On Whales and Their Usefulness

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On Whales and their Usefulness

N°1

April 2010

On Whales and their Usefulness

Summary

Introduction ……………………………………………………………………………………………... 3

I – Stage 1……………………………………………………………………………………………….. 5 Amphipods, sharks, hagfish, black seasnail, grenadiers, sablefish padgy cuskeel

II – Stage 2……………………………………………………………………………………….…… 10 Sea cucumbers, annelids, osedax, crabs.

III – Stage 3…………………..……………………………………………………………………...... 13 Sulphophilic period

IV – Stage 4……………………………………………………………………………………….….. 14 The reef

Conclusions……………………………………………………………………………………………… 14

Recommandations …………………………………………………………………………………… 14

Map:……………………………………………………………………………………………………... 15 Inventory of studied whale remain sights

Bibliography……………………………………………………………………………………………... 16

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On Whales and their Usefulness

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et al. 200 Braby © A polar crab on grey whale remains grazing on a carpet made of bone scavenging organisms

Introduction

Scientists have long thought that animal and vegetal life in the sea was exclusively dependent on solar energy and photosynthesis. After the discovery in 1977 of hydrothermal vents and cold seeps in the deep-sea, they thought that only these geological phenomenons could generate and assemble biological communities based on the association of bacteria transforming sulphur into organic matter and fauna evolving in an obscure yet colourful environment; but ten years later new discoveries have proved that whale carcasses and their skeletons in the aphotic zones of the ocean are also sources of life thanks to the symbiosis between bacteria and many extreme and hyper specialised animal species.

The deep-sea includes water and seafloors below 200m, representing 64% of the Earth’s surface and 90% of the world’s oceans which feature an average depth of 3,730m. The oceans’ seafloors have long been seen as an isolated compartment yet recent advances of knowledge show that deep waters and species are vertically and horizontally connected to shallow waters through currents; this enrichment process takes place in both directions. Thus it is known for example that deep-sea fish species are contaminated by PCBs from surface waters.

Ecological services rendered to the Earth by the deep-sea are beginning to be better understood, for instance primary food production of chemosynthetic bacteria and the recycling of ocean nutriments without which primary production in the ocean photic zones would collapse.

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When dead whales fall to the dark seafloor, where phytoplankton cannot develop, carcasses are used both as food and habitats by hundreds of fish and invertebrate species. For instance, the octopus below resides in a grey whale skull 2,891m deep.

Whales are accused by whaling countries of depleting commercial fish stocks, but their role after death as well as that of other marine mammals in conservation of marine biodiversity and dispersal of deep sea species is largely unknown and underestimated. On the contrary, the reduction of whale falls caused by historical and ongoing hunting as well as pollution is a disadvantage for biodiversity and fish.

In the deep-sea, whale falls resemble oases in terrestrial deserts, along with sea snow, made up of dead plankton, crustacean molts, shell waste, diverse excretions and riverine inputs, falling at a rate of approximately 300m a day eventually covering the abyssal depths, the arrival of a food reserve such as a 40 ton whale is an opportunity for fish and other scavengers. All at once, the equivalent of 2,000 years of organic carbon falls, concentrate on about 50m² of sediment.

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200 © MBARI Whale remains and biodiversity: sea cucumbers, crabs and a profusion of osedax worms.

In the case of larger specimens, the decomposing of a whale carcass could last over 100 years and follows four overlapping stages:

1- The mobile scavenger stage, including fish and amphipods, which can last up to ten years when flesh and soft tissues are removed from the carcass.

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2- The opportunistic stage includes bacteria and invertebrate species on the skeleton and surrounding sediments. 3- The sulphur stage lasting up to 50 years during which worms and bivalves live in symbiosis with bacteria transforming sulphur hydrogen into organic and nutritious sulphur. 4- The reef stage.

