The Benefits Of Having Stuff Grow All Over You

One would think that epibiotic growth, that is, commensal organisms attached to a living surface, would be neutral at best and a hindrance to locomotion at worst* for the basibiont, the substrate organism. 'Fouling' by epibiotic growth is a virtually omnipresent pressure in aquatic environments, so basibionts variably avoid, defend against, or tolerate epibiotic growth (Wahl 1989). Since there are potential examples beyond count, given the tendencies of this blog I'll focus on some recently described examples of tolerance from big vertebrates.

* Potential disadvantages for the basibionts includes increase in weight, decrease in flexibility, increase in friction, damage from anchoring, damage due to grazers preying on epibionts, and so forth (Wahl 1989 - citing various).

The loricariid catfish Pterygoplichthys (possibly P. disjunctivus and hybrids) was accidentally introduced to Florida and has been observed interacting with manatees while both species were present near springs during the winter, avoiding unsuitably low temperatures (Nico et al. 2009). The interaction is that the catfish graze upon the grazers:

A mother and calf with 16 loricariids. Note that manatees are typically covered in epibiotic growth. The authors recorded another instance of over 40 catfish on one individual, almost obscuring it from view. Photograph by James P. Reid, taken from Nico et al. (2009).

The heavy covering of epibionts on manatees indicates tolerance and implies either a neutral impact or a beneficial one. Nico et al. (2009) speculate that while the epibiont layer probably does not provide notable protection against UV radiation (as manatee skin is very thick), it could play a role in heat absorption. Manatee behavior towards the armored catfish is contradictory; while some individuals ignore them (Fig. 1) even if as many as 40 catfish are involved, others apparently avoid congregations of catfish and others still are irritated by the fish and attempt to dislodge them (Nico et al. 2009). Since the interaction is so recent, perhaps it is possible that manatees have not learned or evolved a standardized response. Manatees generally ignore other fish including remora species that feed on their fecal matter and bluegills that apparently feed on epibionts (Williams et al. 2003, Powell 1984); however they are not tolerant of a porgy species which occasionally nips at them (Nico et al. 2009 - citing pers. com.). The grazing on manatees could be beneficial for the removal of parasites and removal of diseased and damaged tissue, although it also carries the risk of disease transmission (Nico et al. 2009). This is a surprisingly complicated situation and clearly the role of epibionts needs to be further investigated, as do the risks and benefits of allowing fish to graze. Nico et al. (2009) speculate that manatees that avoid loricariids may move to colder water, where they expend more energy than normal attempting to maintain body heat.

The interaction between cetaceans and their epibionts seems to be less obscure than the manatee situation. In dealing with Orcinus orca predation, mysticetes have adopted fight or flight countermeasures; the Balaenoptera species are fliers while the right whales (Eubalaena spp.), bowhead whale (Balaena mysticetus), humpback whale (Megaptera novaeangliae) and grey whale (Eschrichtius robustus) are fighters (Ford and Reeves 2008). Although the number of documented cases of orcas killing mysticetes are few, the rate of scarring suggests that predation attempts are significant, likely for juveniles (Ford and Reeves 2008). The ability to sprint at considerable speeds in the Balaenoptera species seems to be a direct evolutionary response to predation, but the fight species may have evolved to be slow and maneuverable primarily because of their ecological niches (Ford and Reeves 2008). Possibly mirroring the evolution of horns in some bovids, the offensive structures in right whales and humpback whales are used both for intraspecific male combat and interspecific defense and it is not clear for what purpose they originally evolved (Ford and Reeves 2008). Although right whales and humpback whale will swing or lunge with their heads, flippers and flukes are the primary means of defense for these species; gray whales roll on their backs to protect their vulnerable ventrum (Ford and Reeves 2008).

Right whales have hardened patches of skin known as callosities on the dorsal, lateral, and ventral surfaces of the head. These callosities host thousands of amphipods, epibionts with no obvious beneficial function for the whales - apparently the cornified epidermal tissue provides their ideal habitat and harboring the arthropod is a side effect for possessing the morphology. Southern right whales, however, possess barnacles which probably do have a function in making the callosities more formidable.

The Southern Right Whale has callosities with both amphipods and barnacles. From here. Has anyone every suggested that right whales may be responsible for sightings of 'marine saurians'?

Humpback whales lack callosities, but they have analogous barnacles which fulfill the same function - and provide an unambiguous example of a positive epibiotic interaction. Humpbacks can have up to 450 kg of large barnacles ( up to a 5 cm diameter) concentrated on the head, leading edge of their flippers, tips of the tail flukes, throat pleats, and near the genital slit (Ford and Reeves 2008 - citing Clark 1966, Slijper 1962). While intraspecific purposes are also likely, it is probably no coincidence that humpback whales defend against orcas using their head, flippers, and flukes (Ford and Reeves 2008). It seems like the throat and genital regions would be particularly susceptible to either biting or ramming attacks, further suggesting the defensive function of the barnacles.

Grey whales have often continuous encrustations of barnacles on the dorsal portions of their rostrum, anterior portion of their backs as well as their flippers, fluke, and elsewhere (Ford and Reeves citing Rice and Wolman 1971). Considering the defensive behavior of the whales, once again it appears that the barnacle placement is no coincidence. Exactly how these whales attract barnacles to particular portions of their body certainly is a good question; how do the callosities of some right whales have barnacles and others don't?

Epibiosis certainly doesn't end with heat balance (maybe) and creating weapons, Wahl (1989) notes that other potential benefits for the basibiont include a supply of vitamins and/or nitrogen compounds, water retention during low tide, camouflage, mask chemical cues, and drag reduction (!) - thanks to hydrophobic bacteria on skin. There are of course many, many potential disadvantages as well.

