Are there really plenty of fish in the sea?

We started trying to manage fisheries using science-based principles more than 150 years ago. Today, despite great improvements, we are still struggling to manage fisheries well. Perhaps the greatest missing piece in our understanding is an ability to accurately link the number of spawning adult fish with the number of their offspring that survive to replenish the population. Recognition that individual differences play a role in the dynamics of natural populations promises to greatly improve fisheries management.

A classic example of our inability to effectively manage harvested fish populations is the collapse of the northwest Atlantic cod fishery. Despite being managed using best practices, in 1992 the number of cod had collapsed to less than 1% of the number present in 1977. A moratorium was declared to allow the fishery to recover. It was predicted to rebound within a decade, but twenty years on and cod stocks are still at less than 5% of their previous levels and some authorities suggest the fishery may never fully recover.

An Atlantic cod, Gadus morhua (photo Wikipedia).

Most fishes are highly fecund, releasing tens to hundreds of thousands or even millions of eggs. Mortality during the early life of fish is incredibly high, often with fewer than one in a thousand surviving the first few days. But, because of the shear number of offspring, small changes in the mortality rate can lead to enormous differences in the number of fish that survive to replenish the population. The great difficulty has been to determine which factors contribute to changes in mortality rate.

Predation and starvation are the two greatest sources of mortality for fish eggs and larvae. Neither of these is random. Bigger, better provisioned eggs are more likely to produce larvae that survive the larval period and replenish the adult population. There are also characteristics of the parents that effect the survival of their offspring, such as when and where they choose to spawn, and how big or old they are.

Predators of fish eggs and larvae are numerous. Jellyfish, like Aurelia aurita, are among them (photo Wikipedia).

Early hypotheses about what regulated survival in the larval period focused on starvation. Hjort's 'critical period' hypothesis (1914) proposed that food resources must be present when larval fish were switching from using their yolk reserves to feeding. Cushing's 'match-mismatch' hypothesis (1975, 1990) recognised that as larvae grow they need progressively larger prey and timing of prey requirement needs to be a match with the timing of prey availability.

Good evidence to support these hypotheses has only emerged recently, with the arrival of technology that can provide long-term measurements over large spatial scales. Platt et al. (2003) combined data from remote-sensing satellites with long-term population surveys of haddock, Melanogrammus aeglefinus. Their data showed that when the peak of spawning occurred after the peak in the spring plankton bloom, survival of larval haddock was much higher.

A haddock, Melanogrammus aeglefinus (photo Wikipedia).

Beaugrand et al. (2003) used data from continuous plankton sampling devices that are opportunistically attached to merchant ships. The devices gave them not only plankton abundance data, but allowed them to measure the size of prey species. Data on cod, Gadus morhua, were obtained from two largely overlapping population surveys. Like Platt et al., they found that the timing of the plankton bloom was important for larval survival, but they also found that the abundance and average size of prey species were important too.

Predation was recognised early on as an important factor influencing the survival of fish larvae. However, research into its effects on fish populations didn't begin in earnest until the 1970's. The research showed that bigger, faster growing larvae were more likely to survive that larval period. Several, subtly different mechanisms were proposed to explain this pattern and are often combined into the 'growth-predation' hypothesis. 

Testing the growth-predation hypothesis in the wild has proved tricky. But, fish have structures in their ears called otoliths that lay down growth rings a bit like the growth rings in a tree. Because the growth rings in otoliths are laid down daily in many fish species they can be used as proxy measurements of size and growth. Several studies have used otoliths to calculate size and growth rates and have universally supported the growth-predation hypothesis (e.g. Hare & Cowen 1997, Meekan et al. 2006).

The otolith of a black rockfish, Sebastes melanops, showing the light and dark bands of yearly growth increments. Smaller daily increments are visible under higher magnifications (photo Vanessa von Biela, USGS).

Mothers are one of the most important influences on the size and growth rate of larval fish, particularly early in life when mortality is highest. The time that mothers spawn determines the match between hatching and the availability of food resources. The amount that mothers invest in their offspring also influences their survival. Bigger eggs typically hatch into bigger larvae that grow faster and are more resistant to starvation Spawning time and investment can depend on the characteristics of mothers.