I- Stage 1

From 40 to 60 kg of flesh and soft tissues are removed per day. Thirty-eight faunal species have been identified. Macro fauna can be defined as organisms visible to the naked eye. The chronological scheme is as follows: crustacean plankton, sharks, and scavenger fish. The crustaceans are part of the diet of black snailfish, sablefish, crabs and opportunistic fish. This stage is characterised by high density but low diversity of species. Large numbers of amphipods and copepods consume most of the flesh. They break through the skin and create tunnels that ease access to muscles and fatty tissue for other predators.

Amphipods

AWI d'Acoz/ d'Udekem © Cédric / Wikimedia© Uwe Kils

The order of amphipods in the crustaceans class are present in the world’s ocean down to the hadal zones, situated below the abyssal zone. They resemble shrimps. Amphipods are eaten by fish, invertebrates, penguins, birds and marine mammals. Mean length ranges between 4 and 10 mm. The best known amphipod species are sand fleas or talitridae that jump onto beaches and feed off organic waste in the inter-tidal zone. They are usually carnivorous and waste eating organisms. These planktonic organisms do not have autonomous swimming capabilities over long distances therefore they are displaced by currents.

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Sharks

Among the first to arrive at the whale fall are Pacific sleeper sharks (Somniosus pacificus) who can reach depths of 2,000m. These polar sharks are physiologically adapted to very low temperatures. Many are incidentally caught by trawlers in the Gulf of Alaska. Biology and physical characteristics of the Pacific sleeper shark are poorly known particularly concerning the reproduction cycle and gestation time. At birth, they can measure less than 40 cm and adults could reach up to 7 m long. Due to lack of data, the conservation status of the Pacific sleeper shark is unknown. Pacific sleeper sharks of 1.5 to 3.5 meters were seen feeding voraciously on the carcass of a grey whale and close to another carcass. From the observation of bite marks, it has been estimated that these sharks consume more of the whale flesh than other fish species.

I 2004 MBAR -

According to a Swedish study, bite marks on a Minke whale fall (Balaenoptera acutostrata) in the North Sea show the presence of a different species of sharks. This species could be the Greenland shark (Somniosus microcephalus). Historical exploitation of this shark peaked in 1910, its liver oil was sought for its alleged strengthening virtues. Today it is occasionally a by- catch from trawling and other fishing methods. It is for this reason that it is now considered an endangered species.

Hagfish

Hagfish (Myxinidae) can be sighted by the hundreds on whale falls, mainly black hagfish (Eptatretus deani) and Whiteheaded hagfish (Myxine circifrons). Hagfish designates a uniform group of about 60 species found in cold and deep water.

They are considered to be the most primitive forms of fish. There is no notable difference between a 300 million year old fossil and a specimen living today. They live about 5 years and their mean length is 60 cm long. Ranging across the oceans, they can live in depths of 3,000 m and can inhabit areas as close as 40 m below the water surface and have developed surprising capabilities. They constitute the only fish species known to have in their blood the same level of salt as in the immediate surroundings. When attacked, they produce from 5 grams of excreted dry fibre up to 20 litres of a viscous substance obtained from the excretion of the fibre and its mixing with seawater. This substance could clog the gills of predatory fish. They owe their name to the Greek word musca (mucus). Hagfish feed off dead or dying fish and marine mammals. A large number are found in the by-catches of trawlers specialised in deep sea fishing; they seem to have acquired the habit of preying on trapped dead or dying fish.

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They take up residence inside the carcass of the whales where they can resist exceptionally high levels of carbon gas and methane for days. Hagfish are thought to have been attracted to carcasses off the Californian coast from a perimeter of 0.6 to 0.8 km by smell or other sensor signals.