References:

Ford, John K. B.; Reeves, Randall R. 2008. Fight or flight: antipredator strategies of baleen whales. Mammal Rev. 38(1), 50–86.

Nico, Leo G; Loftus, William F.; Reid, James P. 2009. Interactions between non-native armored suckermouth catfish (Loricariidae: Pterygoplichthys) and native Florida manatee (Trichechus manatus latirostris) in artesian springs. Aquatic Invasions 4(3), 511-519. Available.

Powell, J. A. 1984. Observations of cleaning behavior in the bluegill (Lepomis macrochirus), a centrarchid. Copeia 1984, 996-998.

Wahl, Martin. 1989. Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar. Ecol. Prog. Ser. 58, 175-189. Available.

Williams, E. H. Jr.; Mignucci-Giannoni, A. A.; Bunkley-Williams, L.; Bonde, R. K.; Self-Sullivan, C.; Preen, A.; Cockcroft, V. G. 2003. Echeneid-sirenian associations, withinformation on sharksucker diet. Journal of Fish Biology 63(5), 1176-1183. Available.

The Ateleopodids; or, Jellynose Fishes

I probably shouldn't admit this, but I was unaware of this order of fishes until National Geographic updated an AP story concerning a strange fish captured near Brazil with input from an ichthyologist. Few 'fish' clades* have an elongate body with a prominent first dorsal fin located almost directly behind the head, so I reasoned the the catch was some sort of aberrant macrourid... whoops.

* That is, 'fish' in the paraphyletic sense. Other actinopterygians with roughly similar morphology include (larval?) Stylephoriformes (no longer thought to be Lampridiformes, Miya et al. 2007) and several derived families within Lampriformes (see below). Captain Hanna's Mystery Fish (a probable lampridiform) had this morphology as well. The only non-actinopterygian example that comes to mind are members of Chimaeriformes, distant relatives of sharks and rays.

The 'jellynose fish' order is Ateleopodiformes; the former is a reference to the (sometimes - see below) bulbous snout and the order name, meaning 'imperfect feet', likely refers to the pelvic fins which are typically reduced to a single ray. Fishbase 'remarks' that other characters include a largely cartilaginous skeleton, a dorsal fin with 3-13 rays, a small caudal fin confluent with the long anal fin, and 7 branchiostegal rays. It is curious that National Geographic states that ateleopodids are "well-known" as the opposite appears to be the case; Prokofiev (2006) remarks that the clade is "very poorly studied" and Sasaki et al. (2006) note that there has yet to be a comprehensive morphological review.

Ateleopodids are paedomorphic and specialized, which has complicated analysis of their phylogeny (Sasaki et al. 2006). Early workers placed ateleopodids near (Sasaki et al. 2006 - citing Rosen and Patterson 1969) or within (Miya et al. 2001 - citing Nelson 1976, 1984) Lampridiformes, although one analysis placed them in an unresolved trichotomy with Stomiiformes and derived teleosts (Sasaki et al. 2006 - citing Olney et al. 1993). Sasaki et al. (2006) described the cranial morphology in detail and noted that ateleopodids and lampridiformes share the character complex of deep insertion of the rostral cartilage into an open space in the ethmoid region - albeit with differing methods of insertion. The two groups also share early life history characters such as large pelagic eggs and newly-hatched larvae with dorsal, pectoral, and pelvic fins (the latter positioned posterior to the yolk sac); at least one member of each group also possesses spotty educationalists muscles separated from the epaxial muscle mass (Sasaki et al. 2006 - citing various). Quite interestingly, mitogenomic evidence has placed Ateleopodiformes and Lampridiformes as sister groups (Miya et al. 2001). Since a long body with a prominent first dorsal fin appears in ateleopodids and derived lampridiformes (Miya et al. 2001), this indicates that the morphology is either due to parallel evolution or (less likely in my opinion) that opahs and velifers are secondarily shortened.

Evolutionary relationships aside, Sasaki et al. (2006) document the incredible phenotypic plasticity exhibited by ateleopodids. The 'jellynose' appearance does not occur in all ateleopodids, and in fact its presence is variable within species.

Ateleopus japonicus from Sasaki et al. (2006). These are young individuals, the top individual is pelagic and the bottom is benthopelagic.

Phenotypic plasticity can be explained as one genotype expressing multiple phenotypes due to differing environmental conditions. The Journal of Experimental Biology has a whole open-access issue devoted to the concept -this article in particular sums the concept up well. Anyways, pelagic individuals have a flat head and terminal mouth and benthopelagic individuals have the 'jellynose' condition with a rounded head and more subterminal mouth (Sasaki et al. 2006). The 'pelagic' condition is the default and at some point early in development the low jaw shortens and the upper jaw shifts posteriorly, 'folding' the head in the process (Sasaki et al. 2006). The authors unfortunately did not mention phenotypic plasticity by name, it was beyond the scope of the morphology-centric paper, which leaves an opening for a followup...

Guentherus katoi, Senou et al. (2008). 643.7 mm (25") SL. Photograph by H. Senou.

While the taxonomic status of the Brazil fish cannot be determined at the present time, one new species has been described quite recently. Three large specimens of Guentherus katoi were caught in a trawl off Japan in 2006; like the other member of its genus (the enormous G. altivela) there are three free pelvic fin rays followed by normal rays (as opposed to one) and the body shape is far from anguilliform (Senou et al. 2008). G. katoi differs from G. altivela in having a somewhat smaller head (25.6-26% SL vs. 26.4-35% SL), and larger orbits (5.2-6% SL vs. 2.4-3.5% SL); curiously, the G. katoi specimens had a small adipose fin behind the dorsal fin, and lacked scales, pores, and a lateral line (!) (Senou et al. 2008).

I think that about wraps it up for the ateleopodids, what started off as a commentary on a news item has blown up beyond recognition.