It's widely documented that larger, older mothers produce more offspring. Fecundity typically increases with the volume of the body cavity, which is roughly proportional to the cube of female length. Berkeley et al. (2004) also showed that larger, older female black rockfish, Sebastes melanops, invested more into their offspring, resulting in faster growing larvae that were more resistant to starvation. 

The blue rockfish, Sebastes mystinus, looks similar to the black rockfish (photo Wikipedia)

The Berkeley et al. paper became frequently cited to make the case that larger, older females needed better protection (e.g. Palumbi 2004, Birkeland & Dayton 2005). Harvesting large females might be much worse for the population because they produce more offspring that have a greater chance of surviving the larval period. Most fisheries remove the larger, older individuals, even when they are not targeted, which might explain why collapsed stocks struggle to recover faster than expected, like the Atlantic cod.

Marshall et al. (2010) argued that it was unjustified to conclude that larger females produce larvae that greater chance of survival. Decades of empirical and theoretical work has shown that the only time mothers should produce larger eggs is when they are releasing offspring into a poorer quality environment. Berkeley et al. tested larvae in common conditions and, therefore, they didn't expose larvae to the conditions that they would have experienced in the wild. 

Larger mothers might provide their offspring with a poorer quality environment in a number of ways. They might expose their offspring to greater competition with their siblings because they release far more larvae. Female size can predict the timing of spawning, and does in the black rockfish, which exposes larvae to different environmental conditions. Therefore, the larger offspring produced by larger mothers might have similar chances of surviving the larval period under natural conditions.

There is some evidence that the decades of theoretical and empirical work might not have captured the whole picture. If all larvae have roughly the same chance of making it through the larval period you would expect that the diversity of surviving larvae would be roughly proportional to the numbers released. Hedgecock et al (2007) estimated that in one cohort of the Pacific oyster, Ostrea edulis, only 10 - 20 individuals produced all of the surviving offspring.

Beldade et al. (2012) conducted a similar study to Hedgecock et al., but they were able to link surviving larvae with adults. They found that larger mothers contributed disproportionally more to the number of larvae that returned to the same population and that greater fecundity alone did not account for the disparity. It's not entirely compelling because it is possible that smaller mothers are producing larvae that preferentially disperse away. It is a tantalizing hint that larger, older mothers really matter more for population replenishment.

Most fisheries models currently do not account for the differences in the survival chances of larvae or the potential differences in the contribution of mothers to the next generation. They treat the survival of all larvae as equally likely, or ignore the larval period altogether. Such models are failing to produce accurate predictions of future stock numbers. Greater understanding of mortality processes in the larval period and the rise of individual based models promise to greatly improve the way fisheries are managed.

References:

Beaugrand, G., Brander, K., Alistair Lindley, J., Souissi, S., & Reid, P. (2003). Plankton effect on cod recruitment in the North Sea. Nature, 426 (6967), 661-664 DOI: 10.1038/nature02164

Beldade, R., Holbrook, S., Schmitt, R., Planes, S., Malone, D., & Bernardi, G. (2012). Larger female fish contribute disproportionately more to self-replenishment. Proceedings of the Royal Society B: Biological Sciences, 279 (1736), 2116-2121 DOI: 10.1098/rspb.2011.2433

Berkeley, S., Chapman, C., & Sogard, S. (2004). Maternal age as a determininant of larval growth and survival in a marine fish, Sebastes melanops. Ecology, 85 (5), 1258-1264 DOI: 10.1890/03-0706

Cushing, D. (1969). The Regularity of the Spawning Season of Some Fishes. ICES Journal of Marine Science, 33 (1), 81-92 DOI: 10.1093/icesjms/33.1.81  

Cushing, D. H. (1990). Plankton production and year-class strength in fish populations - an update of the match mismatch hypothesis. Advances in Marine Biology, 26, 249-293 DOI: 10.1016/S0065-2881(08)60202-3  

Hare, J., & Cowen, R. (1997). Size, Growth, Development, and Survival of the Planktonic Larvae of Pomatomus saltatrix (Pisces: Pomatomidae). Ecology, 78 (8) DOI: 10.2307/2265903

Hedgecock, D., Launey, S., Pudovkin, A., Naciri, Y., Lapègue, S., & Bonhomme, F. (2006). Small effective number of parents (N-b) inferred for a naturally spawned cohort of juvenile European flat oysters Ostrea edulis. Marine Biology, 150 (6), 1173-1182 DOI: 10.1007/s00227-006-0441-y