: Source http://leatherplaza.tripod.com/

They are eaten in Asian countries and their smooth skin is used to make leather, called “eel skin leather”, mainly in Japan and South Korea. Fishery efforts peaked in 1986, worsened by the regular loss of over 200 traps a month that long after continued “ghost fishing”. In California, fishermen use M5-222, a chemical anesthesia, to kill the hagfish caught in traps. Korean importers demand that the skins be without traces of bite marks or other defects. Stocks of hagfish seem to be largely depleting in Korean waters and in Asian waters in general, therefore local industries have to look for imports. The know-how of Korean tanners is then exported around the world. Due to insufficient data the status of the hagfish is unknown because of this lack of knowledge concerning population rates, fishing aimed at the many species of hagfish threaten to lead them to extinction.

Black seasnail

The black seasnail (Paraliparis bathibius) is a fish of the liparid or sea snail family, of about 25 cm in length which lives in the deep ocean between 1,000 and 4,000m. The black seasnail feeds on amphipods, benthic gasteropods and small waste eating shrimp that rapidly colonise the whale fall.

Some species such as the Pseudoliparis amblystomopsis live in the hadal zone between 6,000 and 11,000m deep and support pressures of up to 8,000 tonnes per m². Unlike other deep sea fish, the seasnails live in groups and are very mobile. Species of the hadal zone are unique to their environment that is in the trenches of the Pacific Ocean: the Peru-Chile trench the Tonga-

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Kermadec trench and in the North West the Japan trench. Each species is confined, because the larval dissemination is refrained by geological configurations.

Two species of liparid fish live in symbiosis with the gold king crab (lithodes aesquipinus) in subarctic waters (Alaska, Bering Sea, Aleutian Islands). The brachial chambers of the gold king crab offer to snailfish eggs and larvae an environment which is ventilated and protected from predators, except fishermen. Species of liparid fish and king crab (with no other precision given) were found on whale falls.

Grenadiers 7

Grenadiers are commonly observed on whale fall sites. The most noted species is the abyssal grenadier (Coryphaenoides armatus) that lives around depths of 5,000m, but the deep sea grenadier (Coryphaenoides profundicolus) (around 4,800m) and the california grenadier (Nezumia stegidolepsis) (up to 900m) and other non specified species from the Macrouridae family have also been seen. It does not seem to feed preferentially off the whales flesh, but mainly on shrimp, amphipodes and other invertebrates which colonise the carcass first.

In the world’s ocean deep sea fish have been submitted to dragnet fishing for 40 years. During the 70s some species such as emperors (Hoplostethus atlanticus) or Beryx (Bericidae) were severely exploited and decimated. These slow growing fish with late sexual maturity associated with low fecundity rates are very vulnerable to uncontrolled fishing activities. The decrease of whale falls, in particular healthy adult individuals belonging to the larger species such as blue whales (Balaenoptera musculus) and sperm whales (Physeter macrocephalus), is undoubtedly an additional factor of food depletion for deep sea fish, more particularly in the foreground are those submitted to fishing such as the rock grenadier that lives in depths of 180 to 2,200m, its stocks are at very low levels, and even nearing extinction. It should be noted that the passage of trawl nets on the ocean floor could destroy these biological oasis which are made up of whale remains.

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Sablefish

The sablefish (Anoplopoma fimbria) participate actively in the mobile scavenger stage following observations of a gray whale’s remains (Eschrichtius robustus) discovered in the Santa Calatina Bassin off the coast of California.

The sablefish is present only in the Pacific Ocean. Attaining maturity at around 5 years, with a life span of up to 90 years, the oldest specimen captured was 113 years old, mean measures are 55cm long. The sablefish lives at depths of 300 to 1,800m. Feeding on small fish, benthic worms, plankton and crustacean that are found in abundance on whale falls. The larvae feed exclusively on calanoid copepods, a zooplankton found in large numbers around carcasses. A yearly population recruitment figure of the sablefish is directly related to the abundance of copepods.

Sablefish fisheries had an estimated value of $ 29 million US in the early 2000s, but the annual quota of 2,800 tonnes has been reduced. A large number of by-catches occur during this type of fishing especially birds and in particular albatross (Phoebastria albatrus) who are threatened by extinction. According to fishermen sightings, sperm whales try to catch sablefish caught on longline fishing hooks and are scared off with dissuasive grenades. At least one sperm whale has been killed by such practices. The largest part of the fishing is carried out in the United States and in Canada and is exported to Asia, mainly to Japan.