References:

Miya, Masakai, et al. (2001). Mitogenomic Exploration of Higher Teleostean Phylogenies: A Case Studyfor Moderate-Scale Evolutionary Genomics with 38 Newly Determined Complete Mitochondrial DNA Sequences. Mol. Biol. Evol. 18, 1993–2009.

Miya, Masakai, et al. (2007). Mitochondrial genome and a nuclear gene indicate a novelphylogenetic position of deep-sea tube-eye fish (Stylephoridae). Ichthyological Research 54, 323-332.

Prokofiev, A. M. (2006). New Finding of Ateleopus purpureus Tanaka, 1915 Ateleopodiformes: Ateleopodidae) in the Pacific Waters of Japan. Journal of Ichthyology. 46, 342-344.

Sasaki, Kunio, et al. (2006). Cranial morphology of Ateleopus japonicus (Ateleopodidae: Ateleopodiformes), with a discussion on metamorphic mouth migration and lampridiform affinities. Ichthyological Research 53, 254-263.

Senou, H., et al. (2008). A New Species of the Genus Guentherus (Ateleopodiformes: Ateleopodidae) from Japan. Bull. Natl. Mus. Nat. Sci., Ser. A, Suppl. 2, 13–19

The Molids, part 4: The least of the Molids (but not the least interesting); Ranzania

Not to be confused with the plant genus of the same name.

Photograph from Wikipedia

Poor neglected Ranzania, how has it been over a month since I've last discussed molids? Now that I've hit a clear patch with projects and activities, I'll finally be able to complete that last, nagging chapter on molids.

Had I been aware from the outset, I would have made Ranzania the subject of the first chapter; this taxa lacks many of the traits which define (Mola + Masturus) and, I suppose, could be regarded as a 'transitional form' between other tetraodontiformes and derived molids. I use that term cautiously because Ranzania isn't some unmodified holdover from the last common ancestor of molids - nothing is a true 'living fossil' or 'missing link', but basal members of a clade can still be useful for inferring evolution.

It deserves a mention that Raven (1939) thought that Ranzania was the most specialized of the molids based on the extreme development of the erector and depressor muscles of the dorsal and anal fins (see below) - this seems strange because the author recognizes several 'primitive' characters present in Ranzania including inclinator muscles for the aforementioned fins and the vestige of the puffing apparatus (m. retractor postclavicularis). These days phylogeny is no longer determined from a single character; the character-taxon matrix from Gregorova et al. (2009) has 57 characters and includes the extant molids (Ranzania, Masturus, Mola), the extinct ones (Austromola) and non-molid tetraodontiformes (Triodon, Lagocephalus), the latter of which is the most basal member of the clade and the former of which is in the sister group to molids. Ranzania has one unique character* state (pseudocaudal fin rays branch >5 times) in this analysis and shares 32 characters exclusively with other molids (but not always all of them); on the flip side Ranzania has 19 characters states present in non-molid tetraodontiformes such as an elongate pectoral fin, a body depth two times longer than deep, an absent 'carapace' (thick layer of collagenous tissue under scales), gill rakers not concealed in thick layers of skin, no secondary post-metamorphosis, and densely ossified bone (as opposed to weakly ossified and spongy) (Gregorova et al. 2009). Oh yes, and molecular evidence agrees that Ranzania is the most basal molid (Bass et al. 2005).

* Ranzania also has a vertical mouth slit, an unique apomorphy as far as I can tell. Molids lack muscles capable of closing this structure (Raven 1939).

External, musculature, and skeletal morphology of Ranzania. Taken from Johnson and Britz (2005) - itself modified from Fraser-Brunner (1951) and Raven (1939). In 'B', note that the entire lateral muscular mass is composed of muscles controlling the dorsal and anal fins - this is a singularly extreme development, even amongst molids. Juveniles have a slimmer body and evenly-sized dorsal and anal lateralis muscles, adults (pictured) have a thicker body due to more developed anal lateralis muscles (Raven 1939). Fishbase mentions that there are two more anal fin rays than dorsal. These aren't traits we would expect from an underwater 'flier', however Robison (1975) mentions that Ranzania is negatively buoyant and sinks head-first - is this morphology due to stabilization needs?

Morphological oddities, and lack thereof, aside, Ranzania also appears to occupy an unusual niche for a molid. Juveniles eat planktonic crustaceans such as calanoid and cyclopoid copepods, ostracods, and amphipods (Robison 1975) and adults also reportedly consume small crustaceans in addition to lanternfish, hyperiid amphipods, crab larvae (megalops and zoae), and pteropods (OceanSunfish.org citing Fitch 1969). The other, larger molids (Ranzania reportedly only reaches 1 m in length) are famous for consuming jellyfish in bulk, although they will consume a variety of prey including bottom dwelling and deep water species (OceanSunfish again for the save). This abstract suggests that the range of Mola is influenced by temperature while the range of Ranzania is influenced by productivity of zooplankton and small fish, itself influenced by large-scale atmospheric conditions; Castro and Ramos (2002) found captures of Ranzania to coincide with a warming process of the sea surface although if I had access to the former study I'm sure they'd discuss this.

Although typically stated to be a tropical to subtropical species (e.g. Castro and Ramos 2002), Ranzania can occur up to 71 degrees north (Castro and Ramos 2002 mention its occurrence in Scandinavia, huh) and Fishbase accurately describes the species as cosmopolitan. The only extant recognized species is R. laevis, but considering the vast range it would not be surprising if a study of population genetics turned up distinct clades possibly worthy of species-status. Fossil Ranzania species have been reported from the Middle to Late Miocene (see Gregorova et al. 2009 for a review) but I am cautious of species assigned to the clade solely on the basis of polygonal scale plates. Molecular estimations of molid divergence suggest that the Ranzania lineage diverged between 17.6-52.1 mya (Early Miocene to Early Miocene), which supports the assignment of the aforementioned fossils to Ranzania.