Hjort, J (1914). Fluctuations in the great fisheries of northern Europe viewed in the light of biological research. Reun. Cons. Int. Explor. Mer, 20, 1-228

Marshall, D., Heppell, S., Munch, S., & Warner, R. (2010). The relationship between maternal phenotype and offspring quality: Do older mothers really produce the best offspring? Ecology, 91 (10), 2862-2873 DOI: 10.1890/09-0156.1   

Meekan, M., Vigliola, L., Hansen, A., Doherty, P., Halford, A., & Carleton, J. (2006). Bigger is better: size-selective mortality throughout the life history of a fast-growing clupeid, Spratelloides gracilis. Marine Ecology Progress Series, 317, 237-244 DOI: 10.3354/meps317237

Platt, T., Fuentes-Yaco, C., & Frank, K. (2003). Spring algal bloom and larval fish survival. Nature, 423 (6938), 398-399 DOI: 10.1038/423398b

Seaweek!

Seaweek is coming up fast. It's organised by the Marine Education Society of Australia and running from the 2nd to the 10th of March. I've been invited to participate in a day of activities at Rickets Point Marine Sanctuary on the 7th. I'll be talking to primary and high school students about marine introduced species. The day will bring together marine experts from MESA, Parks Victoria, Melbourne Aquarium, Monash University, the Earth Watch Institute, the Ocean Ark Alliance, the Gould League, Marine Care Ricketts Point, Pelican Expeditions, Nautilus Educational and the Australian Youth Climate Coalition (and me, who is not from any of those organisations).

The theme for Seaweek 13 is ‘Sustainable Seas’. The theme provides a focus for students in schools and for communities to inform and inspire them about the diversity of our marine and coastal environments and how, through good management and individual action, we can all contribute towards the sustainability of these environments.

Aims

• Highlight the sustainable management of Australia’s marine environment;
• Identify factors that threaten the sustainability of marine and coastal ecosystems;
• Facilitate the communication of sustainable marine management projects to the education community;
• Initiate interest and actions for supporting sustainable marine management that help us learn more about and contribute towards the sustainability of our marine and coastal environments; and
• Provide schools with educational resources available on the MESA website for school’s classroom based activities.

Find out more about Seaweek here.

Attack of the jellyfish swarm

Jellyfish are not as charismatic as some marine species and consequently they have not received much research attention. Recently though, there has been increasing interest in them because their numbers appear to be on the rise worldwide. There are a few hypotheses about why this might be the case floating around in the literature.

The beautiful and under appreciated jellyfish, Cyanea capillata. Perhaps the World's biggest (photo Wikipedia).

Corals, which are in the same phylum (Cnidaria) as jellyfish, have been on the decline in northern Australia and other parts of the world. Two major hypotheses have been proposed to explain this; overfishing reducing herbivorous fish numbers leading to algal overgrowth and agricultural runoff decreasing water clarity through sedimentation and by promoting phytoplankton growth. These same pressures are thought to have a positive effect on jellyfish populations.

Overfishing is argued to increase jellyfish numbers by reducing predation and competition for food, particularly of young jellyfish. While agricultural runoff stimulates phytoplankton blooms that directly or indirectly provide increased amounts of food to jellyfish. Some others argue that changes to marine communities that are occurring as a result of climate change are tipping the ecological balance in favour of jellyfish. But there isn't much agreement, even among experts, about whether jellyfish have actually increased globally.

Nomura jellyfish, Nemopilema nomurai, causing problems for Japanese fishermen (Photo Shin-ichi Uye)

Recently, a collaboration of scientists from around the world have conducted one of the most comprehensive and rigorous analyses of the available data on jellyfish numbers. Condon et al. found that jellyfish numbers go through cyclical population booms roughly every 20 years. Their data suggest that increasing jellyfish numbers in the last few years are simply a part of this 20-year population oscillation. But, there is a hint in the data that since 1970 jellyfish numbers have be increasing.

During the last population minimum, which occurred in 1993, jellyfish numbers were higher relative to previous population minimums. This resulted in a weak, but statistically significant trend towards increasing jellyfish abundance in the last 40 years. The authors caution that the trend is too weak, given the limitations of the data set, to conclude that jellyfish populations really are on the increase. Data collected in the next few years should be able to determine, with confidence, whether the upwards trend is real.

