 272, 395-401.
Ruppert, Edward E. et al. 2004. Invertebrate Zoology: A Functional Evolutionary Approach. Seventh Edition. Thomson, Brooks/Cole, United States.
Schram, F. R. and Koenemann, S. 2004. Are crustaceans monophyletic? In J. Cracraft and M. J. Donaghue (eds.). Assembling the Tree of Life. Oxford University Press, Oxford, pp. 319-329.
Yager, Jill and Humphreys, W. F. 1996. Lasionectes exleyi, sp. nov., the First Remipede Crustacean Recorded from Australia and the Indian Ocean, with a Key to the World Species. Invertebrate Taxonomy 10, 171-187.
Yager, Jill. 1981. Remipedia, a new class of Crustacea from a marine cave in the Bahamas. Journal of Crustacean Biology 1, 328-333.
I have an inexplicable intellectual attraction to relictual organisms, making remipedes fascinating to me despite my relative unfamiliarity with Crustacea. I should point out that the popular conception of a "crustacean" is essentially synonymous with Decapoda (shrimp, lobsters, crabs, etc.) and excludes all of the other various clades of mandible-bearing arthropods with two pairs of antennae, two maxillae pairs and division into tagma (e.g. cephalothorax, pereon, pleon). Remipedes are the exception to the latter trait and simply possess a head with a long, homonomously segmented trunk somewhat reminiscent of myriapods (especially chilopods = centipedes), onychophorans and some polychaete annelids. It was long assumed that arthropods evolved from a long-bodied annelid-like ancestor so early remipede morphological workers (i.e. those in the 80's and 90's!) assumed that remipedes lay at the base of the crustacean phylogenetic tree; one worker even used remipedes to root the crustacean phylogenetic tree and placed them in a more basal position than Burgess Shale arthropods (Odaraia, Canadaspis) (Schram and Koenemann 2004). As we'll see later, the only modern consensus about remipede relations is that they aren't at the base of the "crustacean" family tree...
The unpigmented, eyeless, marine cave-dwelling members of class Remipedia were first discovered off the Bahamas in 1979* and were described by Yeager (1981). Remipedes were later found in other Caribbean locales such as the Yucatan peninsula, the Turks and Caicos, Cuba, and the Canary islands - incredibly they've also been found in roughly antipodal Western Australia as well (Yager and Humphreys 1996). Yager (1981) suggested that a remipede had in fact been described before: the enigmatic Carboniferous Tesnusocaris (described in 1955) which also possessed homonomous segments with paddle-like appendages. Emerson and Schram (1990) re-described Tesnusocaris with both a pair of uniramous ventrolateral appendages used for swimming and a midventral pair used for sculling; the authors hypothesized that this two appendage pair state is a "missing link" between uniramous and biramous appendages. Koenemann et al. (2007a) found some aspects of the authors' reconstruction questionable** (the two limb pairs per segment?) but still used their description of Tesnusocaris as an outgroup for their phylogeny of modern remipedes (Nectiopoda) - despite potential weirdness Tesnusocaris still did have distinctively remipedian head appendages. The Mazon Creek assemblage of Illinois (home of Pohlsepia and Tullimonstrum) yielded the remipede Cryptocaris which also has the three pairs of prehensile cephalic appendages (maxillule, maxilla and maxilliped), but was not complete enough for analysis by Koenemann et al. (2007a). So, it looks like Remipedia has an even worse ghost lineage syndrome than octopuses.
* Another class of possibly primitive crustaceans, Cephalocarida, was discovered off Long Island Sound in 1953. Granted, remipedes are ~1.5-4.5 cm in length and cephalocarids are 4 mm, but discovering new classes still sounds like a major surprise.
** They cite a later paper from the same authors in 1991 from the Proceedings of the San Diego Society of Natural History. I'm assuming that it's a more thorough version of their Science article.
Not much is known about the reproduction, life history and behavior of remipedes; what is known is fascinating, if somewhat contradictory. Being blind, remipedes have a gigantic olfactory apparatus and use their second pair of antennae to drive currents past the "fields of aesthetascs" on their first antennae pair; their ability to detect low odor concentrations has been confirmed by observations of their quick attraction to dead fish (Fanenbruck et al. 2004). Remipedes have been observed to be slow swimmers but they are not strict scavengers, they have raptorial mouthparts including a fang-like first maxillae and have been observed engaging in predatory behavior (Kohlhage and Yager 1994, Fanenbruck et al. 2004). The maxillule fangs connect to glands which are presumably involved in injecting prey; while empirical evidence of injection doesn't exist, the probable mechanics of injection have been worked out (van der Ham and Felgenhauer 2007). The potentially injected substance is apparently an oxygen-carrying respiratory pigment (!) - another substance capable of turning the hemocyanin-like compound into a harmful phenoloxidase has yet to be discovered (van der Ham and Felgenhauer 2007). In case you're diving in obscure marine caves, don't worry about remipede bites as they apparently have no adverse affect on people (Koenemann et al. 2007b). While the aforementioned evidence seemingly suggests that remipedes are sluggish marine centipede analogues - lab observations of Speleonectes indicate that they spend almost all of their time (>99%) filter feeding (Koenemann et al. 2007b). Koenemann's website has a video summary (warning, 50 megabytes) of 2-3 months of observed behavior, including some of the rare instances of predation (3!). From the video, it can be noted that the thoracic appendages are always moving (even at rest) and remipedes are capable of a fast "snake-like" strikes and coiling (Koenemann et al. 2007b). Even though these remipedes aren't very big animals (~4 cm), I would hesitate in calling them sluggish (note that some parts of the video are at 5x). It seems likely that remipedes spend most of their time filter feeding in the wild as well and engage in facultative predation/scavenging whenever something comes their way - the lack of these behaviors in the lab could be artifacts due to the environment and/or the (relatively) high abundance of potential prey.