I think that about does it for Ranzania and the other molids. But not for weird fish...

References:

Bass, Anna L., et al. (2005). Evolutionary divergence among lineages of the ocean sunfish family, Molidae (Tetraodontiformes). Marine Biology 148, 405-414.

Castro, J. J. and Ramos, A. G. (2002). The occurrence of Ranzania laevis off the Island of GranCanaria, the Canary Islands, related to sea warming. Journal of Fish Biology 60, 271-273.

Gregorova, Ruzena, et al. (2009). A Giant Early Miocene Sunfish from the North Alpine Foreland Basin (Austria) and its Implication for Molid Phylogeny. Journal of Vertebrate Paleontology 29, 359-371.

Johnson, G. David, and Britz, Ralf. (2005). Leis’ Conundrum: Homology of the Clavus of the Ocean Sunfishes. 2. Ontogeny of the Median Fins and Axial Skeleton of Ranzania laevis (Teleostei, Tetraodontiformes, Molidae).

Raven, Henry C. (1939). Notes on the Anatomy of Ranzania truncata. Am Mus Novitates 1038, 1-7.

Robison, Bruce H. (1975). Observations on Living Juvenile Specimens of the Slender Mola, Ranzania laevis (Pisces, Molidae). Pacific Science 29, 27-29. Available.

The Molids, part 3: Enough with Mola!

In the first two posts I've mostly discussed Mola, a clade of three genetically distinct species whose morphological and biogeographical differences have just begun to be investigated. While Mola mola was a "flagship" species which obfuscated [previously recognized] diversity, there are other molids which are effectively unknown to Western public consciousness.

The so-called sharp tail/fin mola Masturus, taken from here. The dorsal fin is of course heavily damaged and while the clavus also looks attenuated compared to those of other specimens, the rounded edge seems to suggest that it isn't damaged. Liu et al. (2009) recovered a linear relationship of total length and standard length (TL - SL = clavus length) and fairly similar proportions in males and females - the large sample of primarily immature fish may have masked differing clavus proportions in large individuals.

As the above photo illustrates, Masturus is very similar in appearance to the Mola species and can be easily differentiated by a projection of the clavus (hence the common name). Gregorova et al. (2009) found Masturus and Mola to be sister taxa with the only differences (4 characters of 57 total) relating to one less caudal vertebrae in Masturus and clavus rays terminating in bony plates exclusively in Mola. Bass et al. (2005) recovered the same topology with combined d-loop and cyt b data; d-loop data in the same study also revealed that the small sample (n = 5) of Masturus did not show clear differences across ocean basins. This seems curious since the same authors mention unpublished tracking data which showed no indication of ocean basin-scale movement or large-scale migrations in the species* (Bass et al. 2005). Also interesting was that the authors only discussed Ma. lanceolatus and didn't mention Ma. oxyuropterus; the small sample size leaves open the possibility of an additional species despite the wide geographic sampling (including the type locality for Ma. oxyuropterus). Who knows, there could be another Mola-like situation at hand here...

* Seitz et al. (2002) tagged a 1 m (TL) individual which travelled 9.7 km/day - although where it traveled was not mentioned. Contrary to prior suggestions, the fish was epi-pelagic (preferring waters <>2.7% of its time in the top 5 m of the water column and could apparently dive below 1000 m (Seitz et al. 2002). I'd assume that older individuals are more tolerant of of cold water, but due to the extreme rarity of surface behavior in Masturus it may be a while before this is confirmed.

Masturus has very recently become the target of a fishery off Eastern Taiwan and this gave Liu et al. (2009) an opportunity to examine the basic biology of the species. The population ranged in length from 42 to 192 cm (SL - the clavus was often damaged) with most individuals between 80 and 119 cm (Liu et al. 2009). All specimens over 158 cm SL were female although since only one gravid individual was recorded it appears likely that this locale is not a spawning ground for the species (Liu et al. 2009). The authors speculated that juveniles may frequent inshore nurseries (where the fisheries primarily operate) while the adults occur further offshore - they noted that specimens greatly exceeding the maxima in their study have been recorded (262.5 cm SL/313.8 cm TL - another 337 cm TL*) (Liu et al. 2009). Vertebra centra were examined for rings and working under the assumption that ring count correlated with age (it did correlate with size) this indicates that their largest female was 23 years old and longevities were estimated to be 105 and 82 years for females and males, respectively (Liu et al. 2009). The authors note that the lack of very young and old specimens can greatly affect growth estimates and of course it can't be emphasized enough that ring formation may be caused by events which do not occur annually. It seems unlikely that data pools as extensive as that of Liu et al. (2009) will be encountered elsewhere (fortunately, in a way) and it appears exceedingly unlikely that a mark-recapture study or study of captive specimens** can resolve the questions of growth and longevity in Masturus - presumably a model species can be used to answer the question that the authors brought up but couldn't answer: if the fishery will lead to a decline of stocks.

* Assuming this is a female, it would have a SL of 282 cm from the equation established in Liu et al. (2009) and 281 cm extrapolating from the largest fish with both TL/SL measurements - this seems to imply that the clavus length has the same proportion throughout life after all. A male, by the way, would have an estimated SL of 277 cm, implying that this is not a dimorphic trait.

What's especially confusing to me is that estimating the weight of the 282 cm SL individual from the equations set up by the authors yields weights of ~1000-1200 kg (the larger from a male) and scaling up from their largest individual (195 cm SL, 409) also yields ~1200 kg. This seems very strange since a 2.7 m Mola (TL?) weighs around 2.3 tonnes - how on earth can a Masturus of roughly the same linear dimensions weigh around half as much? More data on large Masturus individuals, with clearly differentiated total and standard lengths, is desirable to solve this puzzle!