Although they found no strong evidence that jellyfish numbers are increasing worldwide, there was good evidence that numbers are increasing in some regions. These regions included the Sea of Japan, North Atlantic shelf regions, the Barents Sea, and parts of the Mediterranean Sea. All of these regions exhibited the 20 year oscillation, but local factors seem to have acted in concert with the global population fluctuations. Notably, fishing is heavy in many, if not all, of those regions.

 

Condon, R., Duarte, C., Pitt, K., Robinson, K., Lucas, C., Sutherland, K., Mianzan, H., Bogeberg, M., Purcell, J., Decker, M., Uye, S., Madin, L., Brodeur, R., Haddock, S., Malej, A., Parry, G., Eriksen, E., Quinones, J., Acha, M., Harvey, M., Arthur, J., & Graham, W. (2013). Recurrent jellyfish blooms are a consequence of global oscillations Proceedings of the National Academy of Sciences, 110 (3), 1000-1005 DOI: 10.1073/pnas.1210920110

Australia's new marine parks revisited

Last month I wrote about the release of a draft plan for a set of marine parks in Australian Federal waters. I expressed concern that the large area and their distance from shore would make enforcement of the fully protected areas difficult. It seems I'm not alone in this concern. Three marine scientists in Western Australia have written an article in The Conversation expressing similar concerns and others about the design of the marine parks, including the under-representation of some habitats within the parks.

Marine parks and the Great Barrier Reef World Heritage Area

One of the biggest stories in marine conservation in Australia this year is the announcement that 2.3 million square kilometers of Australian waters will receive some form of protection in marine reserves. About a third, or 800 thousand square kilometers will be fully protected as Marine National Parks. This new announcement takes the total area protected by the Federal Government to 3.1 million square kilometers. Which is all cause for some optimism.

A map of the newly declared marine reserve network in Australia. Green denotes the areas which are fully protected as Marine National Parks. Yellow denotes 'special protection areas' which exclude commercial fishing, but allow recreational fishing. Dark blue denotes 'special purpose zones', which allow only some forms of commercial fishing. Light blue denotes 'multiple use zones', which only prevent the most destructive commercial fishing practices. The grey areas in the south-east are the bits of the reserve network that were established in 2007. If you would like a PDF of the map, and other information go here.

The largest contiguous protected area is the Coral Sea Marine Reserve, which adds to the already established Great Barrier Reef Marine Park. There was a storm of criticism when the Coral Sea Marine Reserve draft plan was released because many experts believed that it did not go far enough to protect the reef. In a rare win for the environment, the Australian Government extended the boundaries in the final plan.

A map of the Coral Sea Marine Reserve. Colours denote the same levels of protection as above. If you would like a PDF of the map, and other information go here.

There is, however, still significant disquiet about the future of the Great Barrier Reef, which is estimated to have lost half of its coral cover in the last 50 years. A UNESCO mission to Australian in March strongly criticised the management of the reef and indicated that its listing as a World Heritage Area was at risk of being downgraded. Several of the threats that UNESCO identified will not be addressed by the new marine reserves. 

The UNESCO mission identified climate change, catchment runoff, coastal development, ports and shipping, and fishing as the most pressing threats to the Great Barrier Reef World Heritage Area. Three of these (catchment runoff, coastal development and climate change), are due to activities outside the marine reserve and World Heritage Area. Moreover, the other activities will be allowed in at least some areas of the new marine reserve. 

The cynic in me can't help also noticing two things. Firstly, that the bulk of the areas that receive full protection as marine national parks are generally those which are furthest offshore, where impacts are already low. And, secondly, that there will need to be enforcement of the new restrictions, but there is mention of additional funds to achieve this. Apparently, enforcing compliance will be achieved using existing infrastructure; infrastructure that is already used for other important activities.

Despite my slight cynicism, I think the new marine reserve network is excellent news for the conservation of the marine environment in Australia. But, the network doesn't address all of the threats to Australia's seas. And there are at least three state governments (Victoria, Queensland and Western Australia) that have ignored environmental threats and sought to erode existing protections. It would be incredibly embarrassing for Australia on the world stage and disastrous for Queensland's marine tourism industry if UNESCO were to downgrade the Great Barrier Reef World Heritage Area listing.