The Pudgy Cuskeel

The pudgy cuskeel (Spectruculus grandis) is another deep sea fish belonging to the Ophidiidae family. It feeds on cephalopods, decapods, shrimp, polycheats, echinoderms and planctonic crustacean; such food resources are present around whale carcasses. The commercial interest seems to be minor yet as the pudgy cuskeel is present in deep sea fishing areas it is therefore

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II – Stage 2

According to the size and weight of the whale fall, this stage can last from 4 months to 5 years. After the removal of flesh and soft tissue from the carcass lying on the sea floor, sediments up to 3 meters around the carcass are enriched by organic material which accumulates as would crumbs after a feast. Within 4 months, the density of macrofauna visible to the naked eye exceeds 40,000 individuals per m², which is the highest density ever observed in the deep sea. Meanwhile, the sediment enrichment can be active over a 30 meter distance according to observations which took place on the gray whale of Santa Cruz where, 18 months after it sank on the sea floor the density of nematods was comparable to the areas richest in phytodetritus. Nematods are an essential link in marine life cycles. Whale fall therefore generate complex ecosystems and trophic webs between worms, amphipods, decapods, echinoderms, clams and fish.

Sea cucumbers

The Scotoplanes clarki is visible at densities of 60 to 90 individuals per m² in sediments around a whale fall. They grind and consume the sediments and organic matter, modify the habitat structure and facilitate the installation of other species. This process avoids the accumulation of decomposing organic matter. Sea cucumbers are farmers. The common species in the Atlantic Ocean is the Isostichopus badinonotus which measures 20cm and transforms 160 grams of ocean debris in 24 hours.

They are threatened by over exploitation to cater for international luxury food and aquarium markets as well as biomedical research. The observed density in shallow waters where the sea cucumbers are exploited is around one individual per m².

Annelids

Between 1,000 and 1,670m deep, a sperm whale and two gray whales carcasses were colonized by a yet unknown species of annelid. With extraordinary abundance attaining densities of 8,000 individuals per m², forming a sort of waving yellow-to-red mat covering the bones or sediments. The fact that there is no other known habitat leads one to believe that Vigtorniella flokati is a whale carcass specialist in the deep sea. The feeding mechanism of this species remains unknown but it is hypothesised by scientists that it finds nourishment in dissolved organic carbon produced by soft tissue and bones. No predation has been observed on this species but V. flokati could be a prey to galathea crabs and other invertebrates. The prolific larvae and their long life span enable the species to reproduce rapidly on a chosen site as well as to be projected along with plankton dispersion toward other sites to be colonized. Along the grey whale migration path between Mexico and Alaska at least one carcass would be on the ocean floor every 16km. Thanks to their dynamics and specialisation the V. flokati and its likes could be the builders of a unique biological corridor, a sort of biological benthic path linking the deep sunken whale fall sites.

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Another whale loving species (Vryenkoekia balaenophilia) was discovered on the same grey whale carcasses. This swimming worm 2.5cm long is covered with about 50 antennas it belongs to a genus which is generally not adapted to the abyssal depths, with the notable exception of the S. methanicola identified on a cold seep in the Gulf of Mexico.

Osedax

More surprising yet, a worm species which belongs to an unknown genus consume the protein and oil of the bones. They are the Osedax, bone eaters. A whale skeleton weighing 40 tonnes contains between 2,000 and 3,000kg of lipids. Planted like 2cm long flowers on their substrate, their nutritional process is helped by colonies of bacteria specialised in the degradation of complex organic matter. This original symbiosis ensures the species’ strength, its abundance, good reproduction rates and proves to be particularly efficient. This illustrates the important role of whales at the end of their life cycle in the protection and Osedax mucofloris mucofloris Osedax strengthening of biodiversity. This abyssal protein and lipid - refinery associating a foreman and its subcontractors proves yet again the extraordinary potential of whales and the complexity of their useful role.

