Invasion of the Armored Suckermouths!

Alternate title: Endangered pelicans try to swallow invasive catfish. Pelicans suffocate. Die.

Due to the probability of a cease-and-desist letter from England, I'll weave the hinted-at tale above into the tapestry of woe that the armored suckermouth catfishes have caused.

My highly derivative alternate title refers to a phenomenon that occurred in Oct. 1992* in the lower Loiza and Gurabo Rivers of Puerto Rico: at least twenty Brown Pelicans (Pelecanus occidentalis, a locally endangered species at the time) were found strangled to death with large armored suckermouth catfish (over 40 cm, 16" in length) lodged in their throats (Bunkley-Williams et al. 1994). It is worth pointing out that Brown Pelicans typically take prey under 25 cm in length (ref.), do not have bills over 16"/40 cm in length (according to this), and weigh 2-5 kg compared to the ~1 kg that the catfish weighed**. The possibility that Brown Pelicans can successfully swallow prey of that size cannot be precluded, so the extensive armor and unusual morphology*** of the catfish may have been the fatal factors. As to why the phenomenon was so widespread, the catfish became established in Puerto Rico only a few years before and their ease of capture may have prompted curiosity towards a new potential food source. No more reports have been published, so it is possible that the local Brown Pelican population has learned to avoid the catfish, which are probably now permanently established. And sorry to those seeking out morbid photos of the failed loricariid consumption, photographs do not seem to have been published, or even taken as far as I know.

* The table actually says "Ott 1992", I'm fairly certain it's a typo and not some hyper-obscure Latin abbreviation.

** The first recorded loricariid from Puerto Rico was a 1.8 kg, 51.2 cm "Hypostomus plecostomus" - this identification is dubious and the (lost) specimen was presumably the same species as the ones the pelicans swallowed (Bunkley-Williams et al. 1994). Anyways, extrapolating from that record gives 0.86 kg for a 40 cm specimen - I stated ~1 kg due to uncertainty and the implication that 40 cm was a minimum. 
*** Hoover et al. (2004) suggest that the dorsal and pectoral defensive spines were the cause of the mortalities.

Bunkley-Williams et al. (1994) identified the invasive loricariid catfish species as Liposarcus multiradiatus, which is now (again, actually) known as Pterygoplichthys multiradiatus. Puerto Rico has no native loricariids* and while a report occurred as early as 1983 (a likely accidental), P. multiradiatus became established in eight rivers and two reservoirs in the early 1990's, with numbers significant enough to support a local fishery in one area (Bunkley-Williams et al. 1994). While there are markets for the fish in the food and pet industries (at least one fish farm existed on the island for the latter purpose), Bunkley-Williams et al. (1994) suggested that the unexpectedly large size reached by the species led to amateur aquarists discarding them. The catfish appear to be incredibly tolerant of handling stress and can even reportedly survive out of the water for hours** (Bunkley-Williams et al. 1994).


* The type locality of Lasiancistrus guacharote (formerly Hypostomus) was Puerto Rico, but it turns out that this is in error, the species is actually from Venezuela and Columbia (Armbruster 2005). 
** Over 30 hours, in fact (Armbruster 1998 citing Val and De Almeida-Val 1995). They accomplish this by breathing air into an enlarged and highly vascularized stomach, which primarily functions to survive low-oxygen conditions in water (Armbruster 1998). Hoover et al. (2004) documented Pterygoplichthys specimens which apparently entered a period of estivation in burrows, from which they recovered as soon as they returned to water. The implication is that they can survive considerably longer than 30 hours out of the water. Oh, and they can also move on land during extreme environmental conditions.


If the trouble caused by Pterygoplichthys multiradiatus seems familiar, that's because a couple posts ago I discussed how P. disjunctivus (and/or hybrid descendants) specimens in Florida grazed on manatees to a likely deleterious effect. I didn't properly introduce the loricariid catfishes then, and I'm not sure how I passed on such a succulent tangent. So here's a scenic detour through the world of these bizarre armored suckermouth catfishes.