Further reading

For the UNESCO mission report go here.

For the Great Barrier Reef Outlook Report, which sparked the UNESCO mission, go here.

For an interesting expert commentary on the UNESCO report go here.

UPDATE:
Just after posting this article I found another article that is more hopeful that the protections granted by the new marine reserves will be adequately enforced. I think they can be too, but enforcement needs funding and I haven't seen those details yet.

Japanese incursion

Two days ago a Japanese vessel, the Yushin Maru No. 3, associated with the whaling fleet in the Southern Ocean sailed 8 nautical miles into Australia's Territorial Waters in pursuit of a Sea Shepherd vessel. The Yushin Maru No. 3 is a harpoon ship used for whale catching and is unwelcome in Australian Territorial Waters where whaling is illegal. Despite Australian Government protests to Japan the vessel stayed within Australian waters for more than 24 hours. Moreover, it stayed within Australian waters for several hours after it was said to be leaving. It continues the pugnacious approach that Japan has adopted in its dispute with Australia over its whaling activities in the Southern Ocean. 

The Yushin Maru No. 2, a harpoon vessel similar to the Yushin Maru No. 3

Although the vessel is now within Australian's Exclusive Economic Zone there is apparently little legal recourse for Australia as long as the vessel does not hunt whales. Australia has  claimed its Exclusive Economic Zone as a whale sanctuary. Under international law Australia should have the legal right to regulate fishing, including whaling, within this zone. But, Japan continues to hunt whales within the sanctuary under the guise of scientific research*. Finally, after much dithering by both major political parties, Australia launched legal proceedings against Japan over the whaling in the International Court of Justice. Australia submitted its case in May 2011 and Japan is due to make its submission in March this year.

Map of Antarctic territorial claims. Australia claims two territories (orange) which sandwich the French claim (dark blue). Norway claims the next largest territory (purple). New Zealand (green) also claims territory. The UK (red), Chile (yellow) and Argentina (light blue) have overlapping claims.

Any reduction in the area that Japanese can catch whales in as a result of Australia's action in the International Court for Justice is, unfortunately, unlikely to have a great effect on the supply of whale meat in Japan. Australia claims and exclusive economic zone in the waters off its Antarctic territory, but Japan and most of the rest of the world does not recognise this claim. Indeed, only four countries who also claim large exclusive economic zones in the Antarctic recognise Australia's claim. Japan is therefore likely to be able to continue whaling in these areas. Moreover, Iceland now exports whale meat to Japan, reportedly earning the country $US 17 million in the last four years. Like Japan, Iceland's whale hunt is conducted under the guise of scientific research. I guess they have a lot of collaborators in Japan...

The Japanese and Icelandic whale research programmes produce few, if any, valuable data on whales. Moreover, non-lethal research can be used to produce much of the same information. Scientific reviews of the research programmes conducted by the International Whaling Commission have found that experimental designs are shoddy, and that the information is either not required for management or obtainable by non-lethal means. That has not stopped either of the countries from whaling. Indeed, Japan has tried to use their data to argue that whale numbers are growing and need to be culled to preserve commercially important fish species. Of greater threat to Japan's commercially important fish stocks is certainly Japan's fishing fleets. I'll write more on that sometime.

*As Terry Pratchett and Neil Gaiman joke in Good Omens, the research is primarily concerned with determining how many whales can be caught during the whaling season.

Coral Sea Marine Park

The Australian Government is considering submissions to its Coral Sea Commonwealth Marine Reserve proposal. The proposal is seen by many leading scientists as insufficient to properly protect the area from fishing and other impacts (e.g. here and here).

Should the park go ahead as it is currently proposed it will be the largest marine park ever established. But, less than half of it will be given full protection and this area is the part furthest from shore and already the least impacted by commercial and recreational fishing.

Overfishing is a significant threat to coral reefs and is likely to decrease the resilience of coral reefs to climate change¹. It would be good to get greater protection of this area from fishing activities. If you would like to contribute go here for a guide to writing a submission, or go here to view the proposal. The consultation process ends on February 24, 2012.

1 Pandolfi, J. M., Connolly, S. R., Marshall, D. J., Cohen, A. L. Projecting Coral Reef Futures Under Global Warming and Ocean Acidification. Science 333 no. 6041, 418-422, doi:10.1126/science.1204794 (2011).