** At least one Mola in an aquarium gained weight extremely quickly and possibly abnormally. If they can actually grow this quickly in the wild then perhaps the Masturus fishery won't totally wreck the population... in the near future.

It's amazing that a species for whom the discovery of a single specimen was notable several decades ago (e.g. Gudger 1935) is now being harvested by the ton - and hardly any more is known about it. While the cosmopolitan range of the species and lack of direct harvesting in most locales probably prevents it from being in any direct danger, exploiting an organism with little known about its basic biology is a dangerous game.

There's still one more molid left, the smallest, most basal, and arguably most neglected of them all!

References:

Bass, Anna L., et al. 2005. Evolutionary divergence among lineages of the ocean sunfish family, Molidae (Tetraodontiformes). Marine Biology 148, 404-415

Gregorova, Ruzena, et al. 2009. A giant early Miocene sunfish from the North Apline Foreland basin (Austria) and its implications for molid phylogeny. Journal of Vertebrate Paleontology 29, 359–371.

Gudger, E. W. 1935. A photograph and description of Masturus lanceolatus taken at Tahiti, May, 1930. American Museum Novitates 778, 1-7. Available

Liu, Kwang-Ming, et al. 2009. Age and growth estimates of the sharptail mola, Masturus lanceolatus, in waters of eastern Taiwan. Fisheries Research 95, 154-160

Seitz, A. C., et al. 2002. Behaviour of a sharptail mola in the Gulf of Mexico. Journal of Fish Biology 60, 1597–1602.

The Molids, part 2: Beyond Mola mola

In the previous post I argued that molids were among the strangest of fishes on the basis of peculiarities such as their loss of a caudal fin and the development of an analgous clavus from the dorsal and anal fins, non-bilaterally symmetrical flight from those dorsal and anal fins, half a trunk lateral line (related to clavus development?), a diet heavy in jellyfish despite body masses often in the hundreds of kilograms (and sometimes tonnes), and so forth. I forgot to work in the outrageous fecundity of females (300 million eggs in a 1.4 m individual) and the two larval stages which resemble pufferfish. Most of these figures pertain to Mola mola, but there are of course other species of extant molids.

It's always interesting how some clades have a "flagship" species of sorts with all the charisma and press while the majority of the diversity languishes in obscurity. Molid taxonomy has long been a mess with 54 proposed species and missing type specimens, but these days 3 "genera" and 3-5 species are typically listed (Bass et al. 2005, also citing Parente 2003, Fishbase). Bass et al. (2005) used data from the d-loop and cytochrome b of molids to establish a phylogeny of the group and were surprised that some Southern hemisphere Mola specimens were estimated to have diverged 2.8-7.5 mya from the other major clade (Bass et al. 2005). The authors resurrected the name Mola ramsayi for the divergent clade and noted that both species were recorded from South Africa (Bass et al. 2005). It appears that field workers are not able to distinguish the species (voucher specimens were lacking for Bass et al.'s study, however) which implies very similar morphology and prior workers suggested that M. ramsayi can be distinguished by more numerous fin rays and larger ossicles on the clavus (Bass et al. 2005, also citing Giglioli 1883, Fraser-Brunner 1951). Also unexpected was that the Atlantic and Indo-Pacific M. mola populations were estimated to have diverged very recently (0.05-0.32 mya) while the M. ramsayi populations in the southern portions of the same oceans apparently diverged much earlier (1.55-4.10 mya) (Bass et al. 2005). Further studies will be needed to clear up the biogeography and morphology of M. ramsayi, and things certainly haven't gotten any simpler...

Yoshita et al. (2009) examined mitochondrial D-loop data from 119 Mola specimens and found three distinct clades, two of which overlap off Japan. The group A clade (n = 20) mostly occurred off the Eastern coast of Japan (2 were from Australia) and was remarkable for being composed entirely of females (and unsexed fish) with an average total length of ~2.6 m (+/- 0.5 m) which increased with latitude - all 9 specimens from the Northeast of Japan were over 249 cm and one measured 332 cm* (Yoshita et al. 2009). The group A Mola clade also had distinctive morphological traits such as a well-developed head bump, a proportionally longer anterior portion of the body, a proportionally deeper body, 14-17 clavus fin rays, 8-15 clavus ossicles, and a clavus edge that was never wavy (Yoshita et al. 2009). It appears that the historical Fiona specimen (not the world record holder, see the footnote) displays this morphology - as opposed to this more typical aquarium specimen. The authors suggest that the infrequency, size, and possible sex bias of group A specimens caught off Japan indicates that the main population could occur near the Bonin Islands (a migration route could be present) and suggest that the clade may be primarily a Southern Hemisphere one (Yoshita et al. 2009). Alternately, it was suggested that group A could have a migration route from the Eastern or Northern parts of the Pacific to Japan since the northeastern Japanese and subtropical group A fish showed significant divergence (Yoshita et al. 2009). It is not clear if group A is synonymous with Mola ramsayi and if not, presumably either another name could be resurrected or one will be coined if none of the prior names provided an appropriate description.

* This is probably the largest reliably recorded bony fish to date. Fishbase mentions a 333 cm specimen (not the 10'2"/3.1 Fiona specimen) but I can't find the source to assess its reliability. The 332 cm female fish (caught in 2004) was no outlier as 323 cm (2004 - unsexed), 325 cm (1999 - unsexed), and 330 cm (2002 - unsexed) fish were all recently found in a small sample - all were from Japan and Group A (Yoshita et al. 2009). This fascinating article reveals that the Fiona specimen (3.1 m/2.2 tonnes) was probably never weighed since a 2.7 m Mola (from Japan, of course) weighed 2.3 tonnes - by my calculations the Fiona specimen was about 1.3 tonnes "short" and a 3.3 m Mola could weigh over, gulp, 4 tonnes.