P. multiradiatus from the Wikipedia Commons.

Ideally, the common name "armored suckermouth catfishes" should be used for Loricariidae since they are not the only clade with extensive armor (Callichthyidae) nor are they the only ones with a sucker mouth (Astroblepidae). Loricariidae and Astroblepidae are sister clades (indicating the suckermouth is a shared derived character) and Callichthyidae is a more distant relative (indicating the extensive armor is convergent, unless lost numerous times) in the greater clade Loricarioidea, which includes everything from parasites to a monotypic oddity. Loricariidae itself has a staggering array of morphological variability: Panaque nigrolineatus (Ancistrinae) has an incredibly large head, Tim Burton-esque stripes, and the ability to digest wood with the aid of bacteria; some species (e.g. Farlowella amazonum - Loricariinae) have a body shape reminiscent of pipefish (likely for similar camouflage needs); the Sturisoma species and relatives (Loricariinae as well) look similar except with very exaggerated fins; dwarf suckermouths (Otocinclus et al. - Hypoptopomatinae) look more like generic tetra-like fishes than highly derived catfishes at first glance; one Ancistrus species is a blind cave-dweller, others have bizarre facial tentacles (Ancistrinae); Chaetostoma sovichthys (Ancistrinae) and relatives hardly look like fish at all in dorsal view - more like a revisitation of Cephalaspis or even the ichthyological answer to Triops. The point is, with 700+ species, Loricariidae is a very successful clade - considering they're mostly freshwater* and restricted to one continent. Adriaens et al. (2009) discussed the highly derived jaw morphology** which apparently allowed the loricariids to radiate into the algae-scraped niche; exactly how the numerous species differ niche-wise has not had much discussion.The species Adriaens et al. (2009) used as a model for their study of loricariid jaw mechanics? - Pterygoplichthys disjunctivus.

* Although sources like Fishbase state that they are strictly freshwater, Hoover et al. (2004) report that they occur in brackish water. 
** Catfish jaw morphology is normally conservative, but loricariid jaws have a uniquely mobile upper jaw (as in, it typically doesn't move at all in other catfishes) and the bones of the lower jaw are decoupled to allow for asymmetric scraping movement. 


Back to the invasive loricariids. As it appears that the most widespread and damaging taxa are a few related Pterygoplichthys species (e.g. within the genus), I'll be focusing on those sailfin catfishes - distinguishable by their large dorsal fins consisting of more than 10 rays. In addition to Puerto Rico and Florida, Hawaii has a particularly noteworthy population of Pterygoplichthys and several other genera of loricariids (Bunkley-Williams et al. 1994 - citing various). In the Philippines, P. disjunctivus and P. pardalis were present in the Laguna Lake region since the 1950's and in the early 2000's were found in the Agusan marsh, one of the largest in Asia (Hubilla et al. 2007). Members of Pterygoplichthys are also established in Taiwan, Singapore, Malaysia, Indonesia, and Mexico (Page and Robins 2006, Armando et al. 2007). While Pterygoplichthys spp. are reported from a few states in the mainland USA, there is a chance that like could go from localized to very widespread and wreak havoc (Hoover et al. 2004). So what makes these loricariids particularly damaging invasive species?

The Pterygoplichthys species are capable of far more severe impacts than choking pelicans and cleaning manatees. In fact, Hoover (2004) states that the variety and severity of the ecological impacts from the catfish are unprecedented. I can't emphasize that enough. Loricariids burrow into the banks of streams and lakes in order to spawn and take refuge from droughts and cold temperatures; this behavior can erode away 4 meters of bank annually and cause increased silt loads and turbidity (Hoover et al. 2004, Hubilla et al. 2007). The increased turbidity slows down photosynthesis and likely has negative effects on the food web and energy flow (Hubilla et al. 2007). The catfishes also plow into the substrate and uproot plants, which likely reduces the abundance of native plants and may even aid in the spread of invasive plants (Hoover 2004). Invasive Pterygoplichthys, being large and bewilderingly resilient species, likely outcompete the native algae consumers, aggressively drive them away, and consume the eggs of those species and others (Hoover 2004). The presence of a ravenous algae grazer may also reduce cover for aquatic insects and disrupt the food chain by prematurely diverting nutrients into feces Hoover 2004). Having owned Hypostomus plecostomus specimens in my life, I can't help but wonder if the prodigious amount of feces that loricariids produce has some sort of impact as well.