To this day 5 Osedax species have been identified on whale falls and ten are thought to belong to the same genus.

A new species Osedax mucofloris of the Osedax genus was discovered in August 2004 on the vertebrates of a minke whale (Balaenoptera acutorostrata), 9 months after it was sunk off the coast of Sweden at a depth of 125m.

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Crabs

Aquarium Institute Research © NOAA/Monterey Bay Galathea crab (Munidopsis sp.) 1,400 meters deep

Several species of galathea crabs (of the family of Galatheidae) mainly of the Munidopsis genus were observed on whale skeletons. They feed on edible fragments of dead animals or debris left by other animals. At least 16 species of Munidopsis are known to live on hydrothermal vents; a remarkable new species was discovered in 2005, the furry galathea (Kiwai hirsuta) at a depth of 2,500m. It is presumed to be carnivorous and necrophagous. This 15cm long galathea has the particularity of being covered with fur that harbours filamentous bacteria. The role of this bacteria is yet unknown. The presence of these galathea near hydrothermal vents and whale falls illustrate the similarities between these two ecosystems.

Snow crabs (commercial name). The 4 known species of the genus Chionoecet live in the Bering Sea. They feed on worms, gasteropods and fragments of fish. They are eaten by deep sea fish and humans. Following over fishing between 1970 and 1991 when catches reached 150 000 tonnes, a preservation plan was put in place by the United States. Levels are still low today and fishing is limited to 30 000 tonnes a year. The crabs participate in the ultimate “cleaning” of the carcass.

At the end of this phase all that is left is the whale skeleton, entirely striped.

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III- Stage 3

The sulphur resources of the bones enable the implantation of specialised bacterial colonies whether specialised autonomous or symbiotic with clams, molluscs, and vestimentiferan worms. It is the sulphophilic or “sulphur loving” stage. When there are strong, solid and calcium rich whale bones from healthy mature animals the sulphophilic stage can last from 40 to 80 years. It is characterised by several key elements: 1- bacterial mats specialized in sulphur chemistry covering the surface of the bones, pores and interstitial spaces, 2- large populations of clams harbouring sulphophilic bacteria and feeding on them. 3- important assemblages with more than 30 000 individuals made up of bivalves, amphipods, polycheates, limpets, gastropods and crustaceans.

Many gastropods are carnivorous and were observed feeding on bivalves. There would be at least 3 different levels of food chains on the skeleton during this stage. Bivalves, polychaetes and gastropods, among which certain species were unknown until recently, such as the Cocculina craigsmithi, they represent the majority of species present during this phase. The Cocculina craigsmithi was named in tribute to Craig Smith, researcher at the University of Hawaii who has devoted his work since 1987 towards pointing out and illustrating the richness and importance of whale falls for biodiversity.

Biocenoses on and around whale falls on the seafloor are remarkably rich in diversity and density. With an average number of 185 species, whale skeletons develop a sustainable ecosystem. About thirty species are common in sulphur reducing ecosystems such as abyssal hydrothermal vents and cold seeps; this leads scientists to evidence the link between geological phenomenons such as deep vents and biological phenomenons like the assembling of biodiversity occurring during the “second life” of the whale. Annelids (B. guaymamensis) and sulphur reducing bacteria (Beggitoata sp)- the former feeding on the latter- have been observed both on hydrothermal vents and on the carcass of a grey whale 1,900km apart. A

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Remains of sulphophilic assemblages gathered on whale fossils over 30 million years old prove the durability of this recycling mechanism and the valorisation of sulphuric hydrogen.

IV – Stage 4

Suspension feeders such as Crinoids, Ctenophores and Cnidarians settle on whale bone remains, taking advantage of the improved water flow. A new species of sea anemone was identified in 2007 on the bone of a grey whale. These natural reefs can last for a century.