Oh, and since Austria has a rather northerly latitude, it could be possible that the Austromola fossils represent a similar population consisting of very large animals (females?) and the actual median length could be the same as the Mola species.

Group B Mola were found to be widely distributed in the Kuroshio current and grouped with M. mola from outside Japan, including Atlantic specimens Yoshita et al. (2009). This clade was notable for having a much smaller mean size (1 m =/- 0.6 m, n = 86), a wavy clavus in larger individuals (1.9-2.7 m, n = 11), a smooth band at the base of the clavus (also present in group B), 12 rays and 8-9 ossicles on the clavus, recorded males, and no significant differences between the sexes (Yoshita et al. 2009). The morphology and genetics of this group match what was previously established for Mola mola (Yoshita et al. 2009)..

Group C Mola corresponded somewhat with the species Mola ramsayi established by Bass et al. (2005) - although one member of that clade from Australia was placed in group A by Yoshita et al. (2009) - oddly enough authors of the latter study did find a group C individual from New South Wales, Australia. The monophyly of group C was supported by a very high bootstrap by Yoshita et al. (2009) but it should be noted that the sample size was only 3 and it was found to be the sister clade to group A. While the evidence presented by the authors suggests of three Mola species, clearly group C needs many more samples in order to be convincingly demonstrated to be a distinct species. And then people need to argue over which clade gets to be M. ramsayi... there's a long way to go.

The re-recognition of multiple Mola species is going to necessitate a revision of basic biological information. Future studies will have to be careful to differentiate between populations/species as to not create chimerical data - hopefully then we'll get a clearer picture of just how these species are separated geographically and possibly behaviorally and ecologically. If large (entirely female?) group B individuals really are a minor presence in very heavily fished areas, perhaps this should be looked into as a concern for conservation.

I'm not done with molids yet - Mola is not the only one!

References:

Bass, Anna L., et al. 2005. Evolutionary divergence among lineages of the ocean sunfish family, Molidae (Tetraodontiformes). Marine Biology 148, 404-415

Wood, Gerald. 1982. Guinness Book of Animal Facts and Feats. Third Edition.

Yoshita, Yukiko, et al. 2009. Phylogenetic relationship of two Mola sunfishes (Tetraodontiformes: Molidae) occurring around the coast of Japan, with notes on their geographical distribution and morphological characteristics. Ichthyological Research 56, 232-244

The Molids, part 1: Intro and Mola mola

Of all the variations on the vertebrate "fish" body plan, molids are among the most bizarre. Yes, I'm well aware of how strange some other "fish" are. Members of the already oddball clade Tetraodontiformes, molids have the general appearance of swimming heads (German: "Schwimmender kopf"), have the fewest vertebrae of any "fish" (16-18) and lack the following structures*: caudal bones, ribs, pelvic fins, [fin] spines, girdles, and swim bladders (Fishbase, Bass et al. 2005 - citing Tyler 1980). Their skeletons have to be seen in order to be believed and it's hard to imagine how reconstructions would look if these animals were only known from fossils. While other large aquatic vertebrates have generally similar tapering/streamlined body shapes (sea turtles excepted), molids have taken a more... attenuated approach:

Taken from here.

* Although Fishbase reports the lateral line to be absent, this was recently discovered not to be the case. Nakae and Sasaki (2006) noted that there are six cephalic and one trunk lateral lines; the latter structure has only 27 superficial neuromasts and is limited to the anterior portion of the fish. Interestingly, the same study discovered that what appears to be the caudal fin of molids (the clavus) is in fact derived from the dorsal and anal fins.

Mola mola is the largest extant actinopterygian ("bony fish") with a reported average length of 1.8 m (counting the clavus) and weight of one tonne (Wood 1987); they can reach 3.32 m and probably exceed four tonnes (see the next post for an explanation). Molids have a cartilaginous, weakly ossified, spongy skeleton and as a result were only known from fossil jaws and dermal plates until recently when three extraordinary upper Miocene (~22 mya) specimens were described from Austria (Gregorova et al. 2009). The Austromola angerhoferi individuals were estimated from Mola mola proportions to have total lengths of 1.5-1.7 m, 2.4 m, and 3.2 m - this would seem to suggest that Austromola had a much larger average size than the extant species (However - a Mola subpopulation off Japan has an even larger average size) (Gregorova et al. 2009). Potentially phenomenal size aside, Austromola bridges the gap between the Eocene (~42 mya) Eomola and Miocene to Pliocene fossils of extinct Mola and Ranzania species; Austromola is the sister taxa to Mola + Masturus which is in turn the sister clade to Ranzania (Gregorova et al. 2009). More on those non-Mola mola molids in the next post.

Much like the basking shark, recent tracking data demonstrates that molas are much more mobile than was previously anticipated. Despite the common name "oceanic sunfish", three small (~14-18 kg) specimens showed a general diel pattern (deeper at day and vice versa) and had a maximum recorded depth of 472 m - excluding one incident where the tracker went below 2000 m and presumably indicated the death of the fish (Sims et al. 2009). The diel pattern wasn't strictly adhered to as some fish stayed below 200 m for most of the day and at other times fish moved from their maximum depth to the surface in 4 hours (Sims et al. 2009). Vertical movements in Mola may be related to finding maximum prey concentrations (when the prey is on the move); other hypotheses for surfacing (not necessarily mutually exclusive) include warming, recovering from time spent in sub-oxic waters, or even to have parasites removed by sea birds (Sims et al. 2009). Prey densities also appear to be the driving force of Mola movements to high latitudes during summer and movements back are possibly due to thermal tolerance issues (Sims et al. 2009). Global warming could thus expand the seasonal thermal window at high latitudes for Mola and overfishing and eutrophication could increase jellyfish blooms - molids are some of the few large predators which have top-down control over the cnidarians (Sims et al. 2009). Exactly what sort of impact bycatch* has on molid populations is also an interesting question - this certainly seem like a species worth looking into.