So what can be done to prevent the potential ravaging of aquatic freshwater ecosystems by invasive loricariids? Bunkley-Williams (1994) discussed the possibility of large predatory fish controlling Pterygoplichthys numbers (Peacock bass, Cichla ocellaris, and Largemouth bass, Micropterus salmoides), however they concluded that there was no known effective predator, disease, or parasite. The Philippines populations also do not appear to have any significant predation, even from native fishermen gillnets as they are damaged from the large fish (Hubilla et al. 2007). Hoover et al. (2004) and Hubilla (2007) suggest that fisheries, possibly with government incentive, could be a way of controlling populations (presumably with better equipment) as the fish are valued for their flesh and eggs. Hoover et al. (2004) also suggested protecting banks from burrowing and isolating the "infected" areas as method for preventing the problem from becoming very widespread. Hoover et al. (2004) and Bunkley-Williams et al. (1994) suggest public education to the prevent further release of loricariids and the latter publication proposed a program to return unwanted fish from amateur aquariums. Those two papers and Hubilla (2007) all suggest that environmental laws should be strengthened in order to prevent multiple Pterygoplichthys species or even multiple loricariid genera from being established. Bunkley-Williams (1994) doubt that the invasive species can ever be eradicated, but the chances of controlling the spread of the catfishes are still good if people recognize the problem before it gets completely out of control.

I'll admit that when I was a kid I released a large loricariid into a quarry before I moved. Even though it had no chances of becoming widespread, it was still a very dumb decision. So please, if you own these catfishes, whatever you do, don't release them into the wild!

References:

Adriaens, Dominique, et al. (2009). Extensive Jaw Mobility in Suckermouth Armored Catfishes (Loricariidae): A Morphological and Kinematic Analysis of Substrate Scraping Mode of Feeding. Journal of Experimental Biology 212, 116-125. Available.

Armando, T. et al. (2007). Amazon Sailfin Catfish Pterygoplichthys pardalis (Castelnau, 1855) (Loricariidae), another exotic species established in Southeastern Mexico. The Southwestern Naturalist 52(1), 141-144.

Armbruster, Jonathan W. (2005). The loricariid catfish genus Lasiancistrus (Siluriformes) with descriptions of two new species. Neotropical Ichthyology 3(4), 549-569. Available.

Armbruster, Jonathan W. (1998). Modifications of the Digestive Tract for Holding Air in Loricariid and Scoloplacid Catfishes. Copeia 1998(3), 663-675. Available.

Bunkley-Williams, Lucy, et al. (1994). The South American Sailfin Armored Catfish, Liposarcus multiradiatus (Hancock), a New Exotic Established in Puerto Rican Fresh Waters. Caribbean Journal of Science 30(1-2), 90-94. Available.

Hoover, Jan Jeffrey, et al. (2004). Suckermouth Catfishes: Threats to Aquatic Ecosystems of the United States? ANSRP Bulletin 04(1). Available.

Hubilla, Marianne, et al. (2007). Janitor Fishes Pterygoplichthys disjunctivus in the Agusan Marsh: a Thread to Freshwater Biodiversity. Journal of Environmental Science and Management 10(1), 10-21. Available.

Page, Lawrence W. and Robins, Robert H. (2006). Identification of Sailfin Catfishes (Teleostei: Loricariidae) in Southeastern Asia. The Raffles Bulletin of Zoology 54(2), 455-457. Available.

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 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.

On the Importance of Vultures

Torgos - of no relation to Manos. Taken from here.

Our anthropocentric stigma against scavengers is totally underserved and in fact, carrion consumption is a valuable ecological "service". The word "scavenger" is used fast and loose in popular parlance but the label should be restricted to animals which depend heavily on carrion; just about every vertebrate which can consume meat (including many "herbivores") won't hesitate to snack on a corpse here and there - even humans. The three independent lineages of vultures have specialized for locating and feeding on carrion and utilize the resource to the degree that they can be known as "obligate scavengers" - although it should be noted that it is not their sole food source.