So, what are remipedes?
Despite looking like hypothetical ancestral arthropods, remipedes are obviously quite specialized. If we ignore their confusing mosaic of morphological traits for the time being, molecular evidence gives us a wide range of opinions on their placement. Regier et al. (2005) suggested close kinship with cephalocarids and a somewhat more distant relation with branchiopods (both viewed as morphologically "primitive"), oh and all of those groups were in a clade containing hexapods, i.e. insects and kin! The authors note that all of the members probably had ancestors either near-shore or in marginal (read: really weird) marine habitats, possibly the result of competition from other crustaceans, myriapods and chelicerates (Regier 2005). Cook et al. (2005) used mtDNA to place remipedes in a derived clade with Collembola (hexapods!) - mind you in thus study both hexapods and crustaceans were paraphyletic! Since none of the other studies reach any consistent placement, let's look at morphology.
Unexpectedly, remipedes have an order of magnitude more neurons than other taxa like branchiopods and maxillopods and their complex brains resemble those of malacostracans and hexapods (Fanenbruck et al. 2004). Also unexpected are the recently discovered larvae of remipedes, which happen to be non-feeding (lecithotrophic) in a manner similar to malacostracans such as euphausiaceans and dendrobranchiates (Koenemann et al. 2007c). Remipedes larvae share many traits with the lecithotrophic malacostracans but differ in having three pairs of uniramous cephalic limbs, biramous trunk limbs and caudal rami developing on an anal somite rather than a teslon (Koenemann et al. 2007c). The first trait is especially odd since you would expect a maxilliped to resemble a trunk appendage during development, but this somehow is not the case. Convergence can't be ruled out of course, but the coincidence of similar brain morphology and occasionally similar development is interesting (unless the two are somehow connected). Koenemann et al. (2007c) echo a previous study which tenuously concluded that remipedes, cephalocarids and "most of the maxillopodans and malacostracans" form a clade to the exclusion of other crustaceans.
The previous study Koenemann et al. (2007c) are referencing (Schram and Koenemann 2004) used extinct and extant arthropods (including Tesnusocaris) in their analysis. One of the characters united remipedes with Eucrustacea was gonopore placement on the 6th through 8th thoracic segments - I'm not sure how this was coded in for remipedes. Interestingly, even this analysis found insects to lay within the group traditionally known as "crustaceans" - could it be that molecular and morphological camps are finally starting to agree?
This of course isn't everything on remipedes, but it should at least give an idea of the pioneering work being done on this fascinating group. Well, this took far too long to write, I've got obligations to fulfill like crazy...
References:
Cook, Charles E. et al. 2005. Mitochondrial genomes suggest that hexapods and crustaceans are mutually paraphyletic. Proc Biol Sci. 272, 1295–1304
Emerson, Michael J. and Schram, Frederick R. 1990. The Origin of Crustacean Biramous Appendages and the Evolution of Arthropoda. Science 250, 667-669
Fanenbruck, Martin et al. 2004. The brain of the Remipedia (Crustacea) and an alternative hypothesis on their phylogenetic relationships. PNAS 101, 3868-3873.
van der Ham, Joris L. and Felgenhauer, Bruce E. 2007. The functional morphology of the putative injecting apparatus of Speleonectes tanumekes (Remipedia). Journal of Crustacean Biology 27, 1-9
Koenemann, Stefan et al. 2007a. Phylogenetic analysis of Remipedia (Crustacea). Diversity & Evolution 7, 33–51
Koenemann, Stefan et al. 2007b. Behavior of Remipedia in the Laboratory, with supporting Field Observations. 2007. Journal of Crustacean Biology 27, 534-542
Koenemann, Stefan et al. 2007c. Post-embryonic development of remipede crustaceans. Evolution & Development 9, 117-121
Kohlhage, Klaus and Yager, Jill. 1994. An Analysis of Swimming in Remipede Crustaceans. Philosophical Transactions: Biological Sciences 346, 213-221
Regier, Jerome C. et al. 2005. Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proc Biol Sci. 272, 395-401.
Ruppert, Edward E. et al. 2004. Invertebrate Zoology: A Functional Evolutionary Approach. Seventh Edition. Thomson, Brooks/Cole, United States.
Schram, F. R. and Koenemann, S. 2004. Are crustaceans monophyletic? In J. Cracraft and M. J. Donaghue (eds.). Assembling the Tree of Life. Oxford University Press, Oxford, pp. 319-329.
Yager, Jill and Humphreys, W. F. 1996. Lasionectes exleyi, sp. nov., the First Remipede Crustacean Recorded from Australia and the Indian Ocean, with a Key to the World Species. Invertebrate Taxonomy 10, 171-187.
Yager, Jill. 1981. Remipedia, a new class of Crustacea from a marine cave in the Bahamas. Journal of Crustacean Biology 1, 328-333.
2 comments:
Well ignore the first comment I left you, you do have pictures of it. Are they rare? How likely is it that I've seen one before and just didn't know it? At any rate your posts always leave me amazed at how much I don't know about my co-inhabitants of this planet. Even if they are pretty disgusting looking, and I would most certainly squish one if I saw it, the least I can do is acknowledge its existence.
Great read tthankyou
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