* So exactly how numerous are molids? Aerial observations in the Irish and Celtic seas observed small individuals (0.5 to 0.7 m) at a density of about 1 individual per 100 square kilometers working under the assumption that they are not at the surface 3/4 of the time (Houghton et al. 2006). The authors note that the largest Mola specimen from British waters only weighed 363 kg (slightly above average?) which would either suggest that adult individuals don't bask often or are rarely present - or both. It's worth noting that molids are very commonly caught as bycatch (29-93% of all catch, in some instances), and while fish are released alive, this activity must have substantial (but as yet unknowable) impacts on the fish (Houghton et al. 2006). It takes an estimated 20 years to grow a large 3 m Mola mola in the wild, but one aquarium fish went from 26 kg to 400 kg in only 14 months.

Another Mola tracking study took a novel approach by including the leatherback turtle Dermochelys coriacea. Unexpectedly, the giant species have converged to feed on low-nutrient jellyfish prey - however Mola can feed extensively at depths around 500 m while the turtles spent time almost exclusively in the upper 200 m (Hays et al. 2009). Unlike Sims et al. (2009) the Mola specimens were closer to the reported average (1.08-1.60 m, 67-213 kg) - the turtle were fair-sized as well (~1.7 m and ~450 kg for 2 specimens) (Hays et al. 2009). It is interesting that in South Africa at least, molas stay broadly in the same location and leatherback turtles migrate extensively despite having a similar diet (Hays et al. 2009). The reason why there are multiple large jellyfish feeders (there are other molids after all...) wasn't explored by Hays et al. (2009) but this is of course an area of ecology that we are just beginning to understand. I'm going to assume that the turtles have some sort of advantage in shallower waters (capable of handling larger prey?) and that an equilibrium between the species probably varies between geographical locations (if oxygen levels at depth play a role, for instance).

But on a different note, as tracking studies imply, molids are not the planktonic weak swimmers they were long assumed to be. Watanabe and Sato (2008) used larger Mola specimens for their study (48, 59, 153 kg) and found that the tracked fish swam actively by stroking their fins and had cruising speeds roughly comparable to sturgeons, salmon, marlin, and blue sharks; larger fish swam slower to maintain the same Reynold's number (Watanabe and Sato 2008). Mola acceleration data indicated a one-stroke cycle with lift-based thrust similar to that previously reported in penguins - this is the only known instance of "wings" which are not bilaterally symmetrical (Watanabe and Sato 2008). The dorsal and anal fins are symmetrical in shape with identical muscle mass although the muscle morphology differs markedly; the aspect ratio of the fin/wings decreases possibly due to reasons of mechanical strength (Watanabe and Sato 2008). Watanabe and Sato (2008) also determined that Mola is neutrally buoyant due to a layer of gelatinous tissue (similar to deep-sea fishes); the incompressible tissue gives stable buoyancy at every depth unlike fish which rely on swim bladders for neutral buoyancy (Watanabe and Sato 2008).

More molids soon!

References:

Hays, Graeme C., et al. 2009. Vertical niche overlap by two ocean giants with similar diets: Ocean sunfish and leatherback turtles. Journal of Experimental Marine Biology and Ecology 370, 134–143

Houghton, Jonathon D. R., et al. 2006. The ocean sunfish Mola mola: insights into distribution, abundance and behaviour in the Irish and Celtic Seas. J. Mar. Biol. Ass. U.K. 86, 1237-1243

Gregorova, Ruzena, et al. 2009. A giant early Miocene sunfish from the North Apline Foreland basin (Austria) and its implications for molid phylogeny. Journal of Vertebrate Paleontology 29, 359–371.

Nakae, Masanori and Sasaki, Kunio. 2006. Peripheral nervous system of the ocean sunfish Mola mola (Tetraodontiformes: Molidae). Ichthyological Research 53, 233-246. Available

Sims, David W., et al. 2009. Satellite tracking of the World's largest bony fish, the ocean sunfish (Mola mola L.) in the North East Atlantic. Journal of Experimental Marine Biology and Ecology370, 127–133

Watanabe, Yuuki and Sato, Katsufumi. 2008. Functional Dorsoventral Symmetry in Relation to Lift-Based Swimming in the Ocean Sunfish Mola mola. PLoS ONE. Available

Wood, Gerald. 1982. The Guinness Book of Animal Facts and Feats. Third Edition.

The Basking Shark

First off, thanks to Markus Bühler of Bestiarium for inspiring this post by sending me this:

A juvenile basking shark 2.6 m in length from Izawa and Shibata (1993). I was completely unaware of this morphological feature - possible because only a handful of smaller specimens are known. Apparently the elongated snout functions in a similar manner as the cephalic fins of Manta rays.

As the above photo hopefully illustrates, many aspects of basking shark biology remain poorly known. I have a blatant bias towards covering large animals, but given the vulnerability and emerging literature on the animal, I think I can justify this post.

Tracking Basking Sharks

The most interesting aspect of basking shark biology which is now receiving long overdue attention is data on their range and movements. For several decades it was widely assumed (based on very circumstantial evidence) that basking sharks shed their gill rakers and "hibernated" in deep water for the winter! Basking sharks are observed year-round in Monterey Bay, although this population is apparently atypical (Francis and Duffy 2002). Francis and Duffy (2002) analyzed 203 basking shark records (consisting of sightings, captures, and strandings) from New Zealand and determined that basking sharks were swimming in midwater during the winter and did not lose their gillrakers. Sims et al. (2003) used "pop-up" satellite transmitters to gather tracking data for the first time in nearly two decades and directly demonstrated that hibernation does not occur (this study occured off the UK); the study also demonstrated that the sharks traveled extensively vertically and horizontally to productive areas. Skomal et al. (2004) demonstrated that the sharks do not hibernate off the West Atlantic and I think that old hibernation hypothesis can be regarded as completely dead.