Conclusion

After their life cycle, whales offer to marine biodiversity, from bacteria to benthic macrofauna, important resources and a lasting habitat. The amount of carbon gas and methane contained in the carcass and the sulphur from the skeleton force specialised bacterial species and macrofauna to transform this hostile environment into a lasting ecosystem structured by multiple food chains. All species observed are different from those present in the surrounding environment of the whale fall. The whale ecosystem presents chemical, biological and trophic similarities with hydrothermal vents and cold seeps. In the world’s oceans, whales therefore contribute to the implantation and dissemination of chemical processes and primary species which are the initial link for life in the deep sea and for the recycling of nutriments coming from the ocean surface. Taking this into account, the distribution of whale carcasses on the ocean seabed must be included in ocean and biodiversity restoration plans.

Recommendations

This recommendation applies to all maritime countries. Robin des Bois appreciates efforts carried out by Sweden, United States, and Japan to ballast and sink whole dead whales and other cetaceans and thus to observe the created ecosystems. Whale reefs have to be protected from destructive human activities. France who claims the second largest international maritime domain does not participate in this research or in the vision which points at the positive and unique contribution of whales to biodiversity and marine species’ balance including in its commercial aspects. Robin des Bois would like France’s technical and scientific means and know-how in deep sea and cetology to be better mobilised in view of clarifying and understanding better the role and the networks of natural reefs made up of whale remains on the seabed below the migrating and schooling areas.

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Bennett, B. A., Smith, C.R., Glaser, B., Maybaum, H.L. 1994. Faunal community structure of a chemoautotrophic assemblage on whale bones in the deep northeast Pacific Ocean. Marine Ecology Progress Series 108: 205-223.

Braby, C.E., Rouse, G.W., Johnson, S.J., Jones, W.J., Vrijenhoek, R.C. 2007. Bathymetric and temporal variation among Osedax boneworms and associated megafauna on whale-falls in Monteray Bay, California. Deep-Sea Research I 54 (2007) 1773- 1791.

Dahlgren, T.G., Glover, A.G, Baco, A., Smith, C.R. 2004 Fauna of whale falls: systematics and ecology of a new polychaete (Annelida: Chrysopetalidae) from the deep Pacific Ocean. Deep- Sea Research I 51: 1873-1889.

Dahlgren, T.G., Wiklund H., Källström, B., Lundälv, T. Smith, C.R. , Glover, A.G. 2006. A shallow-water whale-fall experiment in the north Atlantic. Cah. Biol. Mar. 47: 385-389.

Debenham, N.J., Lambshead, P.J.D., Ferrero, T.J., Smith, C.R., 2004 The impact of whale falls on nematode abundance in the deep sea. Deep-Sea Research I 51: 701-706.

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Jones, E.G., Collins, M.A., Bageley, P.M., Addison, S., Priede, I.G. 1998. The fate of cetacean carcasses in the deep sea: observations on consumption rates and succession of scavenging species in the abyssal north-east Atlantic Ocean. Proceedings of the Royal Society 265, 1119- 1127.

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Pjeijel, F., Rouse, G.W., Ruta, C., Wiklund, H., Nygren, A. 2008. Vrijenhoekia balenophilia, a new hesionid poychaete from a whale fall off California. Zoological Journal of the Linnean Society 152, 625-634.

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Publication Director: Jacky Bonnemains Redaction, documentation, iconography, cartography Emilie Courtin, Charlotte Nithart, Christine Bossard, Leslie Del Angel, Rachel Downey, Michelle Johnson, Kerry Sheehan Translation Jacky Bonnemains, Emilie Courtin; Miriam Potter, Meghan Faulkner

Robin des Bois Association de protection de l’Homme et de l’environnement Depuis 1985 / Since 1985 14, rue de l’Atlas 75019 Paris – France Tel : 33 1 48 04 09 36 – Fax : 33 1 01 48 04 56 41 [email protected] www.robindesbois.org

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