Just to get the word out, nothing said in this article applies to the so-called "Palm-nut vulture" Gypohierax angolensis which is specialized for eating palm nuts (!) and feeds on fish (!!), live prey, and then carrion to a lesser extent (Mundy et al. 1992). Gypohierax is closely related to the gypaetine vultures (both fairly aberrant)... but also Polyboroides and Eutriorchis (Griffiths et al. 2007, Lerner and Mindell 2005). Oh, and the whole "New World"/"Old World" schism is a false dichotomy as these vultures didn't pay attention to those biogeographical rules earlier in their evolution. Anyways, back to the post:

Carrion is an ephemeral and unpredictable resource so it is no surprise that the vertebrates which depend on it the most can fly. Vultures all have large wingspans and locomote by soaring flight (Ruxton and Houston 2004); their stomach acid has a very low pH (1) and is apparently capable of resisting/detoxifying bacteria (Sekercioglu 2006); bald heads and necks don't correlate well with messy feeding habits (contra Mundy et al. 1992) but function along with postural changes as a thermoregulatory mechanism vital to these birds which may deal with rapidly-changing temperatures ranging from <0>70 °C (due to altitude) (Ward et al. 2008). Hertel (1995) outlined the morphological traits shared by these lineages: the long, narrow, shallow, and highly curved maxilla is designed for hooking or slicing large chunks of meat (comparable in function to a meathook); the deep ramus is an adaptation for dorsoventral forces correlated with rapid consumption; there is a large angle between the foramen magnum and basicranium reflecting the strait line of pulling force of the head and neck (avivores, in comparison, have an angle approaching 90 degrees); the narrow ramus and shallow mandibular symphysis indicate a lack of resistance to struggling prey; the occipital distance is greater and orbits are smaller (scavengers are less dependant on eyesight, apparently).

First: Accipiter cooperi - modified from here. This species is a functional avivore and contrasts strongly in form and function with the scavenger lineages. Hertel (1995) compared them to staplers or churchkey can openers function-wise.

Second: Neophron percnopterus - modified from here. A member of the gypaetine vulture lineage(s?). Skull indices of this species and one of its extinct North American relatives (Neophrontops americanus) are well into the "scavenger" ecomorph range despite the extant species taking a broad range of food in addition to carrion (Hertel 1995, Mundy et al. 1992).

Third: Gyps tenuirostris - modified from here. An aegypiine vulture - of all the 13 species in this lineage the 8 Gyps are the most specialized for scavenging (Mundy et al. 1992).

Fourth: Coragyps atratus - modified from here. A member of the cathartid lineage; they're distant relatives of the other vulture lineages but it isn't clear to what degree.

Although functionally similar, there are distinct lineages of gypaetine, aegypiine, and cathartid vultures. The birds which can be called gypaetine vultures are abarrent scavengers; Gypaetus barbatus feeds mostly on bone marrow (it appears to retain vulture-like skull indices despite this); Neophron percnopterus keeps a low profile at large mammal carcasses, is an important small animal scavenger/predator, feeds on eggs, and also consumes fecal matter (preferring carnivore and... human) (Mundy et al 1992). The gypaetine vultures are more basal in the order Falconiformes/Accipitriformes and appear to be allied to the pernine kites; the more familiar aegypiine vultures are more derived and have been recovered in a position somewhere near some of the serpent eagles (long story - see Griffiths et al. 2007 and Lerner and Mindell 2005). Cathartids are, well, certainly not storks and are either basal member of Falconiformes/Accipitriformes (also a long story) or a distinct (ordinal-level?) clade located nearby in a huge mess (see Livezey and Zusi (2007) & Hackett et al. (2008) for the former placement - Morgan-Richards et al. (2008) (and similar mtDNA studies it cites) for the latter).

I think we have been sufficiently introduced to vultures.

So just why is scavenging important? It isn't just some biological curiosity - most animals die from causes unrelated to predation and most of their biomass is consumed by vertebrates (and not microbes and invertebrates) (Devault et al. 2003). Turkey vultures (Cathartes aura) were observed to scavenge every experimentally placed carcass (which wasn't badly decomposed) in a forested environment within three days and vultures on the Serengeti have been observed to consume most of the large, conspicuous carcasses (Devault et al. 2003 - citing Houston 1979, 1986, 1988). So forget the image of vultures cleaning up after lions on the savannah - they consume staggering amounts of biomass from carcasses the size of mice to elephants in temperate and tropical environments worldwide (except Australia...).

It is unfortunate that the loss of Gyps vultures in South Asia due to diclofenac poisoning has demonstrated just how important they were in the ecosystem. The near-extinction of the vultures caused an explosion in the feral dog and rat population and the potential for disease could impact domestic animals and humans (Pain et al. 2003, Prakash et al. 2005). Interestingly, while the importance of facultative scavengers cannot be overstated, these scavengers (such as crows, gulls, starlings) lack the ability to deal with pathogens present in vultures and are more prone to spreading them (Blanco et al. 2006).

Although it appears that vultures are important ecosystem players, facultative scavengers seem to get the job done without them in boreal areas, Australia, and some islands. Perhaps areas with relatively low terrestrial production simply can't support the needs of obligate scavengers and the more generalized species wholly exclude them. The fossil record before the K/T event does not appear to show a community of vulture analogues as none of the pterosaurs and basal birds (that I'm aware of!) show the characteristic skull indices outlined by Hertel (1995) - so presumably a wide variety of facultative scavengers can cover for vultures even in areas with high production. Whatever was going on, in a good portion of our world today vultures are vital parts of the ecosystem and their worldwide decline could be disastrous for a number of as-yet unseen reasons.

Obligate scavengers will even eat facultative scavengers.

Photo taken from here.

References:

Blanco et al. 2006. Faecal bacteria associated with different diets of wintering red kites: influence of livestock carcass dumps in microflora alteration and pathogen acquisition. J. Appl. Ecol. 43, 990–999.

DeVault, Travis L. et al. 2003. Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102, 225-234

Hertel, Fritz. 1995. Ecomorphological Indicators of Feeding Behavior in Recent and Fossil Raptors. The Auk 112, 890-903.

Griffiths, Carole S. et al. 2007. Phylogeny, diversity, and classification of the Accipitridae based on DNA sequences of the RAG-1 exon. J. Avon. Biol. 38, 587-602

Hackett, Shannon J. et al. 2008. A Phylogenomic study of Birds Reveals Their Evolutionary History. Science 320, 1763-1768.

Lerner, H. R. L. and Mindell, D. P. 2005. Phylogeny of eagles, Old World vultures, and other Accipitridae based on nuclear and mitochondrial DNA. Mol. Phyl. Evol. 37, 327-346

Livezy, Bradley C. and Zusi, Richard L. 2007. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion. Zool. J. Linn. Soc. 149, 1-95

Morgan-Richards, Mary et al. 2008. Bird evolution: testing the Metaves clade with six new mitochondrial genomes. BMC Evolutionary Biology 8

Mundy, Peter et al. 1992. The Vulture of Africa. Academic Press

Pain, D. et al. 2003. Causes and effects of temporospatial declines of Gyps vultures. Asia. Cons. Biol. 17, 661–671.

Prakash, V. et al. 2005. Catastrophic collapse of Indian white-backed Gyps bengalensis and long-billed Gyps indicus vulture populations. Biol. Cons. 109, 381–390.

Ruxton, Graeme D. and Houston, David C. 2004. Obligate vertebrate scavengers must be large soaring fliers. Journal of Theoretical Biology 228, 431-436

Sekercioglu, Cagan H. 2006. Increasing awareness of avian ecological functions. TRENDS in Ecology and Evolution 21, 464-471

Ward, Jennifer et al. 2008. Why do vultures have bald heads? The role of postural adjustment and bare skin areas in thermoregulation. Journal of Thermal Biology 33, 168-173.

Whelan, Christopher J. et al. 2008. Ecosystem services provided by birds. Annals of the New York Academy of Sciences 1134, 25-60