Of course, these recent studies have done more than refute the bizarrely widespread hibernation hypothesis. Francis and Duffy (2002) provided unique records of basking sharks 4 km into the brackish Lake Ellesmere - made all the more impressive by (much more common) records of sharks off the continental shelf in water at least 904 m deep. Mancusi et al. (2005) provided the first data on basking sharks from the Eastern Mediterranean and Sandoval-Castillo et al. (2005) provided the first definitive records from Mexico (Pacific coast) - which leads up nicely to Skomal et al. (2009). Skomal et al. (2009) discovered, amazingly, that basking sharks do not have an antitropical distribution as widely assumed previously, but do live in the tropics after all! Sharks tagged off Cape Cod, Massachusetts and found tags in the Sargasso Sea, the Bahamas, Puerto Rican Trench, Caribbean Sea, Guyana, and Brazil - the latter record (a 6480 km trip) is the first transequatorial movement recorded via tagging from a "fish". It seems incredible that a species which was once heavily exploited completely avoided human detection over a considerable portion of its range - it goes to show that basic facts about megafauna are still being discerned. Mitochondrial DNA evidence from Hoelzel et al. (2006) demonstrates that basking sharks have low genetic diversity, a very low worldwide population (effective population ~10,000), and suggested a recent population bottleneck and worldwide panmixia; Skomal et al. (2009) suggested that if basking shark stocks are to recover there will have to be a worldwide effort.

Size & Growth

Since asymptotic size is used for growth calculations, this gives me an excuse to discuss basking shark size. The famous Stronsay carcass was described as a 16.8 m "beast" with all sorts of fanciful features - however its vertebrae were found to correspond exactly in morphology and size with a 9.3 m basking shark (then) recently described by Sir Everard Home (Wood 1982). Wood (1982) mentioned another case where a shark was lashed to the size of a boat and estimated via pacing at ~10.4 m - it was found to be 7.36 m when measured out of the water! Apparently other large figures have been obtained by measuring around the curve of the body. Such is the veracity of basking shark size claims - if a carcass hasn't been scientifically measured in recent decades the data should automatically be categorized as apocryphal.

This by all means doesn't mean that basking sharks aren't huge animals. Francis and Duffy (2002) looked at clasper length in assorted male basking sharks from New Zealand and determined that they reached sexual maturity at ~7.5 m in length; if this is accurate (and it may be somewhat conservative) it means that males in the East Coast region (<>

Anyways, Pauly (2002) used 10 m and ~7.5 tonnes* as an asymptotic size for a von Bertalanffy equation and determined (contra previous studies) that basking sharks do in fact grow very slowly, so slow in fact that they may have a gestation period of 2.6 years. The slow growth also implies considerable longevity (~50 years) and presumably a considerable age at maturity (well over 10 years judging by Figure 4) (Pauly 2002). Estimates of the mortality rate due to the fishery indicates it was impossible for any fish species to withstand for long, particularly one as extremely vulnerable as the basking shark (Pauly 2002). Compagno (2002) notes that in some regions basking sharks numbers have shown no signs of recovery even after decades. It's such a shame that some people are just catching on to this whole "responsibility" thing - hopefully those continuing to hunt the fish in East Asia will figure this out before yet another collapse occurs.

* Wood (1982) cites a 2.99 tonne/7 m individual which scales up to ~8.7 tonnes for 10 m. His 4.65 tonne/7.9 average figure scales up to ~9.4 tonnes for 10 m. I'm guessing that the weight estimation in Pauly (2002) is probably too conservative, but it would be nice to have more data on the subject.

That's about all I want to say about basking sharks. It certainly is remarkable that the biology of a species so heavily exploited could still be a largely emerging picture. Things aren't entirely bleak for the species and fortunately it is getting some good publicity.

References:

Compagno, Leonard J. V. 2002. Sharks of the World. Available (in part)

Francis, M. P. and Duffy, C. 2002. Distribution, seasonal abundance and bycatch of basking sharks (Cetorhinus maximus) in New Zealand, with observations on their winter habitat. Marine Biology 140, 831-842

Hoelzel, A. R. et al. 2006. Low worldwide genetic diversity in the basking shark (Cetorhinus maximus). Biol. Lett. 2, 639–642. Available

Izawa, Kunihiko and Shibata, Terukazu. 1993. A Young Basking Shark, Cetorhinus maximus, from Japan. Japan J. Ichthyol. 40, 237-245. Available

Mancusi, Cecilia et al. 2005. On the presence of basking shark (Cetorhinus maximus) in the Mediterranean Sea. Cybium 29, 399-405.

Pauly, D. 2002. Growth and mortality of the Basking Shark Cetorhinus maximus and their Implications for Management of Whale Sharks Rhincodon typus. In: Elasmobranch biodiversity: Conservation and Management. Available

Sandoval-Castillo, J. et al. 2005. First record of basking shark (Cetorhinus maximus) in Mexico? JMBA2 - Biodiversity Records

Sims, David W. et al. 2003. Seasonal movements and behaviour of basking sharks from archival tagging: no evidence of winter hibernation. Mar. Ecol. Prog. Ser. 248, 187-196. Available

Skomal, Gregory B. et al. 2004. Archival tagging of a basking shark, Cetorhinus maximus in the western North Atlantic. J. Mar. Biol. Ass. U.K. 84, 1-6.

Skomal, Gregory B. et al. 2009. Transequatorial Migrations by Basking Sharks in the Western Atlantic Ocean. Current Biology 19, 1–4.

Wood, Gerald. 1982. The Guinness Book of Animal Facts and